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||
<span class="search-input-link user-guide-link" role="navigation" aria-label="User guide">
|
||
<a href="/help/"
|
||
data-ga-category="featured_link"
|
||
data-ga-action="user_guide">
|
||
User Guide
|
||
</a>
|
||
</span>
|
||
|
||
</div>
|
||
</div>
|
||
|
||
|
||
</form>
|
||
|
||
|
||
<div id="article-page-header">
|
||
<div id="article-top-actions-bar" class="article-top-actions-bar">
|
||
<div class="inner-wrap">
|
||
<div class="actions-container">
|
||
<div class="return-to-search">
|
||
|
||
|
||
</div>
|
||
|
||
<div class="multiple-results-actions " role="region" aria-label="save, email, send to">
|
||
<button id="save-results-panel-trigger"
|
||
type="button"
|
||
class="save-results save-results-panel-trigger"
|
||
aria-expanded="false"
|
||
aria-controls="save-action-panel"
|
||
data-ga-category="save_share"
|
||
data-ga-action="save"
|
||
data-ga-label="open">
|
||
Save
|
||
</button><button id="email-results-panel-trigger"
|
||
type="button"
|
||
class="email-results email-results-panel-trigger"
|
||
aria-expanded="false"
|
||
aria-controls="email-action-panel"
|
||
data-ga-category="save_share"
|
||
data-ga-action="email"
|
||
data-ga-label="open">
|
||
Email
|
||
</button><div class="more-actions dropdown-block"><button id="more-actions-trigger"
|
||
type="button"
|
||
class="trigger more-actions-trigger"
|
||
ref="linksrc=show_moreactions_btn"
|
||
aria-label="Send to"
|
||
aria-controls="more-actions-dropdown">Send to</button><div id="more-actions-dropdown" class="dropdown dropdown-container" hidden><div class="content"><ul class="more-actions-links"><li><a class="clipboard-panel-trigger dropdown-block-link "
|
||
href="#"
|
||
role="button"
|
||
data-ga-category="save_share"
|
||
data-ga-action="clipboard"
|
||
data-ga-label="send">
|
||
Clipboard
|
||
</a></li><li><a role="button" class="dropdown-block-link bibliography-trigger-target" href="https://account.ncbi.nlm.nih.gov/?back_url=https%3A%2F%2Fpubmed.ncbi.nlm.nih.gov%2F35264790%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%2F35264790%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="s3txDnC376MExSTK26g1YGRnUU8OW35SJQdCgd5pHHz8rjZAFpT3sOn1sYQ0PEDc">
|
||
</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="s3txDnC376MExSTK26g1YGRnUU8OW35SJQdCgd5pHHz8rjZAFpT3sOn1sYQ0PEDc">
|
||
|
||
|
||
|
||
<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="s3txDnC376MExSTK26g1YGRnUU8OW35SJQdCgd5pHHz8rjZAFpT3sOn1sYQ0PEDc">
|
||
|
||
<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: 35264790 - PubMed</span>
|
||
<input type="hidden" name="email-subject" value="1 selected item: 35264790"/>
|
||
<input type="hidden" name="email-subject-hash" value="85c917d6055672505ce9b92c7c22a3fd6ddef9f094d93f2740595f6035b29e36"/>
|
||
</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="s3txDnC376MExSTK26g1YGRnUU8OW35SJQdCgd5pHHz8rjZAFpT3sOn1sYQ0PEDc">
|
||
|
||
|
||
|
||
<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="s3txDnC376MExSTK26g1YGRnUU8OW35SJQdCgd5pHHz8rjZAFpT3sOn1sYQ0PEDc">
|
||
|
||
|
||
|
||
<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="s3txDnC376MExSTK26g1YGRnUU8OW35SJQdCgd5pHHz8rjZAFpT3sOn1sYQ0PEDc">
|
||
|
||
<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="s3txDnC376MExSTK26g1YGRnUU8OW35SJQdCgd5pHHz8rjZAFpT3sOn1sYQ0PEDc">
|
||
|
||
|
||
|
||
<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="s3txDnC376MExSTK26g1YGRnUU8OW35SJQdCgd5pHHz8rjZAFpT3sOn1sYQ0PEDc">
|
||
|
||
<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="35264790">
|
||
