Lung endothelial cell antigen cross-presentation to CD8+T cells drives malaria-associated lung injury
Identifieur interne : 000A36 ( Ncbi/Merge ); précédent : 000A35; suivant : 000A37Lung endothelial cell antigen cross-presentation to CD8+T cells drives malaria-associated lung injury
Auteurs : Carla Claser [Singapour] ; Samantha Yee Teng Nguee [Singapour] ; Akhila Balachander [Singapour] ; Shanshan Wu Howland [Singapour] ; Etienne Becht [Singapour] ; Bavani Gunasegaran [Singapour] ; Siddesh V. Hartimath [Singapour] ; Audrey W. Q. Lee [Singapour] ; Jacqueline Theng Theng Ho [Singapour] ; Chee Bing Ong [Singapour] ; Evan W. Newell [Singapour] ; Julian Goggi [Singapour] ; Lai Guan Ng [Singapour] ; Laurent Renia [Singapour]Source :
- Nature Communications [ 2041-1723 ] ; 2019.
Abstract
Malaria-associated acute respiratory distress syndrome (ARDS) and acute lung injury (ALI) are life-threatening manifestations of severe malaria infections. The pathogenic mechanisms that lead to respiratory complications, such as vascular leakage, remain unclear. Here, we confirm that depleting CD8+T cells with anti-CD8β antibodies in C57BL/6 mice infected with
Url:
DOI: 10.1038/s41467-019-12017-8
PubMed: 31534124
PubMed Central: 6751193
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Hartimath</name><affiliation wicri:level="1"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0393 4167</institution-id><institution-id institution-id-type="GRID">grid.452254.0</institution-id><institution>Isotopic Molecular Imaging Laboratory,</institution><institution>Singapore Bioimaging Consortium (SBIC), A*STAR,</institution></institution-wrap>11 Biopolis Way, #02-02 Helios, Singapore, 138667 Singapore</nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea>11 Biopolis Way, #02-02 Helios, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Lee, Audrey W Q" sort="Lee, Audrey W Q" uniqKey="Lee A" first="Audrey W. Q." last="Lee">Audrey W. Q. Lee</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0637 0221</institution-id><institution-id institution-id-type="GRID">grid.185448.4</institution-id><institution>Singapore Immunology Network (SIgN),</institution><institution>A*STAR, 8A Biomedical Grove,</institution></institution-wrap>Level 3 & 4 Immunos Building, Singapore, 138648 Singapore</nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea>Level 3 & 4 Immunos Building, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Theng Theng Ho, Jacqueline" sort="Theng Theng Ho, Jacqueline" uniqKey="Theng Theng Ho J" first="Jacqueline" last="Theng Theng Ho">Jacqueline Theng Theng Ho</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0637 0221</institution-id><institution-id institution-id-type="GRID">grid.185448.4</institution-id><institution>Singapore Immunology Network (SIgN),</institution><institution>A*STAR, 8A Biomedical Grove,</institution></institution-wrap>Level 3 & 4 Immunos Building, Singapore, 138648 Singapore</nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea>Level 3 & 4 Immunos Building, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Bing Ong, Chee" sort="Bing Ong, Chee" uniqKey="Bing Ong C" first="Chee" last="Bing Ong">Chee Bing Ong</name><affiliation wicri:level="1"><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0620 9243</institution-id><institution-id institution-id-type="GRID">grid.418812.6</institution-id><institution>Histolopathology/Advanced Molecular Pathology Lab,</institution><institution>Institute of Molecular and Cell Biology (IMCB), A*STAR,</institution></institution-wrap>61 Biopolis Drive, Level 6 Proteos Building, Singapore, 138673 Singapore</nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea>61 Biopolis Drive, Level 6 Proteos Building, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Newell, Evan W" sort="Newell, Evan W" uniqKey="Newell E" first="Evan W." last="Newell">Evan W. Newell</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0637 0221</institution-id><institution-id institution-id-type="GRID">grid.185448.4</institution-id><institution>Singapore Immunology Network (SIgN),</institution><institution>A*STAR, 8A Biomedical Grove,</institution></institution-wrap>Level 3 & 4 Immunos Building, Singapore, 138648 Singapore</nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea>Level 3 & 4 Immunos Building, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Goggi, Julian" sort="Goggi, Julian" uniqKey="Goggi J" first="Julian" last="Goggi">Julian Goggi</name><affiliation wicri:level="1"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0393 