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|
||
</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%2F38177503%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%2F38177503%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="UarSk1h35eJFhnScBHcE1UTBRokePOSGbXbXXRKpFPw9bOY2e0PGv2pfps2qIpq0">
|
||
</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="UarSk1h35eJFhnScBHcE1UTBRokePOSGbXbXXRKpFPw9bOY2e0PGv2pfps2qIpq0">
|
||
|
||
|
||
|
||
<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="UarSk1h35eJFhnScBHcE1UTBRokePOSGbXbXXRKpFPw9bOY2e0PGv2pfps2qIpq0">
|
||
|
||
<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: 38177503 - PubMed</span>
|
||
<input type="hidden" name="email-subject" value="1 selected item: 38177503"/>
|
||
<input type="hidden" name="email-subject-hash" value="c4ec7cd298e6fdbad6ed83e029cbb7cb5c11f35a20dc8c672817577359dd2ecc"/>
|
||
</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="UarSk1h35eJFhnScBHcE1UTBRokePOSGbXbXXRKpFPw9bOY2e0PGv2pfps2qIpq0">
|
||
|
||
|
||
|
||
<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="UarSk1h35eJFhnScBHcE1UTBRokePOSGbXbXXRKpFPw9bOY2e0PGv2pfps2qIpq0">
|
||
|
||
|
||
|
||
<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="UarSk1h35eJFhnScBHcE1UTBRokePOSGbXbXXRKpFPw9bOY2e0PGv2pfps2qIpq0">
|
||
|
||
<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="UarSk1h35eJFhnScBHcE1UTBRokePOSGbXbXXRKpFPw9bOY2e0PGv2pfps2qIpq0">
|
||
|
||
|
||
|
||
<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="UarSk1h35eJFhnScBHcE1UTBRokePOSGbXbXXRKpFPw9bOY2e0PGv2pfps2qIpq0">
|
||
|
||
<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="38177503">
|
||
<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/10.1038/s44318-023-00001-4"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=False&PrId=3094&itool=Abstract-def&log$=linkouticon&uid=38177503&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="38177503"
|
||
><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/38177503/"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=True&PrId=3494&itool=Abstract-def&log$=linkouticon&uid=38177503&db=pubmed&nlmid=8208664"
|
||
title="Free full text at PubMed Central"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="PMC"
|
||
data-ga-label="38177503"
|
||
><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="/38177503/citations/"
|
||
data-citation-style="nlm"
|
||
data-pubmed-format-link="/38177503/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="38177503" 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%2F38177503%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="UarSk1h35eJFhnScBHcE1UTBRokePOSGbXbXXRKpFPw9bOY2e0PGv2pfps2qIpq0"><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"
|
||
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="sidebar-actions-display-format"><option value="abstract">Abstract</option><option value="pubmed">PubMed</option><option value="pmid">PMID</option></select></div></div></div></div></div></div>
|
||
|
||
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</a></li></ul></div></div></div><span class="period">. </span><span class="cit">2024 Jan;43(2):225-249.</span>
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Structural insights into respiratory complex I deficiency and assembly from the mitochondrial disease-related ndufs4<sup>-/-</sup> mouse
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Structural insights into respiratory complex I deficiency and assembly from the mitochondrial disease-related ndufs4<sup>-/-</sup> mouse
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Respiratory complex I (NADH:ubiquinone oxidoreductase) is essential for cellular energy production and NAD<sup>+</sup> homeostasis. Complex I mutations cause neuromuscular, mitochondrial diseases, such as Leigh Syndrome, but their molecular-level consequences remain poorly understood. Here, we use a popular complex I-linked mitochondrial disease model, the ndufs4<sup>-/-</sup> mouse, to define the structural, biochemical, and functional consequences of the absence of subunit NDUFS4. Cryo-EM analyses of the complex I from ndufs4<sup>-/-</sup> mouse hearts revealed a loose association of the NADH-dehydrogenase module, and discrete classes containing either assembly factor NDUFAF2 or subunit NDUFS6. Subunit NDUFA12, which replaces its paralogue NDUFAF2 in mature complex I, is absent from all classes, compounding the deletion of NDUFS4 and preventing maturation of an NDUFS4-free enzyme. We propose that NDUFAF2 recruits the NADH-dehydrogenase module during assembly of the complex. Taken together, the findings provide new molecular-level understanding of the ndufs4<sup>-/-</sup> mouse model and complex I-linked mitochondrial disease.
