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<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%2F34573045%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%2F34573045%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="ik8crRB1kJbHZMSsQ6ogZhkF4FRdHOjiz7Sh4H4nUkYbTdYitp1itpQjCJzpApRC">
|
||
</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="ik8crRB1kJbHZMSsQ6ogZhkF4FRdHOjiz7Sh4H4nUkYbTdYitp1itpQjCJzpApRC">
|
||
|
||
|
||
|
||
<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="ik8crRB1kJbHZMSsQ6ogZhkF4FRdHOjiz7Sh4H4nUkYbTdYitp1itpQjCJzpApRC">
|
||
|
||
<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: 34573045 - PubMed</span>
|
||
<input type="hidden" name="email-subject" value="1 selected item: 34573045"/>
|
||
<input type="hidden" name="email-subject-hash" value="e5fa0f3e84a0e1ea17f75ee011b2a278ebfa11824aa79100b093eb02f9f66de4"/>
|
||
</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="ik8crRB1kJbHZMSsQ6ogZhkF4FRdHOjiz7Sh4H4nUkYbTdYitp1itpQjCJzpApRC">
|
||
|
||
|
||
|
||
<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="ik8crRB1kJbHZMSsQ6ogZhkF4FRdHOjiz7Sh4H4nUkYbTdYitp1itpQjCJzpApRC">
|
||
|
||
|
||
|
||
<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="ik8crRB1kJbHZMSsQ6ogZhkF4FRdHOjiz7Sh4H4nUkYbTdYitp1itpQjCJzpApRC">
|
||
|
||
<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="ik8crRB1kJbHZMSsQ6ogZhkF4FRdHOjiz7Sh4H4nUkYbTdYitp1itpQjCJzpApRC">
|
||
|
||
|
||
|
||
<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="ik8crRB1kJbHZMSsQ6ogZhkF4FRdHOjiz7Sh4H4nUkYbTdYitp1itpQjCJzpApRC">
|
||
|
||
<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="34573045">
|
||
<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://www.mdpi.com/resolver?pii=antiox10091413"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=False&PrId=6383&itool=Abstract-def&log$=linkouticon&uid=34573045&db=pubmed&nlmid=101668981"
|
||
title="See full text options at MDPI"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="MDPI"
|
||
data-ga-label="34573045"
|
||
><img src="https://cdn.ncbi.nlm.nih.gov/corehtml/query/egifs/https:--res.mdpi.com-data-pubmed-linkout.png" alt="MDPI full text link"><span class="text">
|
||
|
||
MDPI
|
||
|
||
</span></a><a class="link-item
|
||
pmc
|
||
"
|
||
href="https://pmc.ncbi.nlm.nih.gov/articles/pmid/34573045/"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=True&PrId=3494&itool=Abstract-def&log$=linkouticon&uid=34573045&db=pubmed&nlmid=101668981"
|
||
title="Free full text at PubMed Central"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="PMC"
|
||
data-ga-label="34573045"
|
||
><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="/34573045/citations/"
|
||
data-citation-style="nlm"
|
||
data-pubmed-format-link="/34573045/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="34573045" 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%2F34573045%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="ik8crRB1kJbHZMSsQ6ogZhkF4FRdHOjiz7Sh4H4nUkYbTdYitp1itpQjCJzpApRC"><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
|
||
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</a></li></ul></div></div></div><span class="period">. </span><span class="cit">2021 Sep 3;10(9):1413.</span>
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SVCT2 Overexpression and Ascorbic Acid Uptake Increase Cortical Neuron Differentiation, Which Is Dependent on Vitamin C Recycling between Neurons and Astrocytes
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SVCT2 Overexpression and Ascorbic Acid Uptake Increase Cortical Neuron Differentiation, Which Is Dependent on Vitamin C Recycling between Neurons and Astrocytes
