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data-ga-category="featured_link"
|
||
data-ga-action="clipboard">
|
||
Clipboard <span class="amount-in-clipboard"></span>
|
||
</a>
|
||
</div>
|
||
|
||
<span class="search-input-link user-guide-link" role="navigation" aria-label="User guide">
|
||
<a href="/help/"
|
||
data-ga-category="featured_link"
|
||
data-ga-action="user_guide">
|
||
User Guide
|
||
</a>
|
||
</span>
|
||
|
||
</div>
|
||
</div>
|
||
|
||
|
||
</form>
|
||
|
||
|
||
<div id="article-page-header">
|
||
<div id="article-top-actions-bar" class="article-top-actions-bar">
|
||
<div class="inner-wrap">
|
||
<div class="actions-container">
|
||
<div class="return-to-search">
|
||
|
||
|
||
</div>
|
||
|
||
<div class="multiple-results-actions " role="region" aria-label="save, email, send to">
|
||
<button id="save-results-panel-trigger"
|
||
type="button"
|
||
class="save-results save-results-panel-trigger"
|
||
aria-expanded="false"
|
||
aria-controls="save-action-panel"
|
||
data-ga-category="save_share"
|
||
data-ga-action="save"
|
||
data-ga-label="open">
|
||
Save
|
||
</button><button id="email-results-panel-trigger"
|
||
type="button"
|
||
class="email-results email-results-panel-trigger"
|
||
aria-expanded="false"
|
||
aria-controls="email-action-panel"
|
||
data-ga-category="save_share"
|
||
data-ga-action="email"
|
||
data-ga-label="open">
|
||
Email
|
||
</button><div class="more-actions dropdown-block"><button id="more-actions-trigger"
|
||
type="button"
|
||
class="trigger more-actions-trigger"
|
||
ref="linksrc=show_moreactions_btn"
|
||
aria-label="Send to"
|
||
aria-controls="more-actions-dropdown">Send to</button><div id="more-actions-dropdown" class="dropdown dropdown-container" hidden><div class="content"><ul class="more-actions-links"><li><a class="clipboard-panel-trigger dropdown-block-link "
|
||
href="#"
|
||
role="button"
|
||
data-ga-category="save_share"
|
||
data-ga-action="clipboard"
|
||
data-ga-label="send">
|
||
Clipboard
|
||
</a></li><li><a role="button" class="dropdown-block-link bibliography-trigger-target" href="https://account.ncbi.nlm.nih.gov/?back_url=https%3A%2F%2Fpubmed.ncbi.nlm.nih.gov%2F31743734%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%2F31743734%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="LVL4ZTWBVPJ4WQExN3W10ydbxDl3ClaN2Iv9CJpXvqwyQhKnqmz3uGJP5H3fvWI7">
|
||
</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="LVL4ZTWBVPJ4WQExN3W10ydbxDl3ClaN2Iv9CJpXvqwyQhKnqmz3uGJP5H3fvWI7">
|
||
|
||
|
||
|
||
<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="LVL4ZTWBVPJ4WQExN3W10ydbxDl3ClaN2Iv9CJpXvqwyQhKnqmz3uGJP5H3fvWI7">
|
||
|
||
<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: 31743734 - PubMed</span>
|
||
<input type="hidden" name="email-subject" value="1 selected item: 31743734"/>
|
||
<input type="hidden" name="email-subject-hash" value="f8ac7264253848cb31dfbb4c7c74087b5143e950f49f498ea286f1ba5f02e295"/>
|
||
</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="LVL4ZTWBVPJ4WQExN3W10ydbxDl3ClaN2Iv9CJpXvqwyQhKnqmz3uGJP5H3fvWI7">
|
||
|
||
|
||
|
||
<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="LVL4ZTWBVPJ4WQExN3W10ydbxDl3ClaN2Iv9CJpXvqwyQhKnqmz3uGJP5H3fvWI7">
|
||
|
||
|
||
|
||
<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="LVL4ZTWBVPJ4WQExN3W10ydbxDl3ClaN2Iv9CJpXvqwyQhKnqmz3uGJP5H3fvWI7">
|
||
|
||
<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="LVL4ZTWBVPJ4WQExN3W10ydbxDl3ClaN2Iv9CJpXvqwyQhKnqmz3uGJP5H3fvWI7">
|
||
|
||
|
||
|
||
<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="LVL4ZTWBVPJ4WQExN3W10ydbxDl3ClaN2Iv9CJpXvqwyQhKnqmz3uGJP5H3fvWI7">
|
||
|
||
<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="31743734">
|
||
<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://linkinghub.elsevier.com/retrieve/pii/S0016-5085(19)41574-6"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=False&PrId=3048&itool=Abstract-def&log$=linkouticon&uid=31743734&db=pubmed&nlmid=0374630"
|
||
title="See full text options at Elsevier Science"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="Elsevier Science"
|
||
data-ga-label="31743734"
|
||
><img src="https://cdn.ncbi.nlm.nih.gov/corehtml/query/egifs/https:--linkinghub.elsevier.com-ihub-images-elsevieroa.png" alt="Elsevier Science full text link"><span class="text">
