Muscle stem cells contribute to myofibres in sedentary adult mice
Open accessAbstract
Skeletal muscle is essential for mobility, stability and whole body metabolism, and muscle loss, for instance, during sarcopenia, has profound consequences. Satellite cells (muscle stem cells) have been hypothesized, but not yet demonstrated, to contribute to muscle homeostasis and a decline in their contribution to myofibre homeostasis to play a part in sarcopenia. To test their role in muscle maintenance, we genetically labelled and ablated satellite cells in adult sedentary mice. We demonstrate via genetic lineage experiments that, even in the absence of injury, satellite cells contribute to myofibres in all adult muscles, although the extent and timing differs. However, genetic ablation experiments showed that satellite cells are not globally required to maintain myofibre cross-sectional area of uninjured adult muscle. Skeletal muscle satellite cells are muscle stem cells believed to contribute only to regenerating myofibres. Here Keefe et al. show that in adult sedentary mice satellite cells continue to fuse with uninjured myofibres, but they are not globally required for the maintenance of aging muscles.
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Ablating Pax7-expressing MuSCs in aged muscle does not accelerate or slow muscle wasting.
“Conditional ablation of Pax7-expressing MuSCs from aged muscles neither accelerates nor slows muscle wasting17,28.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [28]
The ablation findings are limited because Pax7CreER-DTA models do not fully eliminate MuSCs.
“However, these findings are based on Pax7CreER-DTA models which do not completely ablate the MuSC population.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [28]
Throughout the lifespan of satellite cell depleted mice, sarcopenia is neither exacerbated nor accelerated.
“However, throughout the lifespan of satellite cell depleted mice, sarcopenia is neither exacerbated nor accelerated [28,29].”
From Potential Roles of n-3 PUFAs during Skeletal Muscle Growth and Regeneration (2018) · cites this paper as [28]
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The central role of muscle stem cells in regenerative failure with aging
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“Histological characterization of mice Due to challenging and unreliable labeling reagents such as antibodies for populations such as MuSCs in whole muscle, genetic reporter mouse lines encoding promoter driven fluorescent molecules (Bosnakovski et al., 2008; Keefe et al., 2015; Relaix et al., 2005; Sambasivan et al.,…”
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“During postnatal development, satellite cells (a resident stem cell population of muscular tissue) can differentiate and fuse with existing myofibers, thereby providing new nuclei and organelles to the growing fiber (Keefe et al., 2015).”
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“In steady-state conditions, satellite cells are in a quiescent state (28, 29).”
BackgroundCharacterization of cellular senescence in aging skeletal muscle
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“Through genetic lineage experiments, another study showed that even in the absence of injury, satellite cells contribute to myofibers in all adult muscles, although the extent and timing differed (Keefe et al., 2015).”
BackgroundRegulation of skeletal muscle stem cells by fibroblast growth factors
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“%) are active and maintain adult skeletal musculature (Pawlikowski et al, 2015; Keefe et al, 2015).”
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“In contrast, satellite cells are largely not required to maintain muscle cross-sectional area in aging mice [44].”
BackgroundRedox Control of Skeletal Muscle Regeneration
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“These findings have been recently confirmed in vivo in mice by using genetically labeled MuSCs (164).”
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“In contrast, we observed SC derived progenitor fusion into myofibers without appreciable central nucleation, consistent with previous reports during aging, adolescent maturation, and denervation atrophy (Liu et al., 2015; Keefe et al., 2015; Pawlikowski et al., 2015).”
BackgroundMethodResultInfluentialEstrogen Regulates the Satellite Cell Compartment in Females
Collins, B. C., Arpke, R. W., Larson, A. A., Baumann, C. W., Xie, N., Cabelka, C. A., Nash, N. L., Juppi, H., Laakkonen, E. K., Sipilä, S., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.025 · Cited by 177 · see citing works
“…and as a result the regenerative capacity of skeletal muscle in aged males is impaired, compared to that of younger males (Brack et al., 2005; Carlson and Conboy, 2007; Chakkalakal et al., 2012; Keefe et al., 2015; Shefer et al., 2006), but such age-induced impairments in females is less studied.”
InfluentialStem Cell Aging in Skeletal Muscle Regeneration and Disease
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“Some groups have reported the contribution of MuSCs in sarcopenia, but it remains controversial [86,87].”
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“Although satellite cells contribute to myofibers with varying extent and timing, satellite cell depletion experiments showed that they are not required globally for the maintenance of myofibers during aging (17, 18).”
BackgroundResultRequirement of myomaker-mediated stem cell fusion for skeletal muscle hypertrophy
Goh, Q., & Millay, D. P. (2017) · eLife · doi:10.7554/elife.20007 · Cited by 157 · see citing works
“Additionally, SCs contribute to myofibers during aging of sed- entary mice although SC activity was not globally required to maintain muscle size (Keefe et al., 2015; Pawlikowski et al., 2015).”
BackgroundInfluentialLiu, W., Wei‐LaPierre, L., Klose, A. M., Dirksen, R. T., & Chakkalakal, J. V. (2015) · eLife · doi:10.7554/elife.09221 · Cited by 152 · see citing works
“Similar strategies have shown SCs contribute to myofibers and regulate aspects of skeletal muscle integrity during aging (Fry et al., 2015; Keefe et al., 2015).”
