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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%2F36873931%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%2F36873931%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="2ikThhQFkXcK1zcD8OZOQVXKGW9OdFgkj54YU7j1UyZeV0itL7CQk3toe0R06gOE">
|
||
</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="2ikThhQFkXcK1zcD8OZOQVXKGW9OdFgkj54YU7j1UyZeV0itL7CQk3toe0R06gOE">
|
||
|
||
|
||
|
||
<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="2ikThhQFkXcK1zcD8OZOQVXKGW9OdFgkj54YU7j1UyZeV0itL7CQk3toe0R06gOE">
|
||
|
||
<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: 36873931 - PubMed</span>
|
||
<input type="hidden" name="email-subject" value="1 selected item: 36873931"/>
|
||
<input type="hidden" name="email-subject-hash" value="b716e32bfc8819980fbab32b864f3b224bd0ba0e5dac5b04d0d79d7df77acfb2"/>
|
||
</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="2ikThhQFkXcK1zcD8OZOQVXKGW9OdFgkj54YU7j1UyZeV0itL7CQk3toe0R06gOE">
|
||
|
||
|
||
|
||
<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="2ikThhQFkXcK1zcD8OZOQVXKGW9OdFgkj54YU7j1UyZeV0itL7CQk3toe0R06gOE">
|
||
|
||
|
||
|
||
<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="2ikThhQFkXcK1zcD8OZOQVXKGW9OdFgkj54YU7j1UyZeV0itL7CQk3toe0R06gOE">
|
||
|
||
<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="2ikThhQFkXcK1zcD8OZOQVXKGW9OdFgkj54YU7j1UyZeV0itL7CQk3toe0R06gOE">
|
||
|
||
|
||
|
||
<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="2ikThhQFkXcK1zcD8OZOQVXKGW9OdFgkj54YU7j1UyZeV0itL7CQk3toe0R06gOE">
|
||
|
||
<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="36873931">
|
||
<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/10.3389/fgene.2023.1117821"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=False&PrId=6956&itool=Abstract-def&log$=linkouticon&uid=36873931&db=pubmed&nlmid=101560621"
|
||
title="See full text options at Frontiers Media SA"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="Frontiers Media SA"
|
||
data-ga-label="36873931"
|
||
><img src="https://cdn.ncbi.nlm.nih.gov/corehtml/query/egifs/https:--www.frontiersin.org-alerts-logo-PubMed.png" alt="Frontiers Media SA full text link"><span class="text">
|
||
|
||
Frontiers Media SA
|
||
|
||
</span></a><a class="link-item
|
||
pmc
|
||
"
|
||
href="https://pmc.ncbi.nlm.nih.gov/articles/pmid/36873931/"
|
||
target="_blank"
|
||
rel="noopener"
|
||
|
||
ref="linksrc=fulltextorjournal_fulltext&is_pmc=True&PrId=3494&itool=Abstract-def&log$=linkouticon&uid=36873931&db=pubmed&nlmid=101560621"
|
||
title="Free full text at PubMed Central"
|
||
|
||
data-ga-category="full_text"
|
||
data-ga-action="PMC"
|
||
data-ga-label="36873931"
|
||
><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="/36873931/citations/"
|
||
data-citation-style="nlm"
|
||
data-pubmed-format-link="/36873931/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="36873931" 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%2F36873931%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="2ikThhQFkXcK1zcD8OZOQVXKGW9OdFgkj54YU7j1UyZeV0itL7CQk3toe0R06gOE"><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">
|
||
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</a></li></ul></div></div></div><span class="period">. </span><span class="cit">2023 Feb 17:14:1117821.</span>
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Pathogenic gene variants in <i>CCDC39</i>, <i>CCDC40</i>, <i>RSPH1</i>, <i>RSPH9</i>, <i>HYDIN,</i> and <i>SPEF2</i> cause defects of sperm flagella composition and male infertility
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Pathogenic gene variants in <i>CCDC39</i>, <i>CCDC40</i>, <i>RSPH1</i>, <i>RSPH9</i>, <i>HYDIN,</i> and <i>SPEF2</i> cause defects of sperm flagella composition and male infertility
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data-ga-label="H Omran">H Omran</a><sup class="affiliation-links"><span class="author-sup-separator"> </span><a class="affiliation-link" title="Department of General Pediatrics, University Hospital Münster, Münster, Germany." href="#short-view-affiliation-1" ref="linksrc=author_aff">