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data-ga-label="Francisco Nualart">Francisco Nualart</a><sup class="affiliation-links"><span class="author-sup-separator"> </span><a class="affiliation-link" title="Laboratory of Neurobiology and Stem Cells, NeuroCellT, Department of Cellular Biology, Faculty of Biological Sciences, University of Concepcion, Concepción 4030000, Chile." href="#short-view-affiliation-1" ref="linksrc=author_aff">
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</a><span class="author-sup-separator"> </span><a class="affiliation-link" title="Center for Advanced Microscopy, CMA BIO BIO, University of Concepcion, Concepción 4030000, Chile." href="#short-view-affiliation-2" ref="linksrc=author_aff">
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><sup class="key">1</sup> Laboratory of Neurobiology and Stem Cells, NeuroCellT, Department of Cellular Biology, Faculty of Biological Sciences, University of Concepcion, Concepción 4030000, Chile.</li>
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<li data-affiliation-id="short-view-affiliation-2"
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><sup class="key">2</sup> Center for Advanced Microscopy, CMA BIO BIO, University of Concepcion, Concepción 4030000, Chile.</li>
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<strong class="current-id" title="PubMed ID">34573045</strong>
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During brain development, sodium-vitamin C transporter (SVCT2) has been detected primarily in radial glial cells in situ, with low-to-absent expression in cerebral cortex neuroblasts. However, strong SVCT2 expression is observed during the first postnatal days, resulting in increased intracellular concentration of vitamin C. Hippocampal neurons isolated from SVCT2 knockout mice showed shorter neurites and low clustering of glutamate receptors. Other studies have shown that vitamin C-deprived guinea pigs have reduced spatial memory, suggesting that ascorbic acid (AA) and SVCT2 have important roles in postnatal neuronal differentiation and neurite formation. In this study, SVCT2 lentiviral overexpression induced branching and increased synaptic proteins expression in primary cultures of cortical neurons. Analysis in neuroblastoma 2a (Neuro2a) and human subventricular tumor C3 (HSVT-C3) cells showed similar branching results. SVCT2 was mainly observed in the cell membrane and endoplasmic reticulum; however, it was not detected in the mitochondria. Cellular branching in neuronal cells and in a previously standardized neurosphere assay is dependent on the recycling of vitamin C or reduction in dehydroascorbic acid (DHA, produced by neurons) by glial cells. The effect of WZB117, a selective glucose/DHA transporter 1 (GLUT1) inhibitor expressed in glial cells, was also studied. By inhibiting GLUT1 glial cells, a loss of branching is observed in vitro, which is reproduced in the cerebral cortex in situ. We concluded that vitamin C recycling between neurons and astrocyte-like cells is fundamental to maintain neuronal differentiation in vitro and in vivo. The recycling activity begins at the cerebral postnatal cortex when neurons increase SVCT2 expression and concomitantly, GLUT1 is expressed in glial cells.
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SIM superresolution; SVCT2; ascorbic acid; bystander effect; cortical neurons; dehydroascorbic acid; neurites; neuronal branching; neurospheres; vitamin C; vitamin C recycling.
