Suppressor of cytokine signaling 4 (SOCS4) protects against severe cytokine storm and enhances viral clearance during influenza infection

Suppressor of cytokine signaling (SOCS) proteins are key regulators of innate and adaptive immunity. There is no described biological role for SOCS4, despite broad expression in the hematopoietic system. We demonstrate that mice lacking functional SOCS4 protein rapidly succumb to infection with a pa...

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Published inPLoS pathogens Vol. 10; no. 5; p. e1004134
Main Authors Kedzierski, Lukasz, Linossi, Edmond M, Kolesnik, Tatiana B, Day, E Bridie, Bird, Nicola L, Kile, Benjamin T, Belz, Gabrielle T, Metcalf, Donald, Nicola, Nicos A, Kedzierska, Katherine, Nicholson, Sandra E
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.05.2014
Public Library of Science (PLoS)
Subjects
Adaptive Immunity - genetics
Animals
Antiviral agents
B cells
Biology and Life Sciences
Bone marrow
CD8-Positive T-Lymphocytes - immunology
Chemokines
Cytokines
Cytokines - adverse effects
Cytokines - metabolism
Cytoprotection - genetics
Flow cytometry
Health aspects
Immune system
Infections
Inflammation - genetics
Inflammation - metabolism
Inflammation - prevention & control
Inflammation Mediators - adverse effects
Inflammation Mediators - metabolism
Influenza A Virus, H1N1 Subtype - growth & development
Influenza A Virus, H1N1 Subtype - immunology
Kinases
Lungs
Lymphocytes
Mice
Mice, Inbred BALB C
Mice, Inbred C3H
Mice, Inbred C57BL
Mice, Transgenic
Mortality
Orthomyxoviridae Infections - immunology
Orthomyxoviridae Infections - virology
Physiological aspects
Proteins
Scholarships & fellowships
Suppressor of Cytokine Signaling Proteins - physiology
Swine flu
T cell receptors
T cells
Viral infections
Viral Load - genetics
Virulence (Microbiology)
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Abstract Suppressor of cytokine signaling (SOCS) proteins are key regulators of innate and adaptive immunity. There is no described biological role for SOCS4, despite broad expression in the hematopoietic system. We demonstrate that mice lacking functional SOCS4 protein rapidly succumb to infection with a pathogenic H1N1 influenza virus (PR8) and are hypersusceptible to infection with the less virulent H3N2 (X31) strain. In SOCS4-deficient animals, this led to substantially greater weight loss, dysregulated pro-inflammatory cytokine and chemokine production in the lungs and delayed viral clearance. This was associated with impaired trafficking of influenza-specific CD8 T cells to the site of infection and linked to defects in T cell receptor activation. These results demonstrate that SOCS4 is a critical regulator of anti-viral immunity.
AbstractList Suppressor of cytokine signaling (SOCS) proteins are key regulators of innate and adaptive immunity. There is no described biological role for SOCS4, despite broad expression in the hematopoietic system. We demonstrate that mice lacking functional SOCS4 protein rapidly succumb to infection with a pathogenic H1N1 influenza virus (PR8) and are hypersusceptible to infection with the less virulent H3N2 (X31) strain. In SOCS4-deficient animals, this led to substantially greater weight loss, dysregulated pro-inflammatory cytokine and chemokine production in the lungs and delayed viral clearance. This was associated with impaired trafficking of influenza-specific CD8 T cells to the site of infection and linked to defects in T cell receptor activation. These results demonstrate that SOCS4 is a critical regulator of anti-viral immunity.
Suppressor of cytokine signaling (SOCS) proteins are key regulators of innate and adaptive immunity. There is no described biological role for SOCS4, despite broad expression in the hematopoietic system. We demonstrate that mice lacking functional SOCS4 protein rapidly succumb to infection with a pathogenic H1N1 influenza virus (PR8) and are hypersusceptible to infection with the less virulent H3N2 (X31) strain. In SOCS4-deficient animals, this led to substantially greater weight loss, dysregulated pro-inflammatory cytokine and chemokine production in the lungs and delayed viral clearance. This was associated with impaired trafficking of influenza-specific CD8 T cells to the site of infection and linked to defects in T cell receptor activation. These results demonstrate that SOCS4 is a critical regulator of anti-viral immunity. The suppressor of cytokine signaling proteins are key regulators of immunity. As yet there is no described biological role for SOCS4, despite its broad expression in cells of the immune system. Given the important role of other SOCS proteins in controlling the immune response, we have generated SOCS4-mutant mice and used a mouse influenza infection model to investigate the biological function of SOCS4. We demonstrate that mice lacking SOCS4 rapidly succumb to infection with a pathogenic H1N1 influenza virus and are hypersusceptible to infection with the less virulent H3N2 strain. This is the first demonstration of a functional phenotype in SOCS4-deficient mice. Our study reveals that in SOCS4-deficient animals, there is a dysregulated pro-inflammatory cytokine and chemokine production in the lungs and delayed viral clearance. This is associated with impaired trafficking of virus-specific CD8 T cells to the site of infection and linked to defects in T cell receptor activation. These results demonstrate that SOCS4 is a critical regulator of anti-viral immunity. Understanding the regulation of the inflammatory response to influenza is particularly relevant given the current climate concerning pandemic influenza outbreaks.
  Suppressor of cytokine signaling (SOCS) proteins are key regulators of innate and adaptive immunity. There is no described biological role for SOCS4, despite broad expression in the hematopoietic system. We demonstrate that mice lacking functional SOCS4 protein rapidly succumb to infection with a pathogenic H1N1 influenza virus (PR8) and are hypersusceptible to infection with the less virulent H3N2 (X31) strain. In SOCS4-deficient animals, this led to substantially greater weight loss, dysregulated pro-inflammatory cytokine and chemokine production in the lungs and delayed viral clearance. This was associated with impaired trafficking of influenza-specific CD8 T cells to the site of infection and linked to defects in T cell receptor activation. These results demonstrate that SOCS4 is a critical regulator of anti-viral immunity.