<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://doi.org/10.1038/s41586-022-04416-7"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=False&PrId=3094&itool=Abstract-def&log$=linkouticon&uid=35264790&db=pubmed&nlmid=0410462"
|
||
title="See full text options at Nature Publishing Group"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="Nature Publishing Group"
|
||
data-ga-label="35264790"
|
||
><img src="https://cdn.ncbi.nlm.nih.gov/corehtml/query/egifs/https:--www.nature.com-static-images-logos-nature-portfolio-120.png" alt="Nature Publishing Group full text link"><span class="text">
|
||
|
||
Nature Publishing Group
|
||
|
||
</span></a><a class="link-item
|
||
pmc
|
||
"
|
||
href="https://pmc.ncbi.nlm.nih.gov/articles/pmid/35264790/"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=True&PrId=3494&itool=Abstract-def&log$=linkouticon&uid=35264790&db=pubmed&nlmid=0410462"
|
||
title="Free full text at PubMed Central"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="PMC"
|
||
data-ga-label="35264790"
|
||
><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="/35264790/citations/"
|
||
data-citation-style="nlm"
|
||
data-pubmed-format-link="/35264790/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="35264790" 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%2F35264790%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="s3txDnC376MExSTK26g1YGRnUU8OW35SJQdCgd5pHHz8rjZAFpT3sOn1sYQ0PEDc"><div class="choice-group" role="radiogroup"><ul class="radio-group-items"><li><input type="radio"
|
||
id="collections-action-dialog-new"
|
||
class="collections-new"
|
||
name="collections"
|
||
value="new"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="collections_radio_new"><label for="collections-action-dialog-new">Create a new collection</label></li><li><input type="radio"
|
||
id="collections-action-dialog-existing"
|
||
class="collections-existing"
|
||
name="collections"
|
||
value="existing"
|
||
checked="true"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="collections_radio_existing"><label for="collections-action-dialog-existing">Add to an existing collection</label></li></ul></div><div class="controls-wrapper"><div class="action-panel-control-wrap new-collections-controls"><label for="collections-action-dialog-add-to-new" class="action-panel-label required-field-asterisk">
|
||
Name your collection:
|
||
</label><input
|
||
type="text"
|
||
name="add-to-new-collection"
|
||
id="collections-action-dialog-add-to-new"
|
||
class="collections-action-add-to-new"
|
||
pattern="[^"&=<>\/]*" title="The following characters are not allowed in the Name field: "&=<>/"
|
||
maxlength="100"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="create_collection"
|
||
data-ga-label="non_favorties_collection"><div class="collections-new-name-too-long usa-input-error-message selection-validation-message">
|
||
Name must be less than 100 characters
|
||
</div></div><div class="action-panel-control-wrap existing-collections-controls"><label for="collections-action-dialog-add-to-existing" class="action-panel-label">
|
||
Choose a collection:
|
||
</label><select id="collections-action-dialog-add-to-existing"
|
||
class="action-panel-selector collections-action-add-to-existing"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="select_collection"
|
||
data-ga-label="($('.collections-action-add-to-existing').val() === 'Favorites') ? 'Favorites' : 'non_favorites_collection'"></select><div class="collections-retry-load-on-error usa-input-error-message selection-validation-message">
|
||
Unable to load your collection due to an error<br><a href="#">Please try again</a></div></div></div><div class="action-panel-actions"><button class="action-panel-submit"
|
||
type="submit"
|
||
data-loading-label="Adding..."