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><sup class="key">1</sup> Department of General Pediatrics, University Hospital Münster, Münster, Germany.</li>
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<li data-affiliation-id="short-view-affiliation-2"
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><sup class="key">2</sup> Department of Clinical and Surgical Andrology, Centre of Reproductive Medicine and Andrology, University Hospital Münster, Münster, Germany.</li>
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<li data-affiliation-id="short-view-affiliation-3"
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><sup class="key">3</sup> Centre of Reproductive Medicine and Andrology, University Hospital Münster, University of Münster, Münster, Germany.</li>
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<li data-affiliation-id="short-view-affiliation-4"
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id="short-view-affiliation-4"
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><sup class="key">4</sup> Institute of Reproductive Genetics, University of Münster, Münster, Germany.</li>
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<strong class="current-id" title="PubMed ID">36873931</strong>
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ref="linksrc=article_id_link&article_id=10.3389/fgene.2023.1117821&id_type=DOI"
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10.3389/fgene.2023.1117821
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Primary Ciliary Dyskinesia (PCD) is a rare genetic disorder affecting the function of motile cilia in several organ systems. In PCD, male infertility is caused by defective sperm flagella composition or deficient motile cilia function in the efferent ducts of the male reproductive system. Different PCD-associated genes encoding axonemal components involved in the regulation of ciliary and flagellar beating are also reported to cause infertility due to multiple morphological abnormalities of the sperm flagella (MMAF). Here, we performed genetic testing by next generation sequencing techniques, PCD diagnostics including immunofluorescence-, transmission electron-, and high-speed video microscopy on sperm flagella and andrological work up including semen analyses. We identified ten infertile male individuals with pathogenic variants in <i>CCDC39</i> (one) and <i>CCDC40</i> (two) encoding ruler proteins, <i>RSPH1</i> (two) and <i>RSPH9</i> (one) encoding radial spoke head proteins, and <i>HYDIN</i> (two) and <i>SPEF2</i> (two) encoding CP-associated proteins, respectively. We demonstrate for the first time that pathogenic variants in <i>RSPH1</i> and <i>RSPH9</i> cause male infertility due to sperm cell dysmotility and abnormal flagellar RSPH1 and RSPH9 composition. We also provide novel evidence for MMAF in <i>HYDIN</i>- and <i>RSPH1</i>-mutant individuals. We show absence or severe reduction of CCDC39 and SPEF2 in sperm flagella of <i>CCDC39</i>- and <i>CCDC40</i>-mutant individuals and <i>HYDIN</i>- and <i>SPEF2</i>-mutant individuals, respectively. Thereby, we reveal interactions between CCDC39 and CCDC40 as well as HYDIN and SPEF2 in sperm flagella. Our findings demonstrate that immunofluorescence microscopy in sperm cells is a valuable tool to identify flagellar defects related to the axonemal ruler, radial spoke head and the central pair apparatus, thus aiding the diagnosis of male infertility. This is of particular importance to classify the pathogenicity of genetic defects, especially in cases of missense variants of unknown significance, or to interpret <i>HYDIN</i> variants that are confounded by the presence of the almost identical pseudogene <i>HYDIN2</i>.
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Keywords:
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CP-complex; MMAF; PCD; RS head; asthenozoospermia; axonemal ruler.
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</p>
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<p class="copyright" id="copyright">
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Copyright © 2023 Aprea, Wilken, Krallmann, Nöthe-Menchen, Olbrich, Loges, Dougherty, Bracht, Brenker, Kliesch, Strünker, Tüttelmann, Raidt and Omran.