|
||
|
||
Elsevier Science
|
||
|
||
</span></a><a class="link-item
|
||
pmc
|
||
"
|
||
href="https://pmc.ncbi.nlm.nih.gov/articles/pmid/31743734/"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=True&PrId=3494&itool=Abstract-def&log$=linkouticon&uid=31743734&db=pubmed&nlmid=0374630"
|
||
title="Free full text at PubMed Central"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="PMC"
|
||
data-ga-label="31743734"
|
||
><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="/31743734/citations/"
|
||
data-citation-style="nlm"
|
||
data-pubmed-format-link="/31743734/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="31743734" 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%2F31743734%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="LVL4ZTWBVPJ4WQExN3W10ydbxDl3ClaN2Iv9CJpXvqwyQhKnqmz3uGJP5H3fvWI7"><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"
|
||
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Drug Screen Identifies Leflunomide for Treatment of Inflammatory Bowel Disease Caused by TTC7A Deficiency
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<h1 class="heading-title">
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Drug Screen Identifies Leflunomide for Treatment of Inflammatory Bowel Disease Caused by TTC7A Deficiency
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<span class="authors-list-item "><span class="full-name">Sasha Jardine</span><span class="citation-separator"> et al.</span></span>
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data-ga-label="Aleixo M Muise">Aleixo M Muise</a><sup class="affiliation-links"><span class="author-sup-separator"> </span><a class="affiliation-link" title="SickKids Inflammatory Bowel Disease Centre, The Hospital for Sick Children, Toronto, Ontario, Canada; Cell Biology Program, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada; Department of Pediatrics, Institute of Medical Science and Biochemistry, University of Toronto, The Hospital for Sick Children, Toronto, Ontario, Canada. Electronic address: aleixo.muise@utoronto.ca." href="#short-view-affiliation-8" ref="linksrc=author_aff">
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<li data-affiliation-id="short-view-affiliation-2"
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id="short-view-affiliation-2"
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><sup class="key">2</sup> Division of Gastroenterology, Hepatology and Nutrition, Boston Children's Hospital, Boston, Massachusetts; Harvard Medical School, Boston, Massachusetts.</li>
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<li data-affiliation-id="short-view-affiliation-3"
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id="short-view-affiliation-3"
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><sup class="key">3</sup> Division of Pathology, The Hospital for Sick Children, Toronto, Ontario, Canada.</li>
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<li data-affiliation-id="short-view-affiliation-4"
|
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id="short-view-affiliation-4"
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><sup class="key">4</sup> Dr von Hauner Children's Hospital, Department of Pediatrics, University Hospital, Ludwig Maximilian University Munich, Munich, Germany.</li>
|
||
|
||
<li data-affiliation-id="short-view-affiliation-5"
|
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id="short-view-affiliation-5"
|
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><sup class="key">5</sup> Division of Neurology, and Genetics and Genome Biology Program, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada; Molecular Medicine Program, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada.</li>
|
||
|
||
<li data-affiliation-id="short-view-affiliation-6"
|
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id="short-view-affiliation-6"
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><sup class="key">6</sup> Molecular Medicine Program, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada.</li>
|
||
|
||
<li data-affiliation-id="short-view-affiliation-7"
|
||
id="short-view-affiliation-7"
