Age-related decline of interferon-gamma responses in macrophage impairs satellite cell proliferation and regeneration
Open accessAbstract
Background Impaired muscle regeneration and increased muscle fibrosis are observed in aged muscle accompanied by progressive loss of muscle mass (sarcopenia). However, the underlying mechanism is still unclear. Methods The differentiated expressed genes in young and aged muscles after acute injury by cardiotoxin were identified by RNA‐sequence analysis. Single‐cell RNA‐sequence analysis was used to identify cell clusters and functions in young muscle after acute injury, and flow cytometry analysis and sorting were used to validate the function. The proliferation and differentiation functions of satellite cells were accessed by immunostaining with 5‐ethynyl‐2′‐deoxyuridine and embryonic myosin heavy chain (eMyHC), respectively. Muscle regeneration ability was accessed by histopathological and molecular biological methods. Results Gene expression patterns associated with responses to interferon‐gamma (IFN‐γ) (15 genes; false discovery rate < 0.001) were significantly down‐regulated during muscle regeneration in aged mice (P = 2.25e−7). CD8+ T cells were the main source of increased IFN‐γ after injury, adoptive transfer of wild‐type CD8+ T cells to IFN‐γ‐deficient young mice resulted in 78% increase in cross‐sectional areas (CSAs) of regenerated myofibres (P < 0.05) and 63% decrease in muscle fibrosis (P < 0.05) after injury. Single‐cell RNA‐sequence analysis identified a novel subset of macrophages [named as IFN‐responsive macrophages (IFNRMs)] that specifically expressed IFN‐responsive genes (Ifit3, Isg15, Irf7, etc.) in young mice at 3 days after injury, and the number of this macrophage subset was ~20% lower in aged mice at the same time (P < 0.05). IFNRMs secreted cytokine C‐X‐C motif chemokine 10 (CXCL10) that promoted the proliferation and differentiation of satellite cells via its receptor, CXCR3. Intramuscular recombinant CXCL10 treatment in aged mice rejuvenated the proliferation of satellite cells (80% increase in Ki‐67+Pax7+ cells, P < 0.01) and resulted in 27% increase in CSA of regenerated myofibres (P < 0.01) and 29% decrease in muscle fibrosis (P < 0.05). Conclusions Our study indicates that decline in IFN‐γ response in a novel subset of macrophage contributes to satellite cells dysfunctions in aged skeletal muscles and demonstrates that this mechanism can be targeted to restore age‐associated myogenesis.
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Accumulation of inflammatory macrophages and age-related declines in interferon-gamma signaling delay muscle repair following injury.
“Previous work has shown that the accumulation of inflammatory macrophages and age-related declines in interferon-gamma signaling delay muscle repair following injury”
From Skeletal muscle aging, cellular senescence, and senotherapeutics: current knowledge and future directions (2021) · cites this paper as Zhang et al., 2020
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- Authors
- Zhang, C., Cheng, N., Qiao, B., Zhang, F., Wu, J., Liu, C., Li, Y., & Du, J.
- Affiliations
- Capital Medical University (CN)
- Capital University of Physical Education and Sports (CN)
- Corresponding author
- Du, Jie
- Venue
- Journal of Cachexia Sarcopenia and Muscle
- Publisher
- Wiley
- Published
- 2020-07-29
- Volume
- 11
- Issue
- 5
- Pages
- 1291-1305
- ISSN
- 2190-5991 (ISSN-L)
- 2190-6009
- PMC
- PMC7567146
- OpenAlex
- W3045738499
- Cited by
- 105
- References
- 48
- Citations by year
- 2026: 12 · 2025: 19 · 2024: 23 · 2023: 22 · 2022: 16 · 2021: 11 · 2020: 2
- FWCI
- 4.22
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Journal of Cachexia Sarcopenia and Muscle (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Natural Science Foundation of China (81601871, 81500265, 81871758, 81430050)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
- Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
- Keywords
- aging, muscle regeneration, sarcopenia, satellite cells, interferon-gamma, macrophages, CD8+ T cells, CXCL10, CXCR3, muscle fibrosis, cardiotoxin injury, single-cell RNA sequencing, adoptive transfer, IFIT3
- MeSH terms
- Aging, Animals, Interferon-gamma, Macrophages, Male, Mice, Inbred C57BL, Regeneration, CD8-Positive T-Lymphocytes, Cell Proliferation, Mice
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