|
||
data-pinger-ignore
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="add">
|
||
Add
|
||
</button><button class="action-panel-cancel"
|
||
aria-label="Close 'Add to Collections' panel"
|
||
ref="linksrc=close_collections_panel"
|
||
aria-controls="collections-action-panel"
|
||
aria-expanded="false"
|
||
data-ga-category="collections_button"
|
||
data-ga-action="click"
|
||
data-ga-label="cancel">
|
||
Cancel
|
||
</button></div></form></div></div></div></div><button class="more-actions-button more-actions-dialog-trigger"
|
||
title="Open dialog with more actions to take"
|
||
ref="linksrc=more_actions_btn"></button><div class="display-options" data-format-key="format"
|
||
data-default-format-value="abstract"
|
||
data-current-format-value="abstract" role="region"><button
|
||
class="trigger usa-button"
|
||
title="Change format"
|
||
data-ga-category="display_options"
|
||
data-ga-action="display_options_dialog"><span class="button-label">Display options</span></button><div class="dropdown" hidden><div class="title">
|
||
Display options
|
||
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Ribosome collisions induce mRNA cleavage and ribosome rescue in bacteria
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data-ga-label="Roland Beckmann">Roland Beckmann</a><sup class="affiliation-links"><span class="author-sup-separator"> </span><a class="affiliation-link" title="Gene Center and Department of Biochemistry, University of Munich, Munich, Germany. beckmann@genzentrum.lmu.de." href="#full-view-affiliation-5" ref="linksrc=author_aff">
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6
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Ribosome collisions induce mRNA cleavage and ribosome rescue in bacteria
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6
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|
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><sup class="key">5</sup> Gene Center and Department of Biochemistry, University of Munich, Munich, Germany. beckmann@genzentrum.lmu.de.</li>
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<li data-affiliation-id="short-view-affiliation-6"
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><sup class="key">6</sup> Department of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore, USA. buskirk@jhmi.edu.</li>
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Ribosome rescue pathways recycle stalled ribosomes and target problematic mRNAs and aborted proteins for degradation<sup>1,2</sup>. In bacteria, it remains unclear how rescue pathways distinguish ribosomes stalled in the middle of a transcript from actively translating ribosomes<sup>3-6</sup>. Here, using a genetic screen in Escherichia coli, we discovered a new rescue factor that has endonuclease activity. SmrB cleaves mRNAs upstream of stalled ribosomes, allowing the ribosome rescue factor tmRNA (which acts on truncated mRNAs<sup>3</sup>) to rescue upstream ribosomes. SmrB is recruited to ribosomes and is activated by collisions. Cryo-electron microscopy structures of collided disomes from E. coli and Bacillus subtilis show distinct and conserved arrangements of individual ribosomes and the composite SmrB-binding site. These findings reveal the underlying mechanisms by which ribosome collisions trigger ribosome rescue in bacteria.
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© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
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Conflict of interest 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"><bold>Competing Interests:</bold> The authors declare that there are no competing interests.</p>
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<div class="figure-caption-contents"><p> SmrB is a… </p></div>
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<div class="figure-caption-contents"><p> SmrB is a general ribosome rescue factor. <b> a </b> , Reporter protein… </p></div>
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<div class="figure-caption-contents">SmrB is a general ribosome rescue factor. <b>a</b>, Reporter protein from wild-type and Δ<i>ssrA</i> strains was detected by antibodies against the N-terminal Strep-tag. Arrows indicate the full-length fusion protein (FL) and shorter NanoLuc protein (N). The RpoB protein serves as a loading control. <b>b</b>, Additional reporters to study ribosome rescue in <i>E. coli</i> with various stalling motifs. <b>c</b>, The expression of full-length NanoLuc-Ble protein was monitored with an anti-FLAG antibody; anti-Strep antibodies reveal both full-length NanoLuc-Ble and truncated NanoLuc protein. RpoB serves as a loading control.</div>
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<div class="figure-caption-contents">Phylogenetic tree of SMR domain proteins. Stylized phylogenetic tree depicting relationships between SMR domain clades. Clades with indicated bootstrap support are marked with circles. Clade names are given to the right of the tree. Dotted lines indicate positions with little or no bootstrap support.</div>