|
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><sup class="key">7</sup> Division of Gastroenterology, Hepatology and Nutrition, Boston Children's Hospital, Boston, Massachusetts; Harvard Medical School, Boston, Massachusetts; Division of Gastroenterology, Brigham and Women's Hospital, Boston, Massachusetts.</li>
|
||
|
||
<li data-affiliation-id="short-view-affiliation-8"
|
||
id="short-view-affiliation-8"
|
||
><sup class="key">8</sup> SickKids Inflammatory Bowel Disease Centre, The Hospital for Sick Children, Toronto, Ontario, Canada; Cell Biology Program, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada; Department of Pediatrics, Institute of Medical Science and Biochemistry, University of Toronto, The Hospital for Sick Children, Toronto, Ontario, Canada. Electronic address: aleixo.muise@utoronto.ca.</li>
|
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<strong class="current-id" title="PubMed ID">31743734</strong>
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PMCID:
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PMC7062591
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DOI:
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10.1053/j.gastro.2019.11.019
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<p>
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|
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<strong class="sub-title">
|
||
Background & aims:
|
||
</strong>
|
||
|
||
Mutations in the tetratricopeptide repeat domain 7A gene (TTC7A) cause intestinal epithelial and immune defects. Patients can become immune deficient and develop apoptotic enterocolitis, multiple intestinal atresia, and recurrent intestinal stenosis. The intestinal disease in patients with TTC7A deficiency is severe and untreatable, and it recurs despite resection or allogeneic hematopoietic stem cell transplant. We screened drugs for those that prevent apoptosis of in cells with TTC7A deficiency and tested their effects in an animal model of the disease.
|
||
</p>
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|
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|
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<strong class="sub-title">
|
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Methods:
|
||
</strong>
|
||
|
||
We developed a high-throughput screen to identify compounds approved by the US Food and Drug Administration that reduce activity of caspases 3 and 7 in TTC7A-knockout (TTC7A-KO) HAP1 (human haploid) cells and reduce the susceptibility to apoptosis. We validated the effects of identified agents in HeLa cells that stably express TTC7A with point mutations found in patients. Signaling pathways in cells were analyzed by immunoblots. We tested the effects of identified agents in zebrafish with disruption of ttc7a, which develop intestinal defects, and colonoids derived from biopsy samples of patients with and without mutations in TTC7A. We performed real-time imaging of intestinal peristalsis in zebrafish and histologic analyses of intestinal tissues from patients and zebrafish. Colonoids were analyzed by immunofluorescence and for ion transport.
|
||
</p>
|
||
|
||
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<p>
|
||
|
||
<strong class="sub-title">
|
||
Results:
|
||
</strong>
|
||
|
||
TTC7A-KO HAP1 cells have abnormal morphology and undergo apoptosis, due to increased levels of active caspases 3 and 7. We identified drugs that increased cell viability; leflunomide (used to treat patients with inflammatory conditions) reduced caspase 3 and 7 activity in cells by 96%. TTC7A-KO cells contained cleaved caspase 3 and had reduced levels of phosphorylated AKT and X-linked inhibitor of apoptosis (XIAP); incubation of these cells with leflunomide increased levels of phosphorylated AKT and XIAP and reduced levels of cleaved caspase 3. Administration of leflunomide to ttc7a<sup>-/-</sup> zebrafish increased gut motility, reduced intestinal tract narrowing, increased intestinal cell survival, increased sizes of intestinal luminal spaces, and restored villi and goblet cell morphology. Exposure of patient-derived colonoids to leflunomide increased cell survival, polarity, and transport function.