4167</institution-id><institution-id institution-id-type="GRID">grid.452254.0</institution-id><institution>Isotopic Molecular Imaging Laboratory,</institution><institution>Singapore Bioimaging Consortium (SBIC), A*STAR,</institution></institution-wrap>11 Biopolis Way, #02-02 Helios, Singapore, 138667 Singapore</nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea>11 Biopolis Way, #02-02 Helios, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Guan Ng, Lai" sort="Guan Ng, Lai" uniqKey="Guan Ng L" first="Lai" last="Guan Ng">Lai Guan Ng</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0637 0221</institution-id><institution-id institution-id-type="GRID">grid.185448.4</institution-id><institution>Singapore Immunology Network (SIgN),</institution><institution>A*STAR, 8A Biomedical Grove,</institution></institution-wrap>Level 3 & 4 Immunos Building, Singapore, 138648 Singapore</nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea>Level 3 & 4 Immunos Building, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Renia, Laurent" sort="Renia, Laurent" uniqKey="Renia L" first="Laurent" last="Renia">Laurent Renia</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0637 0221</institution-id><institution-id institution-id-type="GRID">grid.185448.4</institution-id><institution>Singapore Immunology Network (SIgN),</institution><institution>A*STAR, 8A Biomedical Grove,</institution></institution-wrap>Level 3 & 4 Immunos Building, Singapore, 138648 Singapore</nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea>Level 3 & 4 Immunos Building, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2180 6431</institution-id><institution-id institution-id-type="GRID">grid.4280.e</institution-id><institution>Department of Microbiology and Immunology, Yong Loo Lin School of Medicine,</institution><institution>National University of Singapore,</institution></institution-wrap>5 Science Drive 2 Blk MD4, Level 3, Singapore, 117545 Singapore</nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea>5 Science Drive 2 Blk MD4, Level 3, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author></analytic><series><title level="j">Nature Communications</title><idno type="eISSN">2041-1723</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p id="Par1">Malaria-associated acute respiratory distress syndrome (ARDS) and acute lung injury (ALI) are life-threatening manifestations of severe malaria infections. The pathogenic mechanisms that lead to respiratory complications, such as vascular leakage, remain unclear. Here, we confirm that depleting CD8<sup>+</sup>T cells with anti-CD8β antibodies in C57BL/6 mice infected with <italic>P. berghei</italic> ANKA (PbA) prevent pulmonary vascular leakage. When we transfer activated parasite-specific CD8<sup>+</sup>T cells into PbA-infected TCRβ<sup>−/−</sup> mice (devoid of all T-cell populations), pulmonary vascular leakage recapitulates. Additionally, we demonstrate that PbA-infected erythrocyte accumulation leads to lung endothelial cell cross-presentation of parasite antigen to CD8<sup>+</sup>T cells in an IFNγ−dependent manner. In conclusion, pulmonary vascular damage in ALI is a consequence of IFNγ-activated lung endothelial cells capturing, processing, and cross-presenting malaria parasite antigen to specific CD8<sup>+</sup>T cells induced during infection. 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sortKey="Wolf, J" uniqKey="Wolf J">J Wolf</name></author><author><name sortKey="Okerberg, C" uniqKey="Okerberg C">C Okerberg</name></author><author><name sortKey="Herbert, R" uniqKey="Herbert R">R Herbert</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bandura, Dr" uniqKey="Bandura D">DR Bandura</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Becher, B" uniqKey="Becher B">B Becher</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Chen, Sf" uniqKey="Chen S">SF Chen</name></author><author><name sortKey="Fei, X" uniqKey="Fei X">X Fei</name></author><author><name sortKey="Li, Sh" uniqKey="Li S">SH Li</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Nat Commun</journal-id><journal-id journal-id-type="iso-abbrev">Nat Commun</journal-id><journal-title-group><journal-title>Nature Communications</journal-title></journal-title-group><issn pub-type="epub">2041-1723</issn><publisher><publisher-name>Nature Publishing Group UK</publisher-name><publisher-loc>London</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31534124</article-id><article-id pub-id-type="pmc">6751193</article-id><article-id pub-id-type="publisher-id">12017</article-id><article-id