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Complement Activation Contributes to Severe Acute Respiratory Syndrome Coronavirus Pathogenesis

Identifieur interne : 000552 ( Pmc/Checkpoint ); précédent : 000551; suivant : 000553

Complement Activation Contributes to Severe Acute Respiratory Syndrome Coronavirus Pathogenesis

Auteurs : Lisa E. Gralinski [États-Unis] ; Timothy P. Sheahan [États-Unis] ; Thomas E. Morrison [États-Unis] ; Vineet D. Menachery [États-Unis] ; Kara Jensen [États-Unis] ; Sarah R. Leist [États-Unis] ; Alan Whitmore [États-Unis] ; Mark T. Heise [États-Unis] ; Ralph S. Baric [États-Unis]

Source :

RBID : PMC:6178621

Abstract

The complement system is a critical part of host defense to many bacterial, viral, and fungal infections. It works alongside pattern recognition receptors to stimulate host defense systems in advance of activation of the adaptive immune response. In this study, we directly test the role of complement in SARS-CoV pathogenesis using a mouse model and show that respiratory disease is significantly reduced in the absence of complement even though viral load is unchanged. Complement-deficient mice have reduced neutrophilia in their lungs and reduced systemic inflammation, consistent with the observation that SARS-CoV pathogenesis is an immune-driven disease. These data suggest that inhibition of complement signaling might be an effective treatment option following coronavirus infection.


Url:
DOI: 10.1128/mBio.01753-18
PubMed: 30301856
PubMed Central: 6178621


Affiliations:


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PMC:6178621

Le document en format XML

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<p>The complement system is a critical part of host defense to many bacterial, viral, and fungal infections. It works alongside pattern recognition receptors to stimulate host defense systems in advance of activation of the adaptive immune response. In this study, we directly test the role of complement in SARS-CoV pathogenesis using a mouse model and show that respiratory disease is significantly reduced in the absence of complement even though viral load is unchanged. Complement-deficient mice have reduced neutrophilia in their lungs and reduced systemic inflammation, consistent with the observation that SARS-CoV pathogenesis is an immune-driven disease. These data suggest that inhibition of complement signaling might be an effective treatment option following coronavirus infection.</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">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">30301856</article-id>
<article-id pub-id-type="pmc">6178621</article-id>
<article-id pub-id-type="publisher-id">mBio01753-18</article-id>
<article-id pub-id-type="doi">10.1128/mBio.01753-18</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="overline">
<subject>Host-Microbe Biology</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Complement Activation Contributes to Severe Acute Respiratory Syndrome Coronavirus Pathogenesis</article-title>
<alt-title alt-title-type="short-authors">Gralinski et al.</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Gralinski</surname>
<given-names>Lisa E.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sheahan</surname>
<given-names>Timothy P.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Morrison</surname>
<given-names>Thomas E.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Menachery</surname>
<given-names>Vineet D.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Jensen</surname>
<given-names>Kara</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Leist</surname>
<given-names>Sarah R.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Whitmore</surname>
<given-names>Alan</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Heise</surname>
<given-names>Mark T.</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Baric</surname>
<given-names>Ralph S.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<aff id="aff1">
<label>a</label>
<addr-line>Department of Epidemiology, University of North Carolina, Chapel Hill, North Carolina, USA</addr-line>
</aff>
<aff id="aff2">
<label>b</label>
<addr-line>Department of Immunology and Microbiology, University of Colorado School of Medicine, Aurora, Colorado, USA</addr-line>
</aff>
<aff id="aff3">
<label>c</label>
<addr-line>Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, USA</addr-line>
</aff>
<aff id="aff4">
<label>d</label>
<addr-line>Department of Genetics, University of North Carolina, Chapel Hill, North Carolina, USA</addr-line>
</aff>
</contrib-group>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Subbarao</surname>
<given-names>Kanta</given-names>
</name>
<role>Editor</role>
<aff>NIAID, NIH</aff>
</contrib>
</contrib-group>
<contrib-group>
<contrib contrib-type="reviewer">
<name>
<surname>Enjuanes</surname>
<given-names>Luis</given-names>
</name>
<role>Solicited external reviewer</role>
<aff>Centro Nacional de Biotecnologia, CNB-CSIC</aff>
</contrib>
<contrib contrib-type="reviewer">
<name>
<surname>Schultz-Cherry</surname>
<given-names>Stacey</given-names>
</name>
<role>Solicited external reviewer</role>
<aff>St. Jude Children's Research Hospital</aff>
</contrib>
</contrib-group>
<author-notes>
<corresp id="cor1">Address correspondence to Ralph S. Baric,
<email>rbaric@email.unc.edu</email>
.</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>9</day>
<month>10</month>
<year>2018</year>
</pub-date>
<pub-date pub-type="collection">
<season>Sep-Oct</season>
<year>2018</year>
</pub-date>
<volume>9</volume>
<issue>5</issue>
<elocation-id>e01753-18</elocation-id>
<history>
<date date-type="received">
<day>11</day>
<month>8</month>
<year>2018</year>
</date>
<date date-type="accepted">
<day>15</day>
<month>8</month>
<year>2018</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2018 Gralinski et al.</copyright-statement>
<copyright-year>2018</copyright-year>
<copyright-holder>Gralinski et al.</copyright-holder>
<license license-type="open-access" xlink:href="https://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="https://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="mbo005184095001.pdf"></self-uri>
<abstract abstract-type="precis">
<p>The complement system is a critical part of host defense to many bacterial, viral, and fungal infections. It works alongside pattern recognition receptors to stimulate host defense systems in advance of activation of the adaptive immune response. In this study, we directly test the role of complement in SARS-CoV pathogenesis using a mouse model and show that respiratory disease is significantly reduced in the absence of complement even though viral load is unchanged. Complement-deficient mice have reduced neutrophilia in their lungs and reduced systemic inflammation, consistent with the observation that SARS-CoV pathogenesis is an immune-driven disease. These data suggest that inhibition of complement signaling might be an effective treatment option following coronavirus infection.</p>
</abstract>
<abstract>
<title>ABSTRACT</title>
<p>Acute respiratory distress syndrome (ARDS) is immune-driven pathologies that are observed in severe cases of severe acute respiratory syndrome coronavirus (SARS-CoV) infection. SARS-CoV emerged in 2002 to 2003 and led to a global outbreak of SARS. As with the outcome of human infection, intranasal infection of C57BL/6J mice with mouse-adapted SARS-CoV results in high-titer virus replication within the lung, induction of inflammatory cytokines and chemokines, and immune cell infiltration within the lung. Using this model, we investigated the role of the complement system during SARS-CoV infection. We observed activation of the complement cascade in the lung as early as day 1 following SARS-CoV infection. To test whether this activation contributed to protective or pathologic outcomes, we utilized mice deficient in C3 (C3
<sup>–/–</sup>
), the central component of the complement system. Relative to C57BL/6J control mice, SARS-CoV-infected
<italic>C3</italic>
<sup>–/–</sup>
mice exhibited significantly less weight loss and less respiratory dysfunction despite equivalent viral loads in the lung. Significantly fewer neutrophils and inflammatory monocytes were present in the lungs of
<italic>C3</italic>
<sup>–/–</sup>
mice than in C56BL/6J controls, and subsequent studies revealed reduced lung pathology and lower cytokine and chemokine levels in both the lungs and the sera of
<italic>C3</italic>
<sup>–/–</sup>
mice than in controls. These studies identify the complement system as an important host mediator of SARS-CoV-induced disease and suggest that complement activation regulates a systemic proinflammatory response to SARS-CoV infection. Furthermore, these data suggest that SARS-CoV-mediated disease is largely immune driven and that inhibiting complement signaling after SARS-CoV infection might function as an effective immune therapeutic.</p>
</abstract>
<kwd-group>
<title>KEYWORDS</title>
<kwd>SARS-CoV</kwd>
<kwd>animal models</kwd>
<kwd>complement</kwd>
<kwd>coronavirus</kwd>
<kwd>respiratory viruses</kwd>
</kwd-group>
<funding-group>
<award-group id="award1">
<funding-source>
<institution-wrap>
<institution>HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID)</institution>
<institution-id>https://doi.org/10.13039/100000060</institution-id>
</institution-wrap>
</funding-source>
<award-id>AI100625</award-id>
<principal-award-recipient>
<name>
<surname>Baric</surname>
<given-names>Ralph S.</given-names>
</name>
</principal-award-recipient>
<principal-award-recipient>
<name>
<surname>Heise</surname>
<given-names>Mark T.</given-names>
</name>
</principal-award-recipient>
</award-group>
</funding-group>
<counts>
<count count="3" 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="68"></ref-count>
<page-count count="15"></page-count>
<word-count count="9285"></word-count>
</counts>
<custom-meta-group>
<custom-meta>
<meta-name>cover-date</meta-name>
<meta-value>September/October 2018</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>États-Unis</li>
</country>
<region>
<li>Caroline du Nord</li>
<li>Colorado</li>
<li>Texas</li>
</region>
</list>
<tree>
<country name="États-Unis">
<region name="Caroline du Nord">
<name sortKey="Gralinski, Lisa E" sort="Gralinski, Lisa E" uniqKey="Gralinski L" first="Lisa E." last="Gralinski">Lisa E. Gralinski</name>
</region>
<name sortKey="Baric, Ralph S" sort="Baric, Ralph S" uniqKey="Baric R" first="Ralph S." last="Baric">Ralph S. Baric</name>
<name sortKey="Heise, Mark T" sort="Heise, Mark T" uniqKey="Heise M" first="Mark T." last="Heise">Mark T. Heise</name>
<name sortKey="Jensen, Kara" sort="Jensen, Kara" uniqKey="Jensen K" first="Kara" last="Jensen">Kara Jensen</name>
<name sortKey="Leist, Sarah R" sort="Leist, Sarah R" uniqKey="Leist S" first="Sarah R." last="Leist">Sarah R. Leist</name>
<name sortKey="Menachery, Vineet D" sort="Menachery, Vineet D" uniqKey="Menachery V" first="Vineet D." last="Menachery">Vineet D. Menachery</name>
<name sortKey="Menachery, Vineet D" sort="Menachery, Vineet D" uniqKey="Menachery V" first="Vineet D." last="Menachery">Vineet D. Menachery</name>
<name sortKey="Morrison, Thomas E" sort="Morrison, Thomas E" uniqKey="Morrison T" first="Thomas E." last="Morrison">Thomas E. Morrison</name>
<name sortKey="Sheahan, Timothy P" sort="Sheahan, Timothy P" uniqKey="Sheahan T" first="Timothy P." last="Sheahan">Timothy P. Sheahan</name>
<name sortKey="Whitmore, Alan" sort="Whitmore, Alan" uniqKey="Whitmore A" first="Alan" last="Whitmore">Alan Whitmore</name>
</country>
</tree>
</affiliations>
</record>

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