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</a>
|
||
</div>
|
||
|
||
<span class="search-input-link user-guide-link" role="navigation" aria-label="User guide">
|
||
<a href="/help/"
|
||
data-ga-category="featured_link"
|
||
data-ga-action="user_guide">
|
||
User Guide
|
||
</a>
|
||
</span>
|
||
|
||
</div>
|
||
</div>
|
||
|
||
|
||
</form>
|
||
|
||
|
||
<div id="article-page-header">
|
||
<div id="article-top-actions-bar" class="article-top-actions-bar">
|
||
<div class="inner-wrap">
|
||
<div class="actions-container">
|
||
<div class="return-to-search">
|
||
|
||
|
||
</div>
|
||
|
||
<div class="multiple-results-actions " role="region" aria-label="save, email, send to">
|
||
<button id="save-results-panel-trigger"
|
||
type="button"
|
||
class="save-results save-results-panel-trigger"
|
||
aria-expanded="false"
|
||
aria-controls="save-action-panel"
|
||
data-ga-category="save_share"
|
||
data-ga-action="save"
|
||
data-ga-label="open">
|
||
Save
|
||
</button><button id="email-results-panel-trigger"
|
||
type="button"
|
||
class="email-results email-results-panel-trigger"
|
||
aria-expanded="false"
|
||
aria-controls="email-action-panel"
|
||
data-ga-category="save_share"
|
||
data-ga-action="email"
|
||
data-ga-label="open">
|
||
Email
|
||
</button><div class="more-actions dropdown-block"><button id="more-actions-trigger"
|
||
type="button"
|
||
class="trigger more-actions-trigger"
|
||
ref="linksrc=show_moreactions_btn"
|
||
aria-label="Send to"
|
||
aria-controls="more-actions-dropdown">Send to</button><div id="more-actions-dropdown" class="dropdown dropdown-container" hidden><div class="content"><ul class="more-actions-links"><li><a class="clipboard-panel-trigger dropdown-block-link "
|
||
href="#"
|
||
role="button"
|
||
data-ga-category="save_share"
|
||
data-ga-action="clipboard"
|
||
data-ga-label="send">
|
||
Clipboard
|
||
</a></li><li><a role="button" class="dropdown-block-link bibliography-trigger-target" href="https://account.ncbi.nlm.nih.gov/?back_url=https%3A%2F%2Fpubmed.ncbi.nlm.nih.gov%2F23933255%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%2F23933255%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="nvsuMQgeOAqh29MDZcyZfgbfnMzFIwsoEiczpGJAobdLWAStCvb1JoHTVQhRB70I">
|
||
</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="nvsuMQgeOAqh29MDZcyZfgbfnMzFIwsoEiczpGJAobdLWAStCvb1JoHTVQhRB70I">
|
||
|
||
|
||
|
||
<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="nvsuMQgeOAqh29MDZcyZfgbfnMzFIwsoEiczpGJAobdLWAStCvb1JoHTVQhRB70I">
|
||
|
||
<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: 23933255 - PubMed</span>
|
||
<input type="hidden" name="email-subject" value="1 selected item: 23933255"/>
|
||
<input type="hidden" name="email-subject-hash" value="c7bc22dd10a4c3924ec4d05a73be3d0334447000d9452a019b43535d3b24cac4"/>
|
||
</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="nvsuMQgeOAqh29MDZcyZfgbfnMzFIwsoEiczpGJAobdLWAStCvb1JoHTVQhRB70I">
|
||
|
||
|
||
|
||
<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="nvsuMQgeOAqh29MDZcyZfgbfnMzFIwsoEiczpGJAobdLWAStCvb1JoHTVQhRB70I">
|
||
|
||
|
||
|
||
<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="nvsuMQgeOAqh29MDZcyZfgbfnMzFIwsoEiczpGJAobdLWAStCvb1JoHTVQhRB70I">
|
||
|
||
<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="nvsuMQgeOAqh29MDZcyZfgbfnMzFIwsoEiczpGJAobdLWAStCvb1JoHTVQhRB70I">
|
||
|
||
|
||
|
||
<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="nvsuMQgeOAqh29MDZcyZfgbfnMzFIwsoEiczpGJAobdLWAStCvb1JoHTVQhRB70I">
|
||
|
||
<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="23933255">
|
||
<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/S2211-1247(13)00359-8"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=False&PrId=3048&itool=Abstract-def&log$=linkouticon&uid=23933255&db=pubmed&nlmid=101573691"
|
||
title="See full text options at Elsevier Science"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="Elsevier Science"
|
||
data-ga-label="23933255"
|
||
><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/23933255/"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=True&PrId=3494&itool=Abstract-def&log$=linkouticon&uid=23933255&db=pubmed&nlmid=101573691"
|
||
title="Free full text at PubMed Central"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="PMC"
|
||
data-ga-label="23933255"
|
||
><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="/23933255/citations/"
|
||
data-citation-style="nlm"
|
||
data-pubmed-format-link="/23933255/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="23933255" 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%2F23933255%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="nvsuMQgeOAqh29MDZcyZfgbfnMzFIwsoEiczpGJAobdLWAStCvb1JoHTVQhRB70I"><div class="choice-group" role="radiogroup"><ul class="radio-group-items"><li><input type="radio"