|
||
</p>
|
||
|
||
|
||
|
||
|
||
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||
|
||
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||
|
||
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||
|
||
<p>
|
||
|
||
<strong class="sub-title">
|
||
Conclusions:
|
||
</strong>
|
||
|
||
In a drug screen, we identified leflunomide as an agent that reduces apoptosis and activates AKT signaling in TTC7A-KO cells. In zebrafish with disruption of ttc7a, leflunomide restores gut motility, reduces intestinal tract narrowing, and increases intestinal cell survival. This drug might be repurposed for treatment of TTC7A deficiency.
|
||
</p>
|
||
|
||
|
||
|
||
|
||
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||
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</div>
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||
<p>
|
||
|
||
<strong class="sub-title">
|
||
Keywords:
|
||
</strong>
|
||
|
||
Animal Model; Cell Death; Genetic; Monogenic IBD.
|
||
</p>
|
||
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<p class="copyright" id="copyright">
|
||
Copyright © 2020 AGA Institute. Published by Elsevier Inc. All rights reserved.
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</p>
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<p class="disclaimer" id="disclaimer">
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<a href="/disclaimer/" target="_blank" data-ga-category="literature_resources"
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data-ga-action="disclaimer_link" data-ga-label="under_abstract">PubMed Disclaimer</a>
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<div class="conflict-of-interest" id="conflict-of-interest">
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||
<h2 class="title">
|
||
Conflict of interest statement
|
||
</h2>
|
||
|
||
<div class="statement">
|
||
|
||
|
||
|
||
<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">Competing interests.</p>
|
||
|
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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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</div>
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<div class="figures" id="figures">
|
||
<h2 class="title">
|
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Figures
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</h2>
|
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|
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<div class="figures-list" id="slides-container"
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itemscope itemtype="http://schema.org/ImageGallery">
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<figure class="figure-item "
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itemscope itemtype="http://schema.org/ImageObject"
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data-slide-index="0"
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role="button"
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data-image-width="800"
|
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data-image-height="486"
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data-image-alt="Figure 1."
|
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data-pmc-id="PMC7062591"
|
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data-figure-id="F1">
|
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<img class="figure-thumb" itemprop="thumbnail"
|
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id="article-image-0"
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/153a/7062591/b741749d6efa/nihms-1543536-f0018.gif"
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alt="Figure 1." />
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</a>
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<meta itemprop="width" itemtype="http://schema.org/ImageObject" content="800">
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<meta itemprop="height" itemtype="http://schema.org/ImageObject" content="486">
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<div class="caption-wrap">
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 1.. TTC7A-KO cells have an increased… </p>
|
||
</strong>
|
||
|
||
|
||
|
||
|
||
|
||
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|
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|
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|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 1.. TTC7A-KO cells have an increased susceptibility for apoptosis. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> ( <i> A </i> ) Morphology of… </p></div>
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Figure 1.. TTC7A-KO cells have an increased susceptibility for apoptosis.
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<div class="figure-caption-contents">(<i>A</i>) Morphology of WT and TTC7A-KO HAP1 cells, DIC microscopy. Left panels, objective magnification 63× (scale bar 10μm). Right panels, objective magnification 4× (scale bar 190μm). Blebs and filopodia-like processes are indicated by arrow and arrowhead, respectively. Dashed-bars highlight differences in colony sizes after 48 h of culturing. (<i>B</i>) Real-time viability assay. Two-way ANOVA with post hoc test (Sidak), ****p<0.0001, (n=3, 3 replicates). (<i>C</i>) Annexin V-FITC/PI flow cytometry demonstrated that TTC7A-KO have significantly increased Annexin-V staining. Data is quantified in Supplementary Figure 2<i>B</i>. (<i>D</i>) Western blot analysis of untreated and IFNγ (10 ng/ml)//TNFα-treated (30 ng/ml) WT and TTC7A-KO cells, 48 h (n=3). Refer to Supplementary Figure 2C for cleaved Caspase 3 (CC3) quantitation.</div>
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<p> Figure 2.. High-throughput drug screening identifies approved-compounds… </p>
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<p> Figure 2.. High-throughput drug screening identifies approved-compounds that improve the apoptotic phenotype. </p>
|
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<div class="figure-caption-contents"><i> (A) </i> Modeling the…</div>
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Figure 2.. High-throughput drug screening identifies approved-compounds that improve the apoptotic phenotype.
