The Conserved Coronavirus Macrodomain Promotes Virulence and Suppresses the Innate Immune Response during Severe Acute Respiratory Syndrome Coronavirus Infection
Identifieur interne : 000666 ( Pmc/Checkpoint ); précédent : 000665; suivant : 000667The Conserved Coronavirus Macrodomain Promotes Virulence and Suppresses the Innate Immune Response during Severe Acute Respiratory Syndrome Coronavirus Infection
Auteurs : Anthony R. Fehr [États-Unis] ; Rudragouda Channappanavar [États-Unis] ; Gytis Jankevicius [Royaume-Uni] ; Craig Fett [États-Unis] ; Jincun Zhao [États-Unis, République populaire de Chine] ; Jeremiah Athmer [États-Unis] ; David K. Meyerholz [États-Unis] ; Ivan Ahel [Royaume-Uni] ; Stanley Perlman [États-Unis]Source :
- mBio [ 2150-7511 ] ; 2016.
Abstract
ADP-ribosylation is a common posttranslational modification that may have antiviral properties and impact innate immunity. To regulate this activity, macrodomain proteins enzymatically remove covalently attached ADP-ribose from protein targets. All members of the
Url:
DOI: 10.1128/mBio.01721-16
PubMed: 27965448
PubMed Central: 5156301
Affiliations:
- Royaume-Uni, République populaire de Chine, États-Unis
- Angleterre, Iowa, Oxfordshire
- Iowa City, Oxford
- Université d'Oxford, Université de l'Iowa
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<front><div type="abstract" xml:lang="en"><title>ABSTRACT</title>
<p>ADP-ribosylation is a common posttranslational modification that may have antiviral properties and impact innate immunity. To regulate this activity, macrodomain proteins enzymatically remove covalently attached ADP-ribose from protein targets. All members of the <italic>Coronavirinae</italic>
, a subfamily of positive-sense RNA viruses, contain a highly conserved macrodomain within nonstructural protein 3 (nsp3). However, its function or targets during infection remain unknown. We identified several macrodomain mutations that greatly reduced nsp3’s de-ADP-ribosylation activity <italic>in vitro</italic>
. Next, we created recombinant severe acute respiratory syndrome coronavirus (SARS-CoV) strains with these mutations. These mutations led to virus attenuation and a modest reduction of viral loads in infected mice, despite normal replication in cell culture. Further, macrodomain mutant virus elicited an early, enhanced interferon (IFN), interferon-stimulated gene (ISG), and proinflammatory cytokine response in mice and in a human bronchial epithelial cell line. Using a coinfection assay, we found that inclusion of mutant virus in the inoculum protected mice from an otherwise lethal SARS-CoV infection without reducing virus loads, indicating that the changes in innate immune response were physiologically significant. In conclusion, we have established a novel function for the SARS-CoV macrodomain that implicates ADP-ribose in the regulation of the innate immune response and helps to demonstrate why this domain is conserved in CoVs.</p>
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</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">mBio</journal-id>
<journal-id journal-id-type="iso-abbrev">MBio</journal-id>
<journal-id journal-id-type="hwp">mbio</journal-id>
<journal-id journal-id-type="pmc">mbio</journal-id>
<journal-id journal-id-type="publisher-id">mBio</journal-id>
<journal-title-group><journal-title>mBio</journal-title>
</journal-title-group>
<issn pub-type="epub">2150-7511</issn>
<publisher><publisher-name>American Society for Microbiology</publisher-name>
<publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27965448</article-id>
<article-id pub-id-type="pmc">5156301</article-id>
<article-id pub-id-type="publisher-id">mBio01721-16</article-id>
<article-id pub-id-type="doi">10.1128/mBio.01721-16</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>The Conserved Coronavirus Macrodomain Promotes Virulence and Suppresses the Innate Immune Response during Severe Acute Respiratory Syndrome Coronavirus Infection</article-title>
<alt-title alt-title-type="running-head">SARS-CoV Macrodomain Suppresses Innate Immunity</alt-title>
<alt-title alt-title-type="short-authors">Fehr et al.</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Fehr</surname>
<given-names>Anthony R.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Channappanavar</surname>
<given-names>Rudragouda</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jankevicius</surname>
<given-names>Gytis</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fett</surname>
<given-names>Craig</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhao</surname>
