Direct Binding of Retromer to Human Papillomavirus Type 16 Minor Capsid Protein L2 Mediates Endosome Exit during Viral Infection
Identifieur interne : 000009 ( Pmc/Curation ); précédent : 000008; suivant : 000010Direct Binding of Retromer to Human Papillomavirus Type 16 Minor Capsid Protein L2 Mediates Endosome Exit during Viral Infection
Auteurs : Andreea Popa [États-Unis] ; Wei Zhang [États-Unis] ; Megan S. Harrison [États-Unis] ; Kylia Goodner [États-Unis] ; Teymur Kazakov [États-Unis] ; Edward C. Goodwin [États-Unis] ; Alex Lipovsky [États-Unis] ; Christopher G. Burd [États-Unis] ; Daniel Dimaio [États-Unis]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2015.
Abstract
Trafficking of human papillomaviruses to the Golgi apparatus during virus entry requires retromer, an endosomal coat protein complex that mediates the vesicular transport of cellular transmembrane proteins from the endosome to the Golgi apparatus or the plasma membrane. Here we show that the HPV16 L2 minor capsid protein is a retromer cargo, even though L2 is not a transmembrane protein. We show that direct binding of retromer to a conserved sequence in the carboxy-terminus of L2 is required for exit of L2 from the early endosome and delivery to the
Url:
DOI: 10.1371/journal.ppat.1004699
PubMed: 25693203
PubMed Central: 4334968
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<front><div type="abstract" xml:lang="en"><p>Trafficking of human papillomaviruses to the Golgi apparatus during virus entry requires retromer, an endosomal coat protein complex that mediates the vesicular transport of cellular transmembrane proteins from the endosome to the Golgi apparatus or the plasma membrane. Here we show that the HPV16 L2 minor capsid protein is a retromer cargo, even though L2 is not a transmembrane protein. We show that direct binding of retromer to a conserved sequence in the carboxy-terminus of L2 is required for exit of L2 from the early endosome and delivery to the <italic>trans</italic>
-Golgi network during virus entry. This binding site is different from known retromer binding motifs and can be replaced by a sorting signal from a cellular retromer cargo. Thus, HPV16 is an unconventional particulate retromer cargo, and retromer binding initiates retrograde transport of viral components from the endosome to the <italic>trans</italic>
-Golgi network during virus entry. We propose that the carboxy-terminal segment of L2 protein protrudes through the endosomal membrane and is accessed by retromer in the cytoplasm.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Pathog</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS Pathog</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plospath</journal-id>
<journal-title-group><journal-title>PLoS Pathogens</journal-title>
</journal-title-group>
<issn pub-type="ppub">1553-7366</issn>
<issn pub-type="epub">1553-7374</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, CA USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25693203</article-id>
<article-id pub-id-type="pmc">4334968</article-id>
<article-id pub-id-type="doi">10.1371/journal.ppat.1004699</article-id>
<article-id pub-id-type="publisher-id">PPATHOGENS-D-14-02444</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Direct Binding of Retromer to Human Papillomavirus Type 16 Minor Capsid Protein L2 Mediates Endosome Exit during Viral Infection</article-title>
<alt-title alt-title-type="running-head">Retromer Binds HPV16 L2 to Mediate Endosome Exit</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Popa</surname>
<given-names>Andreea</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="currentaff001"><sup>¤</sup>
</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Zhang</surname>
<given-names>Wei</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Harrison</surname>
<given-names>Megan S.</given-names>
</name>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Goodner</surname>
<given-names>Kylia</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kazakov</surname>
<given-names>Teymur</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Goodwin</surname>
<given-names>Edward C.</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lipovsky</surname>
<given-names>Alex</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Burd</surname>
<given-names>Christopher G.</given-names>
</name>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>DiMaio</surname>
<given-names>Daniel</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff004"><sup>4</sup>
</xref>
<xref ref-type="aff" rid="aff005"><sup>5</sup>
</xref>
<xref rid="cor001" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<aff id="aff001"><label>1</label>
<addr-line>Department of Genetics, Yale School of Medicine, New Haven, Connecticut, United States of America</addr-line>
</aff>
<aff id="aff002"><label>2</label>
<addr-line>Department of Cell Biology, Yale School of Medicine, New Haven, Connecticut, United States of America</addr-line>
</aff>
<aff id="aff003"><label>3</label>