|
||
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|
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|
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|
||
<div class="figure-caption-contents"><i>(A)</i> Modeling the high-throughput apoptosis-phenotype assay. Caspase-Glo® 3/7 assay, z’=0.54, data are presented as the mean ±SD. Unpaired t test, ****p<0.0001, (n=3, 8 replicates). <i>(B)</i> Drug screen workflow. See Methods. <i>(C)</i> A sample of plate-results from the Prestwick Chemical Library screen showing mean Caspase 3/7 activity from drug-treated wells (green dots) and DMSO-treated control wells, WT (light blue dashes) and TTC7A-KO cells (dark blue dashes). Tiabendazole and tiaprofenic acid reduced Caspase 3/7 activity below the hit threshold (μ<sub>WT</sub>-3σ), z’= 0.56. <i>(D)</i> Drug screen summary, 0.4% hit rate. Hit compounds represent the 10 drug classification families shown. <i>(E)</i> Comparison of hit compound inhibition of apoptosis in TTC7A-KO cells. Black borders represent FDA-approved drugs and bar colors correspond to Figure 2D. <i>(F)</i> Concentration-response curve for leflunomide inhibition of Caspase 3/7 activity in HAP1 TTC7A-KO cells, IC<sub>50</sub>=1.1 μM, (n=3). (<i>G</i>) Colony size formation in WT, TTC7A-KO, and drug-treated TTC7A-KO cells. Drug abbreviations: cyanocobalamin (CYANO), leflunomide (LEF), tiaprofenic acid (TIA), fenbufen (FEN), and fasudil (FAS). Plotted values represent individual cell colonies, error bars presented as mean ±SD. Statistical significance was relative to the KO/DMSO control. One-way ANOVA with post hoc test (Dunnett), ****p<0.0001, ***p<0.001, **p<0.01, (n=3, 6 replicates per condition). (<i>H</i>) Viability assay. Statistical significance relative to KO/DMSO (blue). WT (*p<0.05), KO/LEF (**p<0.01), KO/TIA (****p<0.0001), KO/FEN (***p<0.001), KO/FAS (****p<0.0001), two-way ANOVA with post hoc test (Dunnett), (n=3, 4 replicates per condition).</div>
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<p> Figure 3.. Leflunomide rescues abnormal intestinal features… </p>
|
||
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|
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<strong class="figure-label">
|
||
<p> Figure 3.. Leflunomide rescues abnormal intestinal features in <i> ttc7a </i> <sup> <i> −/− </i> </sup> zebrafish. </p>
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><i> (A) </i> Histology from <i> ttc7a… </i></div>
|
||
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<strong class="figure-label">
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Figure 3.. Leflunomide rescues abnormal intestinal features in <i>ttc7a</i> <sup><i>−/−</i></sup> zebrafish.
