p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice
Open accessAbstract
Skeletal muscle aging results in a gradual loss of skeletal muscle mass, skeletal muscle function and regenerative capacity, which can lead to sarcopenia and increased mortality. Although the mechanisms underlying sarcopenia remain unclear, the skeletal muscle stem cell, or satellite cell, is required for muscle regeneration. Therefore, identification of signaling pathways affecting satellite cell function during aging may provide insights into therapeutic targets for combating sarcopenia. Here, we show that a cell-autonomous loss in self-renewal occurs via alterations in fibroblast growth factor receptor-1, p38α and p38β mitogen-activated protein kinase signaling in satellite cells from aged mice. We further demonstrate that pharmacological manipulation of these pathways can ameliorate age-associated self-renewal defects. Thus, our data highlight an age-associated deregulation of a satellite cell homeostatic network and reveal potential therapeutic opportunities for the treatment of progressive muscle wasting.
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Oxidative stress present in the elderly dysregulates typical functions and processes of satellite cells such as proliferation, fibrosis, and differentiation involving Notch, Wnt, p38/MAPK, and JAK-STAT3 signaling pathways.
“In addition, Os present in the elderly dysregulates the typical functions and processes of satellite cells such as proliferation, fibrosis, and differentiation involving Notch, Wnt, p38/MAPK, and the JAK-STAT3 signaling pathways [72, 123–125].”
From The critical role of oxidative stress in sarcopenic obesity (2021) · cites this paper as [124]
In aging, the capacity of MuSCs to repair injured muscle declines markedly.
“With aging, muscle tissue homeostasis is progressively disrupted and the ability of MuSCs to repair injured muscle markedly declines.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [55]
MuSCs from older donors have marked deficits in self-renewal, expansion, and contribution to mature myofiber formation.
“MuSCs from older donors exhibited marked deficits both in self-renewal and expansion and in their contributions to mature myofiber formation, the two hallmarks of stem cell function25,29,55,56.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [55]
Together, these cell-autonomous changes restrict MuSC self-renewal and regenerative capacity.
“Cumulatively, these cell autonomous alterations limit MuSC self-renewal and capacity for regeneration25,29,55,56.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [55]
Inhibiting aberrant intrinsic signaling pathways, including p38α/β MAPK and Jak2-Stat3, can rejuvenate the regenerative capacity of aged and geriatric MuSCs.
“Rejuvenation of the regenerative capacity of aged and geriatric MuSC populations can be achieved by biochemical or genetic inhibition of aberrantly regulated intrinsic MuSC signal transduction pathways, including the p38α/β MAPK, and Jak2–Stat3 signaling axes25,29,55,56.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [55]
With aging, MuSCs shift from quiescence to overactivation marked by persistent p38α/β MAPK activity, eventually causing premature differentiation, senescence, and stem cell exhaustion.
“As a result, in the course of aging, MuSCs shift from a quiescent phenotype to an over-activated phenotype characterized by persistent p38α/β MAPK activity that eventually leads to premature differentiation senescence and stem cell exhaustion25,29,55,56.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [55]
Together, findings show that aging MuSCs progressively accumulate intrinsic changes that impair regenerative function, persist after transplantation into young or aged microenvironments, and are inherited by progeny.
“Together, these findings show that intrinsic changes progressively accumulate in MuSCs during aging, which affect their regenerative function25,29,55,56. Moreover, these changes are not altered by transplantation into a youthful or aged microenvironment and are heritably transmitted from the stem cells to their progeny29,56.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [55]
Studies show that MuSCs from 18-22-month-old mice have intrinsic defects that appear before the MuSC number depletion seen in geriatric mice.
“Several studies of MuSC function in muscle regeneration following injury indicate that MuSCs from aged mice (18–22 months) have stem cell–intrinsic defects25,29,55,56 (Fig. 3) that accrue before the depletion of MuSC numbers evident in geriatric mice13,56,72.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [55]
Macrophages drive a pro-inflammatory phase secreting IL-6, TNF-α, and IFN-γ that promotes myogenic proliferation, then an anti-inflammatory phase secreting TGF-β, IGF-1, and IL-10 that supports myogenic differentiation.