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<p class="disclaimer" id="disclaimer">
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<a href="/disclaimer/" target="_blank" data-ga-category="literature_resources"
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data-ga-action="disclaimer_link" data-ga-label="under_abstract">PubMed Disclaimer</a>
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<div class="conflict-of-interest" id="conflict-of-interest">
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<h2 class="title">
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Conflict of interest statement
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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">The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
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<div class="figure-caption-contents"><p> Schematic of the composition of motile 9 + 2 cilia and sperm flagella… </p></div>
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FIGURE 1
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<div class="figure-caption-contents">Schematic of the composition of motile 9 + 2 cilia and sperm flagella as well as representation of selected functional axonemal protein complexes involved in ciliary and flagellar beat regulation. <b>(A)</b> The upper panel shows a schematic representation of a ciliated respiratory epithelial cell (left) and a sperm cell (right). The sperm flagellum is divided into three regions; the mid piece, principal- and end piece. The middle panel shows cross sections through a respiratory cilia and the sperm flagellum. Both share a 9 + 2 axoneme composed of nine outer microtubule doublets (A- and B-tubule) surrounding a centered single pair of microtubules. Each outer A-tubule carries dynein based motor protein complexes, the outer- and inner dynein arms (respectively ODA and IDA). A nexin-link dynein regulatory complex (N-DRC) interconnects the outer doublets, while radial spoke (RS) complexes connect them to the central pair (CP) complex. In the sperm flagellar principal- and mid-piece the axoneme is additionally surrounded by accessory structures, such as the outer dense fibers (ODFs), the fibrous sheath (FS) and the mitochondrial (MT) sheath. <b>(B)</b> The lower panel shows schematics of the axonemal ruler, the RS and the CP complex. The ruler complex is representatively depicted in a longitudinal section of the axoneme. CCDC39 and CCDC40 form a heterodimer that is supposed to be located at the interface of the N-DRC and IDAs (composed of double headed IDA I1 with heavy chains α and β and the intermediate- and light chain (IC/LC) complex, and single headed IDAs a-e, and g) (Olbrich et al., 2015; Yamamoto et al., 2021). The RS complex is composed of a stalk and a head structure. RSPH1 and RSPH9, here highlighted, are known to be components of the RS head in human respiratory cilia (Frommer et al., 2015). The CP-complex is composed of two central microtubules connected by three intermicrotubular bridges. Several protein complexes are associated with the CP, e.g., the C1b and C2b projections, containing the proteins SPEF2 and HYDIN, respectively. In human respiratory cilia localization of SPEF2 depends on functional HYDIN (Cindrić et al., 2019).</div>
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<p> FIGURE 2 </p>
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<div class="figure-caption-contents"><i> CCDC40 </i> -mutant individuals display MMAF…</div>
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||
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<p> FIGURE 2 </p>
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<div class="figure-caption-contents"><i> CCDC40 </i> -mutant individuals display MMAF and CCDC39 is absent from CCDC39- and CCDC40-mutant…</div>
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||
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FIGURE 2
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||
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||
<div class="figure-caption-contents"><i>CCDC40</i>-mutant individuals display MMAF and CCDC39 is absent from CCDC39- and CCDC40-mutant sperm flagellar axonemes. Sperm cells from healthy control donors and infertile male individuals with pathogenic variants in CCDC39 and CCDC40 were co-stained with antibodies directed against acetylated α-tubulin (acet. tubulin; depicted in green) and CCDC39 (depicted in red). <b>(A)</b> In control sperm, immunoreactivity against CCDC39 (red) is observed along the entire flagella length. The CCDC39 signal co-localizes with the flagellar marker acet. tubulin (depicted in yellow in the merged image). <b>(B–D)</b> In sperm flagella of <i>CCDC39</i>-mutant individual OP-122 and <i>CCDC40</i>-mutant individuals OP-11 II2 and OP-1516 II1, no signal against CCDC39 is observed along the flagellar axoneme. <b>(E–G)</b> Sperm cells of <i>CCDC39</i>-mutant individual OP-122 and <i>CCDC40</i>-mutant individuals OP-11 II2 and OP-1516 II1 display morphological abnormalities, comprising short, bend and irregular flagella, as well as head defects. The schematic representatively shows the localization of the CCDC39/CCDC40 heterodimer. Nuclei were stained with Hoechst33342. Scale bars represent 10 µm.</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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<div class="figure-caption-contents"><p> TEM analyses of <i> CCDC40 </i> -mutant… </p></div>
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<div class="figure-caption-contents"><p> TEM analyses of <i> CCDC40 </i> -mutant sperm cells show morphological abnormalities and tubular disorganisation.… </p></div>