|
||
id="collections-action-dialog-new"
|
||
class="collections-new"
|
||
name="collections"
|
||
value="new"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="collections_radio_new"><label for="collections-action-dialog-new">Create a new collection</label></li><li><input type="radio"
|
||
id="collections-action-dialog-existing"
|
||
class="collections-existing"
|
||
name="collections"
|
||
value="existing"
|
||
checked="true"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="collections_radio_existing"><label for="collections-action-dialog-existing">Add to an existing collection</label></li></ul></div><div class="controls-wrapper"><div class="action-panel-control-wrap new-collections-controls"><label for="collections-action-dialog-add-to-new" class="action-panel-label required-field-asterisk">
|
||
Name your collection:
|
||
</label><input
|
||
type="text"
|
||
name="add-to-new-collection"
|
||
id="collections-action-dialog-add-to-new"
|
||
class="collections-action-add-to-new"
|
||
pattern="[^"&=<>\/]*" title="The following characters are not allowed in the Name field: "&=<>/"
|
||
maxlength="100"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="create_collection"
|
||
data-ga-label="non_favorties_collection"><div class="collections-new-name-too-long usa-input-error-message selection-validation-message">
|
||
Name must be less than 100 characters
|
||
</div></div><div class="action-panel-control-wrap existing-collections-controls"><label for="collections-action-dialog-add-to-existing" class="action-panel-label">
|
||
Choose a collection:
|
||
</label><select id="collections-action-dialog-add-to-existing"
|
||
class="action-panel-selector collections-action-add-to-existing"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="select_collection"
|
||
data-ga-label="($('.collections-action-add-to-existing').val() === 'Favorites') ? 'Favorites' : 'non_favorites_collection'"></select><div class="collections-retry-load-on-error usa-input-error-message selection-validation-message">
|
||
Unable to load your collection due to an error<br><a href="#">Please try again</a></div></div></div><div class="action-panel-actions"><button class="action-panel-submit"
|
||
type="submit"
|
||
data-loading-label="Adding..."
|
||
data-pinger-ignore
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="add">
|
||
Add
|
||
</button><button class="action-panel-cancel"
|
||
aria-label="Close 'Add to Collections' panel"
|
||
ref="linksrc=close_collections_panel"
|
||
aria-controls="collections-action-panel"
|
||
aria-expanded="false"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="cancel">
|
||
Cancel
|
||
</button></div></form></div></div></div></div><button class="more-actions-button more-actions-dialog-trigger"
|
||
title="Open dialog with more actions to take"
|
||
ref="linksrc=more_actions_btn"></button><div class="display-options" data-format-key="format"
|
||
data-default-format-value="abstract"
|
||
data-current-format-value="abstract" role="region"><button
|
||
class="trigger usa-button"
|
||
title="Change format"
|
||
data-ga-category="display_options"
|
||
data-ga-action="display_options_dialog"><span class="button-label">Display options</span></button><div class="dropdown" hidden><div class="title">
|
||
Display options
|
||
</div><div class="content"><div class="format-container"><span class="option-label">
|
||
Format
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</a></li></ul></div></div></div><span class="period">. </span><span class="cit">2013 Aug 15;4(3):437-44.</span>
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CDK8-mediated STAT1-S727 phosphorylation restrains NK cell cytotoxicity and tumor surveillance
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CDK8-mediated STAT1-S727 phosphorylation restrains NK cell cytotoxicity and tumor surveillance
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The transcription factor STAT1 is important in natural killer (NK) cells, which provide immediate defense against tumor and virally infected cells. We show that mutation of a single phosphorylation site (Stat1-S727A) enhances NK cell cytotoxicity against a range of tumor cells, accompanied by increased expression of perforin and granzyme B. Stat1-S727A mice display significantly delayed disease onset in NK cell-surveilled tumor models including melanoma, leukemia, and metastasizing breast cancer. Constitutive phosphorylation of S727 depends on cyclin-dependent kinase 8 (CDK8). Inhibition of CDK8-mediated STAT1-S727 phosphorylation may thus represent a therapeutic strategy for stimulating NK cell-mediated tumor surveillance.
