Cited by 177Genetics, Aging, and Longevity in Model OrganismsImmune responses and vaccinationsImmune cells in cancer

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The lung microenvironment shapes a dysfunctional response of alveolar macrophages in aging

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McQuattie-Pimentel, Alexandra C., Ren, Ziyou, Joshi, Nikita, Watanabe, Satoshi, Stoeger, Thomas, Chi, Monica, Lu, Ziyan, Sichizya, Lango, Aillon, Raul Piseaux, Chen, Ching-I, Soberanes, Saul, Chen, Zhangying, Reyfman, Paul A., Walter, James M., Anekalla, Kishore R., Davis, Jennifer M., Helmin, Kathryn A., Runyan, Constance E., Abdala-Valencia, Hiam, Nam, Kiwon, Meliton, Angelo Y., Winter, Deborah R., Morimoto, Richard I., Mutlu, Gökhan M., Bharat, Ankit, Perlman, Harris, Gottardi, Cara J., Ridge, Karen M., Chandel, Navdeep S., Sznajder, Jacob I., Balch, William E., Singer, Benjamin D., Misharin, Alexander V., Budinger, G.R. Scott·2021·Journal of Clinical Investigation

DOI 10.1172/jci140299PMC PMC7919859

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Abstract

Alveolar macrophages orchestrate the response to viral infections. Age-related changes in these cells may underlie the differential severity of pneumonia in older patients. We performed an integrated analysis of single-cell RNA-Seq data that revealed homogenous age-related changes in the alveolar macrophage transcriptome in humans and mice. Using genetic lineage tracing with sequential injury, heterochronic adoptive transfer, and parabiosis, we found that the lung microenvironment drove an age-related resistance of alveolar macrophages to proliferation that persisted during influenza A viral infection. Ligand-receptor pair analysis localized these changes to the extracellular matrix, where hyaluronan was increased in aged animals and altered the proliferative response of bone marrow-derived macrophages to granulocyte macrophage colony-stimulating factor (GM-CSF). Our findings suggest that strategies targeting the aging lung microenvironment will be necessary to restore alveolar macrophage function in aging.

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Authors: McQuattie-Pimentel, A. C., Ren, Z., Joshi, N., Watanabe, S., Stoeger, T., Chi, M., Lu, Z., Sichizya, L., Aillon, R. P., Chen, C.-I., Soberanes, S., Chen, Z., Reyfman, P. A., Walter, J. M., Anekalla, K. R., Davis, J. M., Helmin, K. A., Runyan, C. E., Abdala-Valencia, H., Nam, K., Meliton, A. Y., Winter, D. R., Morimoto, R. I., Mutlu, G. M., Bharat, A., Perlman, H., Gottardi, C. J., Ridge, K. M., Chandel, N. S., Sznajder, J. I., Balch, W. E., Singer, B. D., Misharin, A. V., & Budinger, G. R. S.
Affiliations: Northwestern University (US)
University of Chicago Medical Center (US)
Scripps Research Institute (US)
ORCID: Ren, Ziyou
Joshi, Nikita
Watanabe, Satoshi
Stoeger, Thomas
Lu, Ziyan
Sichizya, Lango
Chen, Ching-I
Soberanes, Saul
Chen, Zhangying
Reyfman, Paul A.
Walter, James M.
Anekalla, Kishore R.
Helmin, Kathryn A.
Runyan, Constance E.
Abdala-Valencia, Hiam
Winter, Deborah R.
Morimoto, Richard I.
Mutlu, Gökhan M.
Bharat, Ankit
Perlman, Harris
Gottardi, Cara J.
Ridge, Karen M.
Chandel, Navdeep S.
Sznajder, Jacob I.
Balch, William E.
Singer, Benjamin D.
Misharin, Alexander V.
Budinger, G.R. Scott
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2021-02-15
Volume: 131
Issue: 4
ISSN: 0021-9738 (ISSN-L)
1558-8238
DOI: 10.1172/jci140299
PMC: PMC7919859
OpenAlex: W3133294399
Cited by: 177
References: 56
Citations by year: 2026: 30 · 2025: 35 · 2024: 31 · 2023: 30 · 2022: 34 · 2021: 17
FWCI: 10.01
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Clinical Investigation (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: NIH (AG490665, HL135124,AG049665,AI135964, HL071643,HL14575)
Veterans Administration (CX01777)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Keywords: alveolar macrophages, lung aging, lung microenvironment, extracellular matrix, hyaluronic acid, macrophage proliferation, influenza A virus infection, GM-CSF signaling, bone marrow-derived macrophages, lineage tracing, parabiosis, single-cell transcriptomics
MeSH terms: RNA-Seq, Aging, Animals, Humans, Lung, Mice, Transgenic, Macrophages, Alveolar, Mice, Cellular Microenvironment

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The lung microenvironment shapes a dysfunctional response of alveolar macrophages in aging

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