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FIGURE 3
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<div class="figure-caption-contents">TEM analyses of <i>CCDC40</i>-mutant sperm cells show morphological abnormalities and tubular disorganisation. <b>(A)</b> TEM micrographs of sperm samples from a healthy control donor, showing a flagellar cross section with a regular 9 + 2 axoneme of microtubule doublets (MTD), (left image), and a longitduinal section showing the axoneme (Ax) at the center, with regularly composed mitochondria (MIT) and fibrous sheath (FS), respectively in the flagellar mid piece and principal piece (right image). <b>(B)</b>
|
||
<i>CCDC40-</i>mutant individual OP-1516 II1 shows morphological abnormalities of the sperm cells. Some sperm cells depict severe head malformations and lack proper flagella, displaying a cytoplasmic bag with unassembled peri-axonemal components, such as outer dense fibers (ODF) and mitochondria (right and middle image). In sperm flagella cross sections, axonemes show severe tubular disorganization (left image).</div>
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<strong class="figure-label">
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<p> FIGURE 4 </p>
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<div class="figure-caption-contents"><i> RSPH1 </i> and <i> RSPH9 </i> mutations cause…</div>
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<p> FIGURE 4 </p>
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<div class="figure-caption-contents"><i> RSPH1 </i> and <i> RSPH9 </i> mutations cause abnormal radial spoke head composition in sperm flagella.…</div>
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<strong class="figure-label">
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FIGURE 4
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<div class="figure-caption-contents"><i>RSPH1</i> and <i>RSPH9</i> mutations cause abnormal radial spoke head composition in sperm flagella. Sperm cells from healthy control donors and infertile male individuals with pathogenic variants in <i>RSPH1</i> and <i>RSPH9</i> were co-stained with antibodies directed against acetylated α-tubulin (acet. tubulin; depicted in green) and RSPH1 and RSPH9, respectively (both depicted in red). <b>(A)</b> In control sperm cells, immunoreactivity against RSPH1 (red) is observed along the entire flagellar length. The RSPH1 signal co-localizes with the flagellar marker acet. tubulin (depicted in yellow in the merged image). <b>(B,C)</b> In sperm flagella of <i>RSPH1</i>-mutant individuals OP-3257 II1 and OP-3957 II1, a severe reduction of the RSPH1 signal or no signal is observed along the flagellar axonemes. <b>(D)</b> Sperm cells of <i>RSPH1</i>-mutant individual OP-3957 II1 display morphological abnormalities, comprising bent flagella and sperm head defects consistent with MMAF. <b>(E)</b> In control sperm cells, RSPH9 (red) shows a panaxonemal staining pattern and co-localization with the flagellar marker acet. tubulin (depicted in yellow in the merged image). <b>(F)</b> In contrast, sperm flagella of the <i>RSPH9</i>-mutant individual OP-2491 II1 display a severe reduction of the RSPH9 signal. The schematic shows the putative localization of the RSPH1 and RSPH9 proteins in the radial spoke head complex. Nuclei were stained with Hoechst33342. Scale bars represent 10 µm.</div>
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ebf6/9981940/527cde0a8509/fgene-14-1117821-g005.gif"
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<p> FIGURE 5 </p>
|
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|
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|
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|
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|
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<div class="figure-caption-contents"><p> TEM analyses of <i> RSPH1 </i> -mutant… </p></div>
|
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|
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<strong class="figure-label">
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<p> FIGURE 5 </p>
|
||
</strong>
|
||
|
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|
||
|
||
<div class="figure-caption-contents"><p> TEM analyses of <i> RSPH1 </i> -mutant sperm cells displayed morphological abnormalities of the midpiece… </p></div>
|
||
|
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|
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|
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|
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<strong class="figure-label">
|
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FIGURE 5
|
||
</strong>
|
||
|
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|
||
|
||
<div class="figure-caption-contents">TEM analyses of <i>RSPH1</i>-mutant sperm cells displayed morphological abnormalities of the midpiece and head region, but preservation of the 9 + 2 axonemal organization. <b>(A)</b> TEM micrographs of sperm samples from a healthy control donor, showing a flagellar cross section with a regular 9 + 2 axoneme of microtubule doublets (MTD), (left image), and a longitudinal section, with regularly arranged mitochondria (MIT) and fibrous sheath (FS), respectively in the flagellar mid piece and principal piece (right image). <b>(B)</b> TEM micrographs of sperm samples from the <i>RSPH1</i>-mutant individual OP-3957 II1 show morphological abnormalities with dysplasia of the flagellar midpiece and abnormal head shapes (respectively indicated by orange and blue arrowheads), or sperm with only a cytoplasmic bag containing unassembled axonemal (Ax) and peri-axonemal components, such as outer dense fibers (ODF) and MIT (right image). Some sperm flagellar cross sections also display a normal ultrastructure with a regularly disposed 9 + 2 axoneme (left image).</div>
