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<span class="search-input-link user-guide-link" role="navigation" aria-label="User guide">
|
||
<a href="/help/"
|
||
data-ga-category="featured_link"
|
||
data-ga-action="user_guide">
|
||
User Guide
|
||
</a>
|
||
</span>
|
||
|
||
</div>
|
||
</div>
|
||
|
||
|
||
</form>
|
||
|
||
|
||
<div id="article-page-header">
|
||
<div id="article-top-actions-bar" class="article-top-actions-bar">
|
||
<div class="inner-wrap">
|
||
<div class="actions-container">
|
||
<div class="return-to-search">
|
||
|
||
|
||
</div>
|
||
|
||
<div class="multiple-results-actions " role="region" aria-label="save, email, send to">
|
||
<button id="save-results-panel-trigger"
|
||
type="button"
|
||
class="save-results save-results-panel-trigger"
|
||
aria-expanded="false"
|
||
aria-controls="save-action-panel"
|
||
data-ga-category="save_share"
|
||
data-ga-action="save"
|
||
data-ga-label="open">
|
||
Save
|
||
</button><button id="email-results-panel-trigger"
|
||
type="button"
|
||
class="email-results email-results-panel-trigger"
|
||
aria-expanded="false"
|
||
aria-controls="email-action-panel"
|
||
data-ga-category="save_share"
|
||
data-ga-action="email"
|
||
data-ga-label="open">
|
||
Email
|
||
</button><div class="more-actions dropdown-block"><button id="more-actions-trigger"
|
||
type="button"
|
||
class="trigger more-actions-trigger"
|
||
ref="linksrc=show_moreactions_btn"
|
||
aria-label="Send to"
|
||
aria-controls="more-actions-dropdown">Send to</button><div id="more-actions-dropdown" class="dropdown dropdown-container" hidden><div class="content"><ul class="more-actions-links"><li><a class="clipboard-panel-trigger dropdown-block-link "
|
||
href="#"
|
||
role="button"
|
||
data-ga-category="save_share"
|
||
data-ga-action="clipboard"
|
||
data-ga-label="send">
|
||
Clipboard
|
||
</a></li><li><a role="button" class="dropdown-block-link bibliography-trigger-target" href="https://account.ncbi.nlm.nih.gov/?back_url=https%3A%2F%2Fpubmed.ncbi.nlm.nih.gov%2F31522987%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%2F31522987%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="9f8bdPGVnAc52VUgUxnU6Mtnv6R1R3KGq2SgQF9hXbZzWm06xQ0WAUZ13azdKEi0">
|
||
</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="9f8bdPGVnAc52VUgUxnU6Mtnv6R1R3KGq2SgQF9hXbZzWm06xQ0WAUZ13azdKEi0">
|
||
|
||
|
||
|
||
<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="9f8bdPGVnAc52VUgUxnU6Mtnv6R1R3KGq2SgQF9hXbZzWm06xQ0WAUZ13azdKEi0">
|
||
|
||
<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: 31522987 - PubMed</span>
|
||
<input type="hidden" name="email-subject" value="1 selected item: 31522987"/>
|
||
<input type="hidden" name="email-subject-hash" value="f4286271f48c984d144a3104042e62e8dedbe5ab7c24e83f20ef8a7bd2d2f368"/>
|
||
</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="9f8bdPGVnAc52VUgUxnU6Mtnv6R1R3KGq2SgQF9hXbZzWm06xQ0WAUZ13azdKEi0">
|
||
|
||
|
||
|
||
<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="9f8bdPGVnAc52VUgUxnU6Mtnv6R1R3KGq2SgQF9hXbZzWm06xQ0WAUZ13azdKEi0">
|
||
|
||
|
||
|
||
<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="9f8bdPGVnAc52VUgUxnU6Mtnv6R1R3KGq2SgQF9hXbZzWm06xQ0WAUZ13azdKEi0">
|
||
|
||
<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="9f8bdPGVnAc52VUgUxnU6Mtnv6R1R3KGq2SgQF9hXbZzWm06xQ0WAUZ13azdKEi0">
|
||
|
||
|
||
|
||
<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="9f8bdPGVnAc52VUgUxnU6Mtnv6R1R3KGq2SgQF9hXbZzWm06xQ0WAUZ13azdKEi0">
|
||
|
||
<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="31522987">
|
||
<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/S1097-2765(19)30594-5"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=False&PrId=3048&itool=Abstract-def&log$=linkouticon&uid=31522987&db=pubmed&nlmid=9802571"
|
||
title="See full text options at Elsevier Science"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="Elsevier Science"
|
||
data-ga-label="31522987"
|
||
><img src="https://cdn.ncbi.nlm.nih.gov/corehtml/query/egifs/https:--linkinghub.elsevier.com-ihub-images-celloa.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/31522987/"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=True&PrId=3494&itool=Abstract-def&log$=linkouticon&uid=31522987&db=pubmed&nlmid=9802571"
|
||
title="Free full text at PubMed Central"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="PMC"
|
||
data-ga-label="31522987"
|
||
><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="/31522987/citations/"
|
||
data-citation-style="nlm"
|
||
data-pubmed-format-link="/31522987/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="31522987" 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%2F31522987%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="9f8bdPGVnAc52VUgUxnU6Mtnv6R1R3KGq2SgQF9hXbZzWm06xQ0WAUZ13azdKEi0"><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
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Distinct Classes of Chromatin Loops Revealed by Deletion of an RNA-Binding Region in CTCF
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data-ga-label="Robert Tjian">Robert Tjian</a><sup class="affiliation-links"><span class="author-sup-separator"> </span><a class="affiliation-link" title="Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Li Ka Shing Center for Biomedical and Health Sciences, Berkeley, CA 94720, USA; CIRM Center of Excellence, University of California, Berkeley, Berkeley, CA 94720, USA; Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, CA 94720, USA. Electronic address: jmlim@berkeley.edu." href="#full-view-affiliation-5" ref="linksrc=author_aff">
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><sup class="key">1</sup> Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Li Ka Shing Center for Biomedical and Health Sciences, Berkeley, CA 94720, USA; CIRM Center of Excellence, University of California, Berkeley, Berkeley, CA 94720, USA; Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, CA 94720, USA; Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA 02142, USA.</li>
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Distinct Classes of Chromatin Loops Revealed by Deletion of an RNA-Binding Region in CTCF
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><sup class="key">5</sup> Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Li Ka Shing Center for Biomedical and Health Sciences, Berkeley, CA 94720, USA; CIRM Center of Excellence, University of California, Berkeley, Berkeley, CA 94720, USA; Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, CA 94720, USA. Electronic address: jmlim@berkeley.edu.</li>
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Mammalian genomes are folded into topologically associating domains (TADs), consisting of chromatin loops anchored by CTCF and cohesin. Some loops are cell-type specific. Here we asked whether CTCF loops are established by a universal or locus-specific mechanism. Investigating the molecular determinants of CTCF clustering, we found that CTCF self-association in vitro is RNase sensitive and that an internal RNA-binding region (RBR<sub>i</sub>) mediates CTCF clustering and RNA interaction in vivo. Strikingly, deleting the RBR<sub>i</sub> impairs about half of all chromatin loops in mESCs and causes deregulation of gene expression. Disrupted loop formation correlates with diminished clustering and chromatin binding of RBR<sub>i</sub> mutant CTCF, which in turn results in a failure to halt cohesin-mediated extrusion. Thus, CTCF loops fall into at least two classes: RBR<sub>i</sub>-independent and RBR<sub>i</sub>-dependent loops. We speculate that evidence for RBR<sub>i</sub>-dependent loops may provide a molecular mechanism for establishing cell-specific CTCF loops, potentially regulated by RNA(s) or other RBR<sub>i</sub>-interacting partners.
