Excessive neutrophil levels in the lung underlie the age-associated increase in influenza mortality

Neutrophils clear viruses, but excessive neutrophil responses induce tissue injury and worsen disease. Aging increases mortality to influenza infection; however, whether this is due to impaired viral clearance or a pathological host immune response is unknown. Here we show that aged mice have higher...

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Published inMucosal immunology Vol. 12; no. 2; pp. 545 - 554
Main Authors Kulkarni, Upasana, Zemans, Rachel L., Smith, Candice A., Wood, Sherri C., Deng, Jane C., Goldstein, Daniel R.
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.03.2019
Elsevier Limited
Subjects
Aging
Aging - physiology
Allergology
Alveoli
Animals
Antibodies
Biomedical and Life Sciences
Biomedicine
Cell Count
Cellular Senescence
Chemokine CXCL1 - metabolism
Chemokine CXCL2 - metabolism
Chemokines
Chemotaxis
Epithelial cells
Epithelial Cells - physiology
Epithelial Cells - virology
Gastroenterology
Geriatrics
Humans
Immune clearance
Immune response
Immunology
Infections
Influenza
Influenza, Human - immunology
Influenza, Human - mortality
Leukocytes (neutrophilic)
Lung - pathology
Mice
Mice, Inbred C57BL
Mortality
Neutrophils
Neutrophils - immunology
Neutrophils - virology
Senescence
Survival Analysis
Viral infections
Online AccessGet full text

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Abstract Neutrophils clear viruses, but excessive neutrophil responses induce tissue injury and worsen disease. Aging increases mortality to influenza infection; however, whether this is due to impaired viral clearance or a pathological host immune response is unknown. Here we show that aged mice have higher levels of lung neutrophils than younger mice after influenza viral infection. Depleting neutrophils after, but not before, infection substantially improves the survival of aged mice without altering viral clearance. Aged alveolar epithelial cells (AECs) have a higher frequency of senescence and secrete higher levels of the neutrophil-attracting chemokines CXCL1 and CXCL2 during influenza infection. These chemokines are required for age-enhanced neutrophil chemotaxis in vitro. Our work suggests that aging increases mortality from influenza in part because senescent AECs secrete more chemokines, leading to excessive neutrophil recruitment. Therapies that mitigate this pathological immune response in the elderly might improve outcomes of influenza and other respiratory infections.
AbstractList Neutrophils clear viruses, but excessive neutrophil responses induce tissue injury and worsen disease. Aging increases mortality to influenza infection; however, whether this is due to impaired viral clearance or a pathological host immune response is unknown. Here, we show that aged mice have higher levels of lung neutrophils than younger mice after influenza viral infection. Depleting neutrophils after, but not before, infection substantially improves the survival of aged mice without altering viral clearance. Aged alveolar epithelial cells (AECs) have a higher frequency of senescence and secrete higher levels of the neutrophil-attracting chemokines CXCL1 and CXCL2 during influenza infection. These chemokines are required for age-enhanced neutrophil chemotaxis in vitro . Our work suggests that aging increases mortality from influenza in part because senescent AECs secrete more chemokines, leading to excessive neutrophil recruitment. Therapies that mitigate this pathological immune response in the elderly might improve outcomes of influenza and other respiratory infections.
Neutrophils clear viruses, but excessive neutrophil responses induce tissue injury and worsen disease. Aging increases mortality to influenza infection; however, whether this is due to impaired viral clearance or a pathological host immune response is unknown. Here we show that aged mice have higher levels of lung neutrophils than younger mice after influenza viral infection. Depleting neutrophils after, but not before, infection substantially improves the survival of aged mice without altering viral clearance. Aged alveolar epithelial cells (AECs) have a higher frequency of senescence and secrete higher levels of the neutrophil-attracting chemokines CXCL1 and CXCL2 during influenza infection. These chemokines are required for age-enhanced neutrophil chemotaxis in vitro. Our work suggests that aging increases mortality from influenza in part because senescent AECs secrete more chemokines, leading to excessive neutrophil recruitment. Therapies that mitigate this pathological immune response in the elderly might improve outcomes of influenza and other respiratory infections.
Author Deng, Jane C.
Wood, Sherri C.
Kulkarni, Upasana
Smith, Candice A.
Goldstein, Daniel R.
Zemans, Rachel L.
AuthorAffiliation 2 Institute of Gerontology, University of Michigan
1 Department of Internal Medicine, University of Michigan
3 Department of Microbiology and Immunology, University of Michigan
AuthorAffiliation_xml – name: 1 Department of Internal Medicine, University of Michigan
– name: 2 Institute of Gerontology, University of Michigan
– name: 3 Department of Microbiology and Immunology, University of Michigan
Author_xml – sequence: 1
  givenname: Upasana
  surname: Kulkarni
  fullname: Kulkarni, Upasana
  organization: Department of Internal Medicine, University of Michigan
– sequence: 2
  givenname: Rachel L.
  surname: Zemans
  fullname: Zemans, Rachel L.
  organization: Department of Internal Medicine, University of Michigan
– sequence: 3
  givenname: Candice A.
  surname: Smith
  fullname: Smith, Candice A.
  organization: Department of Internal Medicine, University of Michigan
– sequence: 4
  givenname: Sherri C.
  surname: Wood
  fullname: Wood, Sherri C.
  organization: Department of Internal Medicine, University of Michigan
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  surname: Goldstein
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  email: drgoldst@umich.edu
  organization: Department of Internal Medicine, University of Michigan, Institute of Gerontology, University of Michigan, Department of Microbiology and Immunology, University of Michigan
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30617300$$D View this record in MEDLINE/PubMed
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U.K. and D.R.G. conceived and designed the experiments. U.K. performed the experiments with the help of C.S. and S.W. Data analysis was done by U.K. D.R.G wrote the first draft of the paper that was then edited by U.K. All authors subsequently contributed in writing and carefully reviewing the experiments and the manuscript.
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Snippet Neutrophils clear viruses, but excessive neutrophil responses induce tissue injury and worsen disease. Aging increases mortality to influenza infection;...
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proquest
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pubmed
springer
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StartPage 545
SubjectTerms Aging
Aging - physiology
Allergology
Alveoli
Animals
Antibodies
Biomedical and Life Sciences
Biomedicine
Cell Count
Cellular Senescence
Chemokine CXCL1 - metabolism
Chemokine CXCL2 - metabolism
Chemokines
Chemotaxis
Epithelial cells
Epithelial Cells - physiology
Epithelial Cells - virology
Gastroenterology
Geriatrics
Humans
Immune clearance
Immune response
Immunology
Infections
Influenza
Influenza, Human - immunology
Influenza, Human - mortality
Leukocytes (neutrophilic)
Lung - pathology
Mice
Mice, Inbred C57BL
Mortality
Neutrophils
Neutrophils - immunology
Neutrophils - virology
Senescence
Survival Analysis
Viral infections
Title Excessive neutrophil levels in the lung underlie the age-associated increase in influenza mortality
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https://search.proquest.com/docview/2165059271
https://pubmed.ncbi.nlm.nih.gov/PMC6375784
Volume 12
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