Autoantibody-Mediated Erythrophagocytosis Increases Tuberculosis Susceptibility in HIV Patients
Identifieur interne : 000849 ( Pmc/Curation ); précédent : 000848; suivant : 000850Autoantibody-Mediated Erythrophagocytosis Increases Tuberculosis Susceptibility in HIV Patients
Auteurs : Youchao Dai [République populaire de Chine] ; Yi Cai [République populaire de Chine] ; Xin Wang [République populaire de Chine] ; Jialou Zhu [République populaire de Chine] ; Xiaoqing Liu [République populaire de Chine] ; Houming Liu [République populaire de Chine] ; Linghua Li [République populaire de Chine] ; Yinze Zhang [République populaire de Chine] ; Shengze Liu [République populaire de Chine] ; Zhihua Wen [République populaire de Chine] ; Carl G. Feng [Australie] ; Xinchun Chen [République populaire de Chine] ; Xiaoping Tang [République populaire de Chine]Source :
- mBio [ 2150-7511 ] ; 2020.
Abstract
HIV infection significantly increases TB susceptibility due to CD4 T-cell loss and macrophage dysfunction. Although it is relatively clear that CD4 T-cell loss represents a direct effect of HIV infection, the mechanism underlying how HIV infection dampens macrophage function is unknown. Here, we show that HIV infection enhances autoantibody-mediated erythrophagocytosis, which dampens macrophage bactericidal activity against TB by inhibiting HO-1-associated autophagy. Our findings reveal a novel mechanism explaining how HIV infection increases susceptibility to TB. We propose that DAT could be a potential measure to identify HIV patients who are at high TB risk and who would be suitable for anti-TB chemotherapy preventive treatment.
Url:
DOI: 10.1128/mBio.03246-19
PubMed: 32098821
PubMed Central: 7042700
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Shenzhen University School of Medicine, Shenzhen</wicri:regionArea></affiliation></author><author><name sortKey="Li, Linghua" sort="Li, Linghua" uniqKey="Li L" first="Linghua" last="Li">Linghua Li</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Research Institute of Infectious Diseases, Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Research Institute of Infectious Diseases, Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou</wicri:regionArea></affiliation></author><author><name sortKey="Zhang, Yinze" sort="Zhang, Yinze" uniqKey="Zhang Y" first="Yinze" last="Zhang">Yinze Zhang</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>International Cancer Center, Shenzhen University General Hospital, Shenzhen University Clinical Medical Academy, Shenzhen, China</addr-line></nlm:aff><country 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Shaoguan</wicri:regionArea></affiliation></author><author><name sortKey="Feng, Carl G" sort="Feng, Carl G" uniqKey="Feng C" first="Carl G." last="Feng">Carl G. Feng</name><affiliation wicri:level="1"><nlm:aff id="aff8"><addr-line>Immunology and Host Defense Group, Department of Infectious Diseases and Immunology, Faculty of Medicine and Health, The University of Sydney, Sydney, NSW, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Immunology and Host Defense Group, Department of Infectious Diseases and Immunology, Faculty of Medicine and Health, The University of Sydney, Sydney, NSW</wicri:regionArea></affiliation></author><author><name sortKey="Chen, Xinchun" sort="Chen, Xinchun" uniqKey="Chen X" first="Xinchun" last="Chen">Xinchun Chen</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Guangdong Key Laboratory of Regional Immunity and Diseases, Department of Pathogen Biology, Shenzhen University School of Medicine, Shenzhen, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Guangdong Key Laboratory of Regional Immunity and Diseases, Department of Pathogen Biology, Shenzhen University School of Medicine, Shenzhen</wicri:regionArea></affiliation></author><author><name sortKey="Tang, Xiaoping" sort="Tang, Xiaoping" uniqKey="Tang X" first="Xiaoping" last="Tang">Xiaoping Tang</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Research Institute of Infectious Diseases, Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Research Institute of Infectious Diseases, Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">32098821</idno><idno type="pmc">7042700</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7042700</idno><idno type="RBID">PMC:7042700</idno><idno type="doi">10.1128/mBio.03246-19</idno><date 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Medical University, Guangzhou</wicri:regionArea></affiliation></author><author><name