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CTCF; Micro-C; RNA; TAD; cohesin; genome organization; loop; loop extrusion; super-resolution imaging.
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Copyright © 2019 Elsevier Inc. All rights reserved.
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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">DECLARATION OF 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">D.R. is a co-founder of Constellation Pharmaceuticals and Fulcrum Therapeutics. All other authors declare no competing interests.</p>
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<p> Figure 1.. CTCF Self-Interacts in an RNA-Dependent… </p>
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Figure 1.. CTCF Self-Interacts in an RNA-Dependent Manner
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<div class="figure-caption-contents">(A) Overview of CTCF domains in the endogenously dual-tagged mESC clone C62. (B) Western blot of total cell lysates from WT mESCs and C62 line. 3xFLAG-Halo-CTCF and V5-SNAP<sub>f</sub>-CTCF are similarly expressed and together roughly equal to CTCF levels in WT cells. (C) Representative coIP experiment indicating RNA-dependent CTCF self-interaction. Top: V5 IP followed by FLAG immunoblotting measures self-coIP efficiency(90% of total IP material loaded); bottom: V5 IP followed by V5 immunoblotting controls for IP efficiency (remaining 10% of IP sample loaded). (D) CTCF self-coIP efficiency after normalization for V5 IP efficiency. Error bars indicate SDs; n = 2. See also Figures S1A–S1E.</div>
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<p> Figure 2.. CTCF RBR <sub> i </sub> Region Mediates CTCF Clustering </p>
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Figure 2.. CTCF RBR<sub>i</sub> Region Mediates CTCF Clustering
|
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<div class="figure-caption-contents">(A) CTCF domains in the mESC clones C59 (Halo-WT CTCF) and C59 ΔRBR<sub>i</sub> (Halo-ΔRBR<sub>i</sub> CTCF). (B) Western blot of total cell lysates from JM8.N4 WT mESCs, C59, and C59 ΔRBR<sub>i</sub>. WT-CTCF and ΔRBR<sub>i</sub>-CTCF have the same number of amino acids, but ΔRBR<sub>i</sub>-CTCF runs slightly slower in BisTris SDS-PAGE. (C) Flow cytometry measurement of Halo-CTCF abundance in live C59 Halo-WT CTCF and C59 ΔRBR<sub>i</sub> mESCs after TMR labeling. (D) Growth assay for C59 Halo-WT CTCF and C59 ΔRBR<sub>i</sub> mESCs. In (C) and (D), error bars indicate mean and SE (n = 4). (E) <i>In vitro</i> RNA-binding assay. An <i>in vitro</i>-transcribed fragment of human WRAP53 mRNA (<i>hWRAP53</i>, nucleotides 1–167) was incubated with recombinant (r-) WT- or ΔRBR<sub>i</sub>-CTCF protein (see STAR Methods). Recovered RNA was run on urea denaturing gels and stained with SYBR Gold; recovered proteins were run on SDS-PAGE and stained with PageBlue. Left: representative experiment (replicates in Figure S1J). Right: RNA binding efficiency of WT- versus ΔRBR<sub>i</sub>-CTCF averaged across three experiments, normalized by recovered proteins. (F) PAR-CLIP of WT-CTCF and ΔRBR<sub>i</sub>-CTCF mESCs. Left: western blot of input and CTCF-IP. Right: autoradiography for <sup>32</sup>P-labeled RNA for input and CTCF-IP. (G and H) Representative PALM reconstructions for Halo-WT CTCF (G) and Halo-ΔRBR<sub>i</sub> CTCF (H). (I) Ripley’s <i>L</i> function for WT-CTCF (52 cells) and ΔRBR<sub>i</sub>-CTCF mESCs (46 cells) (mean and SE). (J) Representative confocal micrographs of mESC colonies. Halo-WT CTCF and Halo-ΔRBR<sub>i</sub> CTCF mESCs were labeled with 500 nM Halo-TMR dye and visualized using a Zeiss LSM 710 laser scanning confocal microscope. See also Figure S1.</div>
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<p> Figure 3.. Compartments Are Largely Unchanged in ΔRBR <sub> i </sub> -CTCF mESCs </p>
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Figure 3.. Compartments Are Largely Unchanged in ΔRBR<sub>i</sub>-CTCF mESCs
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<div class="figure-caption-contents">(A) Overview of Micro-C contact matrices or maps at multiple resolutions in WT-CTCF and ΔRBR<sub>i</sub>-CTCF mESCs. Contact matrix normalization: iterative correction and eigenvector decomposition (ICE); color scale: log<sub>10</sub>. (B) Comparison of chromosome compartments. An example of plaid-like chromosome compartments at Chr17 is shown as ICE balanced contact maps, Pearson’s correlation matrices, and eigenvector analysis for the first principle component at 100 kb resolution, showing no significant difference. (C) Saddle plot for compartmentalization strength. Shows average distance-normalized contact frequencies between 100 kb bins in <i>cis</i> with ascending eigenvector values (log<sub>2</sub>). Upper left and bottom right: contact frequency between B-B and A-A compartments. Upper right and bottom left: frequency of inter-compartment interactions. (D) Genome-wide contact probability scaling plot, showing interaction density (per million reads per bp<sup>2</sup>) against genomic distance from 100 bp to 100 Mb. Biological replicates of WT-CTCF and ΔRBR<sub>i</sub>-CTCF mESCs overlap and decay at slope of −1, as in Lieberman-aiden et al. (2009). Because of potential artifacts introduced by fragment self-ligation, we did not consider reads below 100 bp.</div>
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<p> Figure 4.. TAD Organization Is Changed in… </p>
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<p> Figure 4.. TAD Organization Is Changed in ΔRBR <sub> i </sub> -CTCF mESCs </p>
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<div class="figure-caption-contents"><p> (A) Example of TAD boundary disruption… </p></div>
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<strong class="figure-label">
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Figure 4.. TAD Organization Is Changed in ΔRBR<sub>i</sub>-CTCF mESCs