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<p class="copyright" id="copyright">
|
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Copyright © 2013 The Authors. Published by Elsevier Inc. All rights reserved.
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</p>
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<p class="disclaimer" id="disclaimer">
|
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<a href="/disclaimer/" target="_blank" data-ga-category="literature_resources"
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data-ga-action="disclaimer_link" data-ga-label="under_abstract">PubMed Disclaimer</a>
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</p>
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<div class="figures" id="figures">
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<h2 class="title">
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Figures
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<p> Graphical abstract </p>
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<strong class="figure-label">
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<p> Graphical abstract </p>
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<strong class="figure-label">
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Graphical abstract
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role="button"
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data-image-width="727"
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data-image-alt="Figure 1"
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data-pmc-id="PMC3748339"
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data-figure-id="fig1">
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<img class="figure-thumb" itemprop="thumbnail"
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id="article-image-1"
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/8f30/3748339/8e9413b1f5b6/gr1.gif"
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alt="Figure 1" />
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<strong class="figure-label">
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<p> Figure 1 </p>
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<div class="figure-caption-contents"><p> Presence, Development, and Cytotoxic Function… </p></div>
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<strong class="figure-label">
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<p> Figure 1 </p>
|
||
</strong>
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<div class="figure-caption-contents"><p> Presence, Development, and Cytotoxic Function of <i> Stat1-S727A </i> NK Cells (A) Bone marrow was… </p></div>
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<figcaption id="figure-caption-1" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
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<strong class="figure-label">
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Figure 1
|
||
</strong>
|
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|
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|
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|
||
<div class="figure-caption-contents">Presence, Development, and Cytotoxic Function of <i>Stat1-S727A</i> NK Cells (A) Bone marrow was investigated for NK cell precursors (NKPs, CD3<sup>−</sup>Ter-119<sup>−</sup>GR1<sup>−</sup>B220<sup>−</sup>CD122<sup>+</sup>NK1.1<sup>−</sup>DX5<sup>−</sup>), immature NK cells (iNKs, CD3<sup>−</sup>Ter-119<sup>−</sup>GR1<sup>−</sup>B220<sup>−</sup>CD122<sup>+</sup>NK1.1<sup>+</sup>DX5<sup>−</sup>), and mNKs (CD3<sup>−</sup>Ter-119<sup>−</sup>GR1<sup>−</sup>B220<sup>−</sup>CD122<sup>+</sup>NK1.1<sup>+</sup>DX5<sup>+</sup>). Each symbol represents an individual mouse; small horizontal lines indicate the mean (<sup>∗</sup>p < 0.05, <sup>∗∗</sup>p < 0.01; one-way ANOVA and Tukey’s post hoc test). (B) Number of CD3<sup>−</sup>DX5<sup>+</sup>NKp46<sup>+</sup> NK cells, given as percentages of spleen and blood lymphocytes, is shown. Each symbol represents an individual mouse; horizontal lines indicate the mean (<sup>∗</sup>p < 0.05; one-way ANOVA and Tukey’s post hoc test). (C) NK cell maturation profiles represented by the expression of CD27 and CD11b on CD3<sup>−</sup>NK1.1<sup>+</sup> splenocytes are shown. Data are representative for at least five independent experiments with n > 10 for each genotype. (D) Expression of KLRG1 and NKG2A/C/E on CD3<sup>−</sup>DX5<sup>+</sup>NK1.1<sup>+</sup>NKp46<sup>+</sup> splenocytes is shown. Numbers indicate the percentage of gate<sup>+</sup> (horizontal line) NK cells ± SEM; n ≥ 9 for each genotype. (E) Cytotoxicity of wild-type versus <i>Stat1-S727A</i> NK cells against YAC-1, RMA, RMA-S, and RMA-Rae1 tumor targets at given effector-to-target (E:T) ratios, measured in a 4 hr [<sup>51</sup>Cr]-release