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<meta name="description" content="CLC chloride/proton exchangers may support acidification of endolysosomes and raise their luminal Cl<sup>-</sup> concentration. Disruption of endosomal ClC-3 causes severe neurodegeneration. To assess the importance of ClC-3 Cl<sup>-</sup> /H<sup>+</sup> exchange, we now generate Clcn3<sup>unc/unc</sup> …"><meta name="keywords" content="pmid:32118314, PMC7196918, doi:10.15252/embj.2019103358, Research Support, Non-U.S. Gov't, Stefanie Weinert, Niclas Gimber, Thomas J Jentsch, Animals, COS Cells, Chloride Channels / genetics*, Chloride Channels / metabolism*, Chlorocebus aethiops, Disease Models, Animal, Endosomes / metabolism*, Mice, Mutation, Neurodegenerative Diseases / genetics*, Neurodegenerative Diseases / metabolism, Synaptic Vesicles / metabolism, PubMed Abstract, NIH, NLM, NCBI, National Institutes of Health, National Center for Biotechnology Information, National Library of Medicine, MEDLINE"><meta name="robots" content="index,nofollow,noarchive"><meta property="og:title" content="Uncoupling endosomal CLC chloride/proton exchange causes severe neurodegeneration - PubMed"><meta property="og:url" content="https://pubmed.ncbi.nlm.nih.gov/32118314/"><meta property="og:description" content="CLC chloride/proton exchangers may support acidification of endolysosomes and raise their luminal Cl<sup>-</sup> concentration. Disruption of endosomal ClC-3 causes severe neurodegeneration. To assess the importance of ClC-3 Cl<sup>-</sup> /H<sup>+</sup> exchange, we now generate Clcn3<sup>unc/unc</sup> …"><meta property="og:image" content="https://cdn.ncbi.nlm.nih.gov/pubmed/persistent/pubmed-meta-image-v2.jpg"><meta property="og:image:secure_url" content="https://cdn.ncbi.nlm.nih.gov/pubmed/persistent/pubmed-meta-image-v2.jpg"><meta property="og:type" content="website"><meta property="og:site_name" content="PubMed"><meta name="twitter:domain" content="pubmed.ncbi.nlm.nih.gov"><meta name="twitter:card" content="summary_large_image"><meta name="twitter:title" content="Uncoupling endosomal CLC chloride/proton exchange causes severe neurodegeneration - PubMed"><meta name="twitter:url" content="https://pubmed.ncbi.nlm.nih.gov/32118314/"><meta name="twitter:description" content="CLC chloride/proton exchangers may support acidification of endolysosomes and raise their luminal Cl<sup>-</sup> concentration. Disruption of endosomal ClC-3 causes severe neurodegeneration. To assess the importance of ClC-3 Cl<sup>-</sup> /H<sup>+</sup> exchange, we now generate Clcn3<sup>unc/unc</sup> …"><meta name="twitter:image" content="https://cdn.ncbi.nlm.nih.gov/pubmed/persistent/pubmed-meta-image-v2.jpg">
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||
|
||
<span class="search-input-link user-guide-link" role="navigation" aria-label="User guide">
|
||
<a href="/help/"
|
||
data-ga-category="featured_link"
|
||
data-ga-action="user_guide">
|
||
User Guide
|
||
</a>
|
||
</span>
|
||
|
||
</div>
|
||
</div>
|
||
|
||
|
||
</form>
|
||
|
||
|
||
<div id="article-page-header">
|
||
<div id="article-top-actions-bar" class="article-top-actions-bar">
|
||
<div class="inner-wrap">
|
||
<div class="actions-container">
|
||
<div class="return-to-search">
|
||
|
||
|
||
</div>
|
||
|
||
<div class="multiple-results-actions " role="region" aria-label="save, email, send to">
|
||
<button id="save-results-panel-trigger"
|
||
type="button"
|
||
class="save-results save-results-panel-trigger"
|
||
aria-expanded="false"
|
||
aria-controls="save-action-panel"
|
||
data-ga-category="save_share"
|
||
data-ga-action="save"
|
||
data-ga-label="open">
|
||
Save
|
||
</button><button id="email-results-panel-trigger"
|
||
type="button"
|
||
class="email-results email-results-panel-trigger"
|
||
aria-expanded="false"
|
||
aria-controls="email-action-panel"
|
||
data-ga-category="save_share"
|
||
data-ga-action="email"
|
||
data-ga-label="open">
|
||
Email
|
||
</button><div class="more-actions dropdown-block"><button id="more-actions-trigger"
|
||
type="button"
|
||
class="trigger more-actions-trigger"
|
||
ref="linksrc=show_moreactions_btn"
|
||
aria-label="Send to"
|
||
aria-controls="more-actions-dropdown">Send to</button><div id="more-actions-dropdown" class="dropdown dropdown-container" hidden><div class="content"><ul class="more-actions-links"><li><a class="clipboard-panel-trigger dropdown-block-link "
|
||
href="#"
|
||
role="button"
|
||
data-ga-category="save_share"
|
||
data-ga-action="clipboard"
|
||
data-ga-label="send">
|
||
Clipboard
|
||
</a></li><li><a role="button" class="dropdown-block-link bibliography-trigger-target" href="https://account.ncbi.nlm.nih.gov/?back_url=https%3A%2F%2Fpubmed.ncbi.nlm.nih.gov%2F32118314%2F%23open-bibliography-panel">My Bibliography</a></li><li><a role="button" class="dropdown-block-link collections-trigger-target" href="https://account.ncbi.nlm.nih.gov/?back_url=https%3A%2F%2Fpubmed.ncbi.nlm.nih.gov%2F32118314%2F%23open-collections-panel">Collections</a></li><li><a role="button" class="citation-manager-panel-trigger dropdown-block-link citation-manager-trigger-target" href="#">Citation manager</a></li></ul></div></div></div>
|
||
</div>
|
||
|
||
|
||
|
||
<div class="display-options" data-format-key="format"
|
||
data-default-format-value="abstract"
|
||
data-current-format-value="abstract" role="region">
|
||
<button
|
||
class="trigger usa-button"
|
||
title="Change format"
|
||
data-ga-category="display_options"
|
||
data-ga-action="display_options_dialog">
|
||
<span class="button-label">Display options</span>
|
||
</button>
|
||
|
||
<div class="dropdown" hidden>
|
||
<div class="title">
|
||
Display options
|
||
</div>
|
||
|
||
<div class="content">
|
||
|
||
<div class="format-container">
|
||
<span class="option-label">
|
||
Format
|
||
</span>
|
||
<select name="format" data-initial-value="abstract" aria-label="Display format" id="article-display-format">
|
||
<option value="abstract">Abstract</option>
|
||
|
||
<option value="pubmed">PubMed</option>
|
||
|
||
<option value="pmid">PMID</option>
|
||
|
||
</select>
|
||
</div>
|
||
|
||
</div>
|
||
</div>
|
||
</div>
|
||
<input type="hidden" name="csrfmiddlewaretoken" value="v7NGtwR1NZZjwjtOOqZuXCfnti8PtghvMUxL6mknnAMNqKzErJCwrKL11mQ1mRPP">
|
||
</div>
|
||
</div>
|
||
</div>
|
||
|
||
<div id="article-panels-container" class="article-panels-container">
|
||
<div id="save-action-panel" class="save-action-panel action-panel" aria-hidden="true">
|
||
<div class="inner-wrap">
|
||
<h2 class="action-panel-heading">
|
||
Save citation to file
|
||
</h2>
|
||
<form id="save-action-panel-form"
|
||
class="action-panel-content action-form"
|
||
action="/results-export-ids/"
|
||
data-by-search-action="/results-export-search-data/"
|
||
data-by-ids-action="/results-export-ids/"
|
||
method="post"
|
||
data-by-search-method="post"
|
||
data-by-ids-method="post">
|
||
|
||
<input type="hidden" name="csrfmiddlewaretoken" value="v7NGtwR1NZZjwjtOOqZuXCfnti8PtghvMUxL6mknnAMNqKzErJCwrKL11mQ1mRPP">
|
||
|
||
|
||
|
||
<div class="action-panel-control-wrap">
|
||
<label for="save-action-format" class="action-panel-label">
|
||
Format:
|
||
</label>
|
||
<select id="save-action-format" name="results-format" class="action-panel-selector">
|
||
<option value="summary-text">Summary (text)</option>
|
||
<option value="pubmed-text">PubMed</option>
|
||
<option value="pmid">PMID</option>
|
||
<option value="abstract">Abstract (text)</option>
|
||
<option value="csv">CSV</option>
|
||
</select>
|
||
</div>
|
||
|
||
<div class="action-panel-actions">
|
||
<button class="action-panel-submit"
|
||
type="submit"
|
||
data-loading-label="Saving..."
|
||
data-ga-category="save_share"
|
||
data-ga-action="save"
|
||
data-ga-label="save">
|
||
Create file
|
||
</button>
|
||
<button class="action-panel-cancel"
|
||
aria-label="Close 'Save citations to file' panel"
|
||
ref="linksrc=close_save_panel"
|
||
aria-controls="save-action-panel"
|
||
aria-expanded="false"
|
||
data-ga-category="save_share"
|
||
data-ga-action="save"
|
||
data-ga-label="cancel">
|
||
Cancel
|
||
</button>
|
||
</div>
|
||
</form>
|
||
</div>
|
||
</div>
|
||
|
||
|
||
|
||
|
||
<div id="email-action-panel"
|
||
class="email-action-panel action-panel"
|
||
aria-hidden="true"
|
||
data-recaptcha-script-url="https://www.recaptcha.net/recaptcha/enterprise.js?render=explicit&onload=onloadCaptchaCallback"
|
||
data-recaptcha-enabled="true">
|
||
<div class="inner-wrap">
|
||
<h2 class="action-panel-heading">
|
||
Email citation
|
||
</h2>
|
||
<form id="email-action-panel-form"
|
||
class="action-panel-content action-form"
|
||
action="/send-email/"
|
||
data-by-search-action="/results-export-email-by-search-data/"
|
||
data-by-ids-action="/send-email/"
|
||
data-by-search-method="post"
|
||
data-by-ids-method="post"
|
||
method="post"
|
||
>
|
||
<input type="hidden" name="csrfmiddlewaretoken" value="v7NGtwR1NZZjwjtOOqZuXCfnti8PtghvMUxL6mknnAMNqKzErJCwrKL11mQ1mRPP">
|
||
|
||
<div class="action-panel-control-wrap">
|
||
<span class="action-panel-label">
|
||
Subject:
|
||
</span>
|
||
<span class="email-subject" id="email-subject" aria-label="Email subject">1 selected item: 32118314 - PubMed</span>
|
||
<input type="hidden" name="email-subject" value="1 selected item: 32118314"/>
|
||
<input type="hidden" name="email-subject-hash" value="3c1105919c2b7d1ae2592b816c5179deb1896c014b0e7be1b52915836c6f3b1c"/>
|
||
</div>
|
||
|
||
<div class="action-panel-control-wrap">
|
||
<label for="email-to" class="action-panel-label required-field-asterisk">
|
||
To:
|
||
</label>
|
||
<input type="email" aria-label="Recipient Email Address" placeholder="email@example.com" id="email-to" class="email-to" pattern="^[a-zA-Z0-9_.+-]+@[a-zA-Z0-9-]+\.[a-zA-Z0-9-.]+$" maxlength="100" required>
|
||
</div>
|
||
|
||
<div class="action-panel-control-wrap">
|
||
<label for="email-from" class="action-panel-label">
|
||
From:
|
||
</label>
|
||
<input type="email" aria-label="Sender Email Address" placeholder="email@example.com" id="email-from" class="email-from" pattern="^[a-zA-Z0-9_.+-]+@[a-zA-Z0-9-]+\.[a-zA-Z0-9-.]+$" maxlength="256">
|
||
</div>
|
||
|
||
|
||
|
||
<div class="action-panel-control-wrap">
|
||
<label for="email-citation-format" class="action-panel-label">
|
||
Format:
|
||
</label>
|
||
<select id="email-citation-format" name="citation-format" class="action-panel-selector email-citation-format">
|
||
<option selected="selected" value="summary">Summary</option>
|
||
<option value="summary-text">Summary (text)</option>
|
||
<option value="abstract">Abstract</option>
|
||
<option value="abstract-text">Abstract (text)</option>
|
||
|
||
</select>
|
||
</div>
|
||
<div class="include-supplemental-container">
|
||
<input type="checkbox" aria-label="Include MeSH and other data" name="include-supplemental" id="email-include-supplemental" class="email-include-supplemental">
|
||
<label for="email-include-supplemental" class="email-include-supplemental-label">MeSH and other data</label>
|
||
</div>
|
||
|
||
|
||
|
||
<div class="form-field recaptcha ">
|
||
|
||
|
||
|
||
<div class="g-recaptcha" id="id-recaptcha" data-sitekey="6LfsWHMdAAAAAClKbtOpjQ2pMjgsGxvv7NdZW9uI"></div>
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
<div id="captcha-error-message" class="usa-input-error-message captcha-validation-message" role="alert"></div>
|
||
|
||
|
||
|
||
<div class="action-panel-actions">
|
||
<button class="action-panel-submit"
|
||
type="submit"
|
||
data-loading-label="Sending..."