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<div class="figure-caption-contents">Distribution and architectures of SMR-domain proteins. <b>a</b>, Heat map demonstrating the conservation and distribution of SMR-domain proteins and other related translational quality control factors. Smr-all includes all types of SMR-domain proteins; Smr-euk includes only the eukaryotic branch. <b>b</b>, Domain organization of three representative bacterial proteins containing an SMR domain. <b>c</b>, Multiple alignment of the conserved regions in the N-terminal extension of SMR proteins from proteobacteria. Columns in the alignment are shaded and labeled according to biochemical character: -, negatively charged; h, hydrophobic in yellow; a, aromatic; p, polar in blue; l, aliphatic in yellow; s, small in green; u, tiny in green. Residue positions in the --xxxa motif are colored in white and shaded in black, marked by asterisks above the alignment. Residue positions forming part of the active site of the core SMR domain are colored in white and shaded in red. Sequences are labeled with NCBI accession number and organism abbreviation; abbreviations are provided below alignment. Secondary structure provided at top of alignment. Numbers to left and right of alignment denote positioning of the region. Internal numbers give the size of excised variable insert regions. <b>d</b>, Sequence alignment of SMR domains of representative proteins. Identical residues are shown in white with a red background; conserved residues are shown in red. The identity of each sequence is represented by the gene name, species name, and numbers indicating the beginning and the end of the residues used for the alignment. Ecol, <i>Escherichia coli</i>; Scer, <i>Saccharomyces cerevisiae</i>; Cele, <i>Caenorhabditis elegans</i>; Hsap, <i>Homo sapiens</i>; Atha, <i>Arabidopsis thaliana</i>; Bsub, <i>Bacillus subtilis</i>.</div>
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<div class="figure-caption-contents"><p> SmrB cleavage, tmRNA tagging, and ribosome collisions. <b> a </b> , The results… </p></div>
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|
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Extended Data Fig. 4:
|
||
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|
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|
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|
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|
||
<div class="figure-caption-contents">SmrB cleavage, tmRNA tagging, and ribosome collisions. <b>a</b>, The results of 5’-RACE showing the 5’-ends of downstream fragments in reads per million on the EP* reporter. The first nt in the A site codon in the stall motif is designated as zero. <b>b</b>, The results of 3’-RACE showing the 3’-ends of upstream fragments. <b>c</b>, tmRNA tagging sites on the EP* reporter in the wild-type and Δ<i>smrB</i> strains, corresponding to the residue immediately preceding the tmRNA tag in peptide sequences detected by targeted LC-MS-MS. The relative spectrum count is normalized by the count at the EP* stall site (red) where tmRNA tagging was expected to occur in both the wild-type and Δ<i>smrB</i> strains. The spectrum count corresponds to the mean and the standard deviation of three replicates. The arrow indicates the SmrB cleavage site demonstrated by 5’-RACE. <b>d</b>, 5’-RACE data on the Short SecM reporter reveal the SmrB cleavage sites as in Fig. 2b, zoomed in to show smaller peaks upstream. <b>e</b>, The distribution of FLAG-SmrB in cells treated with 5, 50, or 500 μg/mL erythromycin (ERY) was determined by fractionation over a sucrose gradient and detected with an anti-FLAG antibody.</div>
|
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|
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<p> Extended Data Fig. 5: </p>
|
||
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|
||
|
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|
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|
||
<div class="figure-caption-contents"><p> Cryo-EM data processing for the <i> E. coli </i> disome sample. Shown are… </p></div>
|
||
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|
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|
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Extended Data Fig. 5:
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents">Cryo-EM data processing for the <i>E. coli</i> disome sample. Shown are the classification scheme, representative micrographs (the scale bar is 500 Å), 2D class averages and the Gold standard Fourier Shell Correlation (GSFSC) curve for the volume containing the 70S stalled ribosome and the 30S of the collided ribosome, as well as the full disome.</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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<p> Extended Data Fig. 6: </p>
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> Analysis of the <i> E. coli </i> disome structure and comparison of different… </p></div>
|
||
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||
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|
||
Extended Data Fig. 6:
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">Analysis of the <i>E. coli</i> disome structure and comparison of different disome structures. <b>a</b>, The architecture of the <i>E. coli</i> disome is not compatible with bS1 remaining bound to the stalled ribosome. Aligned models of the 30S subunits of the collided (left) and the stalled (middle) ribosomes are shown in surface representation. The position of bS1 as observed in the collided ribosome is shown in purple and the same position of bS1 in the stalled ribosome is indicated by a dashed line. The clash between bS1 of the stalled ribosome and the 30S subunit of the collided ribosome that would occur upon disome formation is shown on the right. <b>b</b>, Cartoon representation of the individual interactions as they occur at the <i>E. coli</i> disome interface. <b>c</b>, 2D class averages and cryo-EM structure model of an <i>E. coli</i> trisome. <b>d</b>&<b>e</b>, Comparison of the <i>E. coli</i> (<i>E.c</i>.) and <i>B. subtilis</i> (<i>B.s</i>.) disomes displaying full and cut views. Note the smaller space between stalled and collided ribosomes in the <i>B.s</i>. disome interface as illustrated by comparing the positions of uS2 proteins in the zoomed view in <b>c</b>. <b>f</b>, Surface representation of the structural model of the <i>S. cerevisiae</i> disome. <b>g</b>&<b>h</b>, Surface representation of the <i>E. coli</i> and <i>B. subtilis</i> hibernation disomes.</div>