<given-names>Jincun</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Athmer</surname>
<given-names>Jeremiah</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Meyerholz</surname>
<given-names>David K.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ahel</surname>
<given-names>Ivan</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Perlman</surname>
<given-names>Stanley</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<aff id="aff1"><label>a</label>
<addr-line>Department of Microbiology, University of Iowa, Iowa City, Iowa, USA</addr-line>
</aff>
<aff id="aff2"><label>b</label>
<addr-line>Department of Pathology, University of Iowa, Iowa City, Iowa, USA</addr-line>
</aff>
<aff id="aff3"><label>c</label>
<addr-line>Sir William Dunn School of Pathology, University of Oxford, Oxford, United Kingdom</addr-line>
</aff>
<aff id="aff4"><label>d</label>
<addr-line>State Key Laboratory of Respiratory Diseases, Guangzhou Institute of Respiratory Disease, The First Affiliated Hospital of Guangzhou Medical University, Yuexiu District, Guangzhou, Guangdong, China</addr-line>
</aff>
</contrib-group>
<author-notes><corresp id="cor1">Address correspondence to Stanley Perlman, <email>Stanley-Perlman@uiowa.edu</email>
.</corresp>
<fn fn-type="edited-by"><p><bold>Editor</bold>
Mark R. Denison, Vanderbilt University Medical Center</p>
</fn>
</author-notes>
<pub-date pub-type="epub"><day>13</day>
<month>12</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><season>Nov-Dec</season>
<year>2016</year>
</pub-date>
<volume>7</volume>
<issue>6</issue>
<elocation-id>e01721-16</elocation-id>
<history><date date-type="received"><day>16</day>
<month>9</month>
<year>2016</year>
</date>
<date date-type="accepted"><day>16</day>
<month>11</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2016 Fehr et al.</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Fehr et al.</copyright-holder>
<license license-type="open-access" 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 4.0 International license</ext-link>
.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="mbo006163112001.pdf"></self-uri>
<abstract><title>ABSTRACT</title>
<p>ADP-ribosylation is a common posttranslational modification that may have antiviral properties and impact innate immunity. To regulate this activity, macrodomain proteins enzymatically remove covalently attached ADP-ribose from protein targets. All members of the <italic>Coronavirinae</italic>
, a subfamily of positive-sense RNA viruses, contain a highly conserved macrodomain within nonstructural protein 3 (nsp3). However, its function or targets during infection remain unknown. We identified several macrodomain mutations that greatly reduced nsp3’s de-ADP-ribosylation activity <italic>in vitro</italic>
. Next, we created recombinant severe acute respiratory syndrome coronavirus (SARS-CoV) strains with these mutations. These mutations led to virus attenuation and a modest reduction of viral loads in infected mice, despite normal replication in cell culture. Further, macrodomain mutant virus elicited an early, enhanced interferon (IFN), interferon-stimulated gene (ISG), and proinflammatory cytokine response in mice and in a human bronchial epithelial cell line. Using a coinfection assay, we found that inclusion of mutant virus in the inoculum protected mice from an otherwise lethal SARS-CoV infection without reducing virus loads, indicating that the changes in innate immune response were physiologically significant. In conclusion, we have established a novel function for the SARS-CoV macrodomain that implicates ADP-ribose in the regulation of the innate immune response and helps to demonstrate why this domain is conserved in CoVs.</p>
</abstract>
<abstract abstract-type="executive-summary"><title>IMPORTANCE</title>
<p>The macrodomain is a ubiquitous structural domain that removes ADP-ribose from proteins, reversing the activity of ADP-ribosyltransferases. All coronaviruses contain a macrodomain, suggesting that ADP-ribosylation impacts coronavirus infection. However, its function during infection remains unknown. Here, we found that the macrodomain is an important virulence factor for a highly pathogenic human CoV, SARS-CoV. Viruses with macrodomain mutations that abrogate its ability to remove ADP-ribose from protein were unable to cause lethal disease in mice. Importantly, the SARS-CoV macrodomain suppressed the innate immune response during infection. Our data suggest that an early innate immune response can protect mice from lethal disease. Understanding the mechanism used by this enzyme to promote disease will open up novel avenues for coronavirus therapies and give further insight into the role of macrodomains in viral pathogenesis.</p>