|
||
data-ga-category="save_share"
|
||
data-ga-action="email"
|
||
data-ga-label="send">
|
||
Send email
|
||
</button>
|
||
<button class="action-panel-cancel"
|
||
aria-label="Close 'Email citations' panel"
|
||
ref="linksrc=close_email_panel"
|
||
aria-controls="email-action-panel"
|
||
aria-expanded="false"
|
||
data-ga-category="save_share"
|
||
data-ga-action="email"
|
||
data-ga-label="cancel">
|
||
Cancel
|
||
</button>
|
||
</div>
|
||
<input type="hidden" name="email-search-details" value="" />
|
||
<input type="hidden" name="email-search-details-hash" value="0e42663a6c3bd85498fcb88798998fed7bfdc45d457db35281e41afe13cc0524" />
|
||
</form>
|
||
</div>
|
||
</div>
|
||
|
||
<div id="collections-action-panel"
|
||
class="collections-action-panel action-panel in-progress-dots-panel"
|
||
aria-hidden="true"
|
||
data-collections-open-panel-enabled="false"
|
||
data-collections-open-panel-url-hash="#open-collections-panel">
|
||
<div class="inner-wrap">
|
||
<h3 class="action-panel-heading">
|
||
Add to Collections
|
||
</h3>
|
||
|
||
|
||
<form id="collections-action-panel-form"
|
||
class="collections-action-panel-form action-panel-content action-form action-panel-smaller-selectors"
|
||
data-existing-collections-url="/list-existing-collections/"
|
||
data-add-to-existing-collection-url="/add-to-existing-collection/"
|
||
data-create-and-add-to-new-collection-url="/create-and-add-to-new-collection/"
|
||
data-get-article-ids-by-search-url="/get-article-ids-by-search/"
|
||
data-myncbi-max-collection-name-length="100"
|
||
data-add-to-collection-max-amount="1000"
|
||
data-collections-root-url="https://www.ncbi.nlm.nih.gov/myncbi/collections/">
|
||
|
||
<input type="hidden" name="csrfmiddlewaretoken" value="v7NGtwR1NZZjwjtOOqZuXCfnti8PtghvMUxL6mknnAMNqKzErJCwrKL11mQ1mRPP">
|
||
|
||
|
||
|
||
<div class="choice-group" role="radiogroup">
|
||
<ul class="radio-group-items">
|
||
<li>
|
||
<input type="radio"
|
||
id="collections-action-panel-new"
|
||
class="collections-new"
|
||
name="collections"
|
||
value="new"
|
||
data-ga-category="save_share"
|
||
data-ga-action="collections"
|
||
data-ga-label="collections_radio_new">
|
||
<label for="collections-action-panel-new">Create a new collection</label>
|
||
</li>
|
||
<li>
|
||
<input type="radio"
|
||
id="collections-action-panel-existing"
|
||
class="collections-existing"
|
||
name="collections"
|
||
value="existing"
|
||
checked="true"
|
||
data-ga-category="save_share"
|
||
data-ga-action="collections"
|
||
data-ga-label="collections_radio_existing">
|
||
<label for="collections-action-panel-existing">Add to an existing collection</label>
|
||
</li>
|
||
</ul>
|
||
</div>
|
||
|
||
<div class="controls-wrapper">
|
||
<div class="action-panel-control-wrap new-collections-controls">
|
||
<label for="collections-action-panel-add-to-new" class="action-panel-label required-field-asterisk">
|
||
Name your collection:
|
||
</label>
|
||
<input
|
||
type="text"
|
||
name="add-to-new-collection"
|
||
id="collections-action-panel-add-to-new"
|
||
class="collections-action-add-to-new"
|
||
pattern="[^"&=<>\/]*" title="The following characters are not allowed in the Name field: "&=<>/"
|
||
maxlength="100"
|
||
data-ga-category="save_share"
|
||
data-ga-action="create_collection"
|
||
data-ga-label="non_favorties_collection">
|
||
<div class="collections-new-name-too-long usa-input-error-message selection-validation-message">
|
||
Name must be less than 100 characters
|
||
</div>
|
||
</div>
|
||
<div class="action-panel-control-wrap existing-collections-controls">
|
||
<label for="collections-action-panel-add-to-existing" class="action-panel-label">
|
||
Choose a collection:
|
||
</label>
|
||
<select id="collections-action-panel-add-to-existing"
|
||
class="action-panel-selector collections-action-add-to-existing"
|
||
data-ga-category="save_share"
|
||
data-ga-action="select_collection"
|
||
data-ga-label="($('#collections-action-add-to-existing').val() === 'Favorites') ? 'Favorites' : 'non_favorites_collection'">
|
||
</select>
|
||
<div class="collections-retry-load-on-error usa-input-error-message selection-validation-message">
|
||
Unable to load your collection due to an error<br>
|
||
<a href="#">Please try again</a>
|
||
</div>
|
||
</div>
|
||
</div>
|
||
|
||
<div class="action-panel-actions">
|
||
<button class="action-panel-submit"
|
||
type="submit"
|
||
data-loading-label="Adding..."
|
||
data-pinger-ignore
|
||
data-ga-category="save_share"
|
||
data-ga-action="collections"
|
||
data-ga-label="add">
|
||
Add
|
||
</button>
|
||
<button class="action-panel-cancel"
|
||
aria-label="Close 'Add to Collections' panel"
|
||
ref="linksrc=close_collections_panel"
|
||
aria-controls="collections-action-panel"
|
||
aria-expanded="false"
|
||
data-ga-category="save_share"
|
||
data-ga-action="collections"
|
||
data-ga-label="cancel">
|
||
Cancel
|
||
</button>
|
||
</div>
|
||
</form>
|
||
</div>
|
||
</div>
|
||
|
||
<div id="bibliography-action-panel"
|
||
class="bibliography-action-panel action-panel in-progress-dots-panel"
|
||
aria-hidden="true"
|
||
data-bibliography-open-panel-enabled="false"
|
||
data-bibliography-open-panel-url-hash="#open-bibliography-panel">
|
||
<div class="inner-wrap">
|
||
<h3 class="action-panel-heading">
|
||
Add to My Bibliography
|
||
</h3>
|
||
<form id="bibliography-action-panel-form"
|
||
class="bibliography-action-panel-form action-panel-content action-form action-panel-smaller-selectors"
|
||
data-add-to-bibliography-max-amount="100"
|
||
data-add-to-bibliography-batch-size="10"
|
||
data-bibliography-delegates-url="/list-bibliography-delegates/"
|
||
data-add-to-bibliography-url="/add-to-bibliography/"
|
||
data-get-article-ids-by-search-url="/get-article-ids-by-search/"
|
||
data-mybib-root-url="https://www.ncbi.nlm.nih.gov/myncbi/collections/mybibliography/">
|
||
|
||
<input type="hidden" name="csrfmiddlewaretoken" value="v7NGtwR1NZZjwjtOOqZuXCfnti8PtghvMUxL6mknnAMNqKzErJCwrKL11mQ1mRPP">
|
||
|
||
|
||
|
||
<div class="action-panel-control-wrap bibliographies-controls">
|
||
<div class="choice-group">
|
||
<ul class="bibliographies-action-add radio-group-items">
|
||
<li>
|
||
<input name="bibliography" id="my-bibliography" class="my-bibliography" type="radio" checked/>
|
||
<label for="my-bibliography">My Bibliography</label>
|
||
</li>
|
||
</ul>
|
||
</div>
|
||
</div>
|
||
|
||
<div class="bibliographies-retry-load-on-error usa-input-error-message selection-validation-message">
|
||
Unable to load your delegates due to an error<br>
|
||
<a href="#">Please try again</a>
|
||
</div>
|
||
|
||
<div class="action-panel-actions">
|
||
<button class="action-panel-submit"
|
||
type="submit"
|
||
data-loading-label="Adding..."
|
||
data-pinger-ignore>
|
||
Add
|
||
</button>
|
||
<button class="action-panel-cancel"
|
||
aria-label="Close 'Add to bibliography' panel"
|
||
ref="linksrc=close_bibliography_panel"
|
||
aria-controls="bibliography-action-panel"
|
||
aria-expanded="false"
|
||
data-ga-category="save_share"
|
||
data-ga-action="mybib"
|
||
data-ga-label="cancel">
|
||
Cancel
|
||
</button>
|
||
</div>
|
||
</form>
|
||
</div>
|
||
</div>
|
||
|
||
|
||
|
||
|
||
<div id="saved-search-action-panel" class="saved-search-action-panel action-panel " aria-hidden="true"
|
||
data-saved-search-open-panel-enabled="false"
|
||
data-saved-search-open-panel-url-hash="#open-saved-search-panel">
|
||
<div class="inner-wrap">
|
||
<h2 class="action-panel-heading">
|
||
Your saved search
|
||
</h2>
|
||
|
||
<form id="saved-search-action-panel-form"
|
||
class="saved-search-action-panel-form action-panel-content action-form"
|
||
data-create-saved-search-url="/create-saved-search/"
|
||
data-try-search-terms-url="/try-search-term/"
|
||
data-saved-search-root-url="https://www.ncbi.nlm.nih.gov/myncbi/searches/">
|
||
|
||
<input type="hidden" name="csrfmiddlewaretoken" value="v7NGtwR1NZZjwjtOOqZuXCfnti8PtghvMUxL6mknnAMNqKzErJCwrKL11mQ1mRPP">
|
||
|
||
<div class="action-panel-control-wrap">
|
||
<label for="saved-search-name" class="action-panel-label saved-search-name-label required-field-asterisk">
|
||
Name of saved search:
|
||
</label>
|
||
<input maxlength="200"
|
||
type="text"
|
||
name="saved-search-name"
|
||
id="saved-search-name"
|
||
class="saved-search-name"
|
||
value=""
|
||
required
|
||
pattern="[^"&=<>\/]*" title="The following characters are not allowed in the Name field: "&=<>/">
|
||
</div>
|
||
|
||
<div class="action-panel-control-wrap">
|
||
<label for="saved-search-term" class="action-panel-label required-field-asterisk">
|
||
Search terms:
|
||
</label>
|
||
<textarea name="saved-search-term" id="saved-search-term" class="saved-search-term" required></textarea>
|
||
</div>
|
||
<div class="test-search-term-wrap">
|
||
<a href="#" class="try-search-term">Test search terms</a>
|
||
</div>
|
||
<div class="choice-group action-panel-extra-margin-top">
|
||
<span class="action-panel-label" id="fieldset-label">
|
||
Would you like email updates of new search results?
