Cargando…

Macrophage PPAR-γ suppresses long-term lung fibrotic sequelae following acute influenza infection

Influenza virus causes a heterogeneous respiratory infectious disease ranging from self-limiting symptoms to non-resolving pathology in the lungs. Worldwide, seasonal influenza infections claim ~500,000 lives annually. Recent reports describe pathologic pulmonary sequelae that result in remodeling t...

Descripción completa

Detalles Bibliográficos
Autores principales: Huang, Su, Goplen, Nick P., Zhu, Bibo, Cheon, In Su, Son, Youngmin, Wang, Zheng, Li, Chaofan, Dai, Qigang, Jiang, Li, Xiang, Min, Carmona, Eva M., Vassallo, Robert, Limper, Andrew H., Sun, Jie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6777801/
https://www.ncbi.nlm.nih.gov/pubmed/31584978
http://dx.doi.org/10.1371/journal.pone.0223430
_version_ 1783456671416188928
author Huang, Su
Goplen, Nick P.
Zhu, Bibo
Cheon, In Su
Son, Youngmin
Wang, Zheng
Li, Chaofan
Dai, Qigang
Jiang, Li
Xiang, Min
Carmona, Eva M.
Vassallo, Robert
Limper, Andrew H.
Sun, Jie
author_facet Huang, Su
Goplen, Nick P.
Zhu, Bibo
Cheon, In Su
Son, Youngmin
Wang, Zheng
Li, Chaofan
Dai, Qigang
Jiang, Li
Xiang, Min
Carmona, Eva M.
Vassallo, Robert
Limper, Andrew H.
Sun, Jie
author_sort Huang, Su
collection PubMed
description Influenza virus causes a heterogeneous respiratory infectious disease ranging from self-limiting symptoms to non-resolving pathology in the lungs. Worldwide, seasonal influenza infections claim ~500,000 lives annually. Recent reports describe pathologic pulmonary sequelae that result in remodeling the architecture of lung parenchyma following respiratory infections. These dysfunctional recovery processes that disproportionately impact the elderly have been understudied. Macrophages are involved in tissue remodeling and are critical for survival of severe influenza infection. Here, we found intrinsic deficiency of the nuclear receptor PPAR-γ in myeloid cells delayed the resolution of pulmonary inflammation following influenza infection. Mice with myeloid cell-specific PPAR-γ deficiency subsequently presented with increased influenza-induced deposition of pulmonary collagen compared to control mice. This dysfunctional lung remodeling was progressive and sustained for at least 3 months following infection of mice with myeloid PPAR-γ deficiency. These progressive changes were accompanied by a pro-fibrotic gene signature from lung macrophages and preceded by deficiencies in activation of genes involved with damage repair. Importantly similar aberrant gene expression patterns were also found in a secondary analysis of a study where macrophages were isolated from patients with fibrotic interstitial lung disease. Quite unexpectedly, mice with PPAR-γ deficient macrophages were more resistant to bleomycin-induced weight loss whereas extracellular matrix deposition was unaffected compared to controls. Therefore PPAR-γ expression in macrophages may be a pathogen-specific limiter of organ recovery rather than a ubiquitous effector pathway in response to generic damage.
format Online
Article
Text
id pubmed-6777801
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-67778012019-10-13 Macrophage PPAR-γ suppresses long-term lung fibrotic sequelae following acute influenza infection Huang, Su Goplen, Nick P. Zhu, Bibo Cheon, In Su Son, Youngmin Wang, Zheng Li, Chaofan Dai, Qigang Jiang, Li Xiang, Min Carmona, Eva M. Vassallo, Robert Limper, Andrew H. Sun, Jie PLoS One Research Article Influenza virus causes a heterogeneous respiratory infectious disease ranging from self-limiting symptoms to non-resolving pathology in the lungs. Worldwide, seasonal influenza infections claim ~500,000 lives annually. Recent reports describe pathologic pulmonary sequelae that result in remodeling the architecture of lung parenchyma following respiratory infections. These dysfunctional recovery processes that disproportionately impact the elderly have been understudied. Macrophages are involved in tissue remodeling and are critical for survival of severe influenza infection. Here, we found intrinsic deficiency of the nuclear receptor PPAR-γ in myeloid cells delayed the resolution of pulmonary inflammation following influenza infection. Mice with myeloid cell-specific PPAR-γ deficiency subsequently presented with increased influenza-induced deposition of pulmonary collagen compared to control mice. This dysfunctional lung remodeling was progressive and sustained for at least 3 months following infection of mice with myeloid PPAR-γ deficiency. These progressive changes were accompanied by a pro-fibrotic gene signature from lung macrophages and preceded by deficiencies in activation of genes involved with damage repair. Importantly similar aberrant gene expression patterns were also found in a secondary analysis of a study where macrophages were isolated from patients with fibrotic interstitial lung disease. Quite unexpectedly, mice with PPAR-γ deficient macrophages were more resistant to bleomycin-induced weight loss whereas extracellular matrix deposition was unaffected compared to controls. Therefore PPAR-γ expression in macrophages may be a pathogen-specific limiter of organ recovery rather than a ubiquitous effector pathway in response to generic damage. Public Library of Science 2019-10-04 /pmc/articles/PMC6777801/ /pubmed/31584978 http://dx.doi.org/10.1371/journal.pone.0223430 Text en © 2019 Huang et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Huang, Su
Goplen, Nick P.
Zhu, Bibo
Cheon, In Su
Son, Youngmin
Wang, Zheng
Li, Chaofan
Dai, Qigang
Jiang, Li
Xiang, Min
Carmona, Eva M.
Vassallo, Robert
Limper, Andrew H.
Sun, Jie
Macrophage PPAR-γ suppresses long-term lung fibrotic sequelae following acute influenza infection
title Macrophage PPAR-γ suppresses long-term lung fibrotic sequelae following acute influenza infection
title_full Macrophage PPAR-γ suppresses long-term lung fibrotic sequelae following acute influenza infection
title_fullStr Macrophage PPAR-γ suppresses long-term lung fibrotic sequelae following acute influenza infection
title_full_unstemmed Macrophage PPAR-γ suppresses long-term lung fibrotic sequelae following acute influenza infection
title_short Macrophage PPAR-γ suppresses long-term lung fibrotic sequelae following acute influenza infection
title_sort macrophage ppar-γ suppresses long-term lung fibrotic sequelae following acute influenza infection
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6777801/
https://www.ncbi.nlm.nih.gov/pubmed/31584978
http://dx.doi.org/10.1371/journal.pone.0223430
work_keys_str_mv AT huangsu macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT goplennickp macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT zhubibo macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT cheoninsu macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT sonyoungmin macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT wangzheng macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT lichaofan macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT daiqigang macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT jiangli macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT xiangmin macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT carmonaevam macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT vassallorobert macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT limperandrewh macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection
AT sunjie macrophageppargsuppresseslongtermlungfibroticsequelaefollowingacuteinfluenzainfection