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Complex I; Cryo-EM; Leigh Syndrome; Mitochondria; NADH:Ubiquinone Oxidoreductase.
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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 no competing interests.</p>
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Figures
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alt="Figure 1" />
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<strong class="figure-label">
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<p> Figure 1. The NDUFS4 subunit in wild-type… </p>
|
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</strong>
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<strong class="figure-label">
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<p> Figure 1. The NDUFS4 subunit in wild-type complex I from mouse-heart mitochondria. </p>
|
||
</strong>
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<div class="figure-caption-contents"><p> ( <b> A </b> )… </p></div>
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<strong class="figure-label">
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Figure 1. The NDUFS4 subunit in wild-type complex I from mouse-heart mitochondria.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">(<b>A</b>) Overview structures of complex I viewed from the membrane and from the heel showing the locations of NDUFS4 (red), the N-module (blue) and subunits NDUFS6 (cyan), NDUFA12 (purple) and NDUFA7 (gold). (<b>B</b>) View of the front of the hydrophilic domain showing NDUFS4 (red) and the surrounding subunits. (<b>C</b>) Subunits surrounding NDUFA12 on the heel of the complex, and structural elements interacting with the β2-β3 loop of NDUFS4 that passes underneath NDUFS1 to form a junction of NDUSF4, NDUFA12, NDUFA6 and NDUF9 (right, close-up of the boxed region from a different viewpoint to focus on the loop). (<b>D</b>) NDUFS4 approaches four of the seven FeS clusters in the FeS chain between the FMN and the ubiquinone-binding site. Figure created using PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb6ZR2/pdb">6ZR2</ext-link>.</div>
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||
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<img class="figure-thumb" itemprop="thumbnail"
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0f0e/10897435/d273db949c7e/44318_2023_1_Fig2_HTML.gif"
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alt="Figure 2" />
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<strong class="figure-label">
|
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<p> Figure 2. Characterization of <i> ndufs4 </i> <sup> −/− </sup> mouse… </p>
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||
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<strong class="figure-label">
|
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<p> Figure 2. Characterization of <i> ndufs4 </i> <sup> −/− </sup> mouse mitochondrial membranes. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> ( <b> A </b> ) BN-PAGE analyses of heart… </p></div>
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<strong class="figure-label">
|
||
Figure 2. Characterization of <i>ndufs4</i><sup>−/−</sup> mouse mitochondrial membranes.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">(<b>A</b>) BN-PAGE analyses of heart mitochondrial membranes solubilized by 1% DDM and stained with the in-gel NADH-linked NBT assay with 30 µg of protein loaded on each lane. (<b>B</b>) Summary of the complexomic analyses of complex I subunits and assembly factors in wild-type and <i>ndufs4</i><sup><i>−/−</i></sup> heart mitochondrial membranes. The complete datasets are shown in Fig. EV1. (<b>C</b>) The piericidin A-sensitive rates of NADH oxidation by wild-type and <i>ndufs4</i><sup><i>−/−</i></sup> heart mitochondrial membranes using 200 μM NADH. Data are mean averages ± SEM (<i>n</i> = 4 or 6) analyzed with the Student’s <i>t</i>-test (****<i>p</i> < 0.0001). (<b>D</b>) The atpenin A-sensitive rates of succinate oxidation using 5 mM succinate. Data are mean averages ± SEM (<i>n</i> = 6) analyzed with the Student’s t-test. In <b>C</b> and <b>D</b>, each point represents a biological replicate (an individual membrane preparation from more than four mice). (<b>E</b>) Relative quantification of respiratory complexes I to IV in kidney mitochondrial membranes of <i>ndufs4</i><sup>−/−</sup> mice compared to wild-type mice, calculated by normalizing the sum of MS peptide areas for the proteins in each complex to the sum of those for VDAC1, VDAC2, and VDAC3. Data are mean averages of technical replicates ± SEM with propagated error (<i>n</i> = 3 or 4). (<b>F</b>) BN-PAGE analyses of <i>ndufs4</i><sup>−/−</sup> heart mitochondrial membranes solubilized by 1% DDM with and without cross-linking by BS<sup>3</sup> (0.1 mM for 25 min) then stained with NADH-linked NBT. N, N-module of complex I (∼200 kDa); QP, QP subcomplex of complex I (∼800 kDa); SC, supercomplexes. Source data are available online for this figure.</div>