BackgroundMyogenin is an essential regulator of adult myofibre growth and muscle stem cell homeostasis
Ganassi, M., Badodi, S., Wanders, K., Zammit, P. S., & Hughes, S. M. (2020) · eLife · doi:10.7554/elife.60445 · Cited by 152 · see citing works
Regenerative decline of stem cells in sarcopenia
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“…were ablated in young animals, without affecting skeletal muscle myofiber size or composition (Fry et al., 2015); at variance, other studies proposed that satellite cells do contribute to myofibers in all adult muscles in sedentary mice, although the extent and timing differs (Keefe et al., 2015).”
BackgroundMyosin heavy chain-embryonic regulates skeletal muscle differentiation during mammalian development
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“reported that myonuclear number does not decline throughout adulthood in the absence of satellite cells in the plantaris muscle (54, 85).”
BackgroundInfluentialThe Muscle Stem Cell Niche in Health and Disease
Mashinchian, O., Pisconti, A., Moal, E. L., & Bentzinger, C. F. (2017) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2017.08.003 · Cited by 127 · see citing works
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“In contrast, SC depletion well into adulthood leads to EDL myofiber atrophy and loss of myonuclei over a protracted period of time, whereas other muscles, such as the SOL, demonstrate modest, if any, phenotypes (Fry et al., 2015; Keefe et al., 2015; Liu et al., 2017).”
BackgroundMethodInfluentialSomatic mutagenesis in satellite cells associates with human skeletal muscle aging
Franco, I., Johansson, A., Olsson, K., Vrtačnik, P., Lundin, P., Helgadottir, H. T., Larsson, M., Revêchon, G., Bosia, C., Pagnani, A., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03244-6 · Cited by 126 · see citing works
“Some evidence has been provided in mice 7,8 , but a direct demonstration in the human muscle was still lacking.”
Pten is necessary for the quiescence and maintenance of adult muscle stem cells
Yue, F., Bi, P., Wang, C., Shan, T., Nie, Y., Ratliff, T. L., Gavin, T. P., & Kuang, S. (2017) · Nature Communications · doi:10.1038/ncomms14328 · Cited by 121 · see citing works
Fusion and beyond: Satellite cell contributions to loading-induced skeletal muscle adaptation
Murach, K. A., Fry, C. S., Dupont‐Versteegden, E. E., McCarthy, J. J., & Peterson, C. A. (2021) · The FASEB Journal · doi:10.1096/fj.202101096r · Cited by 120 · see citing works
The musculoskeletal syndrome of menopause
Wright, V. J., Schwartzman, J. D., Itinoche, R., & Wittstein, J. R. (2024) · Climacteric · doi:10.1080/13697137.2024.2380363 · Cited by 116 · see citing works
Muñoz‐Cánoves, P., Neves, J., & Sousa‐Victor, P. (2019) · FEBS Journal · doi:10.1111/febs.15182 · Cited by 111 · see citing works
“In addition to their primary role as agents of tissue regeneration after injury, satellite cells also contribute to the homeostatic maintenance of muscle fibers [75, 76].”
BackgroundCellular and molecular mechanisms of sarcopenia: The S100B perspective
Riuzzi, F., Sorci, G., Arcuri, C., Giambanco, I., Bellezza, I., Minelli, A., & Donato, R. (2018) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12363 · Cited by 114 · see citing works
“might not concur to sarcopenia while leading to defective regeneration following acute muscle injury and contributing to age-related muscle fibrosis.(84,85) This would imply that pri-”
Myonuclear accretion is a determinant of exercise-induced remodeling in skeletal muscle
Goh, Q., Song, T., Petrany, M. J., Cramer, A., Sun, C., Sadayappan, S., Lee, S., & Millay, D. P. (2019) · eLife · doi:10.7554/elife.44876 · Cited by 110 · see citing works
Potential Roles of n-3 PUFAs during Skeletal Muscle Growth and Regeneration
Tachtsis, B., Camera, D., & Lacham-Kaplan, O. (2018) · Nutrients · doi:10.3390/nu10030309 · Cited by 104 · see citing works
“However, throughout the lifespan of satellite cell depleted mice, sarcopenia is neither exacerbated nor accelerated [28,29].”
BackgroundAdiponectin promotes muscle regeneration through binding to T-cadherin
Tanaka, Y., Kita, S., Nishizawa, H., Fukuda, S., Fujishima, Y., Obata, Y., Nagao, H., Masuda, S., Nakamura, Y., Shimizu, Y., et al. (2019) · Scientific Reports · doi:10.1038/s41598-018-37115-3 · Cited by 103 · see citing works
Unraveling female reproductive senescence to enhance healthy longevity
Dong, L., Teh, D. B. L., Kennedy, B. K., & Huang, Z. (2023) · Cell Research · doi:10.1038/s41422-022-00718-7 · Cited by 101 · see citing works
“As the expression of ERs is ubiquitous in satellite cells (adult muscle stem cells) of muscle fibers, estrogen stimulates the activation and proliferation of these quiescent stem cells (satellite cells) during muscle repair or injury.(76) Although both ERα and ERβ are present, ERα contributes to the critical signaling…”
BackgroundDisrupted prenatal RNA processing and myogenesis in congenital myotonic dystrophyPreprint
Thomas, J. D., Sznajder, Ł. J., Bardhi, O., Aslam, F. N., Anastasiadis, Z. P., Scotti, M. M., Nishino, I