Rejuvenation of the muscle stem cell population restores strength to injured aged muscles
Open accessAbstract
The elderly often suffer from progressive muscle weakness and regenerative failure. We demonstrate that muscle regeneration is impaired with aging owing in part to a cell-autonomous functional decline in skeletal muscle stem cells (MuSCs). Two-thirds of MuSCs from aged mice are intrinsically defective relative to MuSCs from young mice, with reduced capacity to repair myofibers and repopulate the stem cell reservoir in vivo following transplantation. This deficiency is correlated with a higher incidence of cells that express senescence markers and is due to elevated activity of the p38α and p38β mitogen-activated kinase pathway. We show that these limitations cannot be overcome by transplantation into the microenvironment of young recipient muscles. In contrast, subjecting the MuSC population from aged mice to transient inhibition of p38α and p38β in conjunction with culture on soft hydrogel substrates rapidly expands the residual functional MuSC population from aged mice, rejuvenating its potential for regeneration and serial transplantation as well as strengthening of damaged muscles of aged mice. These findings reveal a synergy between biophysical and biochemical cues that provides a paradigm for a localized autologous muscle stem cell therapy for the elderly.
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p38 MAPK inhibition has been suggested as an anti-SASP strategy.
“p38 Mitogen-activated protein kinase (MAPK) inhibition has been suggested as an anti-SASP strategy.150”
From Senescence-induced inflammation: an important player and key therapeutic target in atherosclerosis (2020) · cites this paper as [150]
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 [29]
Rejuvenating aged MuSCs requires both biophysical and biochemical cues, suggesting that extrinsic and intrinsic factors must act synergistically.
“Thus, a combination of biophysical and biochemical cues is required to rejuvenate the aged MuSC population, suggesting that a synergistic interplay of extrinsic and intrinsic factors is necessary.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
These findings suggest that changing MuSC function or phenotype in aged muscle will improve repair and may also alleviate sarcopenia.
“These findings suggest that altering the function or phenotype of MuSCs in aged muscle tissue will enhance muscle repair29 and may also ameliorate sarcopenia61.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
The changes include cell-autonomous activation of p38α/β MAPK, FGFR-Sprouty1, Jak2-Stat3, and p16Ink4a-Rb pathways.
“These changes include aberrant and cell-autonomous activation of the stress-associated p38α/β mitogen-activated protein kinase (MAPK) signaling axis, the growth factor-stimulated FGFR–Sprouty1 signaling axis, the cytokine-stimulated Jak2–Stat3 signaling axis, and p16Ink4a (also known as Cdkn2a)–Rb cell cycle inhibitors25,27,29,55,56 (Fig. 2).”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
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 [29]
When aged and young MuSCs are compared in equivalent in vivo repair settings, aged MuSCs show intrinsic changes that reduce self-renewal and repair capacity.
“The prospective isolation methods described above enabled recent findings demonstrating that MuSCs from aged tissues accumulate intrinsic changes that lead to a reduction in self-renewal and repair capacity, relative to young tissues, when placed in equivalent in vivo repair settings22,25,29,55,56 (Fig. 3).”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
Extended exposure to a young muscle environment after transplantation does not suffice to rejuvenate aged MuSCs.
“Remarkably, stem cells derived from primary transplants of aged MuSCs remained severely defective in their ability to engraft and repair damaged muscle tissues in secondary young recipients (Fig. 3), demonstrating that prolonged exposure to a young muscle tissue environment after transplantation is not sufficient to rejuvenate the aged MuSC population29,56.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
Aged MuSCs can be rejuvenated ex vivo by culture on a soft hydrogel with muscle-like stiffness plus transient p38α/β MAPK inhibition.
“In particular, the rejuvenation of MuSCs ex vivo can be achieved by growing MuSCs on a soft hydrogel substrate with muscle-like rigidity (Figs. 3 and 4) and transient treatment with a chemical inhibitor of p38α/β MAPK 29.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
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 [29]
Aged MuSC dysfunction is attributed to changes in several signal transduction cascades that converge on common cell-cycle kinases and myogenic differentiation factors.
“The cell-intrinsic dysfunction of the aged MuSC population arises from alterations in a combination of multiple signal transduction cascades, which converge on a shared set of cell cycle kinases and myogenic differentiation factors.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
In mice, lentiviral knockdown of p16Ink4a or transient ex vivo inhibition of p38α/β MAPK stops progression to senescence and rejuvenates aged MuSCs.
“Notably lentivirally-mediated genetic knockdown of p16Ink4a (officially known as Cdkn2a) (ref. 56) or transient biochemical inhibition of p38α/β MAPK29 ex vivo halts progression toward senescence and facilitates rejuvenation of the aged MuSC population in mouse.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
Aged MuSCs that had been transplanted into young primary recipients remained severely defective in engraftment and repair when serially transplanted into young secondary recipients.
“Remarkably, stem cells derived from primary transplants of aged MuSCs remained severely defective in their ability to engraft and repair damaged muscle tissues in secondary young recipients (Fig. 3), demonstrating that prolonged exposure to a young muscle tissue environment after transplantation is not sufficient to rejuvenate the aged MuSC population29,56.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
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 [29]
These findings suggest that rejuvenation expands a residual highly regenerative subset rather than converting dysfunctional cells into functional ones.
“These findings suggest that rejuvenation of the aged MuSC population results from an expansion of a subset of residual highly regenerative cells rather than a conversion of dysfunctional cells to a functional cell state.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
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 [29]
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 [29]
Time-lapse single-cell tracking showed that only a subset of aged MuSCs, not all, respond to p38α/β MAPK inhibition.