pub-id-type="doi">10.1038/s41467-019-12017-8</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Lung endothelial cell antigen cross-presentation to CD8<sup>+</sup>T cells drives malaria-associated lung injury</article-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes" equal-contrib="yes"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-5395-9632</contrib-id><name><surname>Claser</surname><given-names>Carla</given-names></name><address><email>carla_claser@immunol.a-star.edu.sg</email></address><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Nguee</surname><given-names>Samantha Yee Teng</given-names></name><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-2168-0063</contrib-id><name><surname>Balachander</surname><given-names>Akhila</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0003-4794-1564</contrib-id><name><surname>Wu Howland</surname><given-names>Shanshan</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Becht</surname><given-names>Etienne</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-4783-8404</contrib-id><name><surname>Gunasegaran</surname><given-names>Bavani</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-8248-0866</contrib-id><name><surname>Hartimath</surname><given-names>Siddesh V.</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-7395-5225</contrib-id><name><surname>Lee</surname><given-names>Audrey W. Q.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Theng Theng Ho</surname><given-names>Jacqueline</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-0521-1646</contrib-id><name><surname>Bing Ong</surname><given-names>Chee</given-names></name><xref ref-type="aff" rid="Aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Newell</surname><given-names>Evan W.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-3021-3184</contrib-id><name><surname>Goggi</surname><given-names>Julian</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0003-1905-3586</contrib-id><name><surname>Guan Ng</surname><given-names>Lai</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0003-0349-1557</contrib-id><name><surname>Renia</surname><given-names>Laurent</given-names></name><address><email>renia_laurent@immunol.a-star.edu.sg</email></address><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><aff id="Aff1"><label>1</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0637 0221</institution-id><institution-id institution-id-type="GRID">grid.185448.4</institution-id><institution>Singapore Immunology Network (SIgN),</institution><institution>A*STAR, 8A Biomedical Grove,</institution></institution-wrap>Level 3 & 4 Immunos Building, Singapore, 138648 Singapore</aff><aff id="Aff2"><label>2</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2180 6431</institution-id><institution-id institution-id-type="GRID">grid.4280.e</institution-id><institution>Department of Microbiology and Immunology, Yong Loo Lin School of Medicine,</institution><institution>National University of Singapore,</institution></institution-wrap>5 Science Drive 2 Blk MD4, Level 3, Singapore, 117545 Singapore</aff><aff id="Aff3"><label>3</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0393 4167</institution-id><institution-id institution-id-type="GRID">grid.452254.0</institution-id><institution>Isotopic Molecular Imaging Laboratory,</institution><institution>Singapore Bioimaging Consortium (SBIC), A*STAR,</institution></institution-wrap>11 Biopolis Way, #02-02 Helios, Singapore, 138667 Singapore</aff><aff id="Aff4"><label>4</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0620 9243</institution-id><institution-id institution-id-type="GRID">grid.418812.6</institution-id><institution>Histolopathology/Advanced Molecular Pathology Lab,</institution><institution>Institute of Molecular and Cell Biology (IMCB), A*STAR,</institution></institution-wrap>61 Biopolis Drive, Level 6 Proteos Building, Singapore, 138673 Singapore</aff></contrib-group><pub-date pub-type="epub"><day>18</day><month>9</month><year>2019</year></pub-date><pub-date pub-type="pmc-release"><day>18</day><month>9</month><year>2019</year></pub-date><pub-date pub-type="collection"><year>2019</year></pub-date><volume>10</volume><elocation-id>4241</elocation-id><history><date date-type="received"><day>29</day><month>1</month><year>2019</year></date><date date-type="accepted"><day>15</day><month>8</month><year>2019</year></date></history><permissions><copyright-statement>© The Author(s) 2019</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold> This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>.