Progesterone-Based Therapy Protects Against Influenza by Promoting Lung Repair and Recovery in Females

Over 100 million women use progesterone therapies worldwide. Despite having immunomodulatory and repair properties, their effects on the outcome of viral diseases outside of the reproductive tract have not been evaluated. Administration of exogenous progesterone (at concentrations that mimic the lut...

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Published inPLoS pathogens Vol. 12; no. 9; p. e1005840
Main Authors Hall, Olivia J., Limjunyawong, Nathachit, Vermillion, Meghan S., Robinson, Dionne P., Wohlgemuth, Nicholas, Pekosz, Andrew, Mitzner, Wayne, Klein, Sabra L.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.09.2016
Public Library of Science (PLoS)
Subjects
Amphiregulin - genetics
Amphiregulin - immunology
Animals
Antigens, CD - genetics
Antigens, CD - immunology
Apyrase - genetics
Apyrase - immunology
Biology and life sciences
Birth control
Care and treatment
Cytokines - genetics
Cytokines - immunology
Dosage and administration
Drug therapy
Environmental health
Epidermal growth factor
Female
Females
Funding
Health sciences
Immunology
Infections
Influenza
Influenza A virus
Influenza A virus - immunology
Lung
Lung - immunology
Lung - pathology
Lungs
Management
Maternal mortality
Medicine and health sciences
Mice
Mice, Knockout
Multivariate analysis
Orthomyxoviridae
Orthomyxoviridae Infections - genetics
Orthomyxoviridae Infections - immunology
Orthomyxoviridae Infections - pathology
Progesterone
Public health
Respiratory function
Rodents
Th17 Cells - immunology
Th17 Cells - pathology
Variance analysis
Viral diseases
Women's health
Womens health
United States > US
Maryland
Baltimore Maryland
Online AccessGet full text

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Abstract Over 100 million women use progesterone therapies worldwide. Despite having immunomodulatory and repair properties, their effects on the outcome of viral diseases outside of the reproductive tract have not been evaluated. Administration of exogenous progesterone (at concentrations that mimic the luteal phase) to progesterone-depleted adult female mice conferred protection from both lethal and sublethal influenza A virus (IAV) infection. Progesterone treatment altered the inflammatory environment of the lungs, but had no effects on viral load. Progesterone treatment promoted faster recovery by increasing TGF-β, IL-6, IL-22, numbers of regulatory Th17 cells expressing CD39, and cellular proliferation, reducing protein leakage into the airway, improving pulmonary function, and upregulating the epidermal growth factor amphiregulin (AREG) in the lungs. Administration of rAREG to progesterone-depleted females promoted pulmonary repair and improved the outcome of IAV infection. Progesterone-treatment of AREG-deficient females could not restore protection, indicating that progesterone-mediated induction of AREG caused repair in the lungs and accelerated recovery from IAV infection. Repair and production of AREG by damaged respiratory epithelial cell cultures in vitro was increased by progesterone. Our results illustrate that progesterone is a critical host factor mediating production of AREG by epithelial cells and pulmonary tissue repair following infection, which has important implications for women's health.
AbstractList   Over 100 million women use progesterone therapies worldwide. Despite having immunomodulatory and repair properties, their effects on the outcome of viral diseases outside of the reproductive tract have not been evaluated. Administration of exogenous progesterone (at concentrations that mimic the luteal phase) to progesterone-depleted adult female mice conferred protection from both lethal and sublethal influenza A virus (IAV) infection. Progesterone treatment altered the inflammatory environment of the lungs, but had no effects on viral load. Progesterone treatment promoted faster recovery by increasing TGF-[Beta], IL-6, IL-22, numbers of regulatory Th17 cells expressing CD39, and cellular proliferation, reducing protein leakage into the airway, improving pulmonary function, and upregulating the epidermal growth factor amphiregulin (AREG) in the lungs. Administration of rAREG to progesterone-depleted females promoted pulmonary repair and improved the outcome of IAV infection. Progesterone-treatment of AREG-deficient females could not restore protection, indicating that progesterone-mediated induction of AREG caused repair in the lungs and accelerated recovery from IAV infection. Repair and production of AREG by damaged respiratory epithelial cell cultures in vitro was increased by progesterone. Our results illustrate that progesterone is a critical host factor mediating production of AREG by epithelial cells and pulmonary tissue repair following infection, which has important implications for women's health.