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|
||
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|
||
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|
||
<img class="figure-thumb" itemprop="thumbnail"
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|
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|
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alt="Figure 3" />
|
||
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|
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<strong class="figure-label">
|
||
<p> Figure 3. Characterization of purified <i> ndufs4 </i> <sup> −/−… </sup> </p>
|
||
</strong>
|
||
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|
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<strong class="figure-label">
|
||
<p> Figure 3. Characterization of purified <i> ndufs4 </i> <sup> −/− </sup> complex I. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> Size exclusion chromatography of complex I from… </p></div>
|
||
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||
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<figcaption id="figure-caption-2" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
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<strong class="figure-label">
|
||
Figure 3. Characterization of purified <i>ndufs4</i><sup>−/−</sup> complex I.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">Size exclusion chromatography of complex I from (<b>A</b>) kidney and (<b>B</b>) heart mitochondrial membranes. The absorbance at 280 nm is in dark blue and at 420 nm in red. The peak elution volume of wild-type complex I is marked with a in dashed line. The peak volumes for complex I elution vary (~1.35 in A <i>vs</i>. ~1.6 mL in <b>B</b>) due to use of different columns (of the same type). (<b>C</b>) Rates of kinetic reactions for <i>ndufs4</i><sup><i>−/−</i></sup> heart mitochondrial membranes as a proportion of the wild-type rates (mean ± S.E.M., <i>n</i> ≥ 3 technical replicates). (<b>D</b>) Rates of kinetic reactions for purified <i>ndufs4</i><sup><i>−/−</i></sup> heart complex I as a proportion of the wild-type rates (mean ± S.E.M., <i>n</i> ≥ 3 technical replicates). (<b>E</b>) Loss of FMN from complex I purified from wild-type and <i>ndufs4</i><sup><i>−/−</i></sup> heart as the temperature is increased, measured as the fluorescence of the free flavin (mean ± S.E.M., <i>n</i> = 3 technical replicates). (<b>F</b>) The effect of BS<sup>3</sup> cross-linking on BN-PAGE of the enzymes purified from heart; wild-type enzyme was not cross-linked (BS<sup>3</sup> 0); <i>ndufs4</i><sup><i>−/−</i></sup> complex I was cross-linked with 0.25 mM BS<sup>3</sup> during solubilization from the membranes, and then run as prepared (BS<sup>3</sup> 1); <i>ndufs4</i><sup><i>−/−</i></sup> complex I was reacted again with 2.5 mM BS<sup>3</sup> after size exclusion chromatography (BS<sup>3</sup> 2). The second reaction further increased the stability of the enzyme (compare to the untreated sample in Fig. 2F). Source data are available online for this figure.</div>
|
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|
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<strong class="figure-label">
|
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<p> Figure 4. Structural differences between <i> ndufs4 </i> <sup> −/−… </sup> </p>
|
||
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<strong class="figure-label">
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<p> Figure 4. Structural differences between <i> ndufs4 </i> <sup> −/− </sup> heart complex I (class 2) and the wild-type… </p>
|
||
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<strong class="figure-label">
|
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Figure 4. Structural differences between <i>ndufs4</i><sup>−/−</sup> heart complex I (class 2) and the wild-type enzyme.