sortKey="Cai, Yi" sort="Cai, Yi" uniqKey="Cai Y" first="Yi" last="Cai">Yi Cai</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Guangdong Key Laboratory of Regional Immunity and Diseases, Department of Pathogen Biology, Shenzhen University School of Medicine, Shenzhen, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Guangdong Key Laboratory of Regional Immunity and Diseases, Department of Pathogen Biology, Shenzhen University School of Medicine, Shenzhen</wicri:regionArea></affiliation></author><author><name sortKey="Wang, Xin" sort="Wang, Xin" uniqKey="Wang X" first="Xin" last="Wang">Xin Wang</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>International Cancer Center, Shenzhen University General Hospital, Shenzhen University Clinical Medical Academy, Shenzhen, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>International Cancer Center, Shenzhen University General Hospital, Shenzhen University Clinical Medical Academy, Shenzhen</wicri:regionArea></affiliation></author><author><name sortKey="Zhu, Jialou" sort="Zhu, Jialou" uniqKey="Zhu J" first="Jialou" last="Zhu">Jialou Zhu</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Guangdong Key Laboratory of Regional Immunity and Diseases, Department of Pathogen Biology, Shenzhen University School of Medicine, Shenzhen, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Guangdong Key Laboratory of Regional Immunity and Diseases, Department of Pathogen Biology, Shenzhen University School of Medicine, Shenzhen</wicri:regionArea></affiliation></author><author><name sortKey="Liu, Xiaoqing" sort="Liu, Xiaoqing" uniqKey="Liu X" first="Xiaoqing" last="Liu">Xiaoqing Liu</name><affiliation wicri:level="1"><nlm:aff id="aff4"><addr-line>Department of Infectious Disease, Shenzhen People’s Hospital, 2nd Clinical Medical College of Jinan University, Shenzhen, Guangdong Province, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Infectious Disease, Shenzhen People’s Hospital, 2nd Clinical Medical College of Jinan University, Shenzhen, Guangdong Province</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff5"><addr-line>Integrated Chinese and Western Medicine Postdoctoral Research Station, Jinan University, Guangzhou, Guangdong Province, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Integrated Chinese and Western Medicine Postdoctoral Research Station, Jinan University, Guangzhou, Guangdong Province</wicri:regionArea></affiliation></author><author><name sortKey="Liu, Houming" sort="Liu, Houming" uniqKey="Liu H" first="Houming" last="Liu">Houming Liu</name><affiliation wicri:level="1"><nlm:aff id="aff6"><addr-line>Clinical Laboratory, Shenzhen Third People’s Hospital, Shenzhen University School of Medicine, Shenzhen, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Clinical Laboratory, Shenzhen Third People’s Hospital, Shenzhen University School of Medicine, Shenzhen</wicri:regionArea></affiliation></author><author><name sortKey="Li, Linghua" sort="Li, Linghua" uniqKey="Li L" first="Linghua" last="Li">Linghua Li</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Research Institute of Infectious Diseases, Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Research Institute of Infectious Diseases, Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou</wicri:regionArea></affiliation></author><author><name sortKey="Zhang, Yinze" sort="Zhang, Yinze" uniqKey="Zhang Y" first="Yinze" last="Zhang">Yinze Zhang</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>International Cancer Center, Shenzhen University General Hospital, Shenzhen University Clinical Medical Academy, Shenzhen, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>International Cancer Center, Shenzhen University General Hospital, Shenzhen University Clinical Medical Academy, Shenzhen</wicri:regionArea></affiliation></author><author><name sortKey="Liu, Shengze" sort="Liu, Shengze" uniqKey="Liu S" first="Shengze" last="Liu">Shengze Liu</name><affiliation wicri:level="1"><nlm:aff id="aff7"><addr-line>Yuebei Second People’s Hospital, Shaoguan, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Yuebei Second People’s Hospital, Shaoguan</wicri:regionArea></affiliation></author><author><name sortKey="Wen, Zhihua" sort="Wen, Zhihua" uniqKey="Wen Z" first="Zhihua" last="Wen">Zhihua Wen</name><affiliation wicri:level="1"><nlm:aff id="aff7"><addr-line>Yuebei Second People’s Hospital, Shaoguan, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Yuebei