|
||
</span>
|
||
<fieldset id="saved-search-alert" aria-describedby="fieldset-label">
|
||
<legend class="usa-sr-only">Saved Search Alert Radio Buttons</legend>
|
||
<ul class="radio-group-items">
|
||
<li>
|
||
<input type="radio" id="saved-search-alert-yes" class="saved-search-alert-yes" name="saved-search-alert" value="yes" checked>
|
||
<label for="saved-search-alert-yes" class="action-panel-label">Yes</label>
|
||
</li>
|
||
<li>
|
||
<input aria-label="No radio input" type="radio" id="saved-search-alert-no" class="saved-search-alert-no" name="saved-search-alert" value="no">
|
||
<label for="saved-search-alert-no" class="action-panel-label">No</label>
|
||
</li>
|
||
</ul>
|
||
</fieldset>
|
||
</div>
|
||
|
||
<div class="alert-schedule-wrap">
|
||
<div class="action-panel-control-wrap">
|
||
<label class="action-panel-label">
|
||
Email:
|
||
</label>
|
||
<span aria-label="Email address" id="saved-search-email" class="action-panel-label"><span class="action-panel-label-bold"></span> (<a class="myncbi-account-settings" href="https://www.ncbi.nlm.nih.gov/account/settings/">change</a>)</span>
|
||
</div>
|
||
<div class="action-panel-control-wrap action-panel-extra-margin-top">
|
||
<label for="saved-search-frequency" class="action-panel-label">
|
||
Frequency:
|
||
</label>
|
||
<select id="saved-search-frequency" class="no-border-panel-selector saved-search-frequency">
|
||
<option value="monthly">Monthly</option>
|
||
<option value="weekly">Weekly</option>
|
||
<option value="daily">Daily</option>
|
||
</select>
|
||
</div>
|
||
<div class="action-panel-control-wrap saved-search-monthly-additional">
|
||
<label for="saved-search-monthly-on-day" class="action-panel-label">
|
||
Which day?
|
||
</label>
|
||
<select id="saved-search-monthly-on-day" class="no-border-panel-selector">
|
||
<option value="Sunday">The first Sunday</option>
|
||
<option value="Monday">The first Monday</option>
|
||
<option value="Tuesday">The first Tuesday</option>
|
||
<option value="Wednesday">The first Wednesday</option>
|
||
<option value="Thursday">The first Thursday</option>
|
||
<option value="Friday">The first Friday</option>
|
||
<option value="Saturday">The first Saturday</option>
|
||
<option value="day">The first day</option>
|
||
<option value="weekday">The first weekday</option>
|
||
</select>
|
||
</div>
|
||
<div class="action-panel-control-wrap saved-search-weekly-additional">
|
||
<label for="saved-search-weekly-on-day" class="action-panel-label">
|
||
Which day?
|
||
</label>
|
||
<select id="saved-search-weekly-on-day" class="no-border-panel-selector saved-search-weekly-on-day">
|
||
<option value="Sunday">Sunday</option>
|
||
<option value="Monday">Monday</option>
|
||
<option value="Tuesday">Tuesday</option>
|
||
<option value="Wednesday">Wednesday</option>
|
||
<option value="Thursday">Thursday</option>
|
||
<option value="Friday">Friday</option>
|
||
<option value="Saturday">Saturday</option>
|
||
</select>
|
||
</div>
|
||
<div class="action-panel-control-wrap">
|
||
<label for="saved-search-report" class="action-panel-label">
|
||
Report format:
|
||
</label>
|
||
<select id="saved-search-report" class="no-border-panel-selector saved-search-report">
|
||
<option value="DocSum">Summary</option>
|
||
<option value="DocSumText">Summary (text)</option>
|
||
<option value="Abstract">Abstract</option>
|
||
<option value="AbstractText">Abstract (text)</option>
|
||
<option value="MEDLINE">PubMed</option>
|
||
</select>
|
||
</div>
|
||
<div class="action-panel-control-wrap">
|
||
<label for="saved-search-amount" class="action-panel-label">
|
||
Send at most:
|
||
</label>
|
||
<select id="saved-search-amount" class="no-border-panel-selector saved-search-amount">
|
||
<option value="1">1 item</option>
|
||
<option value="5" selected>5 items</option>
|
||
<option value="10">10 items</option>
|
||
<option value="20">20 items</option>
|
||
<option value="50">50 items</option>
|
||
<option value="100">100 items</option>
|
||
<option value="200">200 items</option>
|
||
</select>
|
||
</div>
|
||
<div>
|
||
<input type="checkbox" id="saved-search-send-if-no-result" class="saved-search-send-if-no-result" name="saved-search-send-if-no-result">
|
||
<label for="saved-search-send-if-no-result" class="action-panel-label smaller-checkbox">
|
||
Send even when there aren't any new results
|
||
</label>
|
||
</div>
|
||
<div class="action-panel-control-wrap option-text-in-email-wrap">
|
||
<label for="saved-search-email-text" class="action-panel-label">
|
||
Optional text in email:
|
||
</label>
|
||
<textarea name="saved-search-email-text"
|
||
id="saved-search-email-text"
|
||
class="saved-search-email-text"></textarea>
|
||
</div>
|
||
|
||
</div>
|
||
|
||
<div class="action-panel-actions">
|
||
<button class="action-panel-submit"
|
||
type="submit"
|
||
data-loading-label="Saving..."
|
||
data-ga-category="save_share"
|
||
data-ga-action="alert"
|
||
data-ga-label="save">
|
||
Save
|
||
</button>
|
||
<button class="action-panel-cancel"
|
||
aria-label="Close 'Your saved search' panel"
|
||
ref="linksrc=close_saved_search_panel"
|
||
aria-controls="saved-search-action-panel"
|
||
aria-expanded="false"
|
||
data-ga-category="save_share"
|
||
data-ga-action="alert"
|
||
data-ga-label="cancel">
|
||
Cancel
|
||
</button>
|
||
</div>
|
||
</form>
|
||
</div>
|
||
</div>
|
||
|
||
<div id="citation-manager-action-panel" class="citation-manager-action-panel action-panel" aria-hidden="true">
|
||
<div class="inner-wrap">
|
||
<h2 class="action-panel-heading">
|
||
Create a file for external citation management software
|
||
</h2>
|
||
<form id="citation-manager-action-panel-form"
|
||
class="action-panel-content action-form"
|
||
action="/results-export-ids/"
|
||
data-by-search-action="/results-export-search-data/"
|
||
data-by-ids-action="/results-export-ids/"
|
||
method="post"
|
||
data-by-search-method="post"
|
||
data-by-ids-method="post">
|
||
|
||
<input type="hidden" name="csrfmiddlewaretoken" value="v7NGtwR1NZZjwjtOOqZuXCfnti8PtghvMUxL6mknnAMNqKzErJCwrKL11mQ1mRPP">
|
||
|
||
|
||
|
||
<input name="results-format" type="hidden" value="pubmed"/>
|
||
|
||
<div class="action-panel-actions">
|
||
<button class="action-panel-submit"
|
||
type="submit"
|
||
data-loading-label="Sending..."
|
||
data-ga-category="save_share"
|
||
data-ga-action="citation_manager"
|
||
data-ga-label="save">
|
||
Create file
|
||
</button>
|
||
<button class="action-panel-cancel"
|
||
aria-label="Close 'Send citations to citation manager' panel"
|
||
ref="linksrc=close_citation_manager_panel"
|
||
aria-controls="citation-manager-action-panel"
|
||
aria-expanded="false"
|
||
data-ga-category="save_share"
|
||
data-ga-action="citation_manager"
|
||
data-ga-label="cancel">
|
||
Cancel
|
||
</button>
|
||
</div>
|
||
</form>
|
||
</div>
|
||
</div>
|
||
|
||
|
||
|
||
|
||
<div id="rss-action-panel" class="rss-action-panel action-panel " aria-hidden="true">
|
||
<div class="inner-wrap">
|
||
<h2 class="action-panel-heading">
|
||
Your RSS Feed
|
||
</h2>
|
||
|
||
<form id="rss-action-panel-form"
|
||
class="rss-action-panel-form action-panel-content action-form"
|
||
data-create-rss-feed-url="/create-rss-feed-url/"
|
||
data-search-form-term-value="">
|
||
|
||
<input type="hidden" name="csrfmiddlewaretoken" value="v7NGtwR1NZZjwjtOOqZuXCfnti8PtghvMUxL6mknnAMNqKzErJCwrKL11mQ1mRPP">
|
||
|
||
<div class="action-panel-control-wrap">
|
||
<label for="rss-name" class="action-panel-label required-field-asterisk">
|
||
Name of RSS Feed:
|
||
</label>
|
||
<input maxlength="200"
|
||
placeholder="Name"
|
||
type="text"
|
||
name="rss-name"
|
||
id="rss-name"
|
||
class="rss-name"
|
||
value=''
|
||
required
|
||
pattern="[^"&=<>\/]*" title="The following characters are not allowed in the Name field: "&=<>/">
|
||
</div>
|
||
|
||
<div class="rss-limit-wrap">
|
||
<div class="action-panel-control-wrap action-panel-extra-margin-top">
|
||
<label for="rss-limit" class="action-panel-label">
|
||
Number of items displayed:
|
||
</label>
|
||
<select id="rss-limit" class="no-border-panel-selector rss-limit">
|
||
<option value="5">5</option>
|
||
<option value="10">10</option>
|
||
<option value="15" selected="selected">15</option>
|
||
<option value="20">20</option>
|
||
<option value="50">50</option>
|
||
<option value="100">100</option>
|
||
</select>
|
||
</div>
|
||
</div>
|
||
|
||
<div class="action-panel-actions">
|
||
<button class="action-panel-submit"
|
||
type="submit"
|
||
data-loading-label="Creating..."