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<div class="figure-caption-contents">(A) Example of TAD boundary disruption in ΔRBR<sub>i</sub>-CTCF mESCs. Snapshot of insulation score curves, 45°-rotated contact maps, and differential contact matrix (from top to bottom) plotted for Chr18: 3M–18M. Insulation scores were calculated using a 200 kb sliding window at 20 kb resolution. A lower value of insulation score means stronger insulation strength. Black arrows: examples of loss of insulation in ΔRBR<sub>i</sub>-CTCF mESCs. Green arrows: unaffected insulators. Differential contact matrices were generated by subtraction of the normalized ΔRBR<sub>i</sub>-CTCF matrix to WT-CTCF matrix. Blue indicates weaker TADs in ΔRBR<sub>i</sub>-CTCF mESCs. Red indicates “bleed-through,” that is, loss of TAD insulation (black arrows). (B) Size distribution of TADs (boundary or insulator-flanked regions). Inset: Venn diagram. ΔRBR<sub>i</sub>-CTCF mESCs lose 1,474 of 3,666 insulators identified in WT-CTCF mESCs. (C) Aggregate peak analysis for TADs. TADs in WT-CTCF mESCs were identified through an additional TAD calling algorithm (arrowhead) and rescaled and aggregated (n = 4,448) at the center of the plot with ICE normalization (left) or distance normalization (right). WT-CTCF is shown on the top half and ΔRBR<sub>i</sub>-CTCF is shown on the bottom half. (D) Genome-wide averaged insulation plotted versus distance around insulation center. Insulation strength is weaker in ΔRBR<sub>i</sub>-CTCF mESCs when centering at WT insulators, but there is no significant change when centering at ΔRBR<sub>i</sub>-CTCF insulators. (E) Browser tracks. Snapshot regions (~200 kb) around the arrows (a, b, and c) indicated in are shown with CTCF and cohesin (Smc1a) ChIP-seq data. (a) and (b) display regions with strong depletion of insulation in ΔRBR<sub>i</sub>-CTCF mESCs, and (c) shows a region with little effect. The blue arrows indicate examples for loss of Smc1a peaks in ΔRBR<sub>i</sub>-CTCF mESCs, and the pink arrow indicates an example for gain or shift of Smc1a peak. See also Figures S2–S6.</div>
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<p> Figure 5.. Genome Organization at the Level… </p>
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<p> Figure 5.. Genome Organization at the Level of Both Loops and Stripes Is Altered in… </p>
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<strong class="figure-label">
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Figure 5.. Genome Organization at the Level of Both Loops and Stripes Is Altered in ΔRBR<sub>i</sub>-CTCF mESCs
|
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<div class="figure-caption-contents">(A) Scatterplot showing individual loop intensities in WT-CTCF versus ΔRBR<sub>i</sub>-CTCF mESCs. A total of 14,372 loops were identified in WT-CTCF mESCs, with a false discovery rate < 0.1. Loop intensity was calculated as log<sub>2</sub> enrichment of center pixel over expected bottom left pixels at 1, 5, or 10 kb resolution. (B) Pie charts showing affected loops. Approximately 8,189 loops are decreased by at least 1.5-fold, and 5,490 loops are decreased by at least 2-fold in ΔRBR<sub>i</sub>-CTCF compared with WT-CTCF mESCs. (C) Aggregate peak analysis for loops. The called loops were aggregated at the center of a 50 kb window at 1 kb resolution. The genome-wide averaged loop enrichment was calculated by the fold enrichment (center pixel/expected bottom left pixels). (D) Snapshots of four representative genomic regions of different CTCF loop types. Zoomed-in contact maps were plotted on the top and bottom panels forWT-CTCF and ΔRBR<sub>i</sub>-CTCF mESCs, respectively. CTCF and cohesin (Smc1a) ChIP-seq data are overlaid. From left to right, examples are shown of RBR<sub>i</sub>-independent loops and of the two sub-types of RBR<sub>i</sub>-dependent loops (with two examples of partial and complete loss of CTCF and cohesin binding for loop type 1). (E) Aggregation plot centered at top CTCF peaks. The contact matrices were aggregated around the top 10,000 CTCF ChIP-seq peaks using a ±600 kb window. WT-CTCF mESCs are shown on the top half of the plot, and ΔRBR<sub>i</sub>-CTCF mESCs are shown on the bottom half. Red arrows indicate stripes or flames. Green arrows and white dashed lines indicate insulation strength. (F) Quantification of stripe length. Stripes enrichments were calculated in log<sub>2</sub> ratio of observed over expected contacts. Significant enrichment was defined as 2fold enrichment labeled shown as a gray dashed line in the plot. (G) Representative contact maps at specific regions showing elongated “stripes” or “flames” in ΔRBR<sub>i</sub>-CTCF mESCs. (H) Loop extrusion sketch. Speculative illustration of why loss of a subset of CTCF boundaries might result in longer stripes assuming loop extrusion (Fudenberg et al., 2017). See also Figures S4 and S6.</div>
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<p> Figure 6.. ΔRBR <sub> i </sub> -CTCF Still Interacts… </p>
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<p> Figure 6.. ΔRBR <sub> i </sub> -CTCF Still Interacts with Cohesin, and Loops Lost in ΔRBR <sub> i… </sub> </p>
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<strong class="figure-label">
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Figure 6.. ΔRBR<sub>i</sub>-CTCF Still Interacts with Cohesin, and Loops Lost in ΔRBR<sub>i</sub>-CTCF mESCs Have Less CTCF and Cohesin Bound
|
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</strong>
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<div class="figure-caption-contents">(A) CoIP experiment showing that ΔRBR<sub>i</sub>-CTCF stills interacts with cohesin. CTCF antibodies can pull down Rad21 cohesin subunit in both WT- and ΔRBR<sub>i</sub>-CTCF mESCs. (B) Heatmaps of CTCF and Smc1a ChIP-Seq signal (deepTools RPGC [readsper genomic content]) around WT-CTCF peaks as called by MACS2, sorted by ΔRBR<sub>i</sub>-CTCF peak intensity. (C) Aggregate peak analysis for differential loop intensity. Loops were sorted into four quartiles on the basis of differential loop intensities between WTCTCF and ΔRBR<sub>i</sub>-CTCF mESCs. A total of 2,974 loops in each quartile were aggregated at the center of a 50 kb window and quantified as above. (D) Cumulative distribution function (CDF) curves of ChIP enrichment at the loop anchors. CTCF and Smc1a ChIP signals were quantified as the log<sub>2</sub> enrichment ± 250 bp around the loop anchor. (E) <i>k</i>-Means clustering analysis of CTCF and cohesin (Smc1a) ChIP-seq data in the Q1 loop anchors. The filtered Q1 loop anchor sites were analyzed using <i>k</i>-means clustering (<i>k</i> = 3). Clustering analysis output are plotted as kernel smoothed histograms. Heatmaps with peaks at the center across a ±3 kb region are shown in Figure S5E. (F) Enrichments of genomic features at loop anchors by ChromHMM analysis(Bogu et al., 2015). Heatmap shows log<sub>2</sub> enrichment of the loop anchors in each chromatin state. Q1 loops are largely depleted in most chromatin states and only slightly enriched in H3K27me3 chromatin. See also Figures S5–S7.</div>
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<p> Figure 7.. Altered Gene Expression in ΔRBR… </p>
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<p> Figure 7.. Altered Gene Expression in ΔRBR <sub> i </sub> -CTCF mESCs and Speculative Models for the… </p>
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Figure 7.. Altered Gene Expression in ΔRBR<sub>i</sub>-CTCF mESCs and Speculative Models for the Role of CTCF’s RBR<sub>i</sub>