|
||
</strong>
|
||
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||
|
||
<div class="figure-caption-contents">(<b>A</b>) View of the active wild-type reference model (PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb6ZR2/pdb">6ZR2</ext-link>) and the <i>ndufs4</i><sup><i>−/−</i></sup> heart class 2 model (PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb8CA3/pdb">8CA3</ext-link>) showing the crevice left by the absence of NDUFS4. Red, NDUFS4; gold, NDUFA7; white, NDUFA9. (<b>B</b>) Local resolutions of the consensus map of <i>ndufs4</i><sup>−/−</sup> heart complex I (class 2, <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://www.ebi.ac.uk/pdbe/entry/emdb/EMD-16516">EMD-16516</ext-link>) and the locally refined N-module map (class 2, <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://www.ebi.ac.uk/pdbe/entry/emdb/EMD-16517">EMD-16517</ext-link>). (<b>C</b>) Overlay of the PDB models for the <i>ndufs4</i><sup>−/−</sup> (PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb8CA3/pdb">8CA3</ext-link>) and wild-type (PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb6ZR2/pdb">6ZR2</ext-link>) enzymes. The wild-type model is shown in semi-transparent, and the rotation of the colored subunits of the N-module between the two enzymes is observed upon global model alignment. Green, NDUFV1; yellow, NDUFV3; purple, NDUFS1; blue, NDUFA2. (<b>D</b>) Overlay of the PDB models for the <i>ndufs4</i><sup>−/−</sup> (PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb8CA3/pdb">8CA3</ext-link>) and wild-type (PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb6ZR2/pdb">6ZR2</ext-link>) enzymes focusing on the NDUFA9 subunit. The wild-type model is shown in white, and subunits of the <i>ndufs4</i><sup>−/−</sup> enzyme are in color. With the models aligned on core subunit ND1, NDUFA9 drops slightly in the <i>ndufs4</i><sup>−/−</sup> enzyme (see arrow). (<b>E</b>) The regions of the active wild-type enzyme which appear disordered in <i>ndufs4</i><sup><i>−/−</i></sup> maps.</div>
|
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<p> Figure 5. NDUFAF2 binding in <i> ndufs4 </i> <sup> −/−… </sup> </p>
|
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<p> Figure 5. NDUFAF2 binding in <i> ndufs4 </i> <sup> −/− </sup> class 3 and comparison of the NDUFAF2- and… </p>
|
||
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||
|
||
<strong class="figure-label">
|
||
Figure 5. NDUFAF2 binding in <i>ndufs4</i><sup>−/−</sup> class 3 and comparison of the NDUFAF2- and NDUFS6-bound <i>ndufs4</i><sup>−/−</sup> structures.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">(<b>A</b>) Complex I models for the wild-type (left, PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb6ZR2/pdb">6ZR2</ext-link>) and <i>ndufs4</i><sup>−/−</sup> classes 1 (PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb8C2S/pdb">8C2S</ext-link>), 2 (PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb8CA3/pdb">8CA3</ext-link>) and 3 (PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb8CA5/pdb">8CA5</ext-link>) shown in surface view for the majority of the complex. Cartoon view is shown for subunits NDUFS6 (teal), NDUFA7 (gold), NDUFA9 (gray), NDUFA12 (purple), and NDUFAF2 (green). Protein compositions are also summarized in Table 1. (<b>B</b>) Relationships between NDUFAF2 and surrounding subunits in class 3, and the equivalent view for class 2. An equivalent view for the wild-type complex is shown in Fig. 1C. (<b>C</b>) Comparison of the AlphaFold-predicted model for mouse NDUFAF2 (AF-Q59J78), experimental models for NDUFAF2 from <i>ndufs4</i><sup>−/−</sup> class 1 (PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb8C2S/pdb">8C2S</ext-link>, green) and <i>Y. lipolytica ndufs6</i><sup><i>−/−</i></sup> (PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb7RFQ/pdb">7RFQ</ext-link>, gray) and subunit NDUFA12 from wild-type mouse (PDB: <ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://doi.org/10.2210/pdb6ZR2/pdb">6ZR2</ext-link>, purple). The AlphaFold pLDDT score indicates the confidence of the model with values above 90 indicating very high confidence and values below 70 low confidence; regions with values below 50 may be intrinsically disordered.</div>
|
||
|
||
|
||
|
||
|
||
</figcaption>
|
||
|
||
|
||
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|
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role="button"
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data-image-width="705"
|
||
data-image-height="383"
|
||
data-image-alt="Figure 6"
|
||
data-pmc-id="PMC10897435"
|
||
data-figure-id="Fig6">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
||
id="article-image-5"
|
||
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0f0e/10897435/21da3e143943/44318_2023_1_Fig6_HTML.gif"
|
||
alt="Figure 6" />
|
||
</a>
|
||
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<meta itemprop="height" itemtype="http://schema.org/ImageObject" content="383">
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|
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|
||
|
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|
||
|
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|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 6. ACADVL association with purified <i> ndufs4… </i> </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
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|
||
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|
||
</div>
|
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<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 6. ACADVL association with purified <i> ndufs4 </i> <sup> <i> −/− </i> </sup> heart complex I. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> ( <b> A </b> ) Cryo-EM density… </p></div>
|
||
|
||
|
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|
||
|
||
</div>
|
||
|
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<figcaption id="figure-caption-5" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