|
||
data-ga-category="save_share"
|
||
data-ga-action="alert"
|
||
data-ga-label="save">
|
||
Create RSS
|
||
</button>
|
||
<button class="action-panel-cancel"
|
||
aria-label="Close 'Your RSS' panel"
|
||
ref="linksrc=close_rss_panel"
|
||
aria-controls="rss-action-panel"
|
||
aria-expanded="false"
|
||
data-ga-category="save_share"
|
||
data-ga-action="alert"
|
||
data-ga-label="cancel">
|
||
Cancel
|
||
</button>
|
||
</div>
|
||
|
||
<div class="action-panel-control-wrap rss-link-copy-wrap">
|
||
<label for="rss-link" class="usa-sr-only">RSS Link</label>
|
||
<input placeholder="Your RSS Feed Link" type="text" name="rss-link" id="rss-link" class="rss-link" title="RSS Link">
|
||
<button
|
||
type="button"
|
||
disabled
|
||
class="rss-link-copy-button disabled"
|
||
data-ga-category="save_share"
|
||
data-ga-action="rss"
|
||
data-ga-label="copy">
|
||
Copy
|
||
</button>
|
||
</div>
|
||
</form>
|
||
</div>
|
||
</div>
|
||
|
||
</div>
|
||
</div>
|
||
|
||
<div class="article-page" id="article-page" data-article-pmid="32118314">
|
||
<aside class="page-sidebar">
|
||
<div class="inner-wrap">
|
||
|
||
<div class="full-text-links">
|
||
<div class="full-view">
|
||
<h3 class="title">
|
||
Full text links
|
||
</h3>
|
||
<div class="full-text-links-list">
|
||
<a class="link-item
|
||
|
||
dialog-focus"
|
||
href="https://doi.org/10.15252/embj.2019103358"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=False&PrId=3094&itool=Abstract-def&log$=linkouticon&uid=32118314&db=pubmed&nlmid=8208664"
|
||
title="See full text options at Nature Publishing Group"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="Nature Publishing Group"
|
||
data-ga-label="32118314"
|
||
><img src="https://cdn.ncbi.nlm.nih.gov/corehtml/query/egifs/https:--www.embopress.org-pb-assets-embo-site-images-pubmed-embojnl_free.gif" alt="Nature Publishing Group full text link"><span class="text">
|
||
|
||
Nature Publishing Group
|
||
|
||
</span></a><a class="link-item
|
||
pmc
|
||
"
|
||
href="https://pmc.ncbi.nlm.nih.gov/articles/pmid/32118314/"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=True&PrId=3494&itool=Abstract-def&log$=linkouticon&uid=32118314&db=pubmed&nlmid=8208664"
|
||
title="Free full text at PubMed Central"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="PMC"
|
||
data-ga-label="32118314"
|
||
><span class="text">
|
||
|
||
Free PMC article
|
||
|
||
</span></a>
|
||
</div>
|
||
|
||
</div>
|
||
|
||
<div class="short-view">
|
||
<a href="#" class="full-text-links-button full-text-links-dialog-trigger">
|
||
Full text links
|
||
</a>
|
||
</div>
|
||
</div>
|
||
|
||
|
||
|
||
|
||
<div class="actions-buttons sidebar"><h3 class="title">Actions</h3><div class="inner-wrap"><button class="citation-button citation-dialog-trigger"
|
||
aria-label="Open dialog with citation text in different styles"
|
||
data-ga-category="save_share"
|
||
data-ga-action="cite"
|
||
data-ga-label="open"
|
||
data-all-citations-url="/32118314/citations/"
|
||
data-citation-style="nlm"
|
||
data-pubmed-format-link="/32118314/export/"><span class="button-label">Cite</span></button><link type="text/css" href="ncbi-overlay-block/src/overlay-block.css"><div class="collections-button-container" data-article-id="32118314" data-article-db="pubmed"><button class="collections-button collections-dialog-trigger"
|
||
aria-label="Save article in MyNCBI collections."
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="collections_button"
|
||
data-collections-open-dialog-enabled="false"
|
||
data-collections-open-dialog-url="https://account.ncbi.nlm.nih.gov/?back_url=https%3A%2F%2Fpubmed.ncbi.nlm.nih.gov%2F32118314%2F%23open-collections-dialog"
|
||
data-in-collections="false"><span class="button-label">Collections</span></button><div class="overlay" role="dialog"><div id="collections-action-dialog"
|
||
class="dialog collections-dialog"
|
||
aria-hidden="true"><div class="title">Add to Collections</div><div class="collections-action-panel action-panel"><form id="collections-action-dialog-form"
|
||
class="collections-action-panel-form action-panel-content action-form action-panel-smaller-selectors"
|
||
data-existing-collections-url="/list-existing-collections/"
|
||
data-add-to-existing-collection-url="/add-to-existing-collection/"
|
||
data-create-and-add-to-new-collection-url="/create-and-add-to-new-collection/"
|
||
data-myncbi-max-collection-name-length="100"
|
||
data-collections-root-url="https://www.ncbi.nlm.nih.gov/myncbi/collections/"><input type="hidden" name="csrfmiddlewaretoken" value="v7NGtwR1NZZjwjtOOqZuXCfnti8PtghvMUxL6mknnAMNqKzErJCwrKL11mQ1mRPP"><div class="choice-group" role="radiogroup"><ul class="radio-group-items"><li><input type="radio"
|
||
id="collections-action-dialog-new"
|
||
class="collections-new"
|
||
name="collections"
|
||
value="new"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="collections_radio_new"><label for="collections-action-dialog-new">Create a new collection</label></li><li><input type="radio"
|
||
id="collections-action-dialog-existing"
|
||
class="collections-existing"
|
||
name="collections"
|
||
value="existing"
|
||
checked="true"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="collections_radio_existing"><label for="collections-action-dialog-existing">Add to an existing collection</label></li></ul></div><div class="controls-wrapper"><div class="action-panel-control-wrap new-collections-controls"><label for="collections-action-dialog-add-to-new" class="action-panel-label required-field-asterisk">
|
||
Name your collection:
|
||
</label><input
|
||
type="text"
|
||
name="add-to-new-collection"
|
||
id="collections-action-dialog-add-to-new"
|
||
class="collections-action-add-to-new"
|
||
pattern="[^"&=<>\/]*" title="The following characters are not allowed in the Name field: "&=<>/"
|
||
maxlength="100"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="create_collection"
|
||
data-ga-label="non_favorties_collection"><div class="collections-new-name-too-long usa-input-error-message selection-validation-message">
|
||
Name must be less than 100 characters
|
||
</div></div><div class="action-panel-control-wrap existing-collections-controls"><label for="collections-action-dialog-add-to-existing" class="action-panel-label">
|
||
Choose a collection:
|
||
</label><select id="collections-action-dialog-add-to-existing"
|
||
class="action-panel-selector collections-action-add-to-existing"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="select_collection"
|
||
data-ga-label="($('.collections-action-add-to-existing').val() === 'Favorites') ? 'Favorites' : 'non_favorites_collection'"></select><div class="collections-retry-load-on-error usa-input-error-message selection-validation-message">
|
||
Unable to load your collection due to an error<br><a href="#">Please try again</a></div></div></div><div class="action-panel-actions"><button class="action-panel-submit"
|
||
type="submit"
|
||
data-loading-label="Adding..."
|
||
data-pinger-ignore
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="add">
|
||
Add
|
||
</button><button class="action-panel-cancel"
|
||
aria-label="Close 'Add to Collections' panel"
|
||
ref="linksrc=close_collections_panel"
|
||
aria-controls="collections-action-panel"
|
||
aria-expanded="false"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="cancel">
|
||
Cancel
|
||
</button></div></form></div></div></div></div><button class="more-actions-button more-actions-dialog-trigger"
|
||
title="Open dialog with more actions to take"
|
||
ref="linksrc=more_actions_btn"></button><div class="display-options" data-format-key="format"
|
||
data-default-format-value="abstract"
|
||
data-current-format-value="abstract" role="region"><button
|
||
class="trigger usa-button"
|
||
title="Change format"
|
||
data-ga-category="display_options"
|
||
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Uncoupling endosomal CLC chloride/proton exchange causes severe neurodegeneration
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Uncoupling endosomal CLC chloride/proton exchange causes severe neurodegeneration
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<p>
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CLC chloride/proton exchangers may support acidification of endolysosomes and raise their luminal Cl<sup>-</sup> concentration. Disruption of endosomal ClC-3 causes severe neurodegeneration. To assess the importance of ClC-3 Cl<sup>-</sup> /H<sup>+</sup> exchange, we now generate Clcn3<sup>unc/unc</sup> mice in which ClC-3 is converted into a Cl<sup>-</sup> channel. Unlike Clcn3<sup>-/-</sup> mice, Clcn3<sup>unc/unc</sup> mice appear normal owing to compensation by ClC-4 with which ClC-3 forms heteromers. ClC-4 protein levels are strongly reduced in Clcn3<sup>-/-</sup> , but not in Clcn3<sup>unc/unc</sup> mice because ClC-3<sup>unc</sup> binds and stabilizes ClC-4 like wild-type ClC-3. Although mice lacking ClC-4 appear healthy, its absence in Clcn3<sup>unc/unc</sup> /Clcn4<sup>-/-</sup> mice entails even stronger neurodegeneration than observed in Clcn3<sup>-/-</sup> mice. A fraction of ClC-3 is found on synaptic vesicles, but miniature postsynaptic currents and synaptic vesicle acidification are not affected in Clcn3<sup>unc/unc</sup> or Clcn3<sup>-/-</sup> mice before neurodegeneration sets in. Both, Cl<sup>-</sup> /H<sup>+</sup> -exchange activity and the stabilizing effect on ClC-4, are central to the biological function of ClC-3.
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Keywords:
|
||
</strong>
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VGLUT1; anion transport; anion-proton exchanger; intracellular trafficking; retina.
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</p>
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© 2020 The Authors. Published under the terms of the CC BY NC ND 4.0 license.