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<div class="figure-caption-contents">(A) Volcano plot comparing gene expression in ΔRBR<sub>i</sub>-CTCF mESCs against WT-CTCF mESCs, measured by RNA-seq followed by differential expression analysis with edgeR and DeSeq2. Plotted are edgeR p values and fold changes. Gray dots, genes not changed (NC) upon CTCF RBR<sub>i</sub> deletion; blue dots, genes called downregulated (DOWN) by both edgeR and DeSeq2 in ΔRBR<sub>i</sub>-CTCF mESCs; red dots, genes called upregulated (UP) by both edgeR and DeSeq2 in ΔRBR<sub>i</sub>-CTCF mESCs (see STAR Methods). edgeR fold change (FC) mean and median values are specified for both downregulated (blue) and upregulated (red) genes. Full analysis in Table S2. (B) For each differentially regulated gene (DOWN or UP) in ΔRBR<sub>i</sub>-CTCF mESCs, we measured the distance in base pairs from its transcription start site (TSS) to the closest disrupted Smc1a called ChIP-seq peak in WT mESCs (and plotted the results as a cumulative distribution function [CDF]). As controls, we randomly selected five groups of ~500 unaltered genes each (not changed [NC]). Scatterplots with single data points in Figure S7. (C) Same as (B), but plotting the distance to the closest Q1 loop anchor. Scatterplots with single data points in Figure S7. (D) Snapshots of three genomic regions showing two genes (<i>Car4, Col2a1</i>) upregulated and one gene (<i>Igsf8</i>) downregulated in ΔRBR<sub>i</sub>-CTCF mESCs compared with WT-CTCF mESCs (more examples in Figure S7). RNA-seq tracks are plotted (top) and deregulated genes marked by black arrowhead. Fold change (FC) in ΔRBR<sub>i</sub>-CTCF mESCs versus WT-CTCF mESCs are also specified. Blue genes are transcribed from the “plus” strand, red genes from the “minus” strand. Zoomed-in contact maps at 1 kb (right, left) or 2 kb resolution (middle). Arrowheads highlight disrupted loops. CTCF and cohesin (Smc1a) ChIP-seq data are overlaid, with arrowheads pointing at disrupted right loop anchors in ΔRBR<sub>i</sub>-CTCF mESCs. ChIP-seq and RNA-seq units: reads per genomic content (deepTools RPGC). (E) Sketch of a CTCF cluster. We observe that CTCF self-association is sensitive to RNase <i>in vitro</i> and that CTCF clustering is partially mediated by its RBR<sub>i</sub>
|
||
<i>in vivo</i>. As such, our results are consistent both with direct CTCF-RNA interactions (left) and indirect CTCF-RNA interactions, perhaps mediated by an unknown factor X. (F) Two types of CTCF loops. Our analysis of ΔRBR<sub>i</sub>-CTCF mESCs uncovers the existence of at least two classes of CTCF loops: RBR<sub>i</sub>-dependent and RBR<sub>i</sub>-independent loops. (G) Does CTCF clustering help block extruding cohesin? Speculative model that clustering of an otherwise small CTCF protein may contribute to efficiently blocking extruding cohesins. (H) Regulation of loops and TADs during differentiation. The ability to turn on and off RBR<sub>i</sub>-dependent CTCF boundaries could potentially provide the means for regulating specific TADs and loops during development by regulating RBR<sub>i</sub> interaction partners. As an illustration, we show a side-by-side comparison of 3D genome reorganization in ΔRBR<sub>i</sub>-CTCF mESCs and differentiated cells at the region around the Olig1 and Olig2 genes (Hi-C data from Bonev et al., 2017). Subdomains and loops (black arrows) are lost in both ΔRBR<sub>i</sub> mESCs and cortical neurons. See also Figures S6 and S7.</div>
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|
||
hidden
|
||
aria-label="Dropdown menu for keyword Cell Line"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
||
href="/?term=%22Cell+Line%22%5BMeSH%5D&sort=date&sort_order=desc"
|
||
data-href="/?term=%22Cell+Line%22%5BMeSH%5D&sort=date&sort_order=desc"
|
||
ref="linksrc=search_in_pubmed_keyword_link&mesh="Cell Line"[MeSH]"
|
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data-ga-category="search"
|
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data-ga-action="mesh_term"
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data-ga-label="Cell Line">
|
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Search in PubMed
|
||
</a></li><li><a class="search-in-mesh-link dropdown-block-link"
|
||
ref="linksrc=search_in_mesh_link"
|
||
href="https://www.ncbi.nlm.nih.gov/mesh?term=Cell+Line"
|
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data-ga-category="search_mesh"
|
||
data-ga-action="mesh_term_link"
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data-ga-label="Cell Line">
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Search in MeSH
|
||
</a></li><li><a class="add-to-search-link dropdown-block-link"
|
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ref="linksrc=add_to_search_link"
|
||
role="button"
|
||
data-search-term=""Cell Line"[MeSH]"
|
||
data-ga-category="search"
|
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data-ga-action="add_to_search"
|
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data-ga-label=""Cell Line"[MeSH]"
|
||
href="#">
|
||
Add to Search
|
||
</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
|
||
aria-label="Toggle dropdown menu for keyword Chromatin / chemistry"
|
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tabindex="0"
|
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aria-controls="keyword-actions-mesh-terms-5"
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aria-expanded="false"
|
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data-pinger-ignore>
|
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Chromatin / chemistry
|
||
</button><div id="keyword-actions-mesh-terms-5"
|
||
class="keyword-actions-dropdown dropdown dropdown-container"
|
||
hidden
|
||
aria-label="Dropdown menu for keyword Chromatin / chemistry"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
||
href="/?term=%22Chromatin%2Fchemistry%22%5BMeSH%5D&sort=date&sort_order=desc"
|
||
data-href="/?term=%22Chromatin%2Fchemistry%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Chromatin/chemistry"[MeSH]"
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data-ga-category="search"
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data-ga-action="mesh_term"
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data-ga-label="Chromatin / chemistry">
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Search in PubMed
|
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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ref="linksrc=search_in_mesh_link"
|
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Chromatin"
|
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data-ga-category="search_mesh"
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data-ga-action="mesh_term_link"
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data-ga-label="Chromatin / chemistry">
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Search in MeSH
|
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</a></li><li><a class="add-to-search-link dropdown-block-link"
|
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ref="linksrc=add_to_search_link"
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role="button"
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data-search-term=""Chromatin/chemistry"[MeSH]"
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data-ga-category="search"
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data-ga-action="add_to_search"
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data-ga-label=""Chromatin/chemistry"[MeSH]"
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href="#">
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
|
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aria-label="Toggle dropdown menu for keyword Chromatin / genetics"
|
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tabindex="0"