<addr-line>Department of Therapeutic Radiology, Yale School of Medicine, New Haven, Connecticut, United States of America</addr-line>
</aff>
<aff id="aff004"><label>4</label>
<addr-line>Department of Molecular Biophysics & Biochemistry, Yale School of Medicine, New Haven, Connecticut, United States of America</addr-line>
</aff>
<aff id="aff005"><label>5</label>
<addr-line>Yale Cancer Center, New Haven, Connecticut, United States of America</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>McBride</surname>
<given-names>Alison Anne</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>National Institute of Allergy and Infectious Diseases, National Institutes of Health, UNITED STATES</addr-line>
</aff>
<author-notes><fn fn-type="conflict" id="coi001"><p>The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con" id="contrib001"><p>Conceived and designed the experiments: AP WZ MSH KG TK ECG AL CGB DD. Performed the experiments: AP WZ KG MSH TK ECG AL. Analyzed the data: AP WZ MSH KG TK ECG AL CGB DD. Wrote the paper: AP WZ MSH KG TK ECG CGB DD.</p>
</fn>
<fn fn-type="current-aff" id="currentaff001"><label>¤</label>
<p>Current address: Department of Pathology, Virginia Commonwealth University, Richmond, Virginia, United States of America</p>
</fn>
<corresp id="cor001">* E-mail: <email>daniel.dimaio@yale.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>18</day>
<month>2</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection"><month>2</month>
<year>2015</year>
</pub-date>
<volume>11</volume>
<issue>2</issue>
<elocation-id>e1004699</elocation-id>
<history><date date-type="received"><day>10</day>
<month>10</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>22</day>
<month>1</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-year>2015</copyright-year>
<copyright-holder>Popa et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="ppat.1004699.pdf"></self-uri>
<abstract><p>Trafficking of human papillomaviruses to the Golgi apparatus during virus entry requires retromer, an endosomal coat protein complex that mediates the vesicular transport of cellular transmembrane proteins from the endosome to the Golgi apparatus or the plasma membrane. Here we show that the HPV16 L2 minor capsid protein is a retromer cargo, even though L2 is not a transmembrane protein. We show that direct binding of retromer to a conserved sequence in the carboxy-terminus of L2 is required for exit of L2 from the early endosome and delivery to the <italic>trans</italic>
-Golgi network during virus entry. This binding site is different from known retromer binding motifs and can be replaced by a sorting signal from a cellular retromer cargo. Thus, HPV16 is an unconventional particulate retromer cargo, and retromer binding initiates retrograde transport of viral components from the endosome to the <italic>trans</italic>
-Golgi network during virus entry. We propose that the carboxy-terminal segment of L2 protein protrudes through the endosomal membrane and is accessed by retromer in the cytoplasm.</p>
</abstract>
<abstract abstract-type="summary"><title>Author Summary</title>
<p>The human papillomaviruses are important carcinogens, but little is known about how these non-enveloped viruses traffic to the nucleus, the site of genome replication. We use imaging, biochemical, and genetic techniques to show that a multi-subunit intracellular trafficking machine known as retromer binds directly to the L2 minor capsid protein in the virus particle to initiate its transport from the endosome to other membrane-bound organelles farther inside the cell. Most notably, knock-down of retromer expression or mutation of newly identified retromer binding sites in L2 cause the accumulation of incoming HPV16 capsids in the endosome and prevent trafficking to the Golgi. These defects can be corrected by insertion of a retromer binding site from a cellular cargo. Because all previously known retromer cargoes are cellular transmembrane proteins, the virus represents a new class of retromer cargo. In addition to elucidating the mechanism of viral endosome escape, these results suggest that retromer may play a more versatile role in cell biology than previously recognized.</p>
</abstract>
<funding-group><funding-statement>AP and WZ were supported in part by Leslie Warner Postdoctoral Fellowships from Yale Cancer Center. MSH was supported by a postdoctoral fellowship from the American Heart Association. KG was supported by a training grant from the National Institutes of Health (T32 HG003198). The work was supported by grants from the National Institutes of Health to DD (AI102876 and CA016038) and to CB (GM060221). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><fig-count count="7"></fig-count>
<table-count count="0"></table-count>
<page-count count="21"></page-count>
</counts>
<custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name>
<meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes><title>Data Availability</title>
<p>All relevant data are within the paper and its Supporting Information files.</p>
</notes>
</front>
</pmc>
</record>
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