Early forming label-retaining muscle stem cells require p27kip1 for maintenance of the primitive state
Open accessAbstract
Across different niches, subsets of highly functional stem cells are maintained in a relatively dormant rather than proliferative state. Our understanding of proliferative dynamics in tissue-specific stem cells during conditions of increased tissue turnover remains limited. Using a TetO-H2B-GFP reporter of proliferative history, we identify skeletal muscle stem cell, or satellite cells, that retain (LRC) or lose (nonLRC) the H2B-GFP label. We show in mice that LRCs and nonLRCs are formed at birth and persist during postnatal growth and adult muscle repair. Functionally, LRCs and nonLRCs are born equivalent and transition during postnatal maturation into distinct and hierarchically organized subsets. Adult LRCs give rise to LRCs and nonLRCs; the former are able to self-renew, whereas the latter are restricted to differentiation. Expression analysis revealed the CIP/KIP family members p21(cip1) (Cdkn1a) and p27(kip1) (Cdkn1b) to be expressed at higher levels in LRCs. In accordance with a crucial role in LRC fate, loss of p27(kip1) promoted proliferation and differentiation of LRCs in vitro and impaired satellite cell self-renewal after muscle injury. By contrast, loss of p21(cip1) only affected nonLRCs, in which myogenic commitment was inhibited. Our results provide evidence that restriction of self-renewal potential to LRCs is established early in life and is maintained during increased tissue turnover through the cell cycle inhibitor p27(kip1). They also reveal the differential role of CIP/KIP family members at discrete steps within the stem cell hierarchy.
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LRCs and nonLRCs are discrete populations of MuSCs with different proliferative histories and different regenerative potentials.
“We previously described LRCs and nonLRCs as discrete populations of MuSCs with different proliferative histories and different regenerative potentials (Chakkalakal et al., 2012, 2014).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as Chakkalakal et al., 2014
LRCs, which undergo fewer divisions during development, are more regenerative than nonLRCs, which undergo many divisions.
“We previously showed that LRCs, which undergo fewer divisions during development, are more regenerative than nonLRCs, which undergo many divisions (Chakkalakal et al., 2012; Chakkalakal et al., 2014).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as Chakkalakal et al., 2014
LRCs are functionally distinct from nonLRCs, and this functional difference persists throughout life.
“LRCs are functionally distinct from nonLRCs, and this functional difference persists throughout life (Chakkalakal et al., 2012, 2014).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as Chakkalakal et al., 2014
The conversion of highly regenerative LRCs to less regenerative nonLRCs is a factor in this regenerative decline.
“We previously found that the conversion of highly regenerative LRCs to less regenerative nonLRCs is a factor in this regenerative decline (Chakkalakal et al., 2012, 2014).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as Chakkalakal et al., 2014
LRCs are believed to be 'reserve' stem cells, whereas nonLRCs are presumed to be precocious in their response based on differentiation assays.
“This result is surprising, as LRCs are believed to be ‘reserve’ stem cells, whereas nonLRCs are presumed to be precocious in their response based on differentiation assays (Chakkalakal et al., 2012, 2014).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as Chakkalakal et al., 2014
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- Authors
- Chakkalakal, J. V., Christensen, J., Xiang, W., Tierney, M. T., Boscolo, F. S., Sacco, A., & Brack, A. S.
- Affiliations
- Harvard University (US)
- University of Copenhagen (DK)
- Sanford Children's Health Research Center, Sanford-Burnham Medical Research Institute, La Jolla, CA 92037, USA
- Sanford Burnham Prebys Medical Discovery Institute (US)
- Corresponding author
- Brack, Andrew S.
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2014-04-15
- Volume
- 141
- Issue
- 8
- Pages
- 1649-1659
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- PMC
- PMC3978835
- OpenAlex
- W2061818216
- Cited by
- 148
- References
- 58
- Citations by year
- 2026: 8 · 2025: 11 · 2024: 10 · 2023: 5 · 2022: 15 · 2021: 15 · 2020: 14 · 2019: 10 · 2018: 15 · 2017: 17 · 2016: 10 · 2015: 16 · 2014: 2
- FWCI
- 6.15
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Development (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (F31AR065923, R01AR060868, AR061303 P30, P30AR061303, R01AR061002)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- skeletal muscle stem cells, satellite cells, label-retaining cells, p27, p21, stem cell self-renewal, stem cell differentiation, muscle regeneration, muscle damage, stem cell hierarchy, tissue turnover, postnatal maturation
- MeSH terms
- Animals, Animals, Newborn, Cell Differentiation, Histones, Mice, Inbred C57BL, Muscular Dystrophy, Animal, Phenotype, Staining and Labeling, Stem Cells, Mice, Inbred mdx, Disease Progression, Muscle, Skeletal, Cell Lineage, Cell Proliferation, Green Fluorescent Proteins, Cyclin-Dependent Kinase Inhibitor p21, Cyclin-Dependent Kinase Inhibitor p27, Mice
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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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