Major alterations in the mononuclear phagocyte landscape associated with COVID-19 severity

Dendritic cells (DCs) and monocytes are crucial mediators of innate and adaptive immune responses during viral infection, but misdirected responses by these cells may contribute to immunopathology. Here, we performed high-dimensional flow cytometry-analysis focusing on mononuclear phagocyte (MNP) li...

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Vydané v:	Proceedings of the National Academy of Sciences - PNAS Ročník 118; číslo 6
Hlavní autori:	Kvedaraite, Egle, Hertwig, Laura, Sinha, Indranil, Ponzetta, Andrea, Hed Myrberg, Ida, Lourda, Magda, Dzidic, Majda, Akber, Mira, Klingström, Jonas, Folkesson, Elin, Muvva, Jagadeeswara Rao, Chen, Puran, Gredmark-Russ, Sara, Brighenti, Susanna, Norrby-Teglund, Anna, Eriksson, Lars I, Rooyackers, Olav, Aleman, Soo, Strålin, Kristoffer, Ljunggren, Hans-Gustaf, Ginhoux, Florent, Björkström, Niklas K, Henter, Jan-Inge, Svensson, Mattias
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	United States 09.02.2021
Predmet:	Adult COVID-19 - epidemiology COVID-19 - immunology COVID-19 - metabolism COVID-19 - virology Cytokines - immunology Dendritic Cells - immunology Female Humans Interferons - immunology Male Middle Aged Monocytes - immunology Mononuclear Phagocyte System - immunology Mononuclear Phagocyte System - metabolism SARS-CoV-2 - immunology Severity of Illness Index Sweden Sweden COVID-19 monocytes DCs pre-DCs
ISSN:	1091-6490, 1091-6490
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Abstract	Dendritic cells (DCs) and monocytes are crucial mediators of innate and adaptive immune responses during viral infection, but misdirected responses by these cells may contribute to immunopathology. Here, we performed high-dimensional flow cytometry-analysis focusing on mononuclear phagocyte (MNP) lineages in SARS-CoV-2-infected patients with moderate and severe COVID-19. We provide a deep and comprehensive map of the MNP landscape in COVID-19. A redistribution of monocyte subsets toward intermediate monocytes and a general decrease in circulating DCs was observed in response to infection. Severe disease coincided with the appearance of monocytic myeloid-derived suppressor cell-like cells and a higher frequency of pre-DC2. Furthermore, phenotypic alterations in MNPs, and their late precursors, were cell-lineage-specific and associated either with the general response against SARS-CoV-2 or COVID-19 severity. This included an interferon-imprint in DC1s observed in all patients and a decreased expression of the coinhibitory molecule CD200R in pre-DCs, DC2s, and DC3 subsets of severely sick patients. Finally, unsupervised analysis revealed that the MNP profile, alone, pointed to a cluster of COVID-19 nonsurvivors. This study provides a reference for the MNP response to SARS-CoV-2 infection and unravels mononuclear phagocyte dysregulations associated with severe COVID-19.
AbstractList	Dendritic cells (DCs) and monocytes are crucial mediators of innate and adaptive immune responses during viral infection, but misdirected responses by these cells may contribute to immunopathology. Here, we performed high-dimensional flow cytometry-analysis focusing on mononuclear phagocyte (MNP) lineages in SARS-CoV-2-infected patients with moderate and severe COVID-19. We provide a deep and comprehensive map of the MNP landscape in COVID-19. A redistribution of monocyte subsets toward intermediate monocytes and a general decrease in circulating DCs was observed in response to infection. Severe disease coincided with the appearance of monocytic myeloid-derived suppressor cell-like cells and a higher frequency of pre-DC2. Furthermore, phenotypic alterations in MNPs, and their late precursors, were cell-lineage-specific and associated either with the general response against SARS-CoV-2 or COVID-19 severity. This included an interferon-imprint in DC1s observed in all patients and a decreased expression of the coinhibitory molecule CD200R in pre-DCs, DC2s, and DC3 subsets of severely sick patients. Finally, unsupervised analysis revealed that the MNP profile, alone, pointed to a cluster of COVID-19 nonsurvivors. This study provides a reference for the MNP response to SARS-CoV-2 infection and unravels mononuclear phagocyte dysregulations associated with severe COVID-19.Dendritic cells (DCs) and monocytes are crucial mediators of innate and adaptive immune responses during viral infection, but misdirected responses by these cells may contribute to immunopathology. Here, we performed high-dimensional flow cytometry-analysis focusing on mononuclear phagocyte (MNP) lineages in SARS-CoV-2-infected patients with moderate and severe COVID-19. We provide a deep and comprehensive map of the MNP landscape in COVID-19. A redistribution of monocyte subsets toward intermediate monocytes and a general decrease in circulating DCs was observed in response to infection. Severe disease coincided with the appearance of monocytic myeloid-derived suppressor cell-like cells and a higher frequency of pre-DC2. Furthermore, phenotypic alterations in MNPs, and their late precursors, were cell-lineage-specific and associated either with the general response against SARS-CoV-2 or COVID-19 severity. This included an interferon-imprint in DC1s observed in all patients and a decreased expression of the coinhibitory molecule CD200R in pre-DCs, DC2s, and DC3 subsets of severely sick patients. Finally, unsupervised analysis revealed that the MNP profile, alone, pointed to a cluster of COVID-19 nonsurvivors. This study provides a reference for the MNP response to SARS-CoV-2 infection and unravels mononuclear phagocyte dysregulations associated with severe COVID-19. Dendritic cells (DCs) and monocytes are crucial mediators of innate and adaptive immune responses during viral infection, but misdirected responses by these cells may contribute to immunopathology. Here, we performed high-dimensional flow cytometry-analysis focusing on mononuclear phagocyte (MNP) lineages in SARS-CoV-2-infected patients with moderate and severe COVID-19. We provide a deep and comprehensive map of the MNP landscape in COVID-19. A redistribution of monocyte subsets toward intermediate monocytes and a general decrease in circulating DCs was observed in response to infection. Severe disease coincided with the appearance of monocytic myeloid-derived suppressor cell-like cells and a higher frequency of pre-DC2. Furthermore, phenotypic alterations in MNPs, and their late precursors, were cell-lineage-specific and associated either with the general response against SARS-CoV-2 or COVID-19 severity. This included an interferon-imprint in DC1s observed in all patients and a decreased expression of the coinhibitory molecule CD200R in pre-DCs, DC2s, and DC3 subsets of severely sick patients. Finally, unsupervised analysis revealed that the MNP profile, alone, pointed to a cluster of COVID-19 nonsurvivors. This study provides a reference for the MNP response to SARS-CoV-2 infection and unravels mononuclear phagocyte dysregulations associated with severe COVID-19.