“For example, single-cell tracking by time-lapse microscopy of clonal division kinetics revealed that only a subset of aged MuSCs respond to chemical inhibition of p38α/β MAPK, not the entire population29.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
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 [29]
Rigidity alone does not maintain aged stem cell function in culture; a combination of 12-kPa rigidity and p38α/β MAPK inhibitor is necessary.
“Notably, rigidity per se does not maintain aged stem cell function in culture. Instead, a combination of biophysical (12-kPa rigidity) and biochemical cues (p38α/β MAPK inhibitor) is necessary29.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
Substrates with stiffness of young adult skeletal muscle (~12 kPa) promote MuSC self-renewal and myoblast differentiation.
“In studies using biomimetic niches, substrates with an elastic stiffness of young adult skeletal muscle (∼12 kPa Young's modulus, the characteristic elastic rigidity of a material), which is five orders of magnitude softer than traditonal tissue culture plastic), promote MuSC self-renewal29,31 and myoblast differentiation94,95 (Fig. 4).”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
MuSCs are heterogeneous even in young mice, and heterogeneity increases with aging.
“MuSCs are not a homogeneous population even in young mice, and MuSC heterogeneity increases during aging14,16,25,29,56,62–64.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [29]
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 [29]
Multiple groups have reported that transplanting satellite cells into dystrophic or injured/irradiated mouse muscle can refill the stem cell pool.
“Several groups have reported successful replenishment of the stem cell pool by satellite cell transplantation into dystrophic or irradiated/injured muscles in mice120,139,140, although the rarity of satellite cells in muscle tissue has been a challenge for translating muscle stem cell transplantation to clinical practice141”
From Stem cell aging: mechanisms, regulators and therapeutic opportunities (2014) · cites this paper as [140]
p38 MAPK inhibition can also be paired with growth on soft hydrogels to improve how well aged muscle stem cells transplant.
“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 [140]
Aged MuSCs show impaired activation.
“However, aged MuSCs have been reported to show impaired activation in multiple studies, suggesting that a defect in activation dynamics may also contribute to impaired regeneration (Brack et al., 2007; Cosgrove et al., 2014; Egerman et al., 2015; Gilbert et al., 2010).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as Cosgrove et al., 2014
Aged MuSCs show a delayed time to first division relative to young cells, with fewer aged cells forming colonies in vitro.
“Likewise, it has been reported that aged MuSCs show a delayed time to first division relative to young cells, with fewer aged cells forming colonies in vitro (Cosgrove et al., 2014; Gilbert et al., 2010).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as Cosgrove et al., 2014
In vitro MuSC activation recapitulates many aspects of in vivo activation.
“However, our in vitro assay allows for a homogeneous activation stimulus across all cells, unlike in vivo injury models and previous work demonstrating that in vitro MuSC activation recapitulates many aspects of in vivo activation (Blau et al., 2015; Cornelison and Wold, 1997; Cosgrove et al., 2014; Gilbert et al., 2010).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as Cosgrove et al., 2014
We surprisingly found minor transcriptional differences between aged and young MuSCs at a given point in the activation process.
“We surprisingly found minor transcriptional differences between aged and young MuSCs at a given point in the activation process, consistent with previous reports (Cosgrove et al., 2014; Keyes et al., 2016; Sousa-Victor et al., 2014).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as Cosgrove et al., 2014
There are dramatic differences in functional potential between aged and young cell populations.
“The lack of unique aged transcriptional states and modest differential expression results between aged and young cells are surprising in light of the dramatic differences in functional potential between aged and young cell populations (Chakkalakal et al., 2012; Cosgrove et al., 2014).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as Cosgrove et al., 2014
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- Authors
- Cosgrove, B. D., Gilbert, P. M., Porpiglia, E., Mourkioti, F., Lee, S. P., Corbel, S. Y., Llewellyn, M. E., Delp, S. L., & Blau, H. M.
- Affiliations
- Stanford Medicine (US)
- University of Toronto (CA)
- Corresponding author
- Gilbert, Penney M
- Blau, Helen M
- ORCID
- Venue
- Nature Medicine
- Published
- 2014-02-16
- Volume
- 20
- Issue
- 3
- Pages
- 255-264
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC3949152
- OpenAlex
- W2138514622
- Cited by
- 677
- References
- 63
- Citations by year
- 2026: 47 · 2025: 28 · 2024: 46 · 2023: 49 · 2022: 49 · 2021: 78 · 2020: 61 · 2019: 43 · 2018: 61 · 2017: 61 · 2016: 73 · 2015: 52 · 2014: 27
- FWCI
- 29.10
- 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 (K99AG042491, R01AG009521, R21AG044815, R01AG020961)
- National Heart, Lung, and Blood Institute (U01HL100397, U01HL099997, R01HL096113)
- National Cancer Institute (T32CA009151, R25CA118681)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR063963, K99AR061465)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Health Sciences › Medicine › Genetics › Neurogenetic and Muscular Disorders Research
- Keywords
- muscle stem cells, skeletal muscle aging, age-related sarcopenia, muscle regeneration, cellular senescence, stem cell rejuvenation, hydrogel substrates, biophysical cues, autologous stem cell therapy, muscle strength
- MeSH terms
- Aging, Animals, Female, Male, Mice, Inbred C57BL, Mice, Transgenic, Muscles, Phenotype, Phosphoproteins, Regeneration, Rejuvenation, Stem Cells, Time Factors, Mice, SCID, Mice, Inbred NOD, Cellular Senescence, Cell Transplantation, Muscle Fibers, Skeletal, Cyclin-Dependent Kinase Inhibitor p16, Hydrogels, Stem Cell Transplantation, Mitogen-Activated Protein Kinase 11, Mitogen-Activated Protein Kinase 14, Cell Proliferation, Green Fluorescent Proteins, Cyclin-Dependent Kinase Inhibitor p21, Mice, Muscle Strength
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