Pandemic H1N1 influenza A viruses suppress immunogenic RIPK3-driven dendritic cell death

Boris M. Hartmann; Randy A. Albrecht; Elena Zaslavsky; German Nudelman; Hanna Pincas; Nada Marjanovic; Michael Schotsaert; Carles Martínez-Romero; Rafael Fenutria; Justin P. Ingram; Irene Ramos; Ana Fernandez-Sesma; Siddharth Balachandran; Adolfo Garciá-Sastre; Stuart C. Sealfon

doi:10.1038/s41467-017-02035-9

Pandemic H1N1 influenza A viruses suppress immunogenic RIPK3-driven dendritic cell death

Boris M. Hartmann, Randy A. Albrecht, Elena Zaslavsky, German Nudelman, Hanna Pincas, Nada Marjanovic, Michael Schotsaert, Carles Martínez-Romero, Rafael Fenutria, Justin P. Ingram, Irene Ramos, Ana Fernandez-Sesma, Siddharth Balachandran, Adolfo Garciá-Sastre, Stuart C. Sealfon

Research output: Contribution to journal › Article › peer-review

39 Scopus citations

Abstract

The risk of emerging pandemic influenza A viruses (IAVs) that approach the devastating 1918 strain motivates finding strain-specific host-pathogen mechanisms. During infection, dendritic cells (DC) mature into antigen-presenting cells that activate T cells, linking innate to adaptive immunity. DC infection with seasonal IAVs, but not with the 1918 and 2009 pandemic strains, induces global RNA degradation. Here, we show that DC infection with seasonal IAV causes immunogenic RIPK3-mediated cell death. Pandemic IAV suppresses this immunogenic DC cell death. Only DC infected with seasonal IAV, but not with pandemic IAV, enhance maturation of uninfected DC and T cell proliferation. In vivo, circulating T cell levels are reduced after pandemic, but not seasonal, IAV infection. Using recombinant viruses, we identify the HA genomic segment as the mediator of cell death inhibition. These results show how pandemic influenza viruses subvert the immune response.

Original language	English
Article number	1931
Pages (from-to)	1931
Journal	Nature Communications
Volume	8
Issue number	1
DOIs	https://doi.org/10.1038/s41467-017-02035-9
State	Published - Dec 1 2017

Keywords

Adaptive Immunity/immunology
CD8-Positive T-Lymphocytes/immunology
Cell Death/immunology
Dendritic Cells/immunology
Humans
Immunity, Innate/immunology
In Vitro Techniques
Influenza A Virus, H1N1 Subtype/immunology
Influenza, Human/immunology
Lymphocyte Activation/immunology
Receptor-Interacting Protein Serine-Threonine Kinases/immunology
T-Lymphocytes/immunology

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Hartmann, B. M., Albrecht, R. A., Zaslavsky, E., Nudelman, G., Pincas, H., Marjanovic, N., Schotsaert, M., Martínez-Romero, C., Fenutria, R., Ingram, J. P., Ramos, I., Fernandez-Sesma, A., Balachandran, S., Garciá-Sastre, A., & Sealfon, S. C. (2017). Pandemic H1N1 influenza A viruses suppress immunogenic RIPK3-driven dendritic cell death. Nature Communications, 8(1), 1931. Article 1931. https://doi.org/10.1038/s41467-017-02035-9

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title = "Pandemic H1N1 influenza A viruses suppress immunogenic RIPK3-driven dendritic cell death",

abstract = "The risk of emerging pandemic influenza A viruses (IAVs) that approach the devastating 1918 strain motivates finding strain-specific host-pathogen mechanisms. During infection, dendritic cells (DC) mature into antigen-presenting cells that activate T cells, linking innate to adaptive immunity. DC infection with seasonal IAVs, but not with the 1918 and 2009 pandemic strains, induces global RNA degradation. Here, we show that DC infection with seasonal IAV causes immunogenic RIPK3-mediated cell death. Pandemic IAV suppresses this immunogenic DC cell death. Only DC infected with seasonal IAV, but not with pandemic IAV, enhance maturation of uninfected DC and T cell proliferation. In vivo, circulating T cell levels are reduced after pandemic, but not seasonal, IAV infection. Using recombinant viruses, we identify the HA genomic segment as the mediator of cell death inhibition. These results show how pandemic influenza viruses subvert the immune response.",

keywords = "Adaptive Immunity/immunology, CD8-Positive T-Lymphocytes/immunology, Cell Death/immunology, Dendritic Cells/immunology, Humans, Immunity, Innate/immunology, In Vitro Techniques, Influenza A Virus, H1N1 Subtype/immunology, Influenza, Human/immunology, Lymphocyte Activation/immunology, Receptor-Interacting Protein Serine-Threonine Kinases/immunology, T-Lymphocytes/immunology",