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><i>(A)</i> Histology from <i>ttc7a</i>
|
||
<sup>−/−</sup> zebrafish (7 dpf) reveals pathological intestinal phenotypes. Control <b>(</b><i>ttc7a</i>
|
||
<sup>+/−</sup>) zebrafish display open luminal spaces with discernible villi projections (grey arrowhead), clefts (black arrowhead), monolayer epithelium (dotted-outlined area), and mature goblet cells with large vesicles (black arrows). <i>ttc7a</i>
|
||
<sup>−/−</sup> zebrafish display narrowing of the intestinal bulb, stratified epithelium (yellow dotted-outlined area), signs of apoptosis (yellow arrows), and goblet cells with numerous small vesicles (yellow boxes). Objective magnification 10× and 40× for insets (scale bar 100 μm, inset scale bar 50 μm), (<i>ttc7a</i>
|
||
<sup>+/−</sup> n=14, <i>ttc7a</i>
|
||
<sup>−/−</sup> n=11). <i>(B)</i> Incidence of the narrow gut phenotype in DMSO and LEF treated fish. One-way ANOVA with post hoc test (Fisher’s LSD), ****p<0.0001, <i>ttc7a</i>
|
||
<sup>+/−</sup> (DMSO n=49, LEF n=12), <i>ttc7a</i>
|
||
<sup>−/−</sup> (DMSO n= 36, LEF n=26). <i>(C)</i> Intestinal histology from treated (see Methods) <i>ttc7a</i><sup>−/−</sup> zebrafish. Leflunomide, cyanocobalamin and tiaprofenic acid suppressed the narrow-gut phenotype with minimal enterocyte crowding. Objective magnification 10×, (scale bar 100 μm). <i>ttc7a</i><sup>+/−</sup> (DMSO n=49) <i>ttc7a</i><sup>−/−</sup> (DMSO n= 36, CYANO n=10, LEF n=26, TIA n= 13, FEN n=13. <i>(D)</i> Assessment of apoptosis. DMSO or leflunomide treatment. <i>ttc7a</i><sup>−/−</sup> zebrafish display fragmented, condensed or engulfed nuclei in the epithelium (arrows). Leflunomide treatment resulted in diminished signs of apoptosis, reduced intestinal epithelial cell crowding, and overall improved epithelium architecture in <i>ttc7a</i><sup>−/−</sup> zebrafish. Refer to Supplementary Figure 7A for the quantitation of apoptotic cells/sample. Objective magnification 70× (scale bar 20 μm), (n=6 per group, across 3 experimental clutches). <i>(E)</i> Staining of the intestinal lumen in control (<i>ttc7a</i><sup>+/−</sup>) and <i>ttc7a-</i>mutant (<i>ttc7a</i><sup>−/−</sup>) zebrafish. Images are from peristalsis assays (Supplementary Video 2): intestinal lumen marked green fluorescent stain (DCFH-DA). <i>ttc7a</i><sup>+/−</sup> fish have discernable villi (yellow arrow) and large continuous intestinal bulbs (double-headed white arrow). Representative <i>ttc7a</i>
|
||
<sup>−/−</sup> intestinal phenotypes (i) atresia point (white arrow heads) (ii) narrow intestinal lumen and (iii) obstruction interrupting the intestinal bulb (white arrow). Objective magnification 4×, (scale bar 100 μm). <i>(F)</i> Incidence of <i>ttc7a</i>-mutant phenotypes. <i>ttc7a</i><sup>−/−</sup> fish have significantly larger populations with motility and narrow lumen pathological phenotypes. Data are presented as the mean ±SD, one-way ANOVA with post hoc test (Fisher’s LSD), **p<0.0054, *p<0.0196, (n=50 total for each group, across 3 experimental clutches). <i>(G)</i> Phenotype summary from drug treated fish. <i>ttc7a</i>
|
||
<sup>−/−</sup> fish with aberrant motility and narrow lumen phenotypes were significantly reduced with cyanocobalamin, leflunomide, tiaprofenic acid, and fenbufen treatment (3–7 dpf). Data are presented as the mean ±SD. Statistical significance was relative to <i>ttc7a</i>
|
||
<sup>−/−</sup> DMSO control, and determined by two-way ANOVA with post hoc test (Dunnett), *p<0.05, **p<0.01, ***p<0.001, ns=not significant (DMSO n=18, CYANO n=21, LEF n=21, TIA n=17, FEN n=18, FAS n=13 for each group across 3 experimental clutches).</div>
|
||
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<p> Figure 4.. p-AKT is reduced in TTC7A-deficiency. </p>
|
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<p> Figure 4.. p-AKT is reduced in TTC7A-deficiency. </p>
|
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<div class="figure-caption-contents"><i> (A) </i> Histopathology analysis of p-AKT in human colon…</div>
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Figure 4.. p-AKT is reduced in TTC7A-deficiency.