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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 conflict of interest.</p>
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<div class="figure-caption-contents"><p> SVCT2 overexpression increased cellular branching.… </p></div>
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<div class="figure-caption-contents"><p> SVCT2 overexpression increased cellular branching. ( <b> A </b> ) RT-PCR analysis of SVCT2 in… </p></div>
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<div class="figure-caption-contents">SVCT2 overexpression increased cellular branching. (<b>A</b>) RT-PCR analysis of SVCT2 in mRNA isolated from nontransduced (lane 2) and EGFP- or hSVCT2wt-EYFP-overexpressing neurons (lanes 3 and 4, respectively). The 100 bp standard (lane 1). RT-PCR analysis of cyclophilin was performed as an internal control. (<b>B</b>) Uptake of 100 μM AA was analyzed in the presence of NaCl or choline at 37 °C in nontransduced and EGFP- or hSVCT2wt-EYFP-overexpressing neurons. (<b>C</b>) Immunofluorescence analysis with an anti-MAP2 antibody (Cy3, red channel) in EGFP- or hSVCT2wt-EYFP- overexpressing neurons (green channel). Both lentiviruses transduced MAP-positive cells; however, SVCT2 overexpression increased the number of neuronal processes in vitro (arrows). (<b>D</b>,<b>F</b>) SVCT2 overexpression in Neuro2a cells analyzed by confocal and SIM superresolution microscopy. hSVCT2-EYFP lentivirus expression (green channel) and anti-SVCT2 detection (red channel). Overexpressed SVCT2 colocalized with anti-SVCT2 antibodies (yellow in merge image) and induced neurite-like processes (arrows). After 72 h of SVCT2 expression, neurites were clearly observed in transduced cells (<b>E</b>). (<b>G</b>–<b>N</b>) SVCT2 overexpression in HSVT-C3 cells. (<b>G</b>) Uptake of 100 μM AA was analyzed in the presence of NaCl or choline at 37 °C in nontransduced and EGFP- or hSVCT2wt-EYFP-overexpressing HSVT-C3 cells. (<b>H</b>) Consecutive z-planes of C3 cells overexpressing SVCT2. The overexpressed protein appeared to be transported in vesicle-like structures (arrows) that fused to the cell membrane and reached the thin filopodia processes (<b>I</b> and inset). (<b>J</b>) The intracellular vesicles had partial colocalization with the RER marker (calreticulin-KDEL-RFP bacculovirus, red-channel) (<b>J</b> and inset); however, the filopodia and bleb-like and ruffes-like structures were positive for phalloidin (<b>K</b>). (<b>L</b>–<b>M</b>) RER (RE-RFP+) and SVCT2-EYFP localization to analyze the size distribution of multivesicular structures (zoom), quantified in the (<b>M</b>) graph. (<b>N</b>) Distribution of mitochondria (Mitotracker-positive) and SVCT2-positive cell structures, where the absence of colocalization was observed. The data represent the means ± SD of three experiments. *** <i>p</i> < 0.001, ** <i>p</i> < 0.01, ns = not significant. Scale bars in (<b>C</b>), 20 μm; in (<b>D</b>,<b>E</b>), 15 μm; in (<b>F</b>,<b>K</b>), 10 μm; in (<b>H</b>), 1 μm; in (<b>I</b>–<b>J</b>,<b>L</b>,<b>N</b>), 5 μm.</div>
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<div class="figure-caption-contents"><p> SVCT2 overexpression in cortical neurons promoted arborization and synaptic gene expression. ( <b> A… </b> </p></div>
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<div class="figure-caption-contents">SVCT2 overexpression in cortical neurons promoted arborization and synaptic gene expression. (<b>A</b>,<b>B</b>) Cortical neurons overexpressing hSVCT2wt-EYFP-A or EGFP-B for 24, 48 and 72 h in vitro. Some cellular processes were indicated with arrows. (<b>C</b>,<b>D</b>) Comparative images between EGFP- or hSVCT2wt-EYFP-overexpressing cortical neurons at 96 h, respectively. (<b>E</b>,<b>F</b>) Representation and Sholl analysis of EGFP- or hSVCT2wt-EYFP-overexpressing cortical neurons at 48 h, applying digitally concentric rings spaced 10 µm apart centered on the soma center to a radius of 100 µm. (<b>G</b>) Sholl analysis plot of EGFP- or hSVCT2wt-EYFP-overexpressing cortical neurons at 48 h. (<b>H</b>–<b>J</b>) QRT-PCR analysis of the alpha-synuclein, rabphilin 