Over 100 million women use progesterone therapies worldwide. Despite having immunomodulatory and repair properties, their effects on the outcome of viral diseases outside of the reproductive tract have not been evaluated. Administration of exogenous progesterone (at concentrations that mimic the luteal phase) to progesterone-depleted adult female mice conferred protection from both lethal and sublethal influenza A virus (IAV) infection. Progesterone treatment altered the inflammatory environment of the lungs, but had no effects on viral load. Progesterone treatment promoted faster recovery by increasing TGF-β, IL-6, IL-22, numbers of regulatory Th17 cells expressing CD39, and cellular proliferation, reducing protein leakage into the airway, improving pulmonary function, and upregulating the epidermal growth factor amphiregulin (AREG) in the lungs. Administration of rAREG to progesterone-depleted females promoted pulmonary repair and improved the outcome of IAV infection. Progesterone-treatment of AREG-deficient females could not restore protection, indicating that progesterone-mediated induction of AREG caused repair in the lungs and accelerated recovery from IAV infection. Repair and production of AREG by damaged respiratory epithelial cell cultures in vitro was increased by progesterone. Our results illustrate that progesterone is a critical host factor mediating production of AREG by epithelial cells and pulmonary tissue repair following infection, which has important implications for women’s health. Worldwide, the use of hormonal contraceptives is on the rise as a primary intervention for improving women’s health outcomes through reduced maternal mortality and increased childhood survival. There are many hormone contraceptive formulations, all of which contain some form of progesterone. Although the effects of hormone contraceptives and progesterone, specifically, have been evaluated in the context of infections of the reproductive tract, the effects of progesterone at other mucosal sites, including the respiratory tract have not been systematically evaluated. We have made the novel observation that administration of progesterone to female mice depleted of progesterone confers protection against both lethal and sublethal influenza A virus infection. In particular, progesterone reduces pulmonary inflammation, improves lung function, repairs the damaged lung epithelium, and promotes faster recovery following influenza A virus infection. Progesterone causes protection against severe outcome from influenza by inducing production of the epidermal growth factor, amphiregulin, by respiratory epithelial cells. This study provides insight into a novel mechanistic role of progesterone in the lungs and illustrates that sex hormone exposure, including through the use of hormonal contraceptives, has significant health effects beyond the reproductive tract.
Over 100 million women use progesterone therapies worldwide. Despite having immunomodulatory and repair properties, their effects on the outcome of viral diseases outside of the reproductive tract have not been evaluated. Administration of exogenous progesterone (at concentrations that mimic the luteal phase) to progesterone-depleted adult female mice conferred protection from both lethal and sublethal influenza A virus (IAV) infection. Progesterone treatment altered the inflammatory environment of the lungs, but had no effects on viral load. Progesterone treatment promoted faster recovery by increasing TGF-β, IL-6, IL-22, numbers of regulatory Th17 cells expressing CD39, and cellular proliferation, reducing protein leakage into the airway, improving pulmonary function, and upregulating the epidermal growth factor amphiregulin (AREG) in the lungs. Administration of rAREG to progesterone-depleted females promoted pulmonary repair and improved the outcome of IAV infection. Progesterone-treatment of AREG-deficient females could not restore protection, indicating that progesterone-mediated induction of AREG caused repair in the lungs and accelerated recovery from IAV infection. Repair and production of AREG by damaged respiratory epithelial cell cultures in vitro was increased by progesterone. Our results illustrate that progesterone is a critical host factor mediating production of AREG by epithelial cells and pulmonary tissue repair following infection, which has important implications for women's health.Over 100 million women use progesterone therapies worldwide. Despite having immunomodulatory and repair properties, their effects on the outcome of viral diseases outside of the reproductive tract have not been evaluated. Administration of exogenous progesterone (at concentrations that mimic the luteal phase) to progesterone-depleted adult female mice conferred protection from both lethal and sublethal influenza A virus (IAV) infection. Progesterone treatment altered the inflammatory environment of the lungs, but had no effects on viral load. Progesterone treatment promoted faster recovery by increasing TGF-β, IL-6, IL-22, numbers of regulatory Th17 cells expressing CD39, and cellular proliferation, reducing protein leakage into the airway, improving pulmonary function, and upregulating the epidermal growth factor amphiregulin (AREG) in the lungs. Administration of rAREG to progesterone-depleted females promoted pulmonary repair and improved the outcome of IAV infection. Progesterone-treatment of AREG-deficient females could not restore protection, indicating that progesterone-mediated induction of AREG caused repair in the lungs and accelerated recovery from IAV infection. Repair and production of AREG by damaged respiratory epithelial cell cultures in vitro was increased by progesterone. Our results illustrate that progesterone is a critical host factor mediating production of AREG by epithelial cells and pulmonary tissue repair following infection, which has important implications for women's health.