|
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aria-controls="keyword-actions-mesh-terms-6"
|
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aria-expanded="false"
|
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data-pinger-ignore>
|
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Chromatin / genetics
|
||
</button><div id="keyword-actions-mesh-terms-6"
|
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class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
||
aria-label="Dropdown menu for keyword Chromatin / genetics"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
||
href="/?term=%22Chromatin%2Fgenetics%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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data-href="/?term=%22Chromatin%2Fgenetics%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Chromatin/genetics"[MeSH]"
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data-ga-action="mesh_term"
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data-ga-label="Chromatin / genetics">
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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ref="linksrc=search_in_mesh_link"
|
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Chromatin"
|
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data-ga-category="search_mesh"
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data-ga-action="mesh_term_link"
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data-ga-label="Chromatin / genetics">
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Search in MeSH
|
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</a></li><li><a class="add-to-search-link dropdown-block-link"
|
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ref="linksrc=add_to_search_link"
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role="button"
|
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data-search-term=""Chromatin/genetics"[MeSH]"
|
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data-ga-category="search"
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data-ga-action="add_to_search"
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data-ga-label=""Chromatin/genetics"[MeSH]"
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href="#">
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link major"
|
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aria-label="Toggle dropdown menu for keyword Chromatin / metabolism*"
|
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tabindex="0"
|
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aria-controls="keyword-actions-mesh-terms-major-7"
|
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aria-expanded="false"
|
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data-pinger-ignore>
|
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Chromatin / metabolism*
|
||
</button><div id="keyword-actions-mesh-terms-major-7"
|
||
class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
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aria-label="Dropdown menu for keyword Chromatin / metabolism*"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
||
href="/?term=%22Chromatin%2Fmetabolism%22%5BMAJR%5D&sort=date&sort_order=desc"
|
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data-href="/?term=%22Chromatin%2Fmetabolism%22%5BMAJR%5D&sort=date&sort_order=desc"
|
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Chromatin/metabolism"[MAJR]"
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data-ga-category="search"
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data-ga-action="mesh_term"
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data-ga-label="Chromatin / metabolism*">
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Search in PubMed
|
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
|
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ref="linksrc=search_in_mesh_link"
|
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Chromatin"
|
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data-ga-category="search_mesh"
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data-ga-action="mesh_term_link"
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data-ga-label="Chromatin / metabolism*">
|
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Search in MeSH
|
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</a></li><li><a class="add-to-search-link dropdown-block-link"
|
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ref="linksrc=add_to_search_link"
|
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role="button"
|
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data-search-term=""Chromatin/metabolism"[MAJR]"
|
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data-ga-category="search"
|
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data-ga-action="add_to_search"
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data-ga-label=""Chromatin/metabolism"[MAJR]"
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href="#">
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
|
||
aria-label="Toggle dropdown menu for keyword Gene Expression Regulation, Developmental"
|
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tabindex="0"
|
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aria-controls="keyword-actions-mesh-terms-8"
|
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aria-expanded="false"
|
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data-pinger-ignore>
|
||
Gene Expression Regulation, Developmental
|
||
</button><div id="keyword-actions-mesh-terms-8"
|
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class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
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aria-label="Dropdown menu for keyword Gene Expression Regulation, Developmental"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
||
href="/?term=%22Gene+Expression+Regulation%2C+Developmental%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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data-href="/?term=%22Gene+Expression+Regulation%2C+Developmental%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Gene Expression Regulation, Developmental"[MeSH]"
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data-ga-action="mesh_term"
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data-ga-label="Gene Expression Regulation, Developmental">
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Gene+Expression+Regulation%2C+Developmental"
|
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data-ga-category="search_mesh"
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Search in MeSH
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</a></li><li><a class="add-to-search-link dropdown-block-link"
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role="button"
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data-search-term=""Gene Expression Regulation, Developmental"[MeSH]"
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data-ga-category="search"
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data-ga-action="add_to_search"
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data-ga-label=""Gene Expression Regulation, Developmental"[MeSH]"
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