|
||
|
||
|
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|
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|
||
<p> Extended Data Fig. 7: </p>
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> Cryo-EM data processing… </p></div>
|
||
|
||
|
||
|
||
|
||
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|
||
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|
||
|
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|
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|
||
|
||
|
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|
||
<strong class="figure-label">
|
||
<p> Extended Data Fig. 7: </p>
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> Cryo-EM data processing for the <i> B. subtilis </i> disome and <i> E. coli… </i> </p></div>
|
||
|
||
|
||
|
||
|
||
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|
||
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||
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|
||
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|
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|
||
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|
||
<strong class="figure-label">
|
||
Extended Data Fig. 7:
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">Cryo-EM data processing for the <i>B. subtilis</i> disome and <i>E. coli</i> trisome sample. <b>a</b>, Shown are the classification scheme, and the Gold standard Fourier Shell Correlation (GSFSC) curves for the final volumes of the <i>B. subtilis</i> disome containing the 70S stalled ribosome and the 70S of the collided ribosome. <b>b</b>, Shown are the 2D class averages, classification scheme, and the Gold standard Fourier Shell Correlation (GSFSC) of the <i>E. coli</i> trisome.</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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|
||
<p> Extended Data Fig. 8: </p>
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> Production of collided… </p></div>
|
||
|
||
|
||
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||
|
||
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|
||
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|
||
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|
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|
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<p> Extended Data Fig. 8: </p>
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> Production of collided and non-collided disomes and relative peak areas of… </p></div>
|
||
|
||
|
||
|
||
|
||
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|
||
|
||
<figcaption id="figure-caption-7" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
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<strong class="figure-label">
|
||
Extended Data Fig. 8:
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">Production of collided and non-collided disomes and relative peak areas of monosomes and disomes in the SmrB nuclease assay. <b>a</b>, mRNA construct to create the collided <i>E. coli</i> disomes and trisomes and below the sucrose density gradient after <i>in vitro</i> translation. The ribosome stalling site is indicated by an asterisk. <b>b</b>, mRNA construct to create the non-collided disomes that were used in the nuclease assay and below the sucrose density gradient after <i>in vitro</i> translation. <b>c</b>, Relative monosome and disome peak area calculated from the sucrose gradient profiles of the SmrB nuclease assay, showing the mean and standard deviation of three replicates. <b>d</b>, The relative decrease of the area of the disome peak upon addition of SmrB is shown as the mean and standard deviation of three replicates. (The mean difference of the relative disome peak area of collided ribosomes between control and SmrB reaction was set to 1).</div>
|
||
|
||
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||
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||
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<p> Extended Data Fig. 9: </p>
|
||
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|
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|
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|
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|
||
<div class="figure-caption-contents"><p> Cryo-EM data processing… </p></div>
|
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<p> Extended Data Fig. 9: </p>
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> Cryo-EM data processing for the <i> E. coli </i> disome sample. Shown are… </p></div>
|
||
|
||
|
||
|
||
|
||
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|
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Extended Data Fig. 9:
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents">Cryo-EM data processing for the <i>E. coli</i> disome sample. Shown are the classification scheme, representative micrographs (the scale bar is 500 Å), 2D class averages and the Gold standard Fourier Shell Correlation (GSFSC) curve for the respective 3D reconstructions. The segmented density for SmrB is colored according to local resolution.</div>
