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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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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