cytotoxicity assay is shown. Symbols represent means, and error bars indicate SEM of triplicates (<sup>∗</sup>p < 0.05, <sup>∗∗∗</sup>p < 0.001; unpaired t test). Data are representative of three independent experiments. (F) R-ADCC against FcR<sup>+</sup> Daudi target cells crosslinked with antibodies against NK1.1, 2B4, and Ly49D is shown. Symbols represent means, and error bars indicate SEM of triplicates (<sup>∗</sup>p < 0.05, <sup>∗∗</sup>p < 0.01; unpaired t test). Data are representative of two independent experiments. (G) IFN-γ and granzyme B protein expression in splenic NK cells (gated on CD3<sup>−</sup>NKp46<sup>+</sup>) ex vivo and after 4 hr stimulation with IL-2 and IL-12 is presented. (H) LAK cells stained intracellularly for perforin under normal culturing conditions and after 4 hr treatment with PMA and ionomycin are shown. See also Figure S1 and Table S1.</div>
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||
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|
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<img class="figure-thumb" itemprop="thumbnail"
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id="article-image-2"
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/8f30/3748339/ee9d0a7c6281/gr2.gif"
|
||
alt="Figure 2" />
|
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|
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<strong class="figure-label">
|
||
<p> Figure 2 </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> Constitutive Basal STAT1-S727 Phosphorylation in… </p></div>
|
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||
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<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
|
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<strong class="figure-label">
|
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<p> Figure 2 </p>
|
||
</strong>
|
||
|
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|
||
|
||
<div class="figure-caption-contents"><p> Constitutive Basal STAT1-S727 Phosphorylation in NK Cells Is Mediated by CDK8 (A) Western… </p></div>
|
||
|
||
|
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<figcaption id="figure-caption-2" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
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<strong class="figure-label">
|
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Figure 2
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">Constitutive Basal STAT1-S727 Phosphorylation in NK Cells Is Mediated by CDK8 (A) Western blot of freshly isolated DX5<sup>+</sup> splenocytes from wild-type animals shows constitutive basal phosphorylation on STAT1-S727 in vivo. (B and C) In vitro-expanded LAK cells from wild-type and <i>Stat1-S727A</i> mice were treated with or without (B) 100 U/ml IFN-β or (C) 5 ng/ml IL-12 for the given times, and the phosphorylation on STAT1-Y701 and STAT1-S727 was investigated by western blot. <i>Stat1</i><sup><i>−/−</i></sup> LAK cells served as negative control and HSC-70 as loading control. (D) Wild-type LAK cells were treated with different kinase inhibitors targeting CDKs (roscovitine and flavopiridol) or MAPK p38 (BIRB 0796 and SB 203580), and the phosphorylation status of STAT1-S727 was determined in a western blot. (E) CDK8 knockdown in primary NK cells with two hairpins led to reduced STAT1-S727 phosphorylation. A random hairpin served as control. (F) Knockdown of CDK8 with five hairpins in an immortalized <i>Ink4a</i><sup><i>−/−</i></sup> NK cell line is shown. A random hairpin served as control. (G) FACS-based cytotoxicity assay of immortalized NK cells transduced with a random hairpin or a hairpin against CDK8 (#3) against YAC-1 target cells is presented. Symbols represent mean, and error bars indicate SEM of triplicates (<sup>∗</sup>p < 0.05, <sup>∗∗∗</sup>p < 0.001; unpaired t test). See also Figure S2.</div>
|
||
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|
||
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<a class="figure-link"
|
||
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||
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|
||
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|
||
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|
||
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|
||
data-figure-id="fig3">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
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|
||
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/8f30/3748339/70b2d9bb2022/gr3.gif"
|
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alt="Figure 3" />
|
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<strong class="figure-label">
|
||
<p> Figure 3 </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><i> Stat1-S727A </i> Mice Are Less Susceptible…</div>
|
||
|
||
