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|
||
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%2F39025454%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%2F39025454%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="pr4S2chXeDuUvFlYKH7LyYouJqjhWr8uGeOXF2KjOehop6rOn0KN26U8hu1tP2GO">
|
||
</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="pr4S2chXeDuUvFlYKH7LyYouJqjhWr8uGeOXF2KjOehop6rOn0KN26U8hu1tP2GO">
|
||
|
||
|
||
|
||
<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="pr4S2chXeDuUvFlYKH7LyYouJqjhWr8uGeOXF2KjOehop6rOn0KN26U8hu1tP2GO">
|
||
|
||
<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: 39025454 - PubMed</span>
|
||
<input type="hidden" name="email-subject" value="1 selected item: 39025454"/>
|
||
<input type="hidden" name="email-subject-hash" value="bcf6df42e2aec1f61f9d5d3951f26efbf842ddfccd5a9db073ad5a8050b7a321"/>
|
||
</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="pr4S2chXeDuUvFlYKH7LyYouJqjhWr8uGeOXF2KjOehop6rOn0KN26U8hu1tP2GO">
|
||
|
||
|
||
|
||
<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="pr4S2chXeDuUvFlYKH7LyYouJqjhWr8uGeOXF2KjOehop6rOn0KN26U8hu1tP2GO">
|
||
|
||
|
||
|
||
<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="pr4S2chXeDuUvFlYKH7LyYouJqjhWr8uGeOXF2KjOehop6rOn0KN26U8hu1tP2GO">
|
||
|
||
<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="pr4S2chXeDuUvFlYKH7LyYouJqjhWr8uGeOXF2KjOehop6rOn0KN26U8hu1tP2GO">
|
||
|
||
|
||
|
||
<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="pr4S2chXeDuUvFlYKH7LyYouJqjhWr8uGeOXF2KjOehop6rOn0KN26U8hu1tP2GO">
|
||
|
||
<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="39025454">
|
||
<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/S0021-9258(24)02085-4"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=False&PrId=3048&itool=Abstract-def&log$=linkouticon&uid=39025454&db=pubmed&nlmid=2985121R"
|
||
title="See full text options at Elsevier Science"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="Elsevier Science"
|
||
data-ga-label="39025454"
|
||
><img src="https://cdn.ncbi.nlm.nih.gov/corehtml/query/egifs/https:--linkinghub.elsevier.com-ihub-images-elsevieroa.png" alt="Elsevier Science full text link"><span class="text">
|
||
|
||
Elsevier Science
|
||
|
||
</span></a><a class="link-item
|
||
pmc
|
||
"
|
||
href="https://pmc.ncbi.nlm.nih.gov/articles/pmid/39025454/"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=True&PrId=3494&itool=Abstract-def&log$=linkouticon&uid=39025454&db=pubmed&nlmid=2985121R"
|
||
title="Free full text at PubMed Central"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="PMC"
|
||
data-ga-label="39025454"
|
||
><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="/39025454/citations/"
|
||
data-citation-style="nlm"
|
||
data-pubmed-format-link="/39025454/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="39025454" 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%2F39025454%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="pr4S2chXeDuUvFlYKH7LyYouJqjhWr8uGeOXF2KjOehop6rOn0KN26U8hu1tP2GO"><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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Molecular characterization of Rft1, an ER membrane protein associated with congenital disorder of glycosylation RFT1-CDG
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Molecular characterization of Rft1, an ER membrane protein associated with congenital disorder of glycosylation RFT1-CDG
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The oligosaccharide needed for protein N-glycosylation is assembled on a lipid carrier via a multistep pathway. Synthesis is initiated on the cytoplasmic face of the endoplasmic reticulum (ER) and completed on the luminal side after transbilayer translocation of a heptasaccharide lipid intermediate. More than 30 congenital disorders of glycosylation (CDGs) are associated with this pathway, including RFT1-CDG which results from defects in the membrane protein Rft1. Rft1 is essential for the viability of yeast and mammalian cells and was proposed as the transporter needed to flip the heptasaccharide lipid intermediate across the ER membrane. However, other studies indicated that Rft1 is not required for heptasaccharide lipid flipping in microsomes or unilamellar vesicles reconstituted with ER membrane proteins, nor is it required for the viability of at least one eukaryote. It is therefore not known what essential role Rft1 plays in N-glycosylation. Here, we present a molecular characterization of human Rft1, using yeast cells as a reporter system. We show that it is a multispanning membrane protein located in the ER, with its N and C termini facing the cytoplasm. It is not N-glycosylated. The majority of RFT1-CDG mutations map to highly conserved regions of the protein. We identify key residues that are important for Rft1's ability to support N-glycosylation and cell viability. Our results provide a necessary platform for future work on this enigmatic protein.