</abstract>
<funding-group><award-group id="award1"><funding-source>Wellcome Trust</funding-source>
<award-id>101794</award-id>
<principal-award-recipient>Ivan Ahel</principal-award-recipient>
</award-group>
<award-group id="award2"><funding-source>EC | European Research Council (ERC)
<named-content content-type="funder-id">http://dx.doi.org/10.13039/501100000781</named-content>
</funding-source>
<award-id>281739</award-id>
<principal-award-recipient>Ivan Ahel</principal-award-recipient>
</award-group>
<award-group id="award3"><funding-source>NRSA</funding-source>
<award-id>T32-AI007260</award-id>
<principal-award-recipient>Anthony R. Fehr</principal-award-recipient>
</award-group>
<award-group id="award4"><funding-source>NRSA</funding-source>
<award-id>F32-113973</award-id>
<principal-award-recipient>Anthony R. Fehr</principal-award-recipient>
</award-group>
<award-group id="award5"><funding-source>HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
<named-content content-type="funder-id">http://dx.doi.org/10.13039/100000060</named-content>
</funding-source>
<award-id>PO1 AI060699</award-id>
<award-id>R01 AI091322</award-id>
<principal-award-recipient>Stanley Perlman</principal-award-recipient>
</award-group>
</funding-group>
<counts><count count="6" count-type="supplementary-material"></count>
<fig-count count="7"></fig-count>
<table-count count="0"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="57"></ref-count>
<page-count count="12"></page-count>
<word-count count="9808"></word-count>
</counts>
<custom-meta-group><custom-meta><meta-name>cover-date</meta-name>
<meta-value>November/December 2016</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Royaume-Uni</li>
<li>République populaire de Chine</li>
<li>États-Unis</li>
</country>
<region><li>Angleterre</li>
<li>Iowa</li>
<li>Oxfordshire</li>
</region>
<settlement><li>Iowa City</li>
<li>Oxford</li>
</settlement>
<orgName><li>Université d'Oxford</li>
<li>Université de l'Iowa</li>
</orgName>
</list>
<tree><country name="États-Unis"><region name="Iowa"><name sortKey="Fehr, Anthony R" sort="Fehr, Anthony R" uniqKey="Fehr A" first="Anthony R." last="Fehr">Anthony R. Fehr</name>
</region>
<name sortKey="Athmer, Jeremiah" sort="Athmer, Jeremiah" uniqKey="Athmer J" first="Jeremiah" last="Athmer">Jeremiah Athmer</name>
<name sortKey="Channappanavar, Rudragouda" sort="Channappanavar, Rudragouda" uniqKey="Channappanavar R" first="Rudragouda" last="Channappanavar">Rudragouda Channappanavar</name>
<name sortKey="Fett, Craig" sort="Fett, Craig" uniqKey="Fett C" first="Craig" last="Fett">Craig Fett</name>
<name sortKey="Meyerholz, David K" sort="Meyerholz, David K" uniqKey="Meyerholz D" first="David K." last="Meyerholz">David K. Meyerholz</name>
<name sortKey="Perlman, Stanley" sort="Perlman, Stanley" uniqKey="Perlman S" first="Stanley" last="Perlman">Stanley Perlman</name>
<name sortKey="Zhao, Jincun" sort="Zhao, Jincun" uniqKey="Zhao J" first="Jincun" last="Zhao">Jincun Zhao</name>
</country>
<country name="Royaume-Uni"><region name="Angleterre"><name sortKey="Jankevicius, Gytis" sort="Jankevicius, Gytis" uniqKey="Jankevicius G" first="Gytis" last="Jankevicius">Gytis Jankevicius</name>
</region>
<name sortKey="Ahel, Ivan" sort="Ahel, Ivan" uniqKey="Ahel I" first="Ivan" last="Ahel">Ivan Ahel</name>
</country>
<country name="République populaire de Chine"><noRegion><name sortKey="Zhao, Jincun" sort="Zhao, Jincun" uniqKey="Zhao J" first="Jincun" last="Zhao">Jincun Zhao</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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EXPLOR_STEP=$WICRI_ROOT/Sante/explor/SrasV1/Data/Pmc/Checkpoint
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Ou
HfdSelect -h $EXPLOR_AREA/Data/Pmc/Checkpoint/biblio.hfd -nk 000666 | SxmlIndent | more
Pour mettre un lien sur cette page dans le réseau Wicri
{{Explor lien |wiki= Sante |area= SrasV1 |flux= Pmc |étape= Checkpoint |type= RBID |clé= PMC:5156301 |texte= The Conserved Coronavirus Macrodomain Promotes Virulence and Suppresses the Innate Immune Response during Severe Acute Respiratory Syndrome Coronavirus Infection }}
Pour générer des pages wiki
HfdIndexSelect -h $EXPLOR_AREA/Data/Pmc/Checkpoint/RBID.i -Sk "pubmed:27965448" \ | HfdSelect -Kh $EXPLOR_AREA/Data/Pmc/Checkpoint/biblio.hfd \ | NlmPubMed2Wicri -a SrasV1
![]() | This area was generated with Dilib version V0.6.33. | ![]() |