3 and synaptotagmin VII mRNA levels in samples isolated from EGFP- or hSVCT2wt-EYFP-overexpressing cortical neurons at 48 h. ** <i>p</i> < 0.01, *** <i>p</i> < 0.001. Results are mRNA levels relative to GAPDH and represent the mean ± SD for three independent experiments. (<b>K</b>,<b>L</b>) Confocal microscopy (<b>K</b>) or superresolution analysis (<b>L</b>) of neurons transduced with hSVCT2-EYFP lentivirus and incubated with anti-MAP1B. (<b>M</b>,<b>N</b>) 3D reconstruction and rendering of the green channel using Imaris 7.4 software (Bitplane) in Z-stack of SIM superresolution images. The presence of numerous dendritic spines of the mushroom type (arrows and asterisk) and thin dendritic spines (arrowheads) was observed (<b>Q</b>–<b>S</b>). (<b>O</b>,<b>P</b>) Confocal microscopy (<b>O</b>) or superresolution analysis (<b>P</b>) of neurons transduced with EGFP-lentivirus and incubated with anti-MAP1B antibodies. Neurites without thin dendritic spines (arrows) were observed. The data represent the means ± SD of three experiments. *** <i>p</i> < 0.001, ** <i>p</i> < 0.01. Scale bars in (<b>A</b>,<b>B</b>), 21 μm; in (<b>C</b>,<b>D</b>), 45 μm; In (<b>K</b>,<b>M</b>,<b>O</b>,<b>Q</b>), 10 μm; in (<b>L</b>,<b>M</b>,<b>P</b>), 5 μm; and (<b>R</b>,<b>S</b>), 2 μm.</div>
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<div class="figure-caption-contents"><p> SVCT2 neuronal clusters are co-distributed… </p></div>
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<p> Figure 3 </p>
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<div class="figure-caption-contents"><p> SVCT2 neuronal clusters are co-distributed with post-synaptic protein. ( <b> A </b> – <b> D </b> )… </p></div>
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Figure 3
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<div class="figure-caption-contents">SVCT2 neuronal clusters are co-distributed with post-synaptic protein. (<b>A</b>–<b>D</b>) SIM Super-Resolution and Wide Field analysis of hSVCT2-EYFP cluster distribution and size in transduced neurons. (<b>E</b>–<b>L</b>) SIM Superresolution analysis to detect the colocalization between the green processes of neurons transduced with EGFP (<b>K</b>,<b>L</b>) or hSVCT2wt-EYFP (<b>E</b>–<b>J</b>) lentivirus and the piccolo presynaptic protein (red) (<b>F</b>–<b>J</b>) in cultures transduced for 48 h. (<b>M</b>–<b>T</b>) SIM Superresolution analysis to detect the colocalization between the green processes of neurons transduced with EGFP (<b>S</b>,<b>T</b>) or hSVCT2wt-EYFP (<b>M</b>–<b>R</b>) lentivirus and the PSD95 post-synaptic protein (red) (<b>O</b>–<b>R</b>) in cultures transduced for 48 h. Processes that overexpressed SVCT2 were also positive for PSD95 and in close proximity with piccolo-positive contacts (arrowheads). SVCT2 clustering on the plasma membranes was observed (arrows). (<b>S</b>,<b>T</b>) SIM Superresolution analysis to detect the colocalization between the green processes of neurons transduced with EGFP and PSD95 protein (red). Scale bars in (<b>B</b>,<b>C</b>,<b>F</b>–<b>J</b>,<b>L</b>–<b>N</b>,<b>P</b>,<b>S</b>,<b>T</b>), 0.5 μm; (<b>E</b>,<b>K</b>), 10 μm.</div>
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<p> Figure 4 </p>
|
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<div class="figure-caption-contents"><p> Astrocyte-like cells induced vitamin C… </p></div>
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<p> Figure 4 </p>
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<div class="figure-caption-contents"><p> Astrocyte-like cells induced vitamin C recycling and maintain neurite processes in neurons overexpressing… </p></div>
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Figure 4