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<h2 class="title">
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Conflict of interest statement
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</h2>
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<div class="statement">
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<p xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:p1="http://pubmed.gov/pub-one">The authors declare that they have no conflict of interest.</p>
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Figures
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<p> Figure EV1. Currents of partially plasma membrane… </p>
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<p> Figure EV1. Currents of partially plasma membrane directed “ <styled-content style="fixed-case"> WT </styled-content> ” ClC‐3 and its E224A… </p>
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Figure EV1. Currents of partially plasma membrane directed “<styled-content style="fixed-case">WT</styled-content>” ClC‐3 and its E224A mutant
|
||
</strong>
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||
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<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"><li><p>When transfected into HeLa cells, wild‐type ClC‐3 (green) localized to enlarged Lamp‐1‐positive (red) late endosomes/lysosomes, GFP‐ClC‐3<sup>4xLA</sup> (green) co‐localizes with Lamp‐1 (red) in normal sized vesicular structures, but is also partially redirected to the plasma membrane. DNA stained with DAPI [scale bar at bottom: 20 μm (for all panels); scale bar in inset: 5 μm].</p></li><li><p>Current–voltage relationships of HeLa cells, either non‐transfected controls or transiently transfected with GFP‐ClC‐3<sup>4xLA</sup> (“WT”) and GFP‐ClC‐3<sup>4xLA</sup> E224A (“E224A”). Cells were examined 48–72 h post‐transfection by whole‐cell patch‐clamp using 1‐s voltage pulses and 20‐mV increments from −80 to +140 mV. n.t., not transfected. Mean values ± SEM “WT”, <i>n</i> = 8; “E224A”, <i>n</i> = 4; n.t., <i>n</i> = 4, *<i>P</i> < 0.05, MW test. Currents of surface‐directed GFP‐ClC‐3<sup>4xLA</sup> were strongly outwardly rectifying and similar to ClC‐3 currents reported by others (Li <i>et al</i>, 2002; Picollo & Pusch, 2005; Matsuda <i>et al</i>, 2008; Guzman <i>et al</i>, 2013) and as described for a ClC‐5/ClC‐3 chimera (Rohrbough <i>et al</i>, 2018). They resembled currents of ClC‐4 and ClC‐5 (Steinmeyer <i>et al</i>, 1995; Friedrich <i>et al</i>, 1999) but were only barely above background. Mutating the “gating glutamate” E224 to alanine abolished rectification, as reported for ClC‐3 (Li <i>et al</i>, 2002; Matsuda <i>et al</i>, 2008; Rohrbough <i>et al</i>, 2018), ClC‐4, and ClC‐5 (Friedrich <i>et al</i>, 1999) and ClC‐7 (Leisle <i>et al</i>, 2011). These low expression levels precluded measurements of H<sup>+</sup>‐transport, but recent studies using ClC‐5/3 chimeras convincingly demonstrate that ClC‐3 is a Cl<sup>−</sup>/H<sup>+</sup>‐antiporter which can be uncoupled by the E224A (“unc”) mutation (Rohrbough <i>et al</i>, 2018).</p></li><li><p>Example traces of GFP‐ClC‐3<sup>4xLA</sup> (“WT”) and GFP‐ClC‐3<sup>4xLA</sup> E224A (“E224A”).</p></li></ol></div>
|
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<p> Figure 1. Hippocampal morphology and expression of… </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
</div>
|
||
|
||
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 1. Hippocampal morphology and expression of intracellular <styled-content style="fixed-case"> CLC </styled-content> proteins of <i> Clcn3 </i> mouse models </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-1" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure 1. Hippocampal morphology and expression of intracellular <styled-content style="fixed-case">CLC</styled-content> proteins of <i>Clcn3</i> mouse models
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"><li><p>Nissl‐stained sagittal brain sections reveal no change in hippocampal morphology between <i>Clcn3</i>
|
||
<sup>unc/unc</sup> and <i>Clcn3</i>
|
||
<sup>+/+</sup> mice at P45 or after 20 months. In contrast, the hippocampus was absent (indicated by asterisk) in 3‐month‐old <i>Clcn3</i>
|
||
<sup>−/−</sup> mice (scale bar: 200 μm).</p></li><li><p>Nissl‐stained paraffin sections show intact retinal layers in 20‐month‐old <i>Clcn3</i>
|
||
<sup>unc/unc</sup> mice. Neurodegeneration in <i>Clcn3</i>
|
||
<sup>−/−</sup> mice, however, results in a loss of retinal structure already at 11 weeks of age (scale bar: 100 μm). GCL, ganglion cell layer; INL, inner nuclear layer; IPL, inner plexiform layer; IS, photoreceptor inner segments; ONL, outer nuclear layer; OPL, outer plexiform layer; OS, photoreceptor outer segments; RPE, retinal pigment epithelium.</p></li><li><p>Immunoblots for ClC‐3, ClC‐4, and CIC‐5 of membrane fractions of WT (+/+), <i>Clcn3</i>
|
||
<sup>unc/unc</sup> (unc/unc)<i>, Clcn3</i>
|
||
<sup>unc/+</sup> (unc/+), and <i>Clcn3</i>
|
||
<sup>−/−</sup> (−/−) mice. β‐Actin, loading control.</p></li><li><p>Representative Western blot for ClC‐4 of membrane fractions from brain and kidney of WT (+/+), <i>Clcn3</i>
|
||
<sup>+/−</sup> (+/−), and <i>Clcn3</i>
|
||
<sup>−/−</sup> (−/−) mice. β‐Actin, loading control.</p></li><li><p>Quantification of ClC‐4 immunoblots including those shown in (C, D) (normalized to actin). Mean values ± SEM. Average from ≥ 5 animals per genotype and at ≥ 2 immunoblots per animal. ***<i>P</i> < 0.0005, **<i>P</i> < 0.005, *<i>P</i> < 0.05 (two‐tailed unpaired <i>t</i>‐test).</p></li></ol> Source data are available online for this figure.</div>
|
||
|
||
|
||
|
||
|
||
</figcaption>
|
||
|
||
|
||
</figure>
|
||
|
||
<figure class="figure-item "
|
||
itemscope itemtype="http://schema.org/ImageObject"
|
||
itemprop="associatedMedia"
|
||
data-slide-index="2"
|
||
data-label-slug="figure-ev2">
|
||
<a class="figure-link"
|
||
href="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3340/7196918/a2e969e6ac91/EMBJ-39-e103358-g005.jpg"
|
||
itemprop="contentUrl"
|
||
aria-describedby="figure-caption-2"
|
||
role="button"
|
||
data-image-width="709"
|
||
data-image-height="571"
|
||
data-image-alt="Figure EV2"
|
||
data-pmc-id="PMC7196918"
|
||
data-figure-id="embj2019103358-fig-0002ev">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
||
id="article-image-2"
|
||
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3340/7196918/02ed9755991a/EMBJ-39-e103358-g005.gif"
|
||
alt="Figure EV2" />
|
||
</a>
|
||
|
||
<meta itemprop="width" itemtype="http://schema.org/ImageObject" content="709">
|
||
<meta itemprop="height" itemtype="http://schema.org/ImageObject" content="571">
|
||
|
||
|
||
<div class="figure-caption figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="caption" aria-hidden="true">
|
||
|
||
<div class="caption-wrap">
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure EV2. Effect of ClC‐3 on ClC‐4… </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
</div>
|
||
|
||
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure EV2. Effect of ClC‐3 on ClC‐4 levels and glycosylation in various tissues </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"> <li> <p> Western blots… </p> </li> </ol></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-2" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure EV2. Effect of ClC‐3 on ClC‐4 levels and glycosylation in various tissues
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"><li><p>Western blots for ClC‐3, ClC‐4, and ClC‐5 of membrane fractions isolated from brain and kidney from mice of the indicated genotypes. Whereas ClC‐4 protein levels depend on ClC‐3, ClC‐3 levels do not depend on ClC‐4. β‐Actin served as a loading control.</p></li><li><p>Immunoblots for ClC‐3 and ClC‐4 of membrane fractions isolated from indicated organs of WT and <i>Clcn3</i>
|
||
<sup>−/−</sup> mice (indicated by +/+ and −/−). β‐Actin, loading control. The different sizes of ClC‐4‐positive bands most likely result from differences in glycosylation between tissues. Disruption of ClC‐3 leads to the appearance, or increase in intensity, of the lowest band that represents the immature protein. The ratio between ClC‐3 and ClC‐4 proteins apparently differs between tissues.</p></li><li><p>Effect of PNGase F on ClC‐4 in brain and liver membrane fractions of WT (+/+) and <i>Clcn3</i>
|
||
<sup>−/−</sup> (−/−) mice. Removal of N‐linked glycans by PNGase F reveals that apparent size differences of ClC‐4 between WT and <i>Clcn3</i>
|
||
<sup>−/−</sup> tissues are owed to less glycosylation of ClC‐4 in the absence of ClC‐3.</p></li><li><p>Treatment of brain and liver membranes with EndoH reveals that a large portion of ClC‐4 in <i>Clcn3</i>
|
||
<sup>−/−</sup> tissue has not left the ER. The arrows are pointing to the fractions of ClC‐4 protein that are sensitive to endoglycosidase H treatment, i.e., has not been modified in the Golgi.</p></li></ol></div>
|
||
|
||
|
||
|
||
|
||
</figcaption>
|
||
|
||
|
||
</figure>
|
||
|
||
<figure class="figure-item "
|
||
itemscope itemtype="http://schema.org/ImageObject"
|
||
itemprop="associatedMedia"
|
||
data-slide-index="3"
|
||
data-label-slug="figure-2">
|
||
<a class="figure-link"
|
||
href="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3340/7196918/b76b7498cf78/EMBJ-39-e103358-g004.jpg"
|
||
itemprop="contentUrl"
|
||
aria-describedby="figure-caption-3"
|
||
role="button"
|
||
data-image-width="709"
|
||
data-image-height="2072"
|
||
data-image-alt="Figure 2"
|
||
data-pmc-id="PMC7196918"
|
||
data-figure-id="embj2019103358-fig-0002">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
||
id="article-image-3"
|
||
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3340/7196918/ba5b2d4b8c90/EMBJ-39-e103358-g004.gif"
|
||
alt="Figure 2" />
|
||
</a>
|
||
|
||
<meta itemprop="width" itemtype="http://schema.org/ImageObject" content="709">
|
||
<meta itemprop="height" itemtype="http://schema.org/ImageObject" content="2072">
|
||
|
||
|
||
<div class="figure-caption figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="caption" aria-hidden="true">
|
||
|
||
<div class="caption-wrap">
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 2. Formation of ClC‐3/ClC‐4 heteromers </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"> <li> <p> Co‐immunoprecipitation… </p> </li> </ol></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
</div>
|
||
|
||
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 2. Formation of ClC‐3/ClC‐4 heteromers </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"> <li> <p> Co‐immunoprecipitation reveals a ClC‐3–ClC‐4 complex. Ten percent of solubilized… </p> </li> </ol></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-3" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure 2. Formation of ClC‐3/ClC‐4 heteromers
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"><li><p>Co‐immunoprecipitation reveals a ClC‐3–ClC‐4 complex. Ten percent of solubilized brain membranes of WT and <i>Clcn3</i>
|
||
<sup>unc/unc</sup> mice were directly loaded on the gel (input, or first immunoprecipitated (IP) with antibodies against ClC‐3 or ClC‐4). Western blots were probed for ClC‐3 and ClC‐4. Equivalent amounts of lysates and precipitates were loaded. * unspecific band/contamination.</p></li><li><p>FRET experiments show homo‐ and heteromerization of ClC‐3 and ClC‐4 constructs [fused to yellow fluorescent protein (YFP) and cyan fluorescent protein (CFP)] overexpressed in COS‐7 cells. Co‐expressed constructs are indicated. Graph represents energy transfer efficiencies from acceptor photobleaching, depicted as bleach corrected values (subtraction of ClC‐4CFP alone). Mean values ± SEM. <i>N</i> = 20 (ClC‐3YFP/ClC‐4CFP); 33 (ClC‐3YFP/ClC‐3CFP); 26 (ClC‐4YFP/ClC‐4CFP); 42 (ClC‐3YFP/Lamp‐1CFP) cells. ***<i>P</i> < 0.0005 (two‐tailed unpaired <i>t</i>‐test).</p></li><li><p>Immunolabeling shows subcellular localization of hClC‐4 (top, green in merge), hClC‐3 (middle, green in merge), and hClC‐3<sup>unc</sup> (bottom, green in merge) of transiently transfected COS‐7 cells, in comparison with either PDI or Lamp‐1 (both red) as marker for the ER and late endosomes/lysosomes, respectively.</p></li><li><p>Co‐localization of hClC‐3 and hClC‐4 in cytoplasmic vesicles of COS‐7 cells transfected with hClC‐4 cDNA [hemagglutinin (HA) tagged] together with either hClC‐3 or hClC‐3<sup>unc</sup>. Immunostaining used antibodies against ClC‐3 and HA tag (green and red in merge, respectively).</p></li></ol>Data information: DNA stained with DAPI in (C) and (D), [scale bar in (C) and (D): 20 μm].Source data are available online for this figure.</div>