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|
||
|
||
</div>
|
||
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|
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<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
|
||
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<strong class="figure-label">
|
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<p> Figure 3 </p>
|
||
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|
||
|
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|
||
|
||
<div class="figure-caption-contents"><i> Stat1-S727A </i> Mice Are Less Susceptible to B16F10 Melanoma and <i> v-abl </i> <sup> <i> + </i> </sup> Leukemic Cells…</div>
|
||
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<figcaption id="figure-caption-3" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
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<strong class="figure-label">
|
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Figure 3
|
||
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|
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|
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|
||
<div class="figure-caption-contents"><i>Stat1-S727A</i> Mice Are Less Susceptible to B16F10 Melanoma and <i>v-abl</i><sup><i>+</i></sup> Leukemic Cells (A) Wild-type, <i>Stat1-S727A</i>, and <i>Stat1</i><sup><i>−/−</i></sup> mice were injected intravenously with B16F10 melanoma cells. At the indicated time points, mice were sacrificed, and tumor nodules visible on the lung surface were counted. Each symbol represents an individual mouse; horizontal lines indicate the mean (<sup>∗∗∗</sup>p < 0.001, one-way ANOVA and Tukey’s post hoc test on day 21, unpaired t test on day 28). (B) Representative lung photographs at the indicated time points after injection of B16F10 melanoma cells are shown. (C) Kaplan-Meier plot of wild-type (n = 7) and <i>Stat1-S727A</i> (n = 7) mice intravenously injected with B16F10 melanoma cells is illustrated. Log rank testing revealed a significant difference in the onset of dyspnea (p = 0.027; MST wild-type = 31 days; MST <i>Stat1-S727A</i> = 40 days). (D) Kaplan-Meier plot of wild-type (n = 8), <i>Stat1-S727A</i> (n = 8), and <i>Stat1</i><sup><i>−/−</i></sup> (n = 6) recipient animals inoculated intravenously with <i>v-abl</i><sup><i>+</i></sup> leukemic cells is presented. <i>Stat1-S727A</i> mice succumb to leukemia with an increased latency (MST = 15 days) than wild-type (MST = 13 days) and <i>Stat1</i><sup><i>−/−</i></sup> (MST = 11.5 days) animals. Log rank test was corrected with Bonferroni for multiple testing and revealed a significant difference between <i>Stat1-S727A</i> and wild-type (p = 0.0053) and between <i>Stat1-S727A</i> and <i>Stat1</i><sup><i>−/−</i></sup> animals (p = 0.0023). (E) Kaplan-Meier plot of <i>Rag2</i><sup><i>−/−</i></sup><i>/Stat1<sup>+/+</sup></i> (n = 6) and <i>Rag2</i><sup><i>−/−</i></sup><i>/Stat1-S727A</i> (n = 6) animals injected intravenously with <i>v-abl</i><sup><i>+</i></sup> leukemic cells is shown. <i>Rag2</i><sup><i>−/−</i></sup><i>/Stat1-S727A</i> mice succumb to leukemia with increased latency (MST = 14 days) than <i>Rag2</i><sup><i>−/−</i></sup>/<i>Stat1</i><sup>+/+</sup> (MST = 12 days) animals. Log rank test was statistically significant (p = 0.017). See also Figure S3.</div>
|
||
|
||
|
||
|
||
|
||
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|
||
|
||
|
||
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|
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|
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|
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||
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|
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|
||
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|
||
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|
||
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|
||
<img class="figure-thumb" itemprop="thumbnail"
|
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|
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/8f30/3748339/a71d0009e83e/gr4.gif"
|
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|
||
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|
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<strong class="figure-label">
|
||
<p> Figure 4 </p>
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><i> Stat1-S727A </i> Mice Are Resistant to…</div>
|
||
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</div>
|
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|
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<strong class="figure-label">
|
||
<p> Figure 4 </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><i> Stat1-S727A </i> Mice Are Resistant to 4T1 Breast Cancer Metastasis into Lungs Wild-type (n…</div>
|
||
|
||
|
||