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<div class="figure-caption-contents">Astrocyte-like cells induced vitamin C recycling and maintain neurite processes in neurons overexpressing SVCT2 and treated with ascorbic acid. (<b>A</b>–<b>D</b>) Confocal microscopy analysis of hSVCT2wt-EYFP- or EGFP- overexpressing cortical neurons transduced for 48 h in vitro and incubated with anti-tubulin BIII (red). The cells were cultured in the absence or presence of ascorbic acid (AA). (<b>A</b>) EGFP-overexpressing cortical neurons treated with AA. (<b>B</b>) hSVCT2wt-EYFP-overexpressing cortical neurons. (<b>C</b>) hSVCT2wt-EYFP- overexpressing cortical neurons treated with AA. (<b>D</b>) hSVCT2wt-EYFP- overexpressing cortical neurons treated with AA and incubated with astrocytes-like cells (U87, recycling cells). (<b>E</b>) Scheme of the experimental procedure of co-culture between neurons and astrocytes. (<b>F</b>) Neurons cultured in different conditions. Quantification analysis of neurons with processes. The data represent the means ± SD of three experiments. *** <i>p</i> < 0.001. Scale bars in (<b>A</b>–<b>D</b>), 25 μm.</div>
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<p> Figure 5 </p>
|
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<div class="figure-caption-contents"><p> Co-culture of neurosp heres and… </p></div>
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<p> Figure 5 </p>
|
||
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|
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<div class="figure-caption-contents"><p> Co-culture of neurosp heres and U87 cells, generation of neurites and effect of… </p></div>
|
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Figure 5
|
||
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||
|
||
<div class="figure-caption-contents">Co-culture of neurosp heres and U87 cells, generation of neurites and effect of the GLUT1 inhibitor, WZB117, on DHA recycling and neurite outgrowth. (<b>A</b>–<b>D</b>) Immunocytochemical analysis using anti- βIII tubulin (green) and Hoechst for nuclear staining (blue). (<b>A</b>) neurospheres and U87 co-cultured cells treated with 100 µM AA for 72 h. (<b>B</b>) Magnified image, highlighting the presence of long neuritic processes (Inset). (<b>C</b>) Neurospheres and U87 co-cultured cells treated with 100 µM AA for 72 h and incubated with 5 µM WZB117 for 24 and 48 h. (<b>D</b>). Magnified image, where short neuritic processes (Inset, arrow heads) or their absence (Inset, long arrow) were observed. (<b>E</b>) Quantification of the percentage of neurospheres with neurites, treated with WZB117 or incubated with DMSO. (<b>F</b>) SytoxGreen detection by IncuCyte<sup>®</sup> analysis to determine cell viability (<i>n</i> = 3). Scale bar; 20 µm. Statistical analysis ANOVA, followed by Tukey posttest. *** <i>p</i> < 0.001. Bar graphs represent mean + SEM. In total, 45–50 neurospheres were quantified by condition. Scale bars, in (<b>A</b>,<b>C</b>), 200 µm; in (<b>B</b>,<b>D</b>), 50 µm; in insets, 20 µm.</div>
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|
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<p> Figure 6 </p>
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> Viability analysis in U87 cells,… </p></div>
|
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|
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|
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<p> Figure 6 </p>
|
||
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|
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|
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|
||
|
||
<div class="figure-caption-contents"><p> Viability analysis in U87 cells, astrocytes and neurons treated with WZB117, a GLUT1… </p></div>
|
||
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Figure 6
|
||
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||
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||
<div class="figure-caption-contents">Viability analysis in U87 cells, astrocytes and neurons treated with WZB117, a GLUT1 inhibitor. (<b>A</b>,<b>B</b>) Cell viability analysis using the XTT method in U87 cells and astrocytes exposed to 5 or 10 µM WZB117 or DMSO. The analyses were carried out after 24 h of incubation with WZB117. (<b>C</b>) Viability analysis using the XTT method in 7 DIV cortical neurons incubated with 25 mM glucose (control), without glucose and lactate (−Glu/−Lac) or without glucose and 5 mM lactate (−Glu/+Lac) for 24 h. (<b>D</b>) Viability analysis performed on cortical neurons treated with 10 µM WZB117 or DMSO for 24 h. Statistical analysis ANOVA, followed by Tukey test. ** <i>p</i> < 0.01; *** <i>p</i> < 0.001. The data represent the means ± SEM of three experiments.</div>