|
||
|
||
|
||
|
||
|
||
</figcaption>
|
||
|
||
|
||
</figure>
|
||
|
||
<figure class="figure-item "
|
||
itemscope itemtype="http://schema.org/ImageObject"
|
||
itemprop="associatedMedia"
|
||
data-slide-index="4"
|
||
data-label-slug="figure-3">
|
||
<a class="figure-link"
|
||
href="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3340/7196918/481d84888299/EMBJ-39-e103358-g006.jpg"
|
||
itemprop="contentUrl"
|
||
aria-describedby="figure-caption-4"
|
||
role="button"
|
||
data-image-width="709"
|
||
data-image-height="2721"
|
||
data-image-alt="Figure 3"
|
||
data-pmc-id="PMC7196918"
|
||
data-figure-id="embj2019103358-fig-0003">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
||
id="article-image-4"
|
||
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3340/7196918/632320ae3dcf/EMBJ-39-e103358-g006.gif"
|
||
alt="Figure 3" />
|
||
</a>
|
||
|
||
<meta itemprop="width" itemtype="http://schema.org/ImageObject" content="709">
|
||
<meta itemprop="height" itemtype="http://schema.org/ImageObject" content="2721">
|
||
|
||
|
||
<div class="figure-caption figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="caption" aria-hidden="true">
|
||
|
||
<div class="caption-wrap">
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 3. Life span and neurodegeneration of… </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
</div>
|
||
|
||
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 3. Life span and neurodegeneration of <i> Clcn3 </i> / <i> Clcn4 </i> mouse models </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"> <li> <p> <i> Clcn3 </i> <sup> unc/ <i> unc </i> </sup> / <i> Clcn4… </i> </p> </li> </ol></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-4" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure 3. Life span and neurodegeneration of <i>Clcn3</i>/<i>Clcn4</i> mouse models
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"><li><p>
|
||
<i>Clcn3</i>
|
||
<sup>unc/<i>unc</i></sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup> and <i>Clcn3</i>
|
||
<sup>−/−</sup> mice died within 3–4 weeks after birth. Approximately 20% of the animals survived in either line (<i>Clcn3</i>
|
||
<sup>unc/<i>unc</i></sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup>, <i>n</i> = 136, and <i>Clcn3</i>
|
||
<sup>−/−</sup>, <i>n</i> = 187). All <i>Clcn3</i>
|
||
<sup>−/−</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup> mice (<i>n</i> = 4) died within 1–2 weeks after birth.</p></li><li><p>Nissl‐stained paraffin sections show progressive neuronal cell loss (arrows) that begins in hippocampal CA1 region of P14 <i>Clcn3</i>
|
||
<sup>unc/unc</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup> mice and results in a complete loss of the hippocampus at P28. Neurodegeneration progresses slower in <i>Clcn3</i>
|
||
<sup>−/−</sup> mice (Stobrawa <i>et al</i>, 2001) (scale bar: 200 μm).</p></li><li><p>Semi‐thin sections of P28 retinae revealed degeneration of photoreceptor cells in the outer nuclear layer and outer and inner segment of <i>Clcn3</i>
|
||
<sup>unc/unc</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup>, but not of <i>Clcn3</i>
|
||
<sup>unc/unc</sup> or <i>Clcn4</i>
|
||
<sup>−/−</sup> mice (scale bar: 50 μm). GCL, ganglion cell layer; INL, inner nuclear layer; IPL, inner plexiform layer; IS, photoreceptor inner segments; ONL, outer nuclear layer; OPL, outer plexiform layer; OS, photoreceptor outer segments; RPE, retinal pigment epithelium.</p></li></ol> Source data are available online for this figure.</div>
|
||
|
||
|
||
|
||
|
||
</figcaption>
|
||
|
||
|
||
</figure>
|
||
|
||
<figure class="figure-item "
|
||
itemscope itemtype="http://schema.org/ImageObject"
|
||
itemprop="associatedMedia"
|
||
data-slide-index="5"
|
||
data-label-slug="figure-4">
|
||
<a class="figure-link"
|
||
href="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3340/7196918/b534750654c5/EMBJ-39-e103358-g008.jpg"
|
||
itemprop="contentUrl"
|
||
aria-describedby="figure-caption-5"
|
||
role="button"
|
||
data-image-width="709"
|
||
data-image-height="782"
|
||
data-image-alt="Figure 4"
|
||
data-pmc-id="PMC7196918"
|
||
data-figure-id="embj2019103358-fig-0004">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
||
id="article-image-5"
|
||
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3340/7196918/b96f9c8e3733/EMBJ-39-e103358-g008.gif"
|
||
alt="Figure 4" />
|
||
</a>
|
||
|
||
<meta itemprop="width" itemtype="http://schema.org/ImageObject" content="709">
|
||
<meta itemprop="height" itemtype="http://schema.org/ImageObject" content="782">
|
||
|
||
|
||
<div class="figure-caption figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="caption" aria-hidden="true">
|
||
|
||
<div class="caption-wrap">
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 4. Subcellular localization of <sup> Venus </sup> ClC‐3… </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
</div>
|
||
|
||
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 4. Subcellular localization of <sup> Venus </sup> ClC‐3 and ClC‐4 in neurons </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:none"> <li> <span class="label"> A </span> <p> GFP antibodies immunolabel <sup> Venus… </sup> </p> </li> </ol></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-5" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure 4. Subcellular localization of <sup>Venus</sup>ClC‐3 and ClC‐4 in neurons
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:none"><li><span class="label">A</span><p>GFP antibodies immunolabel <sup>Venus</sup>ClC‐3 (green) in the somata of CA1 pyramidal neurons of <i>Clcn3</i>
|
||
<sup>ven/ven</sup>, but not <i>Clcn3</i>
|
||
<sup>+/+</sup> brain sections. sp, stratum pyramidale (scale bar: 20 μm).</p></li><li><span class="label">B</span><p>Co‐immunolabeling of <sup>Venus</sup>ClC‐3 (green) with ClC‐4 (red) in the CA3 region of <i>Clcn3</i>
|
||
<sup>ven/ven</sup> mice (scale bar: 20 μm). sl, stratum lucidum; sp, stratum pyramidale.</p></li><li><span class="label">C</span><p>Co‐immunostaining of <sup>Venus</sup>ClC‐3 (green) with EEA1 (red, left panel), Lamp‐1 (red, middle panel), or synaptophysin (red, right panel) in either CA1 or CA3 region of <i>Clcn3</i>
|
||
<sup>ven/ven</sup> mice. Arrows indicate structures of overlap (scale bar: 5 μm).</p></li><li><span class="label">D</span><p>GFP antibody immunolabels <sup>Venus</sup>ClC‐3 (green) in neurites of cultured neurons. EEA1 and VGLUT1 are co‐stained (both in red; left and right panel, respectively). The dendritic marker MAP2 is stained in blue (right panel; scale bars: 10 μm). DNA stained with DAPI.</p></li><li><span class="label">E</span><p>Immunoblot analysis of fractions collected during preparation of SVs from brain of <i>Clcn3</i>
|
||
<sup>ven/ven</sup> mice. <sup>Venus</sup>ClC‐3 (detected with GFP antibody) co‐purified with SV marker protein synaptophysin.</p></li><li><span class="label">F</span><p>Fluorescence of immobilized Venus‐tagged SVs imaged with TIRF microscopy. Scale bar, 2 μm.</p></li><li><span class="label">G, H</span><p>Co‐localization between the Venus‐tagged vesicles with antibodies against VGLUT1 and synaptophysin was analyzed. (G) 11.4 ± 0.6 (SD) of VGLUT1‐labeled SVs and 8.2 ± 2 (SD) of synaptophysin‐labeled SVs showed Venus fluorescence (<i>n</i> = 6). (H) 65 ± 5.4 (SD) and 79.4 ± 3.8 (SD) of Venus‐tagged SVs showed co‐localization with VGLUT1 and synaptophysin, respectively (<i>n</i> = 6).</p></li><li><span class="label">I</span><p>Co‐immunolabeling of <sup>Venus</sup>ClC‐3 (green) with synaptophysin (red) of immobilized SVs imaged with TIRF microscopy. Vesicle in quadrant delimited by dashed line is shown in higher magnification in merge. Scale bar, 2 μm.</p></li></ol> Source data are available online for this figure.</div>
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<p> Figure EV3. Expression and subcellular localization of… </p>
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<p> Figure EV3. Expression and subcellular localization of <sup> Venus </sup> ClC‐3 in cultured glial cells </p>
|
||
</strong>
|
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|
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|
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<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"> <li> <p> Primary cultured glial… </p> </li> </ol></div>
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<strong class="figure-label">
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Figure EV3. Expression and subcellular localization of <sup>Venus</sup>ClC‐3 in cultured glial cells
|
||
</strong>
|
||
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|
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<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"><li><p>Primary cultured glial cells were labeled for <sup>Venus</sup>ClC‐3 (green) and GFAP or APC (red, left and right panel, respectively), markers for astrocytes and oligodendrocytes, respectively (scale bar: 10 μm for main panels; scale bar in insets: 5 μm).</p></li><li><p>Primary cultured astrocytes were labeled for <sup>Venus</sup>ClC‐3 (green) and rab4 (i, red), EEA1 (ii, red), TfR (iii, red), and Lamp‐1 (iv, red) (scale bars: 20 μm in i, iii, and iv; 10 μm in ii). The inlays depict magnified views of boxed sections. DNA stained with DAPI.</p></li></ol></div>
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alt="Figure EV4" />
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<strong class="figure-label">
|
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<p> Figure EV4. Characterization and quantification of ClC‐3… </p>
|
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<strong class="figure-label">
|
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<p> Figure EV4. Characterization and quantification of ClC‐3 in <styled-content style="fixed-case"> LP </styled-content> 2 fraction </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:none"> <li> <span class="label"> A, B </span> <p> Characterization of… </p> </li> </ol></div>
|
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<strong class="figure-label">
|
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Figure EV4. Characterization and quantification of ClC‐3 in <styled-content style="fixed-case">LP</styled-content>2 fraction
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:none"><li><span class="label">A, B</span><p>Characterization of SV‐enriched LP2 fraction. (A) Western blots for ClC‐3, ClC‐4, synaptophysin, and PSD95 (postsynaptic marker) of fractions obtained during synaptic vesicle‐enriched fraction (LP2) preparation using differential centrifugation as described (Huttner <i>et al</i>, 1983; Takamori <i>et al</i>, 2000). (B) Immunoblots for different cellular markers comparing whole lysate (H) and synaptic vesicle‐enriched fraction (LP2) (GM130, Golgi marker; PDI, ER marker; rab4, early endosomes and SV; cathepsin D, lysosomal marker; synaptophysin, SV marker).</p></li><li><span class="label">C–E</span><p>Quantification of ClC‐3 in LP2 fractions (C) Western blot of lysates from HEK cells transiently overexpressing either mVGLUT1 or hClC‐3, which were both fused at their N terminus to GFP. Probing for the GFP tag allows to directly compare the relative amount of ClC‐3 and VGLUT1 in the lysate for its use as calibration standards for anti‐ClC‐3 and anti‐VGLUT1 antibodies in Western blots of tissue standards [as in (D) and (E)]. (<i>n</i> = 3 independent transfections, horizontal lines and error bars represent mean values SEM). The standard contains about 4.33 × more ClC‐3 molecules than the standard for VGLUT1. (D) Example immunoblot for VGLUT1 in which the GFP‐VGLUT1 standard [same lysate as in (A)] is compared to different amounts of LP2 fraction. Below, example plot in which WB signals are plotted against rising amounts of the LP2 fraction, quantified by protein contents. The standard for VGLUT1 roughly corresponds to 2.5 μg of LP2 fraction (averaged from <i>n</i> = 6 Western blots). (E) Same as shown in (D) but for ClC‐3. The standard for ClC‐3 roughly corresponds to 140 μg of the LP2 fraction (<i>n</i> = 7). From (A) and (B), we calculated a molecular ratio for ClC‐3/VGLUT1 ≈ 2.5/(140*4.33) = 4.12 × 10<sup>−3</sup> = 1/243 in our LP2 fraction. Considering that ClC‐3 may form not only hetero‐ but also homodimers and that SVs are ˜ 2‐fold enriched in the SV compared to the LP2 fraction (Huttner <i>et al</i>, 1983) and that there are ˜ 10 copies of VGLUT1 per vesicle (Takamori <i>et al</i>, 2006), our data yield an upper limit of one ClC‐3‐containing transporter on roughly every 25<sup>th</sup> SV. This upper limit assumes that in LP2 fractions ClC‐3 is only present on SVs. Any contamination with other ClC‐3‐containing compartments like endosomes, as found in this work, will lower this estimate. The ˜ 20‐fold lower value for the ClC‐3/VGLUT1 ratio given by (Schenck <i>et al</i>, 2009) may have been caused by their calibration of the VGLUT1 antibody (Synaptic Systems) that recognizes an epitope at the C terminus of VGLUT1. It might have been shielded by the GFP, which these authors fused directly to the carboxy terminus of VGLUT1, thereby overestimating the number of VGLUT1 molecules in their preparation (S. Takamori, <i>personal communication</i>).</p></li></ol></div>