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|
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<figcaption id="figure-caption-4" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
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<strong class="figure-label">
|
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Figure 4
|
||
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<div class="figure-caption-contents"><i>Stat1-S727A</i> Mice Are Resistant to 4T1 Breast Cancer Metastasis into Lungs Wild-type (n = 11), <i>Stat1-S727A</i> (n = 12), and <i>Stat1</i><sup><i>−/−</i></sup> (n = 6) animals received orthotopical transplants of 4T1 breast cancer cells. (A) Primary tumor volumes were measured weekly. Symbols represent mean, and error bars indicate SEM. (B) Some recipients were sacrificed at day 27 (wild-type n = 3, <i>Stat1-S727A</i> n = 6, <i>Stat1</i><sup><i>−/−</i></sup> n = 6) and remaining recipients at day 31, then the primary tumors were weighed. Bar graph depicts mean ± SEM. (C and D) Recipient mice were bled weekly, and (C) WBCs and (D) MDSCs (GR1<sup>+</sup>CD11b<sup>+</sup>) were counted (<sup>∗</sup>p < 0.05, <sup>∗∗</sup>p < 0.01, <sup>∗∗∗</sup>p < 0.001; one-way ANOVA and Tukey’s post hoc test on days 21 and 27; unpaired t test on day 31). Symbols represent means, and error bars indicate SEM. n.s., not significant. (E and F) After termination of the experiment, (E) lungs were weighed, and (F) the percentage (%) of metastatic area in the lung was determined histochemically (<sup>∗</sup>p < 0.05, <sup>∗∗</sup>p < 0.01, <sup>∗∗∗</sup>p < 0.001; one-way ANOVA and Tukey’s post hoc test on day 27; unpaired t test on day 31). Each symbol represents an individual mouse; horizontal lines indicate the mean. (G) Representative H&E-stained lung sections of <i>Stat1</i><sup><i>−/−</i></sup> animals at day 27 and wild-type and <i>Stat1-S727A</i> animals at day 31 post transplantation are shown. See also Figure S4.</div>
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<p> Figure S1 </p>
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<div class="figure-caption-contents"><p> Effect of <i> Stat1-S727A </i> Mutation on… </p></div>
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<div class="figure-caption-contents"><p> Effect of <i> Stat1-S727A </i> Mutation on the Transcription of Effector Molecules, Related to Figure… </p></div>
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<div class="figure-caption-contents">Effect of <i>Stat1-S727A</i> Mutation on the Transcription of Effector Molecules, Related to Figure 1 and Table S2 (A) mRNA expression of <i>Ifng</i> (IFN-γ), <i>Grzma</i> (granzyme A), <i>Grzmb</i> (granzyme B) and <i>Prf1</i> (perforin) were measured in LAK cells derived from wild-type, <i>Stat1-S727A</i> and <i>Stat1<sup>−/−</sup></i> animals under standard culturing conditions and after IL-12 stimulation (<sup>∗</sup>p < 0.05, <sup>∗∗</sup>p < 0.01, <sup>∗∗∗</sup>p < 0.001; one-way ANOVA and Tukey’s post hoc test). The summary of at least 3 independent LAK cell preparations is depicted; all values were normalized to untreated wild-type LAK cells. (B) The recruitment of polymerase II to the <i>Prf1</i> gene was investigated via ChIP in wild-type and <i>Stat1-S727A</i> LAK cells under standard culturing conditions (basal) and after 30 min stimulation with 100 U/ml IFN-β or 5 ng/ml IL-12 (left panel). Polymerase II binding to the B lymphocyte antigen gene <i>Cd19</i> was determined as negative control (right panel). Plotted are means ± SEM. (C and D) In vitro expanded NK cells were stimulated for the indicated periods with 100 U/ml IFN-β (C) or 5 ng/ml IL-12 (D) and the expression level of <i>Tbx21</i> (T-bet) was determined via semiquantitative real time PCR relative to <i>Gapdh</i> (<sup>∗</sup>p < 0.05, <sup>∗∗</sup>p < 0.01, <sup>∗∗∗</sup>p < 0.001; one-way ANOVA and Tukey's post hoc test). (E) The mRNA level of <i>Eomes</i> (Eomesodermin) was measured in expanded NK cells and after 8 hr stimulation with 5 ng/ml IL-12 (<sup>∗</sup>p < 0.05; one-way ANOVA and Tukey's post hoc test). (F) <i>Ikzf2</i> (Helios) mRNA was quantified in freshly isolated splenic NK cells and after 7 days in culture. All values are normalized to untreated wild-type NK cells. Depicted is the summary of at least two independent experiments (<sup>∗</sup>p < 0.05; one-way ANOVA followed by Tukey’s post hoc test). (G) The expression levels of miRNAs involved in the posttranscriptional regulation of perforin and granzyme B were determined in freshly isolated NK cells derived from wild-type and <i>Stat1-S727A</i> mice (n ≥ 3 per genotype, <sup>∗∗∗</sup>p < 0.001; unpaired t test). Plotted are means ± SEM.</div>
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<div class="figure-caption-contents"><p> IL-12 and IFN-β Signaling and… </p></div>
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<div class="figure-caption-contents"><p> IL-12 and IFN-β Signaling and NK Cell Line Characterization, Related to Figure 2… </p></div>
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<div class="figure-caption-contents">IL-12 and IFN-β Signaling and NK Cell Line Characterization, Related to Figure 2 and Table S2 (A) Transcription of <i>Mx1</i>, <i>Mx2</i>, <i>Irf1</i>, <i>Irf7</i> and <i>Gbp2</i> was investigated in isolated, cultivated LAK cells 1 and 2 hr after the treatment with 100 U/ml IFN-β. mRNA levels were measured via semiquantitative real time PCR relative to <i>Gapdh</i>. All values were normalized to untreated wild-type LAK cells. <i>Stat1<sup>−/−</sup></i> LAK cells failed to induce appreciable mRNA levels upon IFN-β stimulation, whereas <i>Stat1-S727A</i> LAK cells did not show any difference compared to wild-type. Presented is the summary of 2 independent experiments with 3-6 replicates per group. Plotted are means ± SEM. (B) Splenocytes from wild-type, <i>Stat1-S727A</i> and <i>Stat1<sup>−/−</sup></i> mice (2 per group) were prepared and subjected to LPS stimulation (100 ng/ml, 1 hr and 4 hr). <i>Il12p40</i> mRNA expression was measured via semiquantitative real time PCR relative to <i>Gapdh</i>. All values were normalized to untreated wild-type LAK cells; shown are means ± SEM (<sup>∗∗</sup>p < 0.01, <sup>∗∗∗</sup>p < 0.001; one-way ANOVA followed by Tukey’s post hoc test). (C) IL-12-induced STAT1, STAT3 and STAT4 activation in LAK cells derived from wild-type, <i>Stat1-S727A</i> and <i>Stat1<sup>−/−</sup></i> animals. HSC-70 served as loading control. (D) <i>Ink4a<sup>−/−</sup></i> splenic NK cells were MACS (DX5) purified, sorted for CD3<sup>-</sup>NK1.1<sup>+</sup> expression and cultivated in vitro under standard conditions (5,000 U/ml IL-2) for several months. Proliferation assay of an immortal NK cell line cultivated under standard conditions, low dose of IL-2 (500 U/ml) and deprived from IL-2 (RPMI compl.). One week after IL-2 deprivation all NK cells underwent apoptosis. (E) Intracellular FACS staining for IFN-γ production in an <i>Ink4a<sup>−/−</sup></i> NK cell line under normal culturing conditions (IL-2) or after stimulation for 4 hr with IL-12 or PMA and ionomycin, respectively. C57BL/6 LAK cells served as positive control, <i>Ifng<sup>−/−</sup></i> LAK cells as negative control. (F) Cytotoxic capacity of an <i>Ink4a<sup>−/−</sup></i> NK cell line against YAC-1 target cells measured in a FACS-based cytotoxicity assay. <i>Ink4a<sup>−/−</sup></i> NK cell lines retained some cytotoxic capacity, although diminished compared to primary wild-type NK cells after 7 days in vitro cultivation. Symbols represent means, and error bars indicate SEM of triplicates.</div>
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<div class="figure-caption-contents"><p> Characterization of Diseased Mice after… </p></div>
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<div class="figure-caption-contents"><p> Characterization of Diseased Mice after <i> v-abl </i> <sup> <i> + </i> </sup> Leukemic Cell Transplantation, Related to Figure… </p></div>
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<div class="figure-caption-contents">Characterization of Diseased Mice after <i>v-abl</i><sup><i>+</i></sup> Leukemic Cell Transplantation, Related to Figure 3 Wild-type (n = 8), <i>Stat1-S727A</i> (n = 8), <i>Stat1<sup>−/−</sup></i> (n = 6), <i>Rag2<sup>−/−</sup></i> (n = 6) and <i>Rag2<sup>−/−</sup>/Stat1-S727A</i> mice (n = 6) were injected intravenously with 10<sup>5</sup><i>v-abl</i><sup><i>+</i></sup> leukemic cells. The mice were checked daily and sacrificed at the first sign of disease. As shown in Figure 3<i>Stat1-S727A</i> and <i>Rag2<sup>−/−</sup>/Stat1-S727A</i> mice survived the leukemic challenge with the longest latency. (A) At the respective day of sacrifice, all mice were investigated for the infiltration of CD19<sup>+</sup>CD43<sup>+</sup>B220<sup>+</sup> leukemic tumor cells into bone marrow (BM), spleen and blood. Disease severity was comparable in all mice at the day of sacrifice. Depicted are means ± SEM (<sup>∗</sup>p < 0.05, one-way ANOVA and Tukey’s post hoc test). (B) Spleen, liver and lymph node (LN) weight, depicted relatively to the body weight, was measured and showed no difference. Plotted are means ± SEM. (C) Numbers of NKp46<sup>+</sup> NK cells were measured in spleen, BM and blood of all animals. Depicted are means ± SEM (<sup>∗</sup>p < 0.05, <sup>∗∗</sup>p < 0.01, <sup>∗∗∗</sup>p < 0.001; one-way ANOVA followed by Tukey’s post hoc test). (D) To measure NK cell maturity and activation, the expression of CD11b (left hand) and B220 (right hand) was determined on NKp46<sup>+</sup> NK cells, respectively. There were no significant differences detectable. Depicted are means ± SEM. This experiment was conducted with 3 different <i>v-abl</i><sup><i>+</i></sup> cell lines with comparable results.</div>
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<div class="figure-caption-contents"><p> 4T1 Breast Cancer Metastasis Formation… </p></div>
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<div class="figure-caption-contents"><p> 4T1 Breast Cancer Metastasis Formation in Immune-Compromised <i> Rag2 </i> <sup> <i> −/− </i> </sup> and <i> Rag2 </i> <sup> <i> −/− </i> </sup> <i> /Il2rg… </i> </p></div>
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<div class="figure-caption-contents">4T1 Breast Cancer Metastasis Formation in Immune-Compromised <i>Rag2</i><sup><i>−/−</i></sup> and <i>Rag2</i><sup><i>−/−</i></sup><i>/Il2rg</i><sup><i>−/−</i></sup> Animals, Related to Figure 4 BALB/c wild-type (n = 5), <i>Rag2<sup>−/−</sup></i> (n = 4) and <i>Rag2<sup>−/−</sup>/Il2rg<sup>−/−</sup></i> (n = 4) animals received orthotopical transplants of 4T1 breast cancer cells. (A) Breast tumor volumes were measured weekly. Symbols represent means and error bars indicate SEM. <i>Rag2<sup>−/−</sup>/Il2rg<sup>−/−</sup></i> animals seemed to develop smaller breast tumors, which was due to increased intra-tumoral necrosis (<sup>∗∗</sup>p < 0.01; one-way ANOVA and Tukey's post hoc test). (B–D) After sacrifice at day 28 post transplantation, primary tumors were prepared and weighed. Plotted are means ± SEM. No significant differences in primary tumor weight were detected. Recipient mice were bled weekly and (C) white blood cell (WBC) counts and (D) the numbers of myeloid-derived suppressor cells (MDSCs, GR1<sup>+</sup>CD11b<sup>+</sup>) were determined as surrogate marker of disease progression. <i>Rag2<sup>−/−</sup></i> animals showed substantially lower WBC and MDSC counts at day 28 post injection. Symbols represent means and error bars indicate SEM. (E and F) After termination of the experiment, (E) lungs were weighed and (F) the percentage of metastatic area in the lung was determined histochemically (<sup>∗</sup>p < 0.05, <sup>∗∗</sup>p < 0.01, <sup>∗∗∗</sup>p < 0.001; one-way ANOVA and Tukey’s post hoc test). Each symbol represents an individual mouse; small horizontal lines indicate the mean. (G) Representative H&E-stained lung sections of wild-type, <i>Rag2<sup>−/−</sup></i> and <i>Rag2<sup>−/−</sup>/Il2rg<sup>−/−</sup></i> animals.</div>
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|
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<span class="docsum-authors full-authors">Ivagnès A, Messaoudene M, Stoll G, Routy B, Fluckiger A, Yamazaki T, Iribarren K, Duong CPM, Fend L, Caignard A, Cremer I, LeCesne A, Adam J, Honoré C, Mir O, Chaigneau L, Berger A, Validire P, Christidis C, Brun-Ly VL, Smyth MJ, Mariette X, Salomon BL, Kroemer G, Rusakiewicz S, Zitvogel L.</span>
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<span class="docsum-authors short-authors">Ivagnès A, et al.</span>
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<span class="docsum-journal-citation full-journal-citation">Oncoimmunology. 2017 Oct 11;7(12):e1386826. doi: 10.1080/2162402X.2017.1386826. eCollection 2018.</span>
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Bancerek J., Poss Z.C., Steinparzer I., Sedlyarov V., Pfaffenwimmer T., Mikulic I., Dölken L., Strobl B., Müller M., Taatjes D.J., Kovarik P. CDK8 kinase phosphorylates transcription factor STAT1 to selectively regulate the interferon response. Immunity. 2013;38:250–262.
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Bromberg J.F., Horvath C.M., Wen Z., Schreiber R.D., Darnell J.E., Jr. Transcriptionally active Stat1 is required for the antiproliferative effects of both interferon alpha and interferon gamma. Proc. Natl. Acad. Sci. USA. 1996;93:7673–7678.
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Cao X., Shores E.W., Hu-Li J., Anver M.R., Kelsall B.L., Russell S.M., Drago J., Noguchi M., Grinberg A., Bloom E.T. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity. 1995;2:223–238.
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Dalton D.K., Pitts-Meek S., Keshav S., Figari I.S., Bradley A., Stewart T.A. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science. 1993;259:1739–1742.
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Alcaide P., Jones T.G., Lord G.M., Glimcher L.H., Hallgren J., Arinobu Y., Akashi K., Paterson A.M., Gurish M.A., Luscinskas F.W. Dendritic cell expression of the transcription factor T-bet regulates mast cell progenitor homing to mucosal tissue. J. Exp. Med. 2007;204:431–439.
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Farlik M., Reutterer B., Schindler C., Greten F., Vogl C., Müller M., Decker T. Nonconventional initiation complex assembly by STAT and NF-kappaB transcription factors regulates nitric oxide synthase expression. Immunity. 2010;33:25–34.
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