Over 100 million women use progesterone therapies worldwide. Despite having immunomodulatory and repair properties, their effects on the outcome of viral diseases outside of the reproductive tract have not been evaluated. Administration of exogenous progesterone (at concentrations that mimic the luteal phase) to progesterone-depleted adult female mice conferred protection from both lethal and sublethal influenza A virus (IAV) infection. Progesterone treatment altered the inflammatory environment of the lungs, but had no effects on viral load. Progesterone treatment promoted faster recovery by increasing TGF-β, IL-6, IL-22, numbers of regulatory Th17 cells expressing CD39, and cellular proliferation, reducing protein leakage into the airway, improving pulmonary function, and upregulating the epidermal growth factor amphiregulin (AREG) in the lungs. Administration of rAREG to progesterone-depleted females promoted pulmonary repair and improved the outcome of IAV infection. Progesterone-treatment of AREG-deficient females could not restore protection, indicating that progesterone-mediated induction of AREG caused repair in the lungs and accelerated recovery from IAV infection. Repair and production of AREG by damaged respiratory epithelial cell cultures in vitro was increased by progesterone. Our results illustrate that progesterone is a critical host factor mediating production of AREG by epithelial cells and pulmonary tissue repair following infection, which has important implications for women's health.
Over 100 million women use progesterone therapies worldwide. Despite having immunomodulatory and repair properties, their effects on the outcome of viral diseases outside of the reproductive tract have not been evaluated. Administration of exogenous progesterone (at concentrations that mimic the luteal phase) to progesterone-depleted adult female mice conferred protection from both lethal and sublethal influenza A virus (IAV) infection. Progesterone treatment altered the inflammatory environment of the lungs, but had no effects on viral load. Progesterone treatment promoted faster recovery by increasing TGF-[beta], IL-6, IL-22, numbers of regulatory Th17 cells expressing CD39, and cellular proliferation, reducing protein leakage into the airway, improving pulmonary function, and upregulating the epidermal growth factor amphiregulin (AREG) in the lungs. Administration of rAREG to progesterone-depleted females promoted pulmonary repair and improved the outcome of IAV infection. Progesterone-treatment of AREG-deficient females could not restore protection, indicating that progesterone-mediated induction of AREG caused repair in the lungs and accelerated recovery from IAV infection. Repair and production of AREG by damaged respiratory epithelial cell cultures in vitro was increased by progesterone. Our results illustrate that progesterone is a critical host factor mediating production of AREG by epithelial cells and pulmonary tissue repair following infection, which has important implications for women's health.
Audience Academic
Author Vermillion, Meghan S.
Limjunyawong, Nathachit
Mitzner, Wayne
Hall, Olivia J.
Wohlgemuth, Nicholas
Pekosz, Andrew
Klein, Sabra L.
Robinson, Dionne P.
AuthorAffiliation 2 Department of Environmental Health Sciences, The Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America
3 Department of Molecular and Comparative Pathobiology, The Johns Hopkins University School of Medicine, Baltimore, Maryland, United States of America
St. Jude Children’s Research Hospital, UNITED STATES
4 Department of Biochemistry and Molecular Biology, The Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America
1 W. Harry Feinstone Department of Molecular Microbiology and Immunology, The Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America
AuthorAffiliation_xml – name: 3 Department of Molecular and Comparative Pathobiology, The Johns Hopkins University School of Medicine, Baltimore, Maryland, United States of America
– name: 2 Department of Environmental Health Sciences, The Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America
– name: 4 Department of Biochemistry and Molecular Biology, The Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America
– name: 1 W. Harry Feinstone Department of Molecular Microbiology and Immunology, The Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America
– name: St. Jude Children’s Research Hospital, UNITED STATES
Author_xml – sequence: 1
  givenname: Olivia J.
  orcidid: 0000-0002-1981-3162
  surname: Hall
  fullname: Hall, Olivia J.
– sequence: 2
  givenname: Nathachit
  orcidid: 0000-0002-9540-6171
  surname: Limjunyawong
  fullname: Limjunyawong, Nathachit
– sequence: 3
  givenname: Meghan S.
  surname: Vermillion
  fullname: Vermillion, Meghan S.
– sequence: 4
  givenname: Dionne P.
  surname: Robinson
  fullname: Robinson, Dionne P.