Second People’s Hospital, Shaoguan</wicri:regionArea></affiliation></author><author><name sortKey="Feng, Carl G" sort="Feng, Carl G" uniqKey="Feng C" first="Carl G." last="Feng">Carl G. Feng</name><affiliation wicri:level="1"><nlm:aff id="aff8"><addr-line>Immunology and Host Defense Group, Department of Infectious Diseases and Immunology, Faculty of Medicine and Health, The University of Sydney, Sydney, NSW, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Immunology and Host Defense Group, Department of Infectious Diseases and Immunology, Faculty of Medicine and Health, The University of Sydney, Sydney, NSW</wicri:regionArea></affiliation></author><author><name sortKey="Chen, Xinchun" sort="Chen, Xinchun" uniqKey="Chen X" first="Xinchun" last="Chen">Xinchun Chen</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Guangdong Key Laboratory of Regional Immunity and Diseases, Department of Pathogen Biology, Shenzhen University School of Medicine, Shenzhen, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Guangdong Key Laboratory of Regional Immunity and Diseases, Department of Pathogen Biology, Shenzhen University School of Medicine, Shenzhen</wicri:regionArea></affiliation></author><author><name sortKey="Tang, Xiaoping" sort="Tang, Xiaoping" uniqKey="Tang X" first="Xiaoping" last="Tang">Xiaoping Tang</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Research Institute of Infectious Diseases, Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Research Institute of Infectious Diseases, Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou</wicri:regionArea></affiliation></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>HIV infection significantly increases TB susceptibility due to CD4 T-cell loss and macrophage dysfunction. Although it is relatively clear that CD4 T-cell loss represents a direct effect of HIV infection, the mechanism underlying how HIV infection dampens macrophage function is unknown. Here, we show that HIV infection enhances autoantibody-mediated erythrophagocytosis, which dampens macrophage bactericidal activity against TB by inhibiting HO-1-associated autophagy. Our findings reveal a novel mechanism explaining how HIV infection increases susceptibility to TB. We propose that DAT could be a potential measure to identify HIV patients who are at high TB risk and who would be suitable for anti-TB chemotherapy preventive treatment.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Bell, Lck" uniqKey="Bell L">LCK Bell</name></author><author><name sortKey="Noursadeghi, M" uniqKey="Noursadeghi M">M Noursadeghi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Getahun, H" uniqKey="Getahun H">H Getahun</name></author><author><name sortKey="Gunneberg, C" uniqKey="Gunneberg C">C Gunneberg</name></author><author><name sortKey="Granich, R" uniqKey="Granich R">R Granich</name></author><author><name sortKey="Nunn, P" uniqKey="Nunn P">P Nunn</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sonnenberg, P" uniqKey="Sonnenberg P">P Sonnenberg</name></author><author><name sortKey="Glynn, Jr" uniqKey="Glynn J">JR 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<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">32098821</article-id><article-id pub-id-type="pmc">7042700</article-id><article-id pub-id-type="publisher-id">mBio03246-19</article-id><article-id pub-id-type="doi">10.1128/mBio.03246-19</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>Autoantibody-Mediated Erythrophagocytosis Increases Tuberculosis Susceptibility in HIV Patients</article-title><alt-title alt-title-type="running-head">HIV Impairs TB Immunity via Erythrophagocytosis</alt-title><alt-title alt-title-type="short-authors">Dai et al.</alt-title></title-group><contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Dai</surname><given-names>Youchao</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Cai</surname><given-names>Yi</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><name><surname>Wang</surname><given-names>Xin</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><name><surname>Zhu</surname><given-names>Jialou</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><name><surname>Liu</surname><given-names>Xiaoqing</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref><xref ref-type="aff" rid="aff5"><sup>e</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><name><surname>Liu</surname><given-names>Houming</given-names></name><xref ref-type="aff" rid="aff6"><sup>f</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><name><surname>Li</surname><given-names>Linghua</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><name><surname>Zhang</surname><given-names>Yinze</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><name><surname>Liu</surname><given-names>Shengze</given-names></name><xref ref-type="aff" rid="aff7"><sup>g</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><name><surname>Wen</surname><given-names>Zhihua</given-names></name><xref ref-type="aff" rid="aff7"><sup>g</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><name><surname>Feng</surname><given-names>Carl G.