|
||
aria-label="Toggle dropdown menu for keyword Male"
|
||
tabindex="0"
|
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aria-controls="keyword-actions-mesh-terms-9"
|
||
aria-expanded="false"
|
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data-pinger-ignore>
|
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Male
|
||
</button><div id="keyword-actions-mesh-terms-9"
|
||
class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
||
aria-label="Dropdown menu for keyword Male"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22Male%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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data-href="/?term=%22Male%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Male"[MeSH]"
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data-ga-category="search"
|
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data-ga-action="mesh_term"
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data-ga-label="Male">
|
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Search in PubMed
|
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
|
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ref="linksrc=search_in_mesh_link"
|
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Male"
|
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data-ga-category="search_mesh"
|
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data-ga-action="mesh_term_link"
|
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data-ga-label="Male">
|
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Search in MeSH
|
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</a></li><li><a class="add-to-search-link dropdown-block-link"
|
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ref="linksrc=add_to_search_link"
|
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role="button"
|
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data-search-term=""Male"[MeSH]"
|
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data-ga-category="search"
|
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data-ga-action="add_to_search"
|
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data-ga-label=""Male"[MeSH]"
|
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href="#">
|
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
|
||
aria-label="Toggle dropdown menu for keyword Mice"
|
||
tabindex="0"
|
||
aria-controls="keyword-actions-mesh-terms-10"
|
||
aria-expanded="false"
|
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data-pinger-ignore>
|
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Mice
|
||
</button><div id="keyword-actions-mesh-terms-10"
|
||
class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
||
aria-label="Dropdown menu for keyword Mice"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22Mice%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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data-href="/?term=%22Mice%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Mice"[MeSH]"
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data-ga-category="search"
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data-ga-action="mesh_term"
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data-ga-label="Mice">
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Search in PubMed
|
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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ref="linksrc=search_in_mesh_link"
|
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Mice"
|
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data-ga-category="search_mesh"
|
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data-ga-action="mesh_term_link"
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data-ga-label="Mice">
|
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Search in MeSH
|
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</a></li><li><a class="add-to-search-link dropdown-block-link"
|
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ref="linksrc=add_to_search_link"
|
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role="button"
|
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data-search-term=""Mice"[MeSH]"
|
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data-ga-category="search"
|
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data-ga-action="add_to_search"
|
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data-ga-label=""Mice"[MeSH]"
|
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href="#">
|
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
|
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aria-label="Toggle dropdown menu for keyword Mice, Transgenic"
|
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tabindex="0"
|
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aria-controls="keyword-actions-mesh-terms-11"
|
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aria-expanded="false"
|
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data-pinger-ignore>
|
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Mice, Transgenic
|
||
</button><div id="keyword-actions-mesh-terms-11"
|
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class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
||
aria-label="Dropdown menu for keyword Mice, Transgenic"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22Mice%2C+Transgenic%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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data-href="/?term=%22Mice%2C+Transgenic%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Mice, Transgenic"[MeSH]"
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data-ga-action="mesh_term"
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data-ga-label="Mice, Transgenic">
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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ref="linksrc=search_in_mesh_link"
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Mice%2C+Transgenic"
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data-ga-category="search_mesh"
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data-ga-action="mesh_term_link"
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data-ga-label="Mice, Transgenic">
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Search in MeSH
|
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</a></li><li><a class="add-to-search-link dropdown-block-link"
|
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ref="linksrc=add_to_search_link"
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role="button"
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data-search-term=""Mice, Transgenic"[MeSH]"
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data-ga-category="search"
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data-ga-action="add_to_search"
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data-ga-label=""Mice, Transgenic"[MeSH]"
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href="#">
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link major"
|
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aria-label="Toggle dropdown menu for keyword Mouse Embryonic Stem Cells / metabolism*"
|
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tabindex="0"
|