– sequence: 5
  givenname: Nicholas
  orcidid: 0000-0002-6450-6452
  surname: Wohlgemuth
  fullname: Wohlgemuth, Nicholas
– sequence: 6
  givenname: Andrew
  surname: Pekosz
  fullname: Pekosz, Andrew
– sequence: 7
  givenname: Wayne
  surname: Mitzner
  fullname: Mitzner, Wayne
– sequence: 8
  givenname: Sabra L.
  orcidid: 0000-0002-0730-5224
  surname: Klein
  fullname: Klein, Sabra L.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/27631986$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2016 Public Library of Science
2016 Public Library of Science. 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: Hall OJ, Limjunyawong N, Vermillion MS, Robinson DP, Wohlgemuth N, Pekosz A, et al. (2016) Progesterone-Based Therapy Protects Against Influenza by Promoting Lung Repair and Recovery in Females. PLoS Pathog 12(9): e1005840. doi:10.1371/journal.ppat.1005840
2016 Hall et al 2016 Hall et al
2016 Public Library of Science. 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: Hall OJ, Limjunyawong N, Vermillion MS, Robinson DP, Wohlgemuth N, Pekosz A, et al. (2016) Progesterone-Based Therapy Protects Against Influenza by Promoting Lung Repair and Recovery in Females. PLoS Pathog 12(9): e1005840. doi:10.1371/journal.ppat.1005840
Copyright_xml – notice: COPYRIGHT 2016 Public Library of Science
– notice: 2016 Public Library of Science. 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: Hall OJ, Limjunyawong N, Vermillion MS, Robinson DP, Wohlgemuth N, Pekosz A, et al. (2016) Progesterone-Based Therapy Protects Against Influenza by Promoting Lung Repair and Recovery in Females. PLoS Pathog 12(9): e1005840. doi:10.1371/journal.ppat.1005840
– notice: 2016 Hall et al 2016 Hall et al
– notice: 2016 Public Library of Science. 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: Hall OJ, Limjunyawong N, Vermillion MS, Robinson DP, Wohlgemuth N, Pekosz A, et al. (2016) Progesterone-Based Therapy Protects Against Influenza by Promoting Lung Repair and Recovery in Females. PLoS Pathog 12(9): e1005840. doi:10.1371/journal.ppat.1005840
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DocumentTitleAlternate Progesterone and Influenza Pathogenesis
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Current address: Nathachit Limjunyawong, The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins School of Medicine, Baltimore, MD, USA
Current address: Dionne P. Robinson, Laboratory of Parasitic Diseases, National Institutes of Health, NIAID, Bethesda, MD, USA
Conceptualization: OJH SLK. Formal analysis: OJH NL MSV. Funding acquisition: AP SLK. Investigation: OJH NL MSV DPR NW. Methodology: AP WM SLK. Project administration: SLK. Resources: AP WM SLK. Supervision: AP WM SLK. Validation: OJH NL MSV DPR NW. Visualization: OJH MSV. Writing – original draft: OJH SLK. Writing – review & editing: OJH NL MSV DPR NW AP WM SLK.
The authors have declared that no competing interests exist.
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Snippet Over 100 million women use progesterone therapies worldwide. Despite having immunomodulatory and repair properties, their effects on the outcome of viral...
  Over 100 million women use progesterone therapies worldwide. Despite having immunomodulatory and repair properties, their effects on the outcome of viral...
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SubjectTerms Amphiregulin - genetics
Amphiregulin - immunology
Animals
Antigens, CD - genetics
Antigens, CD - immunology
Apyrase - genetics
Apyrase - immunology
Biology and life sciences
Birth control
Care and treatment
Cytokines - genetics
Cytokines - immunology
Dosage and administration
Drug therapy
Environmental health
Epidermal growth factor
Female
Females
Funding
Health sciences
Immunology
Infections
Influenza
Influenza A virus
Influenza A virus - immunology
Lung
Lung - immunology
Lung - pathology
Lungs
Management
Maternal mortality
Medicine and health sciences
Mice
Mice, Knockout
Multivariate analysis
Orthomyxoviridae
Orthomyxoviridae Infections - genetics
Orthomyxoviridae Infections - immunology
Orthomyxoviridae Infections - pathology
Progesterone
Public health
Respiratory function
Rodents
Th17 Cells - immunology
Th17 Cells - pathology
Variance analysis
Viral diseases
Women's health
Womens health
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Title Progesterone-Based Therapy Protects Against Influenza by Promoting Lung Repair and Recovery in Females
URI https://www.ncbi.nlm.nih.gov/pubmed/27631986
https://www.proquest.com/docview/1829442750
https://www.proquest.com/docview/1820596263
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https://pubmed.ncbi.nlm.nih.gov/PMC5025002
https://doaj.org/article/af5cdebd38934977926f096f77f2a58b
http://dx.doi.org/10.1371/journal.ppat.1005840
Volume 12
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