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|
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CDG; Ist2; MurJ; N-glycosylation; Nvj1; dolichol-linked oligosaccharide; endoplasmic reticulum; lipid droplet; scramblase; yeast.
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<p class="copyright" id="copyright">
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Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.
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<div class="conflict-of-interest" id="conflict-of-interest">
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<h2 class="title">
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Conflict of interest statement
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</h2>
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<div class="statement">
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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">Conflict of interest The authors declare that they have no conflicts of interest with the contents of this article.</p>
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<p> Figure 1 </p>
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<div class="figure-caption-contents"><b> Functional replacement of yeast Rft1… </b></div>
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<p> Figure 1 </p>
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<div class="figure-caption-contents"><b> Functional replacement of yeast Rft1 by human Rft1. </b> <i> A </i> , protein <i> N </i> -glycosylation…</div>
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Figure 1
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<div class="figure-caption-contents"><b>Functional replacement of yeast Rft1 by human Rft1.</b><i>A</i>, protein <i>N</i>-glycosylation in the ER. Glc<sub>3</sub>Man<sub>9</sub>GlcNAc<sub>2</sub>-PP-dolichol (G3M9-DLO), the oligosaccharide donor for protein <i>N</i>-glycosylation in yeast and humans, is synthesized in two stages. The first stage produces Man<sub>5</sub>GlcNAc<sub>2</sub>-PP-dolichol (M5-DLO) on the cytoplasmic side of the ER. M5-DLO then moves across the membrane to the luminal side (a process facilitated by M5-DLO scramblase) where it is converted to G3M9-DLO. Oligosaccharyltransferase (OST) transfers the G3M9 oligosaccharide from G3M9-DLO to a glycosylation sequon (NXS/T, single letter amino acid code, where X is any amino acid except proline) in a nascent protein as it emerges from the protein translocon into the ER lumen. <i>B</i>, serial 10-fold dilutions of WT (BY4741) and KSY512 (<i>rft1Δ</i>←hRft1(<i>URA3</i>)) cells were spotted on SC plates ± 5-FOA and SD(-Ura) and incubated at 30 °C for 3 days. <i>C</i>, KSY512 (<i>rft1Δ</i>←hRft1(<i>URA3</i>)) cells were transformed with an empty <i>HIS3</i> vector (empty, p413-<i>P</i><sub><i>GPD</i></sub>), or <i>HIS3</i> vectors encoding various Rft1 constructs (xRft1) as follows: yRft1-3xFLAG, hRft1-3xFLAG, ALFA-mNG-yRft1-3xFLAG, and ALFA-mNG-hRft1-3xFLAG. The cells were spotted (10-fold serial dilutions) on the indicated media and photographed after incubation at 30 °C for 3 days. <i>D</i>, WT (BY4741) and KSY512 cells transformed with various Rft1 constructs as in <i>panel C</i> were cultured in YPD liquid medium to log-phase, harvested, and analyzed by SDS-PAGE and immunoblotting with anti-CPY antibody. The annotation on the right indicates migration of mature CPY (with 4 <i>N</i>-glycans), and hypoglycosylated forms with 3, 2, 1 or 0 glycans. <i>E</i>, fluorescently tagged mNG-yRft1 and mNG-hRft1 constructs (expression driven by the GPD promoter) were integrated into WT cells expressing the luminal ER marker mCherry-HDEL. The resulting YAKM301 (P<sub>GPD</sub>-mNG-yRft1 mCherry-HDEL) and YAKM225 (P<sub>GPD</sub>-mNG-hRft1 mCherry-HDEL) cells were cultured in YPD medium to log-phase and imaged by confocal fluorescence microscopy. The scale bar represents 5 μm. 5-FOA, 5-fluoroorotic acid; CPY, carboxypeptidase Y; DLO, dolichol-linked oligosaccharide; ER, endoplasmic reticulum; hRft1, human Rft1; M5-DLO, Man<sub>5</sub>GlcNAc<sub>2</sub>-PP-dolichol; mNG, mNeonGreen; SC, synthetic complete; SD, synthetic defined.</div>
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<div class="figure-caption-contents"><b> Alg14 colocalizes with lipid droplets,… </b></div>