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aria-controls="keyword-actions-mesh-terms-major-12"
|
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aria-expanded="false"
|
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data-pinger-ignore>
|
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Mouse Embryonic Stem Cells / metabolism*
|
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</button><div id="keyword-actions-mesh-terms-major-12"
|
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class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
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aria-label="Dropdown menu for keyword Mouse Embryonic Stem Cells / metabolism*"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22Mouse+Embryonic+Stem+Cells%2Fmetabolism%22%5BMAJR%5D&sort=date&sort_order=desc"
|
||
data-href="/?term=%22Mouse+Embryonic+Stem+Cells%2Fmetabolism%22%5BMAJR%5D&sort=date&sort_order=desc"
|
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Mouse Embryonic Stem Cells/metabolism"[MAJR]"
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data-ga-category="search"
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data-ga-action="mesh_term"
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data-ga-label="Mouse Embryonic Stem Cells / metabolism*">
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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ref="linksrc=search_in_mesh_link"
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Mouse+Embryonic+Stem+Cells"
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data-ga-category="search_mesh"
|
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data-ga-label="Mouse Embryonic Stem Cells / metabolism*">
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Search in MeSH
|
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</a></li><li><a class="add-to-search-link dropdown-block-link"
|
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ref="linksrc=add_to_search_link"
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role="button"
|
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data-search-term=""Mouse Embryonic Stem Cells/metabolism"[MAJR]"
|
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data-ga-category="search"
|
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data-ga-action="add_to_search"
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data-ga-label=""Mouse Embryonic Stem Cells/metabolism"[MAJR]"
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href="#">
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
|
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aria-label="Toggle dropdown menu for keyword Mutation"
|
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tabindex="0"
|
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aria-controls="keyword-actions-mesh-terms-13"
|
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aria-expanded="false"
|
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data-pinger-ignore>
|
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Mutation
|
||
</button><div id="keyword-actions-mesh-terms-13"
|
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class="keyword-actions-dropdown dropdown dropdown-container"
|
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hidden
|
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aria-label="Dropdown menu for keyword Mutation"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
|
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href="/?term=%22Mutation%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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data-href="/?term=%22Mutation%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Mutation"[MeSH]"
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data-ga-category="search"
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data-ga-action="mesh_term"
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data-ga-label="Mutation">
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Mutation"
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data-ga-category="search_mesh"
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data-ga-label="Mutation">
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Search in MeSH
|
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</a></li><li><a class="add-to-search-link dropdown-block-link"
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ref="linksrc=add_to_search_link"
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role="button"
|
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data-search-term=""Mutation"[MeSH]"
|
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data-ga-category="search"
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data-ga-action="add_to_search"
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data-ga-label=""Mutation"[MeSH]"
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href="#">
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
|
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aria-label="Toggle dropdown menu for keyword Nucleic Acid Conformation"
|
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tabindex="0"
|
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aria-controls="keyword-actions-mesh-terms-14"
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aria-expanded="false"
|
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data-pinger-ignore>
|
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Nucleic Acid Conformation
|
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</button><div id="keyword-actions-mesh-terms-14"
|
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class="keyword-actions-dropdown dropdown dropdown-container"
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hidden
|
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aria-label="Dropdown menu for keyword Nucleic Acid Conformation"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
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href="/?term=%22Nucleic+Acid+Conformation%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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data-href="/?term=%22Nucleic+Acid+Conformation%22%5BMeSH%5D&sort=date&sort_order=desc"
|
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ref="linksrc=search_in_pubmed_keyword_link&mesh="Nucleic Acid Conformation"[MeSH]"
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Search in PubMed
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</a></li><li><a class="search-in-mesh-link dropdown-block-link"
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href="https://www.ncbi.nlm.nih.gov/mesh?term=Nucleic+Acid+Conformation"
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Search in MeSH
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</a></li><li><a class="add-to-search-link dropdown-block-link"
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ref="linksrc=add_to_search_link"
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data-search-term=""Nucleic Acid Conformation"[MeSH]"
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
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|
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|
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Protein Binding