</given-names></name><xref ref-type="aff" rid="aff8"><sup>h</sup></xref></contrib><contrib contrib-type="author" corresp="yes" equal-contrib="no"><name><surname>Chen</surname><given-names>Xinchun</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author" corresp="yes" equal-contrib="no"><name><surname>Tang</surname><given-names>Xiaoping</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><aff id="aff1"><label>a</label><addr-line>Research Institute of Infectious Diseases, Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou, China</addr-line></aff><aff id="aff2"><label>b</label><addr-line>Guangdong Key Laboratory of Regional Immunity and Diseases, Department of Pathogen Biology, Shenzhen University School of Medicine, Shenzhen, China</addr-line></aff><aff id="aff3"><label>c</label><addr-line>International Cancer Center, Shenzhen University General Hospital, Shenzhen University Clinical Medical Academy, Shenzhen, China</addr-line></aff><aff id="aff4"><label>d</label><addr-line>Department of Infectious Disease, Shenzhen People’s Hospital, 2nd Clinical Medical College of Jinan University, Shenzhen, Guangdong Province, China</addr-line></aff><aff id="aff5"><label>e</label><addr-line>Integrated Chinese and Western Medicine Postdoctoral Research Station, Jinan University, Guangzhou, Guangdong Province, China</addr-line></aff><aff id="aff6"><label>f</label><addr-line>Clinical Laboratory, Shenzhen Third People’s Hospital, Shenzhen University School of Medicine, Shenzhen, China</addr-line></aff><aff id="aff7"><label>g</label><addr-line>Yuebei Second People’s Hospital, Shaoguan, China</addr-line></aff><aff id="aff8"><label>h</label><addr-line>Immunology and Host Defense Group, Department of Infectious Diseases and Immunology, Faculty of Medicine and Health, The University of Sydney, Sydney, NSW, Australia</addr-line></aff></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>Kaufmann</surname><given-names>Stefan H. E.</given-names></name><role>Editor</role><aff>Max Planck Institute for Infection Biology</aff></contrib></contrib-group><author-notes><corresp id="cor1">Address correspondence to Xinchun Chen, <email>chenxinchun@szu.edu.cn</email>, or Xiaoping Tang, <email>tangxiaopinggz@163.com</email>.</corresp><fn fn-type="equal"><p>Youchao Dai and Yi Cai contributed equally to this article. Author order was determined by the temporal order in which the authors began performing the research.</p></fn></author-notes><pub-date pub-type="collection"><season>Jan-Feb</season><year>2020</year></pub-date><pub-date pub-type="epub"><day>25</day><month>2</month><year>2020</year></pub-date><volume>11</volume><issue>1</issue><elocation-id>e03246-19</elocation-id><history><date date-type="received"><day>10</day><month>12</month><year>2019</year></date><date date-type="accepted"><day>15</day><month>1</month><year>2020</year></date></history><permissions><copyright-statement>Copyright © 2020 Dai et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Dai 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="mBio.03246-19.pdf"></self-uri><abstract abstract-type="precis"><p>HIV infection significantly increases TB susceptibility due to CD4 T-cell loss and macrophage dysfunction. Although it is relatively clear that CD4 T-cell loss represents a direct effect of HIV infection, the mechanism underlying how HIV infection dampens macrophage function is unknown. Here, we show that HIV infection enhances autoantibody-mediated erythrophagocytosis, which dampens macrophage bactericidal activity against TB by inhibiting HO-1-associated autophagy. Our findings reveal a novel mechanism explaining how HIV infection increases susceptibility to TB. We propose that DAT could be a potential measure to identify HIV patients who are at high TB risk and who would be suitable for anti-TB chemotherapy preventive treatment.