author = "Hartmann, {Boris M.} and Albrecht, {Randy A.} and Elena Zaslavsky and German Nudelman and Hanna Pincas and Nada Marjanovic and Michael Schotsaert and Carles Mart{\'i}nez-Romero and Rafael Fenutria and Ingram, {Justin P.} and Irene Ramos and Ana Fernandez-Sesma and Siddharth Balachandran and Adolfo Garci{\'a}-Sastre and Sealfon, {Stuart C.}",

note = "Publisher Copyright: {\textcopyright} 2017 The Author(s).",

year = "2017",

month = dec,

day = "1",

doi = "10.1038/s41467-017-02035-9",

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Hartmann, BM, Albrecht, RA, Zaslavsky, E, Nudelman, G, Pincas, H, Marjanovic, N, Schotsaert, M, Martínez-Romero, C, Fenutria, R, Ingram, JP, Ramos, I, Fernandez-Sesma, A, Balachandran, S, Garciá-Sastre, A & Sealfon, SC 2017, 'Pandemic H1N1 influenza A viruses suppress immunogenic RIPK3-driven dendritic cell death', Nature Communications, vol. 8, no. 1, 1931, pp. 1931. https://doi.org/10.1038/s41467-017-02035-9

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T1 - Pandemic H1N1 influenza A viruses suppress immunogenic RIPK3-driven dendritic cell death

AU - Hartmann, Boris M.

AU - Albrecht, Randy A.

AU - Zaslavsky, Elena

AU - Nudelman, German

AU - Pincas, Hanna

AU - Marjanovic, Nada

AU - Schotsaert, Michael

AU - Martínez-Romero, Carles

AU - Fenutria, Rafael

AU - Ingram, Justin P.

AU - Ramos, Irene

AU - Fernandez-Sesma, Ana

AU - Balachandran, Siddharth

AU - Garciá-Sastre, Adolfo

AU - Sealfon, Stuart C.

PY - 2017/12/1

Y1 - 2017/12/1

N2 - The risk of emerging pandemic influenza A viruses (IAVs) that approach the devastating 1918 strain motivates finding strain-specific host-pathogen mechanisms. During infection, dendritic cells (DC) mature into antigen-presenting cells that activate T cells, linking innate to adaptive immunity. DC infection with seasonal IAVs, but not with the 1918 and 2009 pandemic strains, induces global RNA degradation. Here, we show that DC infection with seasonal IAV causes immunogenic RIPK3-mediated cell death. Pandemic IAV suppresses this immunogenic DC cell death. Only DC infected with seasonal IAV, but not with pandemic IAV, enhance maturation of uninfected DC and T cell proliferation. In vivo, circulating T cell levels are reduced after pandemic, but not seasonal, IAV infection. Using recombinant viruses, we identify the HA genomic segment as the mediator of cell death inhibition. These results show how pandemic influenza viruses subvert the immune response.

AB - The risk of emerging pandemic influenza A viruses (IAVs) that approach the devastating 1918 strain motivates finding strain-specific host-pathogen mechanisms. During infection, dendritic cells (DC) mature into antigen-presenting cells that activate T cells, linking innate to adaptive immunity. DC infection with seasonal IAVs, but not with the 1918 and 2009 pandemic strains, induces global RNA degradation. Here, we show that DC infection with seasonal IAV causes immunogenic RIPK3-mediated cell death. Pandemic IAV suppresses this immunogenic DC cell death. Only DC infected with seasonal IAV, but not with pandemic IAV, enhance maturation of uninfected DC and T cell proliferation. In vivo, circulating T cell levels are reduced after pandemic, but not seasonal, IAV infection. Using recombinant viruses, we identify the HA genomic segment as the mediator of cell death inhibition. These results show how pandemic influenza viruses subvert the immune response.

KW - Adaptive Immunity/immunology

KW - CD8-Positive T-Lymphocytes/immunology

KW - Cell Death/immunology

KW - Dendritic Cells/immunology

KW - Humans

KW - Immunity, Innate/immunology

KW - In Vitro Techniques

KW - Influenza A Virus, H1N1 Subtype/immunology

KW - Influenza, Human/immunology

KW - Lymphocyte Activation/immunology

KW - Receptor-Interacting Protein Serine-Threonine Kinases/immunology

KW - T-Lymphocytes/immunology

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U2 - 10.1038/s41467-017-02035-9

DO - 10.1038/s41467-017-02035-9

M3 - Article

C2 - 29203926

AN - SCOPUS:85037151051

SN - 2041-1723

VL - 8

SP - 1931

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 1931

ER -

Pandemic H1N1 influenza A viruses suppress immunogenic RIPK3-driven dendritic cell death

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