|
||
|
||
|
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|
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<strong class="figure-label">
|
||
<p> Extended Data Fig. 10: </p>
|
||
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|
||
|
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||
<div class="figure-caption-contents"><p> Structural model of… </p></div>
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|
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<strong class="figure-label">
|
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<p> Extended Data Fig. 10: </p>
|
||
</strong>
|
||
|
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|
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|
||
<div class="figure-caption-contents"><p> Structural model of SmrB. <b> a </b> , Secondary structure of SmrB. The… </p></div>
|
||
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|
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<strong class="figure-label">
|
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Extended Data Fig. 10:
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">Structural model of SmrB. <b>a</b>, Secondary structure of SmrB. The DLH to ALA mutation is indicated. <b>b</b>, AF2 prediction models 1–5 as predicted through the API from the Söding lab. The SMR domain is predicted with high confidence, while the linker to the N-terminal helix appears flexible. <b>c</b>, AF2 prediction of the interaction between SmrB and uS2. For this prediction uS2 was fused to the C-terminus of SmrB with a glycine serine linker (39 copies of GS). The prediction shows the N-terminal helix of SmrB folded back onto uS2. <b>d</b>, Adjustment of the AF2 predicted model of SmrB-uS2. Without adjustment according to the cryo-EM density (as shown in D) the SMR domain would clash with the ribosome. <b>e</b>, Top: Cryo-EM density and adjusted model of the SmrB. Middle: Cryo-EM density and rigid body docked model of the N-terminus of SmrB from the collided 30S onto the stalled 30S. A second copy of SmrB was found anchored to uS2 of the stalled ribosome. However, there was no density for the SMR domain of the second SmrB, indicating a high degree of flexibility due to the lack of another ribosome in front of the stalled one. Bottom: in the control disome without SmrB, there is no density for the N-terminus of SmrB. <b>f</b>, Comparison of the AF2 prediction, the homology model, and the adjusted model of SmrB. Compared to the AF2 prediction, the homology model is missing the two N-terminal helices and most of the loops are slightly different (top). The AF2 prediction almost perfectly matched the cryo-EM density map and the corresponding adjusted model (middle and bottom). Only the catalytic loop (carrying the active site mutations) had to be slightly adjusted to prevent clashes with the mRNA. The N-terminus was adjusted as discussed above. <b>g</b>. During the preparation of this manuscript the AF2 prediction for SmrB (YfcN) became available at the alphafold database at EMBL-EBI. The deposited model resembles our final adjusted model very well including the position of the N-terminus. The confidence of the prediction (pLDDT) is indicated.</div>
|
||
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|
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||
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|
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|
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<p> Extended Data Fig. 11: </p>
|
||
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|
||
|
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|
||
|
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<div class="figure-caption-contents"><p> Testing the importance… </p></div>
|
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|
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|
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<p> Extended Data Fig. 11: </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> Testing the importance of structural interactions for SmrB activity. <b> a </b> ,… </p></div>
|
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<strong class="figure-label">
|
||
Extended Data Fig. 11:
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">Testing the importance of structural interactions for SmrB activity. <b>a</b>, Examples of operons containing both uS21 and SMR-domain proteins. <b>b</b>, The distribution of FLAG-tagged full-length SmrB and a construct with only the SMR domain (residues 88–183) was determined by fractionation over sucrose gradient and detection with an anti-FLAG antibody. A non-specific band is marked with *. <b>c</b>, Northern blots using the 3’-probe against the CRP reporters with the short SecM stalling motif in wild-type cells, bL9-deletion strain (Δr<i>plI</i>), and a strain where mCherry is fused to the C-terminus of bL9 (bL9-mCherry). Ethidium bromide staining of 16S rRNA serves as a loading control. <b>d</b>, Northern blots using the 3’-probe against the CRP reporters with the short SecM stalling motif in wild-type cells, a strain where MBP is fused to the N-terminus of uS21, and a strain where GFP is fused to the C-terminus of uS6.</div>
|
||
|
||
|
||
|
||
|
||
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|
||
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||
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||
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|
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data-image-alt="Figure 1."