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<p> Figure 7 </p>
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<div class="figure-caption-contents"><p> Golgi–Cox impregnation and confocal-reflection microscopy… </p></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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<div class="figure-caption-contents"><p> Golgi–Cox impregnation and confocal-reflection microscopy in postnatal rat cerebral cortex injected with lentivirus-EGFP… </p></div>
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Figure 7
|
||
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|
||
<div class="figure-caption-contents">Golgi–Cox impregnation and confocal-reflection microscopy in postnatal rat cerebral cortex injected with lentivirus-EGFP and treated with WZB117. (<b>A</b>) Optic microscopy analysis of the outer cerebral cortex in 8 days of postnatal development rat brain after URG impregnation. (<b>B</b>) Confocal reflection microscopy (CRM) and 3D-Z-stack analysis of neuronal morphology of URG-impregnated neuronal cells. (<b>C</b>,<b>E</b>) Control cerebral cortex with URG-impregnation and CRM (<b>C</b>,<b>E</b> and inset). (<b>D</b>,<b>F</b>) Cerebral cortex treated with WZB117 and lentivirus-EGFP (depicted area in <b>D</b>) for 72 h and analyzed with URG-impregnation and CRM (<b>D</b>,<b>F</b> and inset). Neuronal neurites were analyzed with Z-stack-3D (Insets and arrows head). (<b>G</b>,<b>H</b>) Control rat brain (<b>G</b>) from 8 days of postnatal development or injected with 10 µM WZB117 for 72 h (<b>H</b>, arrows head) analyzed with impregnation with Golgi–Cox and Tile-scan reconstruction. (<b>I</b>) Brightfield microscopy analysis mixed with an epifluorescence image in the same area injected with lentivirus-EGFP and WZB117 (I. Z and depicted zone). The brain area most distant from the injection site was called E. Z. (<b>J</b>) Representative image of neurons present in the E. Z. (<b>K</b>) Representative image of neurons present in the I. Z. (<b>L</b>) Quantification of the total length of neurites quantified in neurons analyzed in the E. Z and I. Z. (<b>M</b>) Comparative analysis of the number of neurites quantified per neuron in the E. Z and I. Z. (<b>N</b>,<b>O</b>) Frequency graph of the number of neurites in the I. Z. and E. Z, respectively. Statistical analysis t-student (*** <i>p</i> < 0.001). Graph shows mean + SEM. In total, 30–40 neurons were quantified per area. Scale bars, in A, 500 µm; in (<b>B</b>), 15 µm; in (<b>C</b>,<b>D</b>), 250 µm; in (<b>E</b>,<b>F</b>), 150 µm; in (<b>G</b>,<b>H</b>), 1 mm; in I, 100 µm; in (<b>J</b>,<b>K</b>), 30 µm.</div>
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Oyarce K., Silva-Alvarez C., Ferrada L., Martinez F., Salazar K., Nualart F. SVCT2 Is Expressed by Cerebellar Precursor Cells, Which Differentiate into Neurons in Response to Ascorbic Acid. Mol. Neurobiol. 2018;55:1136–1149. doi: 10.1007/s12035-016-0366-5.
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Silva-Alvarez C., Salazar K., Cisternas P., Martinez F., Liour S., Jara N., Bertinat R., Nualart F. Apical Polarization of SVCT2 in Apical Radial Glial Cells and Progenitors During Brain Development. Mol. Neurobiol. 2017;54:5449–5467. doi: 10.1007/s12035-016-0081-2.
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Salazar K., Martinez M., Ulloa V., Bertinat R., Martinez F., Jara N., Espinoza F., Bongarzone E.R., Nualart F. SVCT2 Overexpression in Neuroblastoma Cells Induces Cellular Branching that is Associated with ERK Signaling. Mol. Neurobiol. 2016;53:6668–6679. doi: 10.1007/s12035-015-9553-z.
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Pastor P., Cisternas P., Salazar K., Silva-Alvarez C., Oyarce K., Jara N., Espinoza F., Martinez A.D., Nualart F. SVCT2 vitamin C transporter expression in progenitor cells of the postnatal neurogenic niche. Front. Cell. Neurosci. 2013;7:119. doi: 10.3389/fncel.2013.00119.
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