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|
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|
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|
||
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|
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<strong class="figure-label">
|
||
<p> Figure 5. <styled-content style="fixed-case"> ATP </styled-content> ‐induced acidification of synaptic… </p>
|
||
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|
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|
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|
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<p> Figure 5. <styled-content style="fixed-case"> ATP </styled-content> ‐induced acidification of synaptic vesicle‐enriched <styled-content style="fixed-case"> LP </styled-content> 2 fraction derived from different <i> Clcn3… </i> </p>
|
||
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|
||
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||
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||
|
||
|
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||
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<strong class="figure-label">
|
||
Figure 5. <styled-content style="fixed-case">ATP</styled-content>‐induced acidification of synaptic vesicle‐enriched <styled-content style="fixed-case">LP</styled-content>2 fraction derived from different <i>Clcn3</i> and <i>Clcn4</i> mouse models
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"><li><p>Immunoblots for ClC‐3, ClC‐4, VGLUT1, VGLUT2, VGAT, GluR4, and GABA<sub>A‐</sub>R‐α1 of whole lysates from brain of <i>Clcn3</i>
|
||
<sup>+/+</sup> and <i>Clcn3</i>
|
||
<sup>−/−</sup> mice at 2, 6, and 12 weeks of age.</p></li><li><p>Acidification of synaptic vesicle LP2 fractions from <i>Clcn3</i>
|
||
<sup>unc/unc</sup> and <i>Clcn3</i>
|
||
<sup>+/+</sup> mice at 1 year of age (upper panel, <i>n</i> = 2 animals each and ≥ 3 measurements per animal), 10‐week‐old <i>Clcn4</i>
|
||
<sup>−/−</sup> and WT mice (middle panel, <i>n</i> = 3 animals each and ≥ 3 measurements per animal), and 4‐ to 6‐week‐old <i>Clcn3</i>
|
||
<sup>unc/unc</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup> and control mice (lower panel, six animals each with ≥ 2 measurements per animal). A decrease in fluorescence reflects acidification. The protonophore FCCP dissipated the pH gradient. Mean values ± SEM.</p></li><li><p>Quantification of ATP‐induced acidification of LP2 fractions derived from 2, 6, and 10‐ to 12‐week<i>‐</i>old <i>Clcn3</i>
|
||
<sup>−/−</sup> compared to wild‐type mice. Acidification measured by acridine orange fluorescence in the presence of 60 mM KCl. At least two animals in at least two independent experiments were pooled. Each measurement was performed at least three times. Mean ± SEM is shown.*<i>P</i> < 0.05, ***<i>P</i> < 0.0005 (two‐tailed unpaired <i>t</i>‐test).</p></li><li><p>Immunoblot revealed strong reduction of VGLUT1 levels in the homogenate (H) and LP2 fraction of <i>Clcn3</i>
|
||
<sup>unc/unc</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup> mice.</p></li><li><p>Endosomal pH of <i>Clcn3</i>
|
||
<sup>+/+</sup> and <i>Clcn3</i>
|
||
<sup>−/−</sup> primary hippocampal neurons determined with a pH‐sensitive transferrin conjugate. <i>N</i> = 5 independent cell lines with at least two live cell dishes per cell line with about 10 images each and ≥ 10 Tfn‐positive compartments per image and genotype were analyzed. Mean ± SEM is shown.</p></li></ol> Source data are available online for this figure.</div>
|
||
|
||
|
||
|
||
|
||
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|
||
|
||
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||
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|
||
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|
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|
||
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|
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|
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|
||
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|
||
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|
||
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|
||
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|
||
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|
||
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|
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|
||
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|
||
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|
||
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|
||
<p> Figure 6. Impact of <i> Clcn3 </i> and <i> Clcn4… </i> </p>
|
||
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|
||
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|
||
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|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 6. Impact of <i> Clcn3 </i> and <i> Clcn4 </i> genotypes on synaptic vesicle exocytosis </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:none"> <li> <span class="label"> A–E </span> <p> Miniature inhibitory… </p> </li> </ol></div>
|
||
|
||
|
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|
||
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|
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|
||
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|
||
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||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure 6. Impact of <i>Clcn3</i> and <i>Clcn4</i> genotypes on synaptic vesicle exocytosis
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><ol style="list-style-type:none"><li><span class="label">A–E</span><p>Miniature inhibitory postsynaptic currents (mIPSCs) measured in CA1 pyramidal neurons in different mouse models at P14–P16. (A) Example mIPSCs of WT (left) and <i>Clcn3</i>
|
||
<sup>−/−</sup> neurons. (B–E) Mean values ± SEM and cumulative histogram of amplitude (top) and frequency/interevent–interval (bottom) of mIPSCs in different mouse models as indicated. Several cells of three mice of each genotype were analyzed. Compared genotypes were siblings. No difference in amplitude or frequency/interevent–interval distribution of mIPSCs was found in (B) <i>Clcn3</i>
|
||
<sup>−/−</sup> and <i>Clcn3</i>
|
||
<sup>+/+</sup> (<i>Clcn3</i>
|
||
<sup>+/+</sup>: 16 cells, <i>Clcn3</i>
|
||
<sup>−/−</sup>: 15 cells; mean amplitude: <i>P</i> > 0.8, <i>t</i>‐test; mean frequency: <i>P</i> > 0.4, MW test), in (C) <i>Clcn3</i>
|
||
<sup>unc/unc</sup> and <i>Clcn3</i>
|
||
<sup>+/+</sup> (<i>Clcn3</i>
|
||
<sup>+/+</sup>: 21 cells, <i>Clcn3</i>
|
||
<sup>unc/unc</sup>: 13 cells; mean amplitude: <i>P</i> > 0.7; mean frequency: <i>P</i> = 0.3, <i>t</i>‐test), and in (D) <i>Clcn4</i>
|
||
<sup>−/−</sup> and <i>Clcn3</i>
|
||
<sup>+/+</sup> (<i>Clcn3</i>
|
||
<sup>+/+</sup>: 18 cells, <i>Clcn4</i>
|
||
<sup>−/−</sup>: 18 cells; mean amplitude: <i>P</i> > 0.3, <i>t</i>‐test; mean frequency: <i>P</i> = 0.6, MW test). (E) No difference in mean amplitude (<i>P</i> > 0.5, <i>t</i>‐test), in cumulative amplitude and mean frequency of mIPSCs (<i>P</i> > 0.1, <i>t</i>‐test) was found in <i>Clcn3</i>
|
||
<sup>unc/unc</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup> and <i>Clcn3</i>
|
||
<sup>+/+</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup>. The interevent–interval distribution was shifted to the right, indicating a reduced frequency of mIPSCs in <i>Clcn3</i>
|
||
<sup>unc/unc</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup> (KS test, <i>P</i> < 0.05; <i>Clcn3</i>
|
||
<sup>+/+</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup>: 16 cells, <i>Clcn3</i>
|
||
<sup>unc/unc</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup>: 12 cells).</p></li><li><span class="label">F, G</span><p>Miniature excitatory postsynaptic currents (mEPSCs). (F) Example traces of mEPSCs in WT and <i>Clcn3</i>
|
||
<sup>−/−</sup> neurons. (G) No significant difference between <i>Clcn3</i>
|
||
<sup>unc/unc</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup> and <i>Clcn3</i>
|
||
<sup>+/+</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup> mEPSCs in mean amplitudes (<i>P</i> > 0.9, <i>t</i>‐test) or in the distribution of amplitudes (<i>Clcn4</i>
|
||
<sup>−/−</sup>: 12 cells, 2 mice; <i>Clcn3</i>
|
||
<sup>unc/unc</sup>/<i>Clcn4</i>
|
||
<sup>−/−</sup>: eight cells, two mice).</p></li><li><span class="label">H</span><p>Primary hippocampal neurons co‐transfected with ClC‐3 and synaptobrevin (syb2), both luminally tagged with pHluorin or the pH‐sensitive mOrange (Ramirez <i>et al</i>, 2012), respectively, were stimulated by 200 action potentials (APs) at 20 Hz (indicated by bar). Vesicle exocytosis was monitored by fluorescence increase upon exposure to extracellular neutral pH. Note that only Syb2 and not ClC‐3 shows signs of exocytosis. Traces were corrected for photobleaching. The initial decay of the pHluorin signal is probably due to the high light exposure, which forces the fluorophores into a transient dark state (Dean <i>et al</i>, 2011). Averaged fluorescence traces (<i>n</i> = 10), error bars, SEM.</p></li></ol> Source data are available online for this figure.</div>
|
||
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<p> Figure EV5. <i> Clcn3 </i> <sup> −/− </sup> mice display normal… </p>
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</strong>
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<strong class="figure-label">
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<p> Figure EV5. <i> Clcn3 </i> <sup> −/− </sup> mice display normal synaptic ultrastructure </p>
|
||
</strong>
|
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|
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|
||
|
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<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"> <li> <p> Quantification of SVs and endosome‐like vacuoles… </p> </li> </ol></div>
|
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</div>
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<strong class="figure-label">
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Figure EV5. <i>Clcn3</i> <sup>−/−</sup> mice display normal synaptic ultrastructure
|
||
</strong>
|
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|
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|
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|
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<div class="figure-caption-contents"><ol style="list-style-type:upper-alpha"><li><p>Quantification of SVs and endosome‐like vacuoles (ELVs) of glutamatergic spine synapses from layer 4–5 of secondary visual cortex of P14, P21, and P70 days‐old <i>Clcn3</i>
|
||
<sup>+/+</sup> and <i>Clcn3</i>
|
||
<sup>−/−</sup> animals. Mean ± SEM is shown. Five animals per genotype, 20–25 boutons/animal.</p></li><li><p>Example electron micrographs illustrating normal morphology of the pre‐ and postsynapse of <i>Clcn3</i>
|
||
<sup>+/+</sup> and <i>Clcn3</i>
|
||
<sup>−/−</sup> mice (scale bar: 250 nm).</p></li><li><p>Histogram indicating the distribution of synaptic vesicles sizes of <i>Clcn3</i>
|
||
<sup>+/+</sup> and <i>Clcn3</i>
|
||
<sup>−/−</sup> mice. Five animals per genotype, around 150 vesicles/animal.</p></li><li><p>Cumulative plot represents the SV size distribution in <i>Clcn3</i>
|
||
<sup>+/+</sup> and <i>Clcn3</i>
|
||
<sup>−/−</sup> mice. Five animals per genotype, around 150 vesicles/animal.</p></li><li><p>Mean area of all vesicles is unchanged between <i>Clcn3</i>
|
||
<sup>+/+</sup> and <i>Clcn3</i>
|
||
<sup>−/−</sup> mice. Mean ± SEM is shown. Five animals per genotype, around 150 vesicles/animal.</p></li></ol></div>
|
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|
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|
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</figcaption>
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Chloride accumulation in endosomes and lysosomes: facts checked in mice.