|
||
data-pmc-id="PMC8934283"
|
||
data-figure-id="F1">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
||
id="article-image-11"
|
||
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/650c/8934283/bd3c6ff6d543/nihms-1777247-f0001.gif"
|
||
alt="Figure 1." />
|
||
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|
||
|
||
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|
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|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 1. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> SmrB is a ribosome rescue… </p></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
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|
||
|
||
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|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 1. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> SmrB is a ribosome rescue factor. <b> a </b> , Between NanoLuc and the bleomycin… </p></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-11" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure 1.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">SmrB is a ribosome rescue factor. <b>a</b>, Between NanoLuc and the bleomycin resistance gene, we inserted stop codons, no added sequence, or the SecM stalling motif (black). <b>b</b>, Sections of plates with or without 50 μg/mL phleomycin showing growth of wild-type and Δ<i>smrB</i> strains with reporters. <b>c</b>, The results of Tn-seq showing the number of transposon insertions for each gene (rpkm). <b>d</b>, Serial dilutions of wild-type and Δ<i>smrB</i> cultures on plates with and without 200 μg/mL erythromycin. <b>e</b>, Domain organization of <i>E. coli</i> SmrB. Mutations at the conserved DxH and GxG motifs are indicated. <b>f</b>, Full-length SecM reporter protein was detected with anti-FLAG antibodies. Loading control = RpoB. F-SmrB, F-ALA, and F-GAG represent endogenously FLAG-tagged SmrB (not shown). <b>g</b>, SecM reporter mRNA was detected using a 3’-probe. Loading control = 23S rRNA. FL = full-length and Dn = downstream mRNA fragment.</div>
|
||
|
||
|
||
|
||
|
||
</figcaption>
|
||
|
||
|
||
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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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|
||
data-image-alt="Figure 2."
|
||
data-pmc-id="PMC8934283"
|
||
data-figure-id="F2">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
||
id="article-image-12"
|
||
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/650c/8934283/97175a56f336/nihms-1777247-f0002.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> SmrB cleavage at the 5’… </p></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
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|
||
|
||
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|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 2. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> SmrB cleavage at the 5’ boundary of stalled ribosomes promotes ribosome rescue. <b> a… </b> </p></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-12" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure 2.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">SmrB cleavage at the 5’ boundary of stalled ribosomes promotes ribosome rescue. <b>a</b>, Northern blots of reporter mRNA using the 5’-probe and the 3’-probe show full-length (FL) or truncated RNAs (upstream or downstream fragments). Loading control = 23S rRNA. <b>b</b>, 5’-RACE reveals the 5’-ends of downstream fragments in reads per million on the SecM reporter. The first nt in the A-site codon in the stall motif is 0. <b>c</b>, 3’-RACE reveals the 3’-ends of upstream fragments. <b>d</b>, tmRNA tagging sites on the Short SecM reporter in the wild-type and Δ<i>smrB</i> strains were detected by targeted LC-MS-MS. The relative spectrum count is normalized by the count at the SecM stall site (red). The mean and standard deviation of three replicates is shown. The arrow indicates the SmrB cleavage site. <b>e</b>, A model for mRNA processing during ribosome rescue.</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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|
||
data-figure-id="F3">
|
||
<img class="figure-thumb" itemprop="thumbnail"
|
||
id="article-image-13"
|
||
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/650c/8934283/b422173d39f7/nihms-1777247-f0003.gif"
|
||
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|
||
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|
||
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||
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|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 3. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> SmrB acts on collided ribosomes.… </p></div>
|
||
|
||
|
||
|
||
|
||
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|
||
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|
||
|
||