</license-p></license></permissions><abstract id="Abs1"><p id="Par1">Malaria-associated acute respiratory distress syndrome (ARDS) and acute lung injury (ALI) are life-threatening manifestations of severe malaria infections. The pathogenic mechanisms that lead to respiratory complications, such as vascular leakage, remain unclear. Here, we confirm that depleting CD8<sup>+</sup>T cells with anti-CD8β antibodies in C57BL/6 mice infected with <italic>P. berghei</italic> ANKA (PbA) prevent pulmonary vascular leakage. When we transfer activated parasite-specific CD8<sup>+</sup>T cells into PbA-infected TCRβ<sup>−/−</sup> mice (devoid of all T-cell populations), pulmonary vascular leakage recapitulates. Additionally, we demonstrate that PbA-infected erythrocyte accumulation leads to lung endothelial cell cross-presentation of parasite antigen to CD8<sup>+</sup>T cells in an IFNγ−dependent manner. In conclusion, pulmonary vascular damage in ALI is a consequence of IFNγ-activated lung endothelial cells capturing, processing, and cross-presenting malaria parasite antigen to specific CD8<sup>+</sup>T cells induced during infection. The mechanistic understanding of the immunopathogenesis in malaria-associated ARDS and ALI provide the basis for development of adjunct treatments.</p></abstract><abstract id="Abs2" abstract-type="web-summary"><p id="Par2">Severe malaria can be associated with respiratory complications. Here, the authors show that malaria-associated pulmonary vascular damage is a consequence of IFNγ-activated lung endothelial cells capturing, processing, and cross-presenting malaria parasite antigen to specific CD8<sup>+</sup> T cells induced during infection.</p></abstract><kwd-group kwd-group-type="npg-subject"><title>Subject terms</title><kwd>Cellular immunity</kwd><kwd>Antigen-presenting cells</kwd><kwd>Malaria</kwd><kwd>Parasite host response</kwd></kwd-group><funding-group><award-group><funding-source><institution>Agency for Science, Technology and Research (A*STAR) to a core grant to SIgN</institution></funding-source></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2019</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc><affiliations><list><country><li>Singapour</li></country></list><tree><country name="Singapour"><noRegion><name sortKey="Claser, Carla" sort="Claser, Carla" uniqKey="Claser C" first="Carla" last="Claser">Carla Claser</name></noRegion><name sortKey="Balachander, Akhila" sort="Balachander, Akhila" uniqKey="Balachander A" first="Akhila" last="Balachander">Akhila Balachander</name><name sortKey="Becht, Etienne" sort="Becht, Etienne" uniqKey="Becht E" first="Etienne" last="Becht">Etienne Becht</name><name sortKey="Bing Ong, Chee" sort="Bing Ong, Chee" uniqKey="Bing Ong C" first="Chee" last="Bing Ong">Chee Bing Ong</name><name sortKey="Goggi, Julian" sort="Goggi, Julian" uniqKey="Goggi J" first="Julian" last="Goggi">Julian Goggi</name><name sortKey="Guan Ng, Lai" sort="Guan Ng, Lai" uniqKey="Guan Ng L" first="Lai" last="Guan Ng">Lai Guan Ng</name><name sortKey="Gunasegaran, Bavani" sort="Gunasegaran, Bavani" uniqKey="Gunasegaran B" first="Bavani" last="Gunasegaran">Bavani Gunasegaran</name><name sortKey="Hartimath, Siddesh V" sort="Hartimath, Siddesh V" uniqKey="Hartimath S" first="Siddesh V." last="Hartimath">Siddesh V. Hartimath</name><name sortKey="Lee, Audrey W Q" sort="Lee, Audrey W Q" uniqKey="Lee A" first="Audrey W. Q." last="Lee">Audrey W. Q. Lee</name><name sortKey="Newell, Evan W" sort="Newell, Evan W" uniqKey="Newell E" first="Evan W." last="Newell">Evan W. Newell</name><name sortKey="Nguee, Samantha Yee Teng" sort="Nguee, Samantha Yee Teng" uniqKey="Nguee S" first="Samantha Yee Teng" last="Nguee">Samantha Yee Teng Nguee</name><name sortKey="Nguee, Samantha Yee Teng" sort="Nguee, Samantha Yee Teng" uniqKey="Nguee S" first="Samantha Yee Teng" last="Nguee">Samantha Yee Teng Nguee</name><name sortKey="Renia, Laurent" sort="Renia, Laurent" uniqKey="Renia L" first="Laurent" last="Renia">Laurent Renia</name><name sortKey="Renia, Laurent" sort="Renia, Laurent" uniqKey="Renia L" first="Laurent" last="Renia">Laurent Renia</name><name sortKey="Theng Theng Ho, Jacqueline" sort="Theng Theng Ho, Jacqueline" uniqKey="Theng Theng Ho J" first="Jacqueline" last="Theng Theng Ho">Jacqueline Theng Theng Ho</name><name sortKey="Wu Howland, Shanshan" sort="Wu Howland, Shanshan" uniqKey="Wu Howland S" first="Shanshan" last="Wu Howland">Shanshan Wu Howland</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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