Active Replication of Middle East Respiratory Syndrome Coronavirus and Aberrant Induction of Inflammatory Cytokines and Chemokines in Human Macrophages: Implications for Pathogenesis
Identifieur interne : 001172 ( Pmc/Curation ); précédent : 001171; suivant : 001173Active Replication of Middle East Respiratory Syndrome Coronavirus and Aberrant Induction of Inflammatory Cytokines and Chemokines in Human Macrophages: Implications for Pathogenesis
Auteurs : Jie Zhou ; Hin Chu ; Cun Li ; Bosco Ho-Yin Wong ; Zhong-Shan Cheng ; Vincent Kwok-Man Poon ; Tianhao Sun ; Candy Choi-Yi Lau ; Kenneth Kak-Yuen Wong [République populaire de Chine] ; Jimmy Yu-Wai Chan [République populaire de Chine] ; Jasper Fuk-Woo Chan ; Kelvin Kai-Wang To ; Kwok-Hung Chan ; Bo-Jian Zheng ; Kwok-Yung YuenSource :
- The Journal of Infectious Diseases [ 0022-1899 ] ; 2013.
Abstract
Middle East respiratory syndrome coronavirus (MERS-CoV) infection caused severe pneumonia and multiorgan dysfunction and had a higher crude fatality rate (around 50% vs 10%) than SARS coronavirus (SARS-CoV) infection. To understand the pathogenesis, we studied viral replication, cytokine/chemokine response, and antigen presentation in MERS-CoV–infected human monocyte–derived macrophages (MDMs) versus SARS-CoV–infected MDMs. Only MERS-CoV can replicate in MDMs. Both viruses were unable to significantly stimulate the expression of antiviral cytokines (interferon α [IFN-α] and IFN-β) but induced comparable levels of tumor necrosis factor α and interleukin 6. Notably, MERS-CoV induced significantly higher expression levels of interleukin 12, IFN-γ, and chemokines (IP-10/CXCL-10, MCP-1/CCL-2, MIP-1α/CCL-3, RANTES/CCL-5, and interleukin 8) than SARS-CoV. The expression of major histocompatibility complex class I and costimulatory molecules were significantly higher in MERS-CoV–infected MDMs than in SARS-CoV–infected cells. MERS-CoV replication was validated by immunostaining of infected MDMs and ex vivo lung tissue. We conclusively showed that MERS-CoV can establish a productive infection in human macrophages. The aberrant induction of inflammatory cytokines/chemokines could be important in the disease pathogenesis.
Url:
DOI: 10.1093/infdis/jit504
PubMed: 24065148
PubMed Central: 7107356
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<front><div type="abstract" xml:lang="en"><title>Abstract</title>
<p>Middle East respiratory syndrome coronavirus (MERS-CoV) infection caused severe pneumonia and multiorgan dysfunction and had a higher crude fatality rate (around 50% vs 10%) than SARS coronavirus (SARS-CoV) infection. To understand the pathogenesis, we studied viral replication, cytokine/chemokine response, and antigen presentation in MERS-CoV–infected human monocyte–derived macrophages (MDMs) versus SARS-CoV–infected MDMs. Only MERS-CoV can replicate in MDMs. Both viruses were unable to significantly stimulate the expression of antiviral cytokines (interferon α [IFN-α] and IFN-β) but induced comparable levels of tumor necrosis factor α and interleukin 6. Notably, MERS-CoV induced significantly higher expression levels of interleukin 12, IFN-γ, and chemokines (IP-10/CXCL-10, MCP-1/CCL-2, MIP-1α/CCL-3, RANTES/CCL-5, and interleukin 8) than SARS-CoV. The expression of major histocompatibility complex class I and costimulatory molecules were significantly higher in MERS-CoV–infected MDMs than in SARS-CoV–infected cells. MERS-CoV replication was validated by immunostaining of infected MDMs and ex vivo lung tissue. We conclusively showed that MERS-CoV can establish a productive infection in human macrophages. The aberrant induction of inflammatory cytokines/chemokines could be important in the disease pathogenesis.</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">J Infect Dis</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Infect. Dis</journal-id>
<journal-id journal-id-type="publisher-id">jid</journal-id>