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<div class="figure-caption-contents"><b> Alg14 colocalizes with lipid droplets, but Alg2 and Rft1 do not. </b> <i> A </i> ,…</div>
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Figure 2
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<div class="figure-caption-contents"><b>Alg14 colocalizes with lipid droplets, but Alg2 and Rft1 do not.</b><i>A</i>, YAKM275 (P<sub>GPD</sub>-mNG-Alg14 Erg6-mCherry) cells expressing fluorescently tagged Alg14 and Erg6 were cultured in medium supplemented with oleic acid (YPO medium) for 16 h and visualized by confocal fluorescence microscopy. The <i>dotted line</i> indicates the shape of the cells. <i>B</i>, as in <i>panel A</i>, except that YAKM274 (P<sub>GPD</sub>-mNG-Alg2 Erg6-mCherry) cells expressing fluorescently tagged Alg2 and Erg6 were visualized. <i>C</i> and <i>D</i>, as in <i>panel A</i>, except that YAKM302 (P<sub>ADH</sub>-mNG-yRft1 Erg6-mCherry) and YAKM235 (P<sub>ADH</sub>-mNG-hRft1 Erg6-mCherry) cells were visualized. The scale bar represents 5 μm for all panels. hRft1, human Rft1; mNG, mNeonGreen.</div>
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<p> Figure 3 </p>
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<div class="figure-caption-contents"><b> Rft1 is not necessary for… </b></div>
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<div class="figure-caption-contents"><b> Rft1 is not necessary for M5-DLO scrambling in vesicles reconstituted with yeast ER… </b></div>
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<div class="figure-caption-contents"><b>Rft1 is not necessary for M5-DLO scrambling in vesicles reconstituted with yeast ER membrane proteins.</b> Microsomes were prepared by differential centrifugation of a homogenate of KSY512 cells, and salt washed to remove peripheral proteins. The salt-washed membranes were extracted with ice-cold Triton X-100 to solubilize ER membrane proteins. The Triton extract (TE) was mock-treated or incubated with anti-FLAG resin to eliminate hRft1-3xFLAG, then reconstituted with egg phosphatidylcholine and trace quantities of NBD-PC and [<sup>3</sup>H]M5-DLO to generate large unilamellar proteoliposomes (indicated as “TE” and “TE(-Rft1)”) for scramblase activity assays. The protein/phospholipid ratio of the proteoliposomes was ∼45 mg/mmol, based on input values of protein and phospholipid. Protein-free liposomes (L) were prepared in parallel. <i>A</i>, immunoblot using anti-FLAG (<i>top</i>) and anti-Dpm1 (<i>bottom</i>) antibodies. Identical cell equivalents were loaded in the mock-treated and anti-FLAG resin-treated samples. No FLAG signal was detected in the anti-FLAG resin-treated sample even upon loading 10-times more sample (not shown). <i>B</i>, diameter of reconstituted vesicles measured by dynamic light scattering. Error bars = mean ± S.D. (n = 3 technical replicates). <i>C</i>, NBD-PC scramblase activity assay. Dithionite was added at t = 0 s and fluorescence (F) was monitored over time. The TE and TE(-Rft1) traces (F/F<sub>max</sub>, normalized to the average fluorescence (F<sub>max</sub>) prior to dithionite addition) overlap exactly; to improve visualization, the TE(-Rft1) trace is displaced downward (0.05 y-units) and to the right (20 x-units). <i>D</i>, M5-DLO scramblase activity assay. The <i>y</i>-axis indicates the fraction of [<sup>3</sup>H]M5-DLO in the reconstituted vesicles that is captured by exogenously added Con A. For liposomes, the % capture is predicted to be 50%; for proteoliposomes with M5-DLO scramblase activity, the capture efficiency increases, the exact amount depending on the fraction of vesicles that has scramblase activity. See text for details. Error bars = mean ± S.D. (n = 3 technical replicates); ns, no significant difference using ordinary one-way ANOVA. Con A, concanavalin A; DLO, dolichol-linked oligosaccharide; ER, endoplasmic reticulum; hRft1, human Rft1; M5-DLO, Man<sub>5</sub>GlcNAc<sub>2</sub>-PP-dolichol; NBD, nitrobenzoxadiazole; PC, phosphatidylcholine; TE, Triton X 100 extract.</div>
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<div class="figure-caption-contents"><b> Functional architecture of Rft1. </b> <i> A… </i></div>
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<div class="figure-caption-contents"><b> Functional architecture of Rft1. </b> <i> A </i> , topology model of hRft1. The model is…</div>