|
||
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<div class="figure-caption-contents"><i>(A)</i> Histopathology analysis of p-AKT in human colon tissue. Co-staining of cytokeratin 20 (CK20), a marker for the intestinal epithelium, and p-AKT is present in the normal and IBD control, while p-AKT is diminished in TTC7A-deficiency patients. Patient 1 is the colonoid donor and Patient 2 is unpublished with confirmed biallelic mutations. RedDot 2 nuclear counterstain (blue). Sections were magnified at 20× objective. <i>(B)</i> Histopathology analysis of pan-AKT (total AKT) in human colon tissue. Biopsies are the same as described in Figure 5<i>A</i>. Pan-AKT is present in all samples albeit with reduced intensity in the TTC7A-deficiency patient samples. Sections were magnified at 20× objective. <i>(C)</i> Immunoblot for p-AKT, XIAP, and cleaved Caspase 3 in WT and TTC7A-KO cells. After 3 h leflunomide treatment in TTC7A-KO cells, p-AKT and XIAP protein levels are detectable, while cleaved Caspase 3 is diminished. DMSO (*) (n=3). <i>(D)</i> Densitometric analysis of p-AKT, XIAP, and cleaved Caspase 3 from WT and TTC7A-KO cells. One-way ANOVA with post hoc test (Tukey), *p<0.05, **p<0.01, ***p<0.001, ****p<0.0001, (n=3). <i>(E) ttc7a</i><sup><i>+/−</i></sup> and <i>ttc7a</i><sup><i>−/−</i></sup> whole mount zebrafish staining with p-AKT (red), Synaptic vesicle protein 2 (SV2) (green), and RedDot 2 nuclear counterstain (blue). SV2 staining, indicating neuromuscular junctions, is absent from the intestinal epithelial monolayer and aids in differentiating epithelial cells from other nearby cell types. In the DMSO treated panel, p-AKT staining (Ser473) in <i>ttc7a</i><sup><i>+/−</i></sup> fish is evident along the gastrointestinal tract, while absent in <i>ttc7a</i><sup><i>−/−</i></sup> fish. Leflunomide treatment (3–7 dpf) restores p-AKT staining in the intestinal epithelium of <i>ttc7a</i><sup><i>−/−</i></sup> fish. Fish were magnified at 5× objective, (n=4).</div>
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<p> Figure 5.. Leflunomide treatment enhances survival and… </p>
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<p> Figure 5.. Leflunomide treatment enhances survival and function of TTC7A-deficiency patient-colonoids. </p>
|
||
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|
||
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<div class="figure-caption-contents"><p> ( <i> A </i> ) Personalized… </p></div>
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<strong class="figure-label">
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Figure 5.. Leflunomide treatment enhances survival and function of TTC7A-deficiency patient-colonoids.