|
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data-image-alt="FIGURE 6"
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|
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data-figure-id="F6">
|
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<img class="figure-thumb" itemprop="thumbnail"
|
||
id="article-image-5"
|
||
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ebf6/9981940/e11dc24f8a57/fgene-14-1117821-g006.gif"
|
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alt="FIGURE 6" />
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|
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<strong class="figure-label">
|
||
<p> FIGURE 6 </p>
|
||
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|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> SPEF2 is absent or severely… </p></div>
|
||
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|
||
|
||
|
||
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|
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|
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<strong class="figure-label">
|
||
<p> FIGURE 6 </p>
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents"><p> SPEF2 is absent or severely reduced in sperm flagellar axonemes of <i> HYDIN </i> -… </p></div>
|
||
|
||
|
||
|
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|
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|
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<figcaption id="figure-caption-5" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
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<strong class="figure-label">
|
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FIGURE 6
|
||
</strong>
|
||
|
||
|
||
|
||
<div class="figure-caption-contents">SPEF2 is absent or severely reduced in sperm flagellar axonemes of <i>HYDIN</i>- and <i>SPEF2</i>-mutant individuals, presenting with MMAF-associated infertility. Sperm cells from healthy control donors and infertile male individuals with pathogenic variants in <i>HYDIN</i> and <i>SPEF2</i> were co-stained with antibodies directed against acetylated α-tubulin (acet. tubulin; depicted in green) and SPEF2 (depicted in red). <b>(A)</b> In control sperm cells, immunoreactivity against SPEF2 (red) is observed along the entire flagellar length. The SPEF2 signal co-localizes with the flagellar marker acet. tubulin (depicted in yellow in the merged image). <b>(B–E)</b> In sperm cells of both <i>HYDIN</i>-mutant individuals (OP-305 II2 and OP-3022 II2) and <i>SPEF2</i>-mutant individuals (SP-24 and SP-32), a severe reduction of the SPEF2 signal or no signal against SPEF2 was observed along the flagellar axoneme. <b>(F–I)</b> Sperm of both <i>HYDIN</i>-and <i>SPEF2</i>-mutant individuals display a MMAF phenotype with short, bent, coiled and irregular flagella. The schematic representatively shows the localization of HYDIN and SPEF2 within the central pair associated apparatus. Nuclei were stained with Hoechst33342. Scale bars represent 10 µm.</div>
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||
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<p> FIGURE 7 </p>
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<div class="figure-caption-contents"><p> TEM analyses of HYDIN and… </p></div>
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<p> FIGURE 7 </p>
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<div class="figure-caption-contents"><p> TEM analyses of HYDIN and SPEF2-deficient sperm displays morphological abnormalities. <b> (A) </b> TEM micrographs… </p></div>
|
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FIGURE 7
|
||
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||
|
||
|
||
<div class="figure-caption-contents">TEM analyses of HYDIN and SPEF2-deficient sperm displays morphological abnormalities. <b>(A)</b> TEM micrographs of sperm samples from a healthy control donor, showing a flagellar cross section with a regular 9 + 2 axoneme of microtubule doublets (MTD), (left image), and a longitudinal section showing the axoneme (Ax) at the center, with regularly arranged mitochondria (MIT) and fibrous sheath (FS), respectively in the flagellar mid piece and principal piece (right image). The orange arrowheads in the cross section indicate projections of the central pair associated apparatus. <b>(B)</b>
|
||
<i>HYDIN</i>-mutant sperm display flagellar cross sections with either a normal 9 + 2 ultrastructure of the axoneme displaying less pronounced CP projections (upper left image), or 9 + 1 cross sections with only one central microtubule (upper middle image), or a 9 + 0 axoneme without the CP (lower left image). Morphological abnormalities of the sperm flagella are also observed, comprising sperm cells displaying a cytoplasmic bag with unassembled axonemal and peri-axonemal components (upper right image, arrow), or mid piece dysplasia (lower right image, indicate by a blue arrowhead). <b>(C)</b>
|
||
<i>SPEF2</i>-mutant sperm cells also display short and irregular flagella (first left image), or a cytoplasmic bag with unassembled flagellar components (second left image). Flagellar cross sections display either a 9 + 0 structure without the CP (second from the right image), or a 9 + 2 structure (first from the right image).</div>
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Adzhubei I. A., Schmidt S., Peshkin L., Ramensky V. E., Gerasimova A., Bork P., et al. (2010). A method and server for predicting damaging missense mutations. Nat. Methods 7, 248–249. 10.1038/nmeth0410-248
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