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Exercise reduces inflammatory cell production and cardiovascular inflammation via instruction of hematopoietic progenitor cells
Open accessAbstract
A sedentary lifestyle, chronic inflammation and leukocytosis increase atherosclerosis; however, it remains unclear whether regular physical activity influences leukocyte production. Here we show that voluntary running decreases hematopoietic activity in mice. Exercise protects mice and humans with atherosclerosis from chronic leukocytosis but does not compromise emergency hematopoiesis in mice. Mechanistically, exercise diminishes leptin production in adipose tissue, augmenting quiescence-promoting hematopoietic niche factors in leptin-receptor-positive stromal bone marrow cells. Induced deletion of the leptin receptor in Prrx1-creER T2; Lepr fl/fl mice reveals that leptin's effect on bone marrow niche cells regulates hematopoietic stem and progenitor cell (HSPC) proliferation and leukocyte production, as well as cardiovascular inflammation and outcomes. Whereas running wheel withdrawal quickly reverses leptin levels, the impact of exercise on leukocyte production and on the HSPC epigenome and transcriptome persists for several weeks. Together, these data show that physical activity alters HSPCs via modulation of their niche, reducing hematopoietic output of inflammatory leukocytes.
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Metadata
- Authors
- Frodermann, V., Rohde, D., Courties, G., Severe, N., Schloss, M. J., Amatullah, H., McAlpine, C. S., Cremer, S., Hoyer, F. F., Ji, F., van Koeverden, I. D., Herisson, F., Honold, L., Masson, G. S., Zhang, S., Grune, J., Iwamoto, Y., Schmidt, S. P., Wojtkiewicz, G. R., Lee, I.-H., Gustafsson, K., Pasterkamp, G., de Jager, S. C. A., Sadreyev, R. I., MacFadyen, J., Libby, P., Ridker, P., Scadden, D. T., Naxerova, K., Jeffrey, K. L., Swirski, F. K., & Nahrendorf, M.
- Affiliations
- Harvard University (US)
- University Medical Center Utrecht (NL)
- Brigham and Women's Hospital (US)
- Corresponding author
- Nahrendorf, Matthias
- ORCID
- Frodermann, Vanessa
- Rohde, David
- Courties, Gabriel
- Schloss, Maximilian J.
- Amatullah, Hajera
- McAlpine, Cameron S.
- Cremer, Sebastian
- Hoyer, Friedrich F.
- Ji, Fei
- Zhang, Shuang
- Grune, Jana
- Iwamoto, Yoshiko
- Wojtkiewicz, Gregory R.
- Lee, I-Hsiu
- Gustafsson, Karin
- Pasterkamp, Gerard
- de Jager, Saskia C. A.
- Sadreyev, Ruslan I.
- Libby, Peter
- Ridker, Paul
- Scadden, David T.
- Naxerova, Kamila
- Jeffrey, Kate L.
- Nahrendorf, Matthias
- Venue
- Nature Medicine
- Published
- 2019-11
- Volume
- 25
- Issue
- 11
- Pages
- 1761-1771
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC6858591
- OpenAlex
- W2982848656
- Cited by
- 292
- References
- 79
- Citations by year
- 2026: 39 · 2025: 51 · 2024: 42 · 2023: 32 · 2022: 51 · 2021: 47 · 2020: 26 · 2019: 3
- FWCI
- 22.44
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Utrecht University Repository (Utrecht University) (submittedVersion)
- Funders
- U.S. Department of Health & Human Services | NIH | National Heart, Lung, and Blood Institute (HL139598)
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Health Sciences › Medicine › Physiology (medical) › Exercise and Physiological Responses
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- physical activity, voluntary running, hematopoietic stem and progenitor cells, leukocytosis, atherosclerosis, cardiovascular inflammation, leptin, leptin receptor, bone marrow microenvironment, adipose tissue, emergency hematopoiesis, PRRX1, epigenome, transcriptome
- MeSH terms
- Epigenome, Adipose Tissue, Animals, Cardiovascular Diseases, Hematopoiesis, Hematopoietic Stem Cells, Humans, Inflammation, Leukocytes, Leukocytosis, Physical Conditioning, Animal, Exercise, Homeodomain Proteins, Atherosclerosis, Mice, Receptors, Leptin, Sedentary Behavior, Transcriptome
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