|
||
</button><div id="keyword-actions-mesh-terms-15"
|
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aria-label="Dropdown menu for keyword Protein Binding"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
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Protein Interaction Domains and Motifs
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
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</div>
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|
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<div id="substances" class="substances keywords-section">
|
||
<h2 class="title">
|
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Substances
|
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</h2>
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
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aria-label="Toggle dropdown menu for keyword Chromatin"
|
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tabindex="0"
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aria-expanded="false"
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data-pinger-ignore>
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Chromatin
|
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aria-label="Dropdown menu for keyword Chromatin"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
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Search in MeSH
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Add to Search
|
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</a></li></ul></div></div></div></li><li><div class="keyword-actions dropdown-block"><button class="keyword-actions-trigger trigger keyword-link"
|
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aria-label="Toggle dropdown menu for keyword Ctcf protein, mouse"
|
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tabindex="0"
|
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aria-expanded="false"
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data-pinger-ignore>
|
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Ctcf protein, mouse
|
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</button><div id="keyword-actions-substances-2"
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class="keyword-actions-dropdown dropdown dropdown-container"
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hidden
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aria-label="Dropdown menu for keyword Ctcf protein, mouse"><div class="title">Actions</div><div class="content"><ul class="keyword-actions-links"><li><a class="search-in-pubmed-link dropdown-block-link"
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Search in PubMed
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Search in MeSH
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Add to Search
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</a></li></ul></div></div></div></li></ul>
|
||
</div>
|
||
|
||
|
||
|
||
|
||
|
||
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<div id="related-links" class="related-links">
|
||
<h2 class="title">
|
||
Related information
|
||
</h2>
|
||
|
||
<ul class="related-links-list"><li><a title="PubMed links associated with Books" href="https://www.ncbi.nlm.nih.gov/books?linkname=pubmed_books_refs&from_uid=31522987"
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ref="log$=recordlinks&logdbfrom=pubmed&ncbi_uid=31522987&ordinalpos=1&linkpos=1">
|
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Cited in Books
|
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</a></li><li><a title="Related GEO DataSets" href="https://www.ncbi.nlm.nih.gov/gds?linkname=pubmed_gds&from_uid=31522987"
|
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ref="log$=recordlinks&logdbfrom=pubmed&ncbi_uid=31522987&ordinalpos=1&linkpos=2">
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GEO DataSets
|
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</a></li><li><a title="Link to related Genes" href="https://www.ncbi.nlm.nih.gov/gene?linkname=pubmed_gene&from_uid=31522987"
|
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ref="log$=recordlinks&logdbfrom=pubmed&ncbi_uid=31522987&ordinalpos=1&linkpos=3">
|
||
Gene
|
||
</a></li><li><a title="Link to Gene for the GeneRIF subcategory" href="https://www.ncbi.nlm.nih.gov/gene?linkname=pubmed_gene_rif&from_uid=31522987"
|
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ref="log$=recordlinks&logdbfrom=pubmed&ncbi_uid=31522987&ordinalpos=1&linkpos=4">
|
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Gene (GeneRIF)
|
||
</a></li><li><a title="Related information in MedGen" href="https://www.ncbi.nlm.nih.gov/medgen?linkname=pubmed_medgen&from_uid=31522987"
|
||
ref="log$=recordlinks&logdbfrom=pubmed&ncbi_uid=31522987&ordinalpos=1&linkpos=5">
|
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MedGen
|
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</a></li><li><a title="Related records in MedGen based on citations in GeneReviews and Medical Genetics Summaries" href="https://www.ncbi.nlm.nih.gov/medgen?linkname=pubmed_medgen_bookshelf_cited&from_uid=31522987"
|
||
ref="log$=recordlinks&logdbfrom=pubmed&ncbi_uid=31522987&ordinalpos=1&linkpos=6">
|
||
MedGen (Bookshelf cited)
|
||
</a></li><li><a title="Link to Protein RefSeqs" href="https://www.ncbi.nlm.nih.gov/protein?linkname=pubmed_protein_refseq&from_uid=31522987"
|
||
ref="log$=recordlinks&logdbfrom=pubmed&ncbi_uid=31522987&ordinalpos=1&linkpos=7">
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Protein (RefSeq)
|
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</a></li><li><a title="Related Projects" href="https://www.ncbi.nlm.nih.gov/bioproject?linkname=pubmed_bioproject&from_uid=31522987"
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Related Project
|
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</a></li><li><a title="Links to Short Read Archive Experiments" href="https://www.ncbi.nlm.nih.gov/sra?linkname=pubmed_sra&from_uid=31522987"
|
||
ref="log$=recordlinks&logdbfrom=pubmed&ncbi_uid=31522987&ordinalpos=1&linkpos=9">
|
||
SRA
|
||
</a></li></ul>
|
||
</div>
|
||
|
||
|
||
|
||
|
||
|
||
<div id="grants" class="grants">
|
||
<h2 class="title">
|
||
Grants and funding
|
||
</h2>
|
||
<div class="grants-list"><ul id="grants-head-list"><li class="grant-item"><a
|
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title="All articles for grant R01 CA199652/CA/NCI NIH HHS/United States"
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R01 CA199652/CA/NCI NIH HHS/United States
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</a></li><li class="grant-item"><a
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R00 GM130896/GM/NIGMS NIH HHS/United States
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</a></li><li class="grant-item"><a
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</a></li><li class="grant-item"><a
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</a></li></ul><ul id="grants-tail-list" class="list-tail"><li class="grant-item"><a
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</a></li><li class="grant-item"><a
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</a></li><li class="grant-item"><a
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