<journal-id journal-id-type="hwp">jinfdis</journal-id>
<journal-title-group><journal-title>The Journal of Infectious Diseases</journal-title>
</journal-title-group>
<issn pub-type="ppub">0022-1899</issn>
<issn pub-type="epub">1537-6613</issn>
<publisher><publisher-name>Oxford University Press</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">24065148</article-id>
<article-id pub-id-type="pmc">7107356</article-id>
<article-id pub-id-type="doi">10.1093/infdis/jit504</article-id>
<article-id pub-id-type="publisher-id">jit504</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Major Articles and Brief Reports</subject>
<subj-group subj-group-type="category-toc-heading"><subject>Viruses</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Active Replication of Middle East Respiratory Syndrome Coronavirus and Aberrant Induction of Inflammatory Cytokines and Chemokines in Human Macrophages: Implications for Pathogenesis</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Zhou</surname>
<given-names>Jie</given-names>
</name>
<author-comment><title>a</title>
<p>J. Z. and H. C. contributed equally to the study.</p>
</author-comment>
<xref ref-type="aff" rid="af1">1</xref>
<xref ref-type="aff" rid="af2">2</xref>
<xref ref-type="aff" rid="af3">3</xref>
<pmc-comment>kyyuen@hkucc.hku.hk </pmc-comment>
<xref ref-type="corresp" rid="d804669e334"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chu</surname>
<given-names>Hin</given-names>
</name>
<author-comment><title>a</title>
<p>J. Z. and H. C. contributed equally to the study.</p>
</author-comment>
<xref ref-type="aff" rid="af2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Cun</given-names>
</name>
<xref ref-type="aff" rid="af2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wong</surname>
<given-names>Bosco Ho-Yin</given-names>
</name>
<xref ref-type="aff" rid="af2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cheng</surname>
<given-names>Zhong-Shan</given-names>
</name>
<xref ref-type="aff" rid="af2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Poon</surname>
<given-names>Vincent Kwok-Man</given-names>
</name>
<xref ref-type="aff" rid="af2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sun</surname>
<given-names>Tianhao</given-names>
</name>
<xref ref-type="aff" rid="af2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lau</surname>
<given-names>Candy Choi-Yi</given-names>
</name>
<xref ref-type="aff" rid="af2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wong</surname>
<given-names>Kenneth Kak-Yuen</given-names>
</name>
<xref ref-type="aff" rid="af5">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chan</surname>
<given-names>Jimmy Yu-Wai</given-names>
</name>
<xref ref-type="aff" rid="af5">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chan</surname>
<given-names>Jasper Fuk-Woo</given-names>
</name>
<xref ref-type="aff" rid="af1">1</xref>
<xref ref-type="aff" rid="af2">2</xref>
<xref ref-type="aff" rid="af3">3</xref>
<xref ref-type="aff" rid="af4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>To</surname>
<given-names>Kelvin Kai-Wang</given-names>
</name>
<xref ref-type="aff" rid="af1">1</xref>
<xref ref-type="aff" rid="af2">2</xref>
<xref ref-type="aff" rid="af3">3</xref>
<xref ref-type="aff" rid="af4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chan</surname>
<given-names>Kwok-Hung</given-names>
</name>
<xref ref-type="aff" rid="af2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zheng</surname>
<given-names>Bo-Jian</given-names>
</name>
<xref ref-type="aff" rid="af1">1</xref>
<xref ref-type="aff" rid="af2">2</xref>
<xref ref-type="aff" rid="af3">3</xref>
<xref ref-type="aff" rid="af4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yuen</surname>
<given-names>Kwok-Yung</given-names>
</name>
<xref ref-type="aff" rid="af1">1</xref>
<xref ref-type="aff" rid="af2">2</xref>
<xref ref-type="aff" rid="af3">3</xref>
<xref ref-type="aff" rid="af4">4</xref>