</p></abstract><abstract><title>ABSTRACT</title><p>Macrophage dysfunction is associated with increased tuberculosis (TB) susceptibility in patients with human immunodeficiency virus (HIV) infection. However, the mechanisms underlying how HIV infection impairs macrophage function are unclear. Here, we found that levels of autoantibodies against red blood cells (RBCs) were significantly elevated in patients with HIV as determined by direct antiglobulin test (DAT). DAT positivity was significantly associated with TB incidence in both univariate and multivariate analyses (odds ratio [OR] = 11.96 [confidence interval {CI}, 4.68 to 30.93] and 12.65 [3.33 to 52.75], respectively). <italic>Ex vivo</italic> analysis showed that autoantibodies against RBCs enhanced erythrophagocytosis and thus significantly impaired macrophage bactericidal function against intracellular <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>. Mechanistically, autoantibody-mediated erythrophagocytosis increased heme oxygenase-1 (HO-1) expression, which inhibited <named-content content-type="genus-species">M. tuberculosis</named-content>-induced autophagy in macrophages. Silencing <italic>ATG5</italic>, a key component for autophagy, completely abrogated the effect of erythrophagocytosis on macrophage bactericidal activity against <named-content content-type="genus-species">M. tuberculosis</named-content>. In conclusion, we have demonstrated that HIV infection increases autoantibody-mediated erythrophagocytosis. This process impairs macrophage bactericidal activity against <named-content content-type="genus-species">M. tuberculosis</named-content> by inhibiting HO-1-associated autophagy. These findings reveal a novel mechanism as to how HIV infection increases TB susceptibility.</p></abstract><kwd-group><title>KEYWORDS</title><kwd>HIV</kwd><kwd>erythrophagocytosis</kwd><kwd>heme oxygenase-1</kwd><kwd>autophagy</kwd><kwd>tuberculosis</kwd></kwd-group><funding-group><award-group id="award1"><funding-source><institution-wrap><institution>Science and Technology Project of Shenzhen</institution></institution-wrap></funding-source><award-id>JCYJ20160427184123851</award-id><principal-award-recipient><name><surname>Cai</surname><given-names>Yi</given-names></name></principal-award-recipient></award-group><award-group id="award2"><funding-source><institution-wrap><institution>Science and Technology Project of Shenzhen</institution></institution-wrap></funding-source><award-id>JCYJ20160427151540695</award-id><principal-award-recipient><name><surname>Liu</surname><given-names>Houming</given-names></name></principal-award-recipient></award-group><award-group id="award3"><funding-source><institution-wrap><institution>Science and Technology Project of Shenzhen</institution></institution-wrap></funding-source><award-id>JCYJ20170307095303424</award-id><principal-award-recipient><name><surname>Chen</surname><given-names>Xinchun</given-names></name></principal-award-recipient></award-group><award-group id="award4"><funding-source><institution-wrap><institution>Natural Science Foundation of China</institution></institution-wrap></funding-source><award-id>81525016/81772145/91942315</award-id><principal-award-recipient><name><surname>Chen</surname><given-names>Xinchun</given-names></name></principal-award-recipient></award-group><award-group id="award5"><funding-source><institution-wrap><institution>Natural Science Foundation of China</institution></institution-wrap></funding-source><award-id>81770013</award-id><principal-award-recipient><name><surname>Cai</surname><given-names>Yi</given-names></name></principal-award-recipient></award-group><award-group id="award6"><funding-source><institution-wrap><institution>Natural Science Foundation of China</institution></institution-wrap></funding-source><award-id>81871255</award-id><principal-award-recipient><name><surname>Feng</surname><given-names>Carl</given-names></name></principal-award-recipient></award-group></funding-group><counts><count count="8" count-type="supplementary-material"></count><fig-count count="5"></fig-count><table-count count="1"></table-count><equation-count count="0"></equation-count><ref-count count="61"></ref-count><page-count count="14"></page-count><word-count count="10576"></word-count></counts><custom-meta-group><custom-meta><meta-name>cover-date</meta-name><meta-value>January/February 2020</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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