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<span class="docsum-authors full-authors">Schwappach B.</span>
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<span class="docsum-authors short-authors">Schwappach B.</span>
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<span class="docsum-journal-citation full-journal-citation">EMBO J. 2020 May 4;39(9):e104812. doi: 10.15252/embj.2020104812. Epub 2020 Apr 8.</span>
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<span class="docsum-journal-citation short-journal-citation">EMBO J. 2020.</span>
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Accardi A, Miller C (2004) Secondary active transport mediated by a prokaryotic homologue of ClC Cl− channels. Nature 427: 803–807
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
|
||
ref="linksrc=search_in_mesh_link"
|
||
href="https://www.ncbi.nlm.nih.gov/mesh?term=Animals"
|
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data-ga-category="search_mesh"
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data-ga-action="mesh_term_link"
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data-ga-label="Animals">
|
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Search in MeSH
|
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</a></li><li><a class="add-to-search-link dropdown-block-link"
|
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ref="linksrc=add_to_search_link"
|
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role="button"
|
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data-search-term=""Animals"[MeSH]"
|
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data-ga-category="search"
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data-ga-action="add_to_search"
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data-ga-label=""Animals"[MeSH]"
|
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href="#">
|
||
Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
|
||
aria-label="Toggle dropdown menu for keyword COS Cells"
|
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tabindex="0"
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aria-controls="keyword-actions-mesh-terms-1"
|
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aria-expanded="false"
|
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data-pinger-ignore>
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COS Cells
|
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</button><div id="keyword-actions-mesh-terms-1"
|
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class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
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aria-label="Dropdown menu for keyword COS Cells"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22COS+Cells%22%5BMeSH%5D&sort=date&sort_order=desc"
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data-href="/?term=%22COS+Cells%22%5BMeSH%5D&sort=date&sort_order=desc"
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ref="linksrc=search_in_pubmed_keyword_link&mesh="COS Cells"[MeSH]"
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data-ga-label="COS Cells">
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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|
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href="https://www.ncbi.nlm.nih.gov/mesh?term=COS+Cells"
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</a></li><li><a class="add-to-search-link dropdown-block-link"
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data-search-term=""COS Cells"[MeSH]"
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data-ga-label=""COS Cells"[MeSH]"
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link major"
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aria-label="Toggle dropdown menu for keyword Chloride Channels / genetics*"
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aria-expanded="false"
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Chloride Channels / genetics*
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</button><div id="keyword-actions-mesh-terms-major-2"
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hidden
|
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aria-label="Dropdown menu for keyword Chloride Channels / genetics*"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22Chloride+Channels%2Fgenetics%22%5BMAJR%5D&sort=date&sort_order=desc"
|
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data-href="/?term=%22Chloride+Channels%2Fgenetics%22%5BMAJR%5D&sort=date&sort_order=desc"
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Chloride Channels/genetics"[MAJR]"
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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data-ga-category="search"
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data-ga-label=""Chloride Channels/genetics"[MAJR]"
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link major"
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aria-label="Toggle dropdown menu for keyword Chloride Channels / metabolism*"
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tabindex="0"
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aria-expanded="false"
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data-pinger-ignore>
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Chloride Channels / metabolism*
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</button><div id="keyword-actions-mesh-terms-major-3"
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class="keyword-actions-dropdown dropdown dropdown-container"
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hidden
|
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aria-label="Dropdown menu for keyword Chloride Channels / metabolism*"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22Chloride+Channels%2Fmetabolism%22%5BMAJR%5D&sort=date&sort_order=desc"
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data-href="/?term=%22Chloride+Channels%2Fmetabolism%22%5BMAJR%5D&sort=date&sort_order=desc"
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Chloride Channels/metabolism"[MAJR]"
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data-ga-action="mesh_term"
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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</a></li><li><a class="add-to-search-link dropdown-block-link"
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data-search-term=""Chloride Channels/metabolism"[MAJR]"
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data-ga-label=""Chloride Channels/metabolism"[MAJR]"
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
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aria-label="Toggle dropdown menu for keyword Chlorocebus aethiops"
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aria-expanded="false"
|
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data-pinger-ignore>
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Chlorocebus aethiops
|
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</button><div id="keyword-actions-mesh-terms-4"
|
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class="keyword-actions-dropdown dropdown dropdown-container"
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hidden
|
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aria-label="Dropdown menu for keyword Chlorocebus aethiops"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22Chlorocebus+aethiops%22%5BMeSH%5D&sort=date&sort_order=desc"
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data-href="/?term=%22Chlorocebus+aethiops%22%5BMeSH%5D&sort=date&sort_order=desc"
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Chlorocebus aethiops"[MeSH]"
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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Search in MeSH
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</a></li><li><a class="add-to-search-link dropdown-block-link"
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data-search-term=""Chlorocebus aethiops"[MeSH]"
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
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aria-label="Toggle dropdown menu for keyword Disease Models, Animal"
|
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tabindex="0"
|
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aria-expanded="false"
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data-pinger-ignore>
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Disease Models, Animal
|
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</button><div id="keyword-actions-mesh-terms-5"
|
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class="keyword-actions-dropdown dropdown dropdown-container"
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hidden
|
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aria-label="Dropdown menu for keyword Disease Models, Animal"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22Disease+Models%2C+Animal%22%5BMeSH%5D&sort=date&sort_order=desc"
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data-href="/?term=%22Disease+Models%2C+Animal%22%5BMeSH%5D&sort=date&sort_order=desc"
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Disease Models, Animal"[MeSH]"
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Search in PubMed
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Search in MeSH
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link major"
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aria-label="Toggle dropdown menu for keyword Endosomes / metabolism*"
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tabindex="0"
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aria-controls="keyword-actions-mesh-terms-major-6"
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aria-expanded="false"
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data-pinger-ignore>
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Endosomes / metabolism*
|
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</button><div id="keyword-actions-mesh-terms-major-6"
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class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
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aria-label="Dropdown menu for keyword Endosomes / metabolism*"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22Endosomes%2Fmetabolism%22%5BMAJR%5D&sort=date&sort_order=desc"
|
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data-href="/?term=%22Endosomes%2Fmetabolism%22%5BMAJR%5D&sort=date&sort_order=desc"
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Endosomes/metabolism"[MAJR]"
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Search in PubMed
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Endosomes"
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Search in MeSH
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</a></li><li><a class="add-to-search-link dropdown-block-link"
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role="button"
|
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data-search-term=""Endosomes/metabolism"[MAJR]"
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data-ga-category="search"
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data-ga-action="add_to_search"
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data-ga-label=""Endosomes/metabolism"[MAJR]"
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href="#">
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
|
||
aria-label="Toggle dropdown menu for keyword Mice"
|
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tabindex="0"
|
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aria-controls="keyword-actions-mesh-terms-7"
|
||
aria-expanded="false"
|
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data-pinger-ignore>
|
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Mice
|
||
</button><div id="keyword-actions-mesh-terms-7"
|
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class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
||
aria-label="Dropdown menu for keyword Mice"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22Mice%22%5BMeSH%5D&sort=date&sort_order=desc"
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data-href="/?term=%22Mice%22%5BMeSH%5D&sort=date&sort_order=desc"
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Mice"[MeSH]"
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data-ga-label="Mice">
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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ref="linksrc=search_in_mesh_link"
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Mice"
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data-ga-category="search_mesh"
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Search in MeSH
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</a></li><li><a class="add-to-search-link dropdown-block-link"
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data-search-term=""Mice"[MeSH]"
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data-ga-category="search"
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data-ga-action="add_to_search"
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data-ga-label=""Mice"[MeSH]"
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href="#">
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
|
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aria-label="Toggle dropdown menu for keyword Mutation"
|
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tabindex="0"
|
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aria-controls="keyword-actions-mesh-terms-8"
|
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aria-expanded="false"
|
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data-pinger-ignore>
|
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Mutation
|
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</button><div id="keyword-actions-mesh-terms-8"
|
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class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
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aria-label="Dropdown menu for keyword Mutation"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22Mutation%22%5BMeSH%5D&sort=date&sort_order=desc"
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data-href="/?term=%22Mutation%22%5BMeSH%5D&sort=date&sort_order=desc"
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Mutation"[MeSH]"
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Mutation"
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data-ga-category="search_mesh"
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</a></li><li><a class="add-to-search-link dropdown-block-link"
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data-search-term=""Mutation"[MeSH]"
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data-ga-category="search"
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data-ga-label=""Mutation"[MeSH]"
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link major"
|
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aria-label="Toggle dropdown menu for keyword Neurodegenerative Diseases / genetics*"
|
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tabindex="0"
|
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aria-controls="keyword-actions-mesh-terms-major-9"
|
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aria-expanded="false"
|
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data-pinger-ignore>
|
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Neurodegenerative Diseases / genetics*
|
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</button><div id="keyword-actions-mesh-terms-major-9"
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class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
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aria-label="Dropdown menu for keyword Neurodegenerative Diseases / genetics*"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
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href="/?term=%22Neurodegenerative+Diseases%2Fgenetics%22%5BMAJR%5D&sort=date&sort_order=desc"
|
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data-href="/?term=%22Neurodegenerative+Diseases%2Fgenetics%22%5BMAJR%5D&sort=date&sort_order=desc"
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Neurodegenerative Diseases/genetics"[MAJR]"
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Neurodegenerative+Diseases"
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Search in MeSH
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</a></li><li><a class="add-to-search-link dropdown-block-link"
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
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aria-label="Toggle dropdown menu for keyword Neurodegenerative Diseases / metabolism"
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tabindex="0"
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aria-controls="keyword-actions-mesh-terms-10"
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aria-expanded="false"
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data-pinger-ignore>
|
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Neurodegenerative Diseases / metabolism
|
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</button><div id="keyword-actions-mesh-terms-10"
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class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
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aria-label="Dropdown menu for keyword Neurodegenerative Diseases / metabolism"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
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href="/?term=%22Neurodegenerative+Diseases%2Fmetabolism%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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data-href="/?term=%22Neurodegenerative+Diseases%2Fmetabolism%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Neurodegenerative Diseases/metabolism"[MeSH]"
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data-ga-label="Neurodegenerative Diseases / metabolism">
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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ref="linksrc=search_in_mesh_link"
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Neurodegenerative+Diseases"
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Search in MeSH
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</a></li><li><a class="add-to-search-link dropdown-block-link"
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data-ga-category="search"
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Add to Search
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