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||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure 6. ACADVL association with purified <i>ndufs4</i><sup><i>−/−</i></sup> heart complex I.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">(<b>A</b>) Cryo-EM density map showing the location of the ACAD dimer (blue) attached to the detergent micelle (yellow) and next to subunit ND1 (purple). (<b>B</b>) The model for the ACADVL dimer and cryoEM density (at a threshold of 1.74) is shown with the location of the FAD cofactors highlighted in yellow; the FAD density is shown separately also (right, at a threshold of 1.74). (<b>C</b>) The dimeric model of ACADVL aligned to its position relative to complex I, within the detergent micelle. (<b>D</b>) Relative quantification of ACAD9 and ACADVL. The sum of peptide areas for each protein were normalized to the sum of peptide areas for VDAC1, VDAC 2, and VDAC3, and displayed as the ratio between wild-type and <i>ndufs4</i><sup><i>−/−</i></sup> kidney mitochondrial membranes. Data are mean averages of technical replicates ±SEM with propagated error (<i>n</i> = 3 or 4). (<b>E</b>) The short Lys-Lys distances between ACADVL and NDUFA8 that may be responsible for the stabilization of ACAD binding by crosslinking. Source data are available online for this figure.</div>
|
||
|
||
|
||
|
||
|
||
</figcaption>
|
||
|
||
|
||
</figure>
|
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|
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|
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<a class="figure-link"
|
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href="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0f0e/10897435/a21877f0d488/44318_2023_1_Fig7_HTML.jpg"
|
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aria-describedby="figure-caption-6"
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role="button"
|
||
data-image-width="680"
|
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data-image-height="1034"
|
||
data-image-alt="Figure 7"
|
||
data-pmc-id="PMC10897435"
|
||
data-figure-id="Fig7">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
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id="article-image-6"
|
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0f0e/10897435/6d2de45444b4/44318_2023_1_Fig7_HTML.gif"
|
||
alt="Figure 7" />
|
||
</a>
|
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<meta itemprop="width" itemtype="http://schema.org/ImageObject" content="680">
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<meta itemprop="height" itemtype="http://schema.org/ImageObject" content="1034">
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<div class="figure-caption figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="caption" aria-hidden="true">
|
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<div class="caption-wrap">
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 7. Schematic diagram showing our proposed… </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
</div>
|
||
|
||
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 7. Schematic diagram showing our proposed assembly pathway for mouse <i> ndufs4 </i> <sup> <i> −/− </i> </sup> complex I. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> NDUFAF2… </p></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-6" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure 7. Schematic diagram showing our proposed assembly pathway for mouse <i>ndufs4</i><sup><i>−/−</i></sup> complex I.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">NDUFAF2 contains two domains, connected by a flexible linker. NDUFS6 also contains two domains linked together; in the class 2 complex I structure only the N-terminal domain is bound and observed in the density map.</div>
|
||
|
||
|
||
|
||
|
||
</figcaption>
|
||
|
||
|
||
</figure>
|
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<figure class="figure-item tail"
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|
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<a class="figure-link"
|
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href="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0f0e/10897435/4e77c41b193a/44318_2023_1_Fig8_ESM.jpg"
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data-image-width="783"
|
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data-image-height="1099"
|
||
data-image-alt="Figure EV1"
|
||
data-pmc-id="PMC10897435"
|
||
data-figure-id="Fig8">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
||
id="article-image-7"
|
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0f0e/10897435/68bb5eb230a1/44318_2023_1_Fig8_ESM.gif"
|
||
alt="Figure EV1" />
|
||
</a>
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||
<meta itemprop="width" itemtype="http://schema.org/ImageObject" content="783">
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<meta itemprop="height" itemtype="http://schema.org/ImageObject" content="1099">
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<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 EV1. Complexome profiles from BN-PAGE analyses… </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
</div>
|
||
|
||
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure EV1. Complexome profiles from BN-PAGE analyses of solubilized mitochondrial membranes from (A) wild-type and… </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-7" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure EV1. Complexome profiles from BN-PAGE analyses of solubilized mitochondrial membranes from (A) wild-type and (B) <i>ndufs4</i><sup>−/−</sup> mouse heart.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">The heatmap represents the relative protein abundance in each gel slice (based on the peak areas of the three top-scoring peptides for each protein from LC-MS analyses) with the data for each protein normalized to the highest intensity signal within the lane. The prefix “NDU” has been omitted from subunit labels for brevity. Where a protein was not detected in one sample, the column is completely black. Subunits ND3, ND4L and ND6 were not detected in either sample. The masses of complex I-related bands specific to <i>ndufs4</i><sup>−/−</sup> membranes of ~800 (QP subcomplex) and ~200 kDa (N module) were estimated using the migration and masses of known complexes (inset). Source data are available online for this figure.</div>