Author	Hertwig, Laura Norrby-Teglund, Anna Eriksson, Lars I Ljunggren, Hans-Gustaf Dzidic, Majda Chen, Puran Aleman, Soo Hed Myrberg, Ida Klingström, Jonas Sinha, Indranil Brighenti, Susanna Kvedaraite, Egle Lourda, Magda Folkesson, Elin Gredmark-Russ, Sara Björkström, Niklas K Ponzetta, Andrea Akber, Mira Ginhoux, Florent Muvva, Jagadeeswara Rao Strålin, Kristoffer Rooyackers, Olav Svensson, Mattias Henter, Jan-Inge
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University of Singapore Academic Medical Centre, 168753 Singapore, Singapore – sequence: 22 givenname: Niklas K orcidid: 0000-0002-0967-076X surname: Björkström fullname: Björkström, Niklas K organization: Center for Infectious Medicine, Department of Medicine Huddinge, Karolinska Institutet, Karolinska University Hospital, 171 77 Stockholm, Sweden – sequence: 23 givenname: Jan-Inge orcidid: 0000-0002-0629-2126 surname: Henter fullname: Henter, Jan-Inge organization: Pediatric Oncology, Theme of Children's Health, Karolinska University Hospital, 171 77 Stockholm, Sweden – sequence: 24 givenname: Mattias orcidid: 0000-0003-1695-7934 surname: Svensson fullname: Svensson, Mattias organization: Center for Infectious Medicine, Department of Medicine Huddinge, Karolinska Institutet, Karolinska University Hospital, 171 77 Stockholm, Sweden
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ContentType	Journal Article
Contributor	Färnert, Anna Hertwig, Laura Norrby-Teglund, Anna Chen, Puran Dzidic, Majda Wullimann, David Aleman, Soo Butrym, Marta Bergsten, Helena Brighenti, Susanna Chambers, Benedict J Mårtensson, Johan Kvedaraite, Egle von Kries, Andreas Malmberg, Karl-Johan Sönnerborg, Anders Cornillet, Martin Muvva, Jagadeeswara Rao Berglin, Lena Tynell, Janne Michaëlsson, Jakob Loreti, Marco Giulio Marquardt, Nicole Perez-Potti, André Kammann, Tobias Björkström, Niklas K Sohlberg, Ebba Sandberg, John Tyler Haroun-Izquierdo, Alvaro Lourda, Magdalini Svensson, Mattias Unge, Christian Cuapio, Angelica Flodström-Tullberg, Malin Ljunggren, Hans-Gustaf Medina, Laura M Palma Varnaite, Renata Sandberg, Johan K Maleki, Kimia T Klingström, Jonas Mjösberg, Jenny Kalsum, Sadaf Brownlie, Demi Glans, Hedvig Ringqvist, Emma Buggert, Marcus Parrot, Tiphaine Lozano, Isabel Diaz Strålin, Kristoffer Nauclér, Pontus Rivera-Ballesteros, Olga Eriksson, Lars I Kokkinou, Efthymia Moll, Kirsten Maucourant, Christopher Sekine, Takuya Gorin, Jean-Baptiste Gredmark-Russ, Sara Radler, Lena Akb
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Copyright	Copyright © 2021 the Author(s). Published by PNAS.
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Keywords	COVID-19 monocytes DCs pre-DCs
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Snippet	Dendritic cells (DCs) and monocytes are crucial mediators of innate and adaptive immune responses during viral infection, but misdirected responses by these...
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SubjectTerms	Adult COVID-19 - epidemiology COVID-19 - immunology COVID-19 - metabolism COVID-19 - virology Cytokines - immunology Dendritic Cells - immunology Female Humans Interferons - immunology Male Middle Aged Monocytes - immunology Mononuclear Phagocyte System - immunology Mononuclear Phagocyte System - metabolism SARS-CoV-2 - immunology Severity of Illness Index Sweden
Title	Major alterations in the mononuclear phagocyte landscape associated with COVID-19 severity
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