“The macrophages induce a pro-inflammatory phase that in muscle entails secretion of cytokines such as IL-6, TNF-α and IFN-γ, which promote myogenic cell proliferation. This phase is followed by an anti-inflammatory phase during which macrophages secrete TGF-β, IGF-1 and IL-10, which facilitate myogenic differentiation55,67,68.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [55]
Par3 complex mediates asymmetric segregation of MuSCs with active/inactive p38α/β MAPK, yielding committed and uncommitted daughter cells.
“The Par3 complex mediates asymmetric segregation of MuSCs with active (phosphorylated) and inactive p38α/β MAPK, which yields committed and uncommitted daughter cells55,58.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [55]
Aging-related perturbations in FGFR-p38 signaling disrupt asymmetric division, increasing symmetrically committed cells.
“Perturbations in the FGFR–p38 signaling axis that arise in aging disrupt this asymmetric division mechanism, leading to an increase in symmetrically committed cells55.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [55]
Aged or geriatric MuSCs serially transplanted into young recipients have potent regenerative capacity, whereas rejuvenated MuSCs transplanted into aged or geriatric mice are impaired.
“aged or geriatric MuSCs serially transplanted into young recipients have potent regenerative capacity, whereas rejuvenated MuSCs transplanted into aged or geriatric mice are impaired25,27,29,55,56.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [55]
Blocking p38 MAPK signaling in resident muscle stem cells can bring back muscle regeneration in old mice.
“For example, recent studies of aged muscle stem cells have shown that inhibition of the p38 mitogen-activated protein kinase signaling pathway in endogenous muscle stem cells can restore muscle regenerative potential in aged mice142 and can be combined with ex vivo culture on soft hydrogels to enhance the transplantation efficacy of these cells140.”
From Stem cell aging: mechanisms, regulators and therapeutic opportunities (2014) · cites this paper as [142]
Age-related decline in regenerative potential has been attributed to differences in cell signaling and proliferative history.
“Age-related decline in regenerative potential has been attributed to differences in cell signaling (Bernet et al., 2014; Brack et al., 2007; Conboy et al., 2003; Cosgrove et al., 2014) and proliferative history (Chakkalakal et al., 2012).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as Bernet et al., 2014
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- Authors
- Bernet, J. D., Doles, J. D., Hall, J. K., Kelly Tanaka, K., Carter, T. A., & Olwin, B. B.
- Affiliations
- University of Colorado Boulder (US)
- Corresponding author
- Olwin, Bradley B
- Venue
- Nature Medicine
- Published
- 2014-02-16
- Volume
- 20
- Issue
- 3
- Pages
- 265-271
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC4070883
- OpenAlex
- W2059165104
- Cited by
- 573
- References
- 49
- Citations by year
- 2026: 36 · 2025: 32 · 2024: 36 · 2023: 40 · 2022: 38 · 2021: 58 · 2020: 58 · 2019: 44 · 2018: 58 · 2017: 44 · 2016: 59 · 2015: 46 · 2014: 23 · 2013: 1
- FWCI
- 23.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (AG040074, R01AG040074)
- National Institute of General Medical Sciences (T32GM007135)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR49446, R01AR049446)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- p38 MAPK signaling, skeletal muscle aging, age-related sarcopenia, satellite cells, muscle stem cells, stem cell self-renewal, FGF receptor 1, p38α, p38β, muscle regeneration
- MeSH terms
- Aging, Animals, Environment, Female, Flow Cytometry, Ligands, Mice, Inbred C57BL, Mice, Inbred DBA, Phenotype, Stem Cells, Time Factors, Signal Transduction, Gene Expression Regulation, Enzymologic, Fibroblast Growth Factor 1, Cell Transplantation, Muscle, Skeletal, Oligonucleotide Array Sequence Analysis, Satellite Cells, Skeletal Muscle, Mitogen-Activated Protein Kinase 11, Mitogen-Activated Protein Kinase 14, Cell Proliferation, Mice
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