</contrib>
</contrib-group>
<aff id="af1"><label>1</label>
<addr-line>State Key Laboratory of Emerging Infectious Diseases</addr-line>
</aff>
<aff id="af2"><label>2</label>
<addr-line>Department of Microbiology</addr-line>
</aff>
<aff id="af3"><label>3</label>
<addr-line>Research Centre of Infection and Immunology</addr-line>
</aff>
<aff id="af4"><label>4</label>
<addr-line>Carol Yu Centre for Infection</addr-line>
</aff>
<aff id="af5"><label>5</label>
<addr-line>Department of Surgery</addr-line>
,<institution>University of Hong Kong, Hong Kong Special Administrative Region</institution>
,<country>China</country>
</aff>
<author-notes><fn id="AN1" fn-type="con"><label>a</label>
<p>J. Z. and H. C. contributed equally to the study.</p>
</fn>
<corresp id="d804669e334">Correspondence: Kwok-Yung Yuen, MD, Carol Yu Centre for Infection, Department of Microbiology, University of Hong Kong, Queen Mary Hospital, 102 Pokfulam Rd, Pokfulam, Hong Kong Special Administrative Region, China (<email>kyyuen@hkucc.hku.hk</email>
).</corresp>
</author-notes>
<pub-date pub-type="ppub"><day>1</day>
<month>5</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="epub" iso-8601-date="2013-09-24"><day>24</day>
<month>9</month>
<year>2013</year>
</pub-date>
<volume>209</volume>
<issue>9</issue>
<fpage>1331</fpage>
<lpage>1342</lpage>
<history><date date-type="received"><day>17</day>
<month>7</month>
<year>2013</year>
</date>
<date date-type="accepted"><day>27</day>
<month>8</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-statement>© The Author 2013. Published by Oxford University Press on behalf of the Infectious Diseases Society of America. All rights reserved. For Permissions, please e-mail: <email>journals.permissions@oup.com</email>
.</copyright-statement>
<copyright-year>2013</copyright-year>
<license><license-p>This article is made available via the PMC Open Access Subset for unrestricted re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the COVID-19 pandemic or until permissions are revoked in writing. Upon expiration of these permissions, PMC is granted a perpetual license to make this article available via PMC and Europe PMC, consistent with existing copyright protections.</license-p>
</license>
</permissions>
<self-uri xlink:href="jit504.pdf"></self-uri>
<abstract><title>Abstract</title>
<p>Middle East respiratory syndrome coronavirus (MERS-CoV) infection caused severe pneumonia and multiorgan dysfunction and had a higher crude fatality rate (around 50% vs 10%) than SARS coronavirus (SARS-CoV) infection. To understand the pathogenesis, we studied viral replication, cytokine/chemokine response, and antigen presentation in MERS-CoV–infected human monocyte–derived macrophages (MDMs) versus SARS-CoV–infected MDMs. Only MERS-CoV can replicate in MDMs. Both viruses were unable to significantly stimulate the expression of antiviral cytokines (interferon α [IFN-α] and IFN-β) but induced comparable levels of tumor necrosis factor α and interleukin 6. Notably, MERS-CoV induced significantly higher expression levels of interleukin 12, IFN-γ, and chemokines (IP-10/CXCL-10, MCP-1/CCL-2, MIP-1α/CCL-3, RANTES/CCL-5, and interleukin 8) than SARS-CoV. The expression of major histocompatibility complex class I and costimulatory molecules were significantly higher in MERS-CoV–infected MDMs than in SARS-CoV–infected cells. MERS-CoV replication was validated by immunostaining of infected MDMs and ex vivo lung tissue. We conclusively showed that MERS-CoV can establish a productive infection in human macrophages. The aberrant induction of inflammatory cytokines/chemokines could be important in the disease pathogenesis.</p>
</abstract>
<kwd-group><kwd>MERS-CoV</kwd>
<kwd>SARS-CoV</kwd>
<kwd>viral replication</kwd>
<kwd>pathogenesis</kwd>
<kwd>cytokine and chemokine response</kwd>
</kwd-group>
</article-meta>
</front>
</pmc>
</record>
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