Audience Academic
Author Day, E Bridie
Metcalf, Donald
Linossi, Edmond M
Belz, Gabrielle T
Kedzierski, Lukasz
Nicholson, Sandra E
Bird, Nicola L
Kile, Benjamin T
Kedzierska, Katherine
Nicola, Nicos A
Kolesnik, Tatiana B
AuthorAffiliation 3 Department of Microbiology and Immunology, The University of Melbourne, Parkville, Melbourne, Victoria, Australia
1 Walter and Eliza Hall Institute of Medical Research, Parkville, Melbourne, Victoria Australia
2 Department of Medical Biology, The University of Melbourne, Parkville, Melbourne, Victoria, Australia
National Institutes of Health, United States of America
AuthorAffiliation_xml – name: 3 Department of Microbiology and Immunology, The University of Melbourne, Parkville, Melbourne, Victoria, Australia
– name: 2 Department of Medical Biology, The University of Melbourne, Parkville, Melbourne, Victoria, Australia
– name: 1 Walter and Eliza Hall Institute of Medical Research, Parkville, Melbourne, Victoria Australia
– name: National Institutes of Health, United States of America
Author_xml – sequence: 1
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– sequence: 2
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  surname: Linossi
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  organization: Walter and Eliza Hall Institute of Medical Research, Parkville, Melbourne, Victoria Australia; Department of Medical Biology, The University of Melbourne, Parkville, Melbourne, Victoria, Australia
– sequence: 3
  givenname: Tatiana B
  surname: Kolesnik
  fullname: Kolesnik, Tatiana B
  organization: Walter and Eliza Hall Institute of Medical Research, Parkville, Melbourne, Victoria Australia; Department of Medical Biology, The University of Melbourne, Parkville, Melbourne, Victoria, Australia
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  organization: Walter and Eliza Hall Institute of Medical Research, Parkville, Melbourne, Victoria Australia; Department of Medical Biology, The University of Melbourne, Parkville, Melbourne, Victoria, Australia
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  surname: Belz
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  surname: Kedzierska
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ContentType Journal Article
Copyright COPYRIGHT 2014 Public Library of Science
2014 Kedzierski et al 2014 Kedzierski et al
2014 Kedzierski et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Kedzierski L, Linossi EM, Kolesnik TB, Day EB, Bird NL, et al. (2014) Suppressor of Cytokine Signaling 4 (SOCS4) Protects against Severe Cytokine Storm and Enhances Viral Clearance during Influenza Infection. PLoS Pathog 10(5): e1004134. doi:10.1371/journal.ppat.1004134
Copyright_xml – notice: COPYRIGHT 2014 Public Library of Science
– notice: 2014 Kedzierski et al 2014 Kedzierski et al
– notice: 2014 Kedzierski et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Kedzierski L, Linossi EM, Kolesnik TB, Day EB, Bird NL, et al. (2014) Suppressor of Cytokine Signaling 4 (SOCS4) Protects against Severe Cytokine Storm and Enhances Viral Clearance during Influenza Infection. PLoS Pathog 10(5): e1004134. doi:10.1371/journal.ppat.1004134
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Notes Conceived and designed the experiments: LK KK SEN. Performed the experiments: LK EML TBK EBD NLB. Analyzed the data: LK TBK SEN. Contributed reagents/materials/analysis tools: BTK GTB DM NAN KK. Wrote the paper: LK KK SEN.
The authors have declared that no competing interests exist.
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SSID ssj0041316
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Snippet Suppressor of cytokine signaling (SOCS) proteins are key regulators of innate and adaptive immunity. There is no described biological role for SOCS4, despite...
  Suppressor of cytokine signaling (SOCS) proteins are key regulators of innate and adaptive immunity. There is no described biological role for SOCS4, despite...
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StartPage e1004134
SubjectTerms Adaptive Immunity - genetics
Animals
Antiviral agents
B cells
Biology and Life Sciences
Bone marrow
CD8-Positive T-Lymphocytes - immunology
Chemokines
Cytokines
Cytokines - adverse effects
Cytokines - metabolism
Cytoprotection - genetics
Flow cytometry
Health aspects
Immune system
Infections
Inflammation - genetics
Inflammation - metabolism
Inflammation - prevention & control
Inflammation Mediators - adverse effects
Inflammation Mediators - metabolism
Influenza A Virus, H1N1 Subtype - growth & development
Influenza A Virus, H1N1 Subtype - immunology
Kinases
Lungs
Lymphocytes
Mice
Mice, Inbred BALB C
Mice, Inbred C3H
Mice, Inbred C57BL
Mice, Transgenic
Mortality
Orthomyxoviridae Infections - immunology
Orthomyxoviridae Infections - virology
Physiological aspects
Proteins
Scholarships & fellowships
Suppressor of Cytokine Signaling Proteins - physiology
Swine flu
T cell receptors
T cells
Viral infections
Viral Load - genetics
Virulence (Microbiology)
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Title Suppressor of cytokine signaling 4 (SOCS4) protects against severe cytokine storm and enhances viral clearance during influenza infection
URI https://www.ncbi.nlm.nih.gov/pubmed/24809749
https://pubmed.ncbi.nlm.nih.gov/PMC4014316
https://doaj.org/article/e74a61e58a7f4bfba5811da5416a7bf4
http://dx.doi.org/10.1371/journal.ppat.1004134
Volume 10
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