|
||
|
||
|
||
|
||
|
||
</figcaption>
|
||
|
||
|
||
</figure>
|
||
|
||
<figure class="figure-item tail"
|
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|
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<a class="figure-link"
|
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href="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0f0e/10897435/3e331d417cae/44318_2023_1_Fig9_ESM.jpg"
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data-image-width="705"
|
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|
||
data-image-alt="Figure EV2"
|
||
data-pmc-id="PMC10897435"
|
||
data-figure-id="Fig9">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
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id="article-image-8"
|
||
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0f0e/10897435/ff2922d76680/44318_2023_1_Fig9_ESM.gif"
|
||
alt="Figure EV2" />
|
||
</a>
|
||
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||
<meta itemprop="width" itemtype="http://schema.org/ImageObject" content="705">
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|
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<div class="caption-wrap">
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure EV2. Flavin-site kinetics in <i> ndufs4 </i> <sup> <i> −/−… </i> </sup> </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
</div>
|
||
|
||
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure EV2. Flavin-site kinetics in <i> ndufs4 </i> <sup> <i> −/− </i> </sup> mitochondrial membranes compared to wild-type. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> ( <b> A </b> ) Kinetic… </p></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-8" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure EV2. Flavin-site kinetics in <i>ndufs4</i><sup><i>−/−</i></sup> mitochondrial membranes compared to wild-type.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">(<b>A</b>) Kinetic evaluation of the Michaelis constant (<i>K</i><sub>M</sub>) for HAR in the NADH:HAR oxidoreductase reaction catalyzed by mouse heart membranes in the presence of 100 µM NADH. (<b>B</b>) Kinetic evaluation of the Michaelis constant (<i>K</i><sub>M</sub>) for NADH in the presence of 1 mM HAR. (<b>C</b>) Kinetic evaluation of the Michaelis constant (<i>K</i><sub>M</sub>) for NADH in the NADH:FeCN oxidoreductase reaction catalyzed by mouse kidney membranes in the presence of 100 µM FeCN. Due to the scarcity of materials, the assays in panels <b>A</b> and <b>B</b> were performed on different membrane samples, so the absolute rates are not directly comparable between them. Data points are mean averages ± SEM (n = 3 technical replicates). Source data are available online for this figure.</div>
|
||
|
||
|
||
|
||
|
||
</figcaption>
|
||
|
||
|
||
</figure>
|
||
|
||
<figure class="figure-item tail"
|
||
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|
||
<a class="figure-link"
|
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|
||
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|
||
data-pmc-id="PMC10897435"
|
||
data-figure-id="Fig10">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
||
id="article-image-9"
|
||
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0f0e/10897435/66fee95b7b3a/44318_2023_1_Fig10_ESM.gif"
|
||
alt="Figure EV3" />
|
||
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|
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||
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|
||
|
||
<div class="caption-wrap">
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure EV3. SDS PAGE of complex I… </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
</div>
|
||
|
||
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure EV3. SDS PAGE of complex I purified from (A) wild-type and (B) <i> ndufs4 </i> <sup> <i> −/−… </i> </sup> </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-9" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure EV3. SDS PAGE of complex I purified from (A) wild-type and (B) <i>ndufs4</i><sup><i>−/−</i></sup> heart mitochondrial membranes.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">Bands were manually excised, and proteins identified by MALDI-TOF-TOF analyses of tryptic digests. Complex I subunits are labeled in black, known assembly factors in blue, and other proteins detected in red. For proteins labeled in brackets individual peptide scores were below the 95% threshold but their protein scores were above the peptide threshold. Information on protein identification is in Appendix Tables S1 and S2.</div>
|
||
|
||
|
||
|
||
|
||
</figcaption>
|
||
|
||
|
||
</figure>
|
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|
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<figure class="figure-item tail"
|
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|
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|
||
<a class="figure-link"
|
||
href="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0f0e/10897435/5525496d2b0b/44318_2023_1_Fig11_ESM.jpg"
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|
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data-image-width="705"
|
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|
||
data-image-alt="Figure EV4"
|
||
data-pmc-id="PMC10897435"
|
||
data-figure-id="Fig11">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
||
id="article-image-10"
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0f0e/10897435/eb1e53405ca0/44318_2023_1_Fig11_ESM.gif"
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<p> Figure EV4. Views of the cryo-EM density… </p>
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<strong class="figure-label">
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<p> Figure EV4. Views of the cryo-EM density map of complex I from <i> ndufs4 </i> <sup> <i> −/− </i> </sup> kidney… </p>
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<strong class="figure-label">
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Figure EV4. Views of the cryo-EM density map of complex I from <i>ndufs4</i><sup><i>−/−</i></sup> kidney and comparison to the model for wild-type heart complex I.