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|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 3. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> SmrB acts on collided ribosomes. <b> a </b> , The distribution of FLAG-SmrB in a… </p></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-13" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
Figure 3.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">SmrB acts on collided ribosomes. <b>a</b>, The distribution of FLAG-SmrB in a sucrose gradient was observed with anti-FLAG antibodies in samples with and without mupirocin treatment (to induce pauses at Ile codons). A non-specific band is marked with *. <b>b</b>, The distribution of FLAG-SmrB in lysates treated with RNase A. <b>c</b>, Samples treated with four different tetracycline concentrations were analyzed as in a. <b>d</b>, Various lengths of the <i>crp</i> gene were fused to <i>ble</i> with the short SecM motif between them. N represents the number of nucleotides between the start codon and stall site. Reporter mRNA was detected using the 3’-probe. An arrow indicates the downstream fragment. Loading control = 16S rRNA.</div>
|
||
|
||
|
||
|
||
|
||
</figcaption>
|
||
|
||
|
||
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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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|
||
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|
||
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|
||
|
||
|
||
|
||
|
||
|
||
<strong class="figure-label">
|
||
<p> Figure 4. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> Cryo-EM structure of the <i> E.… </i> </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">
|
||
<p> Figure 4. </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> Cryo-EM structure of the <i> E. coli </i> disome. <b> a </b> , Cryo-EM density map of… </p></div>
|
||
|
||
|
||
|
||
|
||
</div>
|
||
|
||
<figcaption id="figure-caption-14" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
|
||
|
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|
||
|
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|
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|
||
<strong class="figure-label">
|
||
Figure 4.
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">Cryo-EM structure of the <i>E. coli</i> disome. <b>a</b>, Cryo-EM density map of the <i>E. coli</i> disome with 50S subunits in grey, 30S subunits of the stalled and collided ribosome in yellow and orange, respectively, tRNAs in green, bS1 in purple, and bL9 in blue. <b>b</b>, Structural model of the <i>E. coli</i> disome. The bL9 proteins from stalled (bL9<sub>S</sub>) and collided (bL9<sub>C</sub>) ribosomes adopt different conformations. <b>c</b>, Interactions at the disome interface (opened up by rotation of the stalled and collided ribosomes); interacting partners are shown in matching colors.</div>
|
||
|
||
|
||
|
||
|
||
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<div class="figure-caption-contents"><p> Cryo-EM structure of the SmrB-bound <i> E. coli </i> disome. <b> a </b> , Disome nuclease assay.… </p></div>
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<div class="figure-caption-contents">Cryo-EM structure of the SmrB-bound <i>E. coli</i> disome. <b>a</b>, Disome nuclease assay. Sucrose gradients showing VemP-stalled disomes alone (ctrl) and incubated with wild-type (SmrB) or nuclease- deficient SmrB (mutant). Y-axes are A260 nm. <b>b</b>, Sucrose gradients showing collided disomes (left) and non-collided disomes (right) alone and with SmrB. Y-axes are A260 nm. <b>c</b>, Cryo-EM density map of the SmrB-bound <i>E. coli</i> disome with SmrB in pink. <b>d</b>, Zoomed view of the disome interface comparing the SmrB bound (left) and unbound (right) maps. <b>e</b>, Isolated cryo-EM density with the fitted SmrB model. <b>f</b>, Structural model of SmrB bound to the <i>E. coli</i> disome. <b>g</b>, Interactions between SmrB and the stalled and collided ribosomes. The disome interface is opened up by rotation of the stalled and collided ribosomes. <b>h & i</b>, Interactions of SmrB with the collided ribosome (h) and the stalled ribosome (i). The orientations with respect to g are indicated. <b>j</b>, Cut view of the SmrB-bound disome showing the mRNA path. <b>k</b>, Interaction of SmrB with the mRNA. The orientation in the upper part of k corresponds to j. Approximately 8 nucleotides of the mRNA are exposed at the disome interface, in reach for SmrB cleavage. The nucleotides at the ribosome boundaries are indicated; the first nucleotide in the A site of the stalled ribosome is 0.</div>
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Ribosome collisions: New ways to initiate ribosome rescue.
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Ribosomes* / metabolism
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</div>
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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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