|
||
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|
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<div class="figure-caption-contents">(<i>A</i>) Personalized medicine approach to evaluate drug efficacy in human TTC7A-deficiency using patient-derived colonoids. Endoscopic biopsies were obtained from healthy control and TTC7A-deficiency (E71K and L304R compound heterozygous, TTC7A<sup>mut</sup>) patients and cultured into colonoids, which were then tested with leflunomide. (<i>B</i>) Leflunomide improves the survival of human colonoids derived from TTC7A-deficiency patients (TTC7A<sup>mut</sup>). Example images of control (TTC7A<sup>+/+</sup>) and TTC7A-deficient (TTC7A<sup>mut</sup>) colonoids with and without leflunomide (10 μM) treatment at 2 and 6 days and grown in the absence of ROCK inhibitor (Y27632). Red arrows indicate examples of dead colonoids. (<i>C</i>) Summary graph showing the percentage of dead TTC7A<sup>mut</sup> colonoids +/− leflunomide treatment. TTC7A<sup>mut</sup> and TTC7A<sup>+/+</sup> colonoids were cultured +/− ROCK inhibitor (Y27632) or with leflunomide and viability was assessed at day 2 and 6. TTC7A<sup>mut</sup> colonoids grown without ROCK inhibitor have significantly increased death, which is reversed following leflunomide treatment. One-way ANOVA with post-hoc test (Tukey-Kramer), *p<0.05. **p<0.01. (<i>D</i>) Immunofluorescence staining of TTC7A<sup>+/+</sup> and TTC7A<sup>mut</sup> colonoids with villin (green) marking the apical brush border and cytokeratin 20 (CK20, red) marking basal epithelial structure and DAPI (blue, nuclei). TTC7A<sup>+/+</sup> colonoids show normal polarity with defined basal CK20 staining. TTC7A<sup>mut</sup> colonoids treated with ROCK inhibitor show grossly normal staining with mild cytological atypia. TTC7A<sup>mut</sup> colonoids without ROCK inhibitor show normal sidedness but abnormal polarity with cytological atypia and basal structural abnormalities which is improved in leflunomide treated colonoids. Quantification of abnormal polarity as assessed by the presence of multiple lumens in colonoids. Percentage of colonoids with multiple lumens in TTC7A-deficient colonoids with and without leflunomide (10 μM). Healthy control colonoids did not have multiple lumens (data not shown). Two tailed t-test, *p<0.05. (<i>E-F</i>) TTC7A-deficient colonoids (TTC7A<sup>mut</sup>) have a reduced swelling response to forskolin stimulation. Example images showing reduced swelling in TTC7A<sup>mut</sup> compared to TTC7A<sup>mut</sup> treated with leflunomide (10 μM). Inset panel show magnified images with red arrows indicating example colonoids pre and post swelling. Summary data showing significantly increased swelling in leflunomide (10 μM) treated TTC7A<sup>mut</sup> colonoids. Two tailed t-test, **p<0.01.</div>
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<div class="figure-caption-contents"><p> ( <i> A </i> ) TTC7A-competent. 1,… </p></div>
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Figure 6.. Model of leflunomide’s mechanism of action in TTC7A-deficiency.
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<div class="figure-caption-contents">(<i>A</i>) TTC7A-competent. 1, TTC7A binds and recruits PI4KIIIα to the plasma membrane. 2, PI4KIIIα phosphorylates PI lipids to create PI4P, precursor to PI (4,5)P<sub>2</sub>/ PI(3,4,5)P<sub>3</sub>. 3, PI3K phosphorylates PI (4,5)P<sub>2</sub>, required for AKT phosphorylation. p-AKT activates multiple downstream substrates that promote cell survival. For example, XIAP polyubiquitylates Pro Caspases 3,7, and 9 for proteasomal degradation, thereby reducing the susceptibility for Caspase-dependent cell death. (<i>B</i>) TTC7A-deficiency + leflunomide. 1, PI4KIIIα trafficking to (or kinase activity at) the plasma membrane is compromised in TTC7A-deficiency resulting in reduced PI4P. 2, Reduced p-AKT provides a rationale for increases in apoptosis. 3, Caspase-dependent apoptosis is frequently associated with TTC7A-deficiency. 4, Leflunomide treatment increases p-AKT and XIAP levels. 5, The apoptotic phenotype is ameliorated when TTC7A-deficient HAP1 cells are treated with leflunomide, suggesting a shift toward a survival phenotype. 6, It has yet to be established how leflunomide mediates p-AKT activation, however, PI3K-inhibition with LY294002 hinders leflunomide’s effect on AKT, XIAP, and Caspase 3 cleavage.</div>
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Avitzur Y, Guo C, Mastropaolo LA, et al. Mutations in tetratricopeptide repeat domain 7A result in a severe form of very early onset inflammatory bowel disease. Gastroenterology 2014;146:1028–39.
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</a></li><li><a class="add-to-search-link dropdown-block-link"
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|
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<div id="mesh-terms" class="mesh-terms keywords-section">
|
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MeSH terms
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Adaptor Proteins, Signal Transducing / metabolism
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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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