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</strong>
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<div class="figure-caption-contents">(<b>A</b>) The density map of complex I from <i>ndufs4</i><sup><i>−/−</i></sup> kidney. (<b>B</b>) The wild-type complex I model (PDB:6ZR2) is docked into the <i>ndufs4</i><sup><i>−/−</i></sup> complex I density map (gray, EMD:16514); no density is present in the locations of NDUFS4 (red model) and NDUFS6 (purple model).</div>
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<p> Figure EV5. The cryo-EM densities for NDUFS6,… </p>
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<strong class="figure-label">
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<p> Figure EV5. The cryo-EM densities for NDUFS6, NDUFA7, NDUFAF2 and NDUFA9. </p>
|
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</strong>
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<div class="figure-caption-contents"><p> The models for wild-type… </p></div>
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<strong class="figure-label">
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Figure EV5. The cryo-EM densities for NDUFS6, NDUFA7, NDUFAF2 and NDUFA9.
|
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</strong>
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<div class="figure-caption-contents">The models for wild-type heart complex I (PDB: 6ZR2, for NDUFS6, NDUFA7 and NDUFA9) and the class 3 model (for NDUFAF2) from were fitted into each density map using the fit-in-map function in Chimera X. The density within 3 Å of each fitted model is shown for (<b>A</b>) subunit NDUFS6; (<b>B</b>) subunit NDUFA7; (<b>C</b>) assembly factor NDUFAF2; and (<b>D</b>) subunit NDUFA9. They are shown for the map of wild-type heart complex I (<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://www.ebi.ac.uk/pdbe/entry/emdb/EMD-11377">EMD-11377</ext-link>); the <i>ndufs4</i><sup><i>−/−</i></sup> heart complex I class 1, 2 and 3 maps; and the <i>ndufs4</i><sup><i>−/−</i></sup> kidney complex I map, with map thresholds of 0.027, 1.76, 2.18, 1.52 and 1.12, respectively.</div>
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Mitochondrial complex I inhibition enhances astrocyte responsiveness to pro-inflammatory stimuli.
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<span class="docsum-authors full-authors">Wischhof L, Mathew AJ, Bonaguro L, Beyer M, Ehninger D, Nicotera P, Bano D.</span>
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<span class="docsum-authors short-authors">Wischhof L, et al.</span>
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<span class="docsum-authors full-authors">Ivanov BS, Bridges HR, Jarman OD, Hirst J.</span>
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Adjobo-Hermans MJW, de Haas R, Willems PHGM, Wojtala A, van Emst-de Vries SE, Wagenaars JA, van den Brand M, Rodenburg RJ, Smeitink JAM, Nijtmans LG, et al. NDUFS4 deletion triggers loss of NDUFA12 in Ndufs4 mice and Leigh syndrome patients: a stabilizing role for NDUFAF2. Biochim Biophys Acta - Bioenerg. 2020;1861:148213. doi: 10.1016/j.bbabio.2020.148213.
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</div>
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<div id="substances" class="substances keywords-section">
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<h2 class="title">
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Substances
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<ul class="keywords-list"><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
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Electron Transport Complex I
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