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<div class="figure-caption-contents"><b>Functional architecture of Rft1.</b><i>A</i>, topology model of hRft1. The model is based on DeepTMHMM (<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://dtu.biolib.com/DeepTMHMM">https://dtu.biolib.com/DeepTMHMM</ext-link>) which predicts 14 transmembrane spans. The protein has its N and C termini oriented toward the cytoplasm. The only <i>N</i>-glycosylation sequon (N<sup>227</sup>IT) is located in the third intracellular loop (ICL3). The relative lengths of the loops are shown roughly to scale. <i>B</i>, hRft1 is not <i>N</i>-glycosylated. A protein extract from hRft1-3xFLAG-expressing KSY512 cells was treated with PNGase F (a control sample was mock-treated in parallel) and subsequently analyzed by SDS-PAGE immunoblotting using anti-FLAG antibodies (to detect hRft1) and anti-CPY antibodies. <i>Left panel</i>, <i>arrowhead</i> indicates migration of hRft1. <i>Right panel</i>, <i>arrowheads</i> indicate the positions of fully glycosylated (4 glycans) and nonglycosylated (0 glycans) CPY; <i>tick marks</i> represent the same molecular weight markers as shown in the <i>left</i> panel. <i>C</i>, fluorescence microscopy assay to test the N<sub>in</sub>, C<sub>in</sub> orientation of hRft1 in the ER membrane. <i>Top panel</i>, the C-terminal domain of Ist2 (residues 590–946) which contains a plasma membrane binding domain is fused to the C terminus of ALFA-mNG-hRft1-3xFLAG. When expressed in yeast, the fusion protein is expected to be enriched in the cER. <i>Bottom panel</i>, C terminally ALFA-nB-tagged Nvj1<sup>1-121</sup> is expressed together with P<sub>ADH</sub>-ALFA-mNG-hRft1 in yeast cells. As the ALFA-nB tag binds to the N-terminal ALFA tag of hRft1, the protein is expected to be enriched in the nER. <i>D</i>, YAKM172 (P<sub>tet</sub>-Rft1 P<sub>ADH</sub>-ALFA-mNG-hRft1), YAKM173 (P<sub>tet</sub>-Rft1 Nvj1-nB P<sub>ADH</sub>-ALFA-mNG-hRft1), and YAKM287 (P<sub>tet</sub>-Rft1 P<sub>ADH</sub>-ALFA-mNG-hRft1-Ist2<sup>590-946</sup>) were visualized by wide-field microscopy (brightfield, <i>left</i> panels; fluorescence, <i>right panels</i>). The <i>middle panels</i> show the normal distribution of ALFA-mNG-hRft1-3xFLAG in cells, similar to images shown in Fig. 1<i>E</i>. <i>Arrows</i> indicate the cER or nER. The <i>dotted line</i> (<i>bottom panel</i>) indicates the shape of an exemplary cell. The scale bar represents 5 μm. <i>E</i>, fluorescence images similar to those shown in panel D were quantified. The total fluorescence (F<sub>total</sub>) and nuclear fluorescence (F<sub>nuc</sub>) of each cell was determined by using ImageJ to measure the fluorescence within approximately circular outlines of the cell and the nucleus. Similar outlines in a cell-free area of the image were used to determine background correction. The graph shows F<sub>nuc</sub>/F<sub>total</sub> (error bars = mean ± S.D. (n > 50)) for WT, nER-restricted and cER-restricted samples. ∗∗∗∗<i>p</i> < 0.0001 using ordinary one-way ANOVA. <i>F</i>, isosurface of the AlphaFold model of hRFT1 colored by electrostatics. Position of the lipid bilayer is shown as <i>golden lattices</i> on the <i>left</i> with the luminal side on <i>top</i> and the cytosolic side below as indicated. The structure can be divided (<i>gray dashed line</i>) into two lobes each containing 7 of the 14 TM. The width of the hydrophilic cavity between the lobes is ∼23 Å as measured along the indicated <i>gold line</i> in the right view. <i>G</i>, cytosolic view of the hRFT1 model colored by ConSurf grade, with higher values indicating greater conservation as indicated in the color bar. CDG-1N associated residues (Table 2) and residues mutated and analyzed in this study are indicated by the numbers (1 = Q21, 2 = R25, 3 = R37, 4 = I43, 5 = R63, 6 = R67, 7 = C70, 8 = K152, 9 = A155, 10 = E260, 11 = G276, 12 = R290, 13 = I296, 14 = E298, 15 = Y301, 16 = G340, 17 = M408, 18 = R442). CDG, congenital disorders of glycosylation; cER, cortical ER; CPY, carboxypeptidase Y; ER, endoplasmic reticulum; hRft1, human Rft1; mNG, mNeonGreen; nB, nanobody; nER, nuclear ER; TM, transmembrane.</div>
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<div class="figure-caption-contents"><b> Analysis of cells expressing hRft1 point mutants. </b> Plasmid shuffling was used to replace…</div>
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<div class="figure-caption-contents"><b>Analysis of cells expressing hRft1 point mutants.</b> Plasmid shuffling was used to replace the hRft1-expressing <i>URA3</i> plasmid in KSY512 cells with <i>HIS3</i> plasmids expressing WT hRft1-3xFLAG or corresponding point mutants. <i>A</i>, KSY512 cells expressing hRft1-3xFLAG variants were cultured in SD(-His) medium to midlog phase and diluted to <i>A</i><sub>600</sub> = 0.01. <i>A</i><sub>600</sub> was measured every 15 min for 36 h in a plate reader. The measurement was repeated 5 times and average data are presented. <i>B</i>, KSY512 cells expressing hRft1 point mutants were cultured in SD (-His) medium to log-phase, harvested, and analyzed by SDS-PAGE and immunoblotting with anti-CPY, anti-Dpm1, and anti-FLAG antibodies. The <i>black dot</i> and <i>white dot</i> in the CPY blot indicate fully glycosylated and nonglycosylated CPY, respectively. <i>C</i>, doubling time was determined from the exponential phase of growth curves, including those shown in <i>panel A</i>. Data are shown as a bar chart (mean ± S.D. (n = 5 technical replicates)) with individual values (∗<i>p</i> = 0.0229 (R67C) and 0.0359 (K152E), ∗∗∗<i>p</i> = 0.0003, ∗∗∗∗<i>p</i> < 0.0001, ns, not significant, ordinary one-way ANOVA with all samples compared with WT). <i>D</i>, hRft1-3xFLAG protein expression levels were quantified by calculating the ratio of the intensity of the hRft1-3xFLAG band to Dpm1 and normalizing to that of the WT sample from immunoblots such as the one shown in <i>panel B</i>. Data are presented as mean ± S.D. (n = 3 biological replicates), with individual values indicated. Ordinary one-way ANOVA revealed no significant differences between the expression level of the mutants in comparison with R63A (chosen as reference because its expression was similar to that of WT hRft1-3xFLAG), except for R37A indicated as ∗<i>p</i> = 0.0138. <i>E</i>, the intensity of each CPY band from immunoblots such as the one shown in <i>panel B</i> was analyzed and quantified to obtain the CPY Glycoscore. Data are presented as mean ± S.D. (n = 3 biological replicates) (∗∗<i>p</i> = 0.0044, ∗∗∗<i>p</i> = 0.0003 (R37A), 0.0008 (C70R), 0.0001 (E260A), and 0.0005 (I296K),∗∗∗∗<i>p</i> < 0.0001, ns, not significant, ordinary one-way ANOVA with all samples compared with WT). <i>F</i>, correlation between doubling time and CPY Glycoscore. Data points are mean ± S. D. (n = 5 for doubling time, n = 3 for CPY Glcosycore). <i>G</i>, correlation between doubling time and expression. Data points are mean ± S.D. (n = 5 for doubling time, n = 3 for expression). <i>H</i>, correlation between CPY Glycoscore and expression. Data points are mean ± S.D. (n = 3). <i>G</i> and <i>H</i>, the <i>light blue</i> shaded <i>box</i> is centered on the median of all expression values (<i>x</i>-axis) with a width ± 20% of the median. The height of the box covers the <i>y</i>-axis data range. CPY, carboxypeptidase Y; hRft1, human Rft1; SD, synthetic defined.</div>
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Molecular characterization of Rft1, an ER membrane protein associated with congenital disorder of glycosylation RFT1-CDG.
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<span class="docsum-authors short-authors">Aebi M, et al.</span>
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<span class="docsum-authors full-authors">Johnsen C, Tabatadze N, Radenkovic S, Botzo G, Kuschel B, Melikishvili G, Morava E.</span>
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<span class="docsum-authors short-authors">Johnsen C, et al.</span>
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<span class="docsum-journal-citation full-journal-citation">Mol Genet Metab. 2024 Jul;142(3):108477. doi: 10.1016/j.ymgme.2024.108477. Epub 2024 Apr 18.</span>
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Ramirez A.S., Locher K.P. Structural and mechanistic studies of the N-glycosylation machinery: from lipid-linked oligosaccharide biosynthesis to glycan transfer. Glycobiology. 2023;33:861–872.
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<div id="substances" class="substances keywords-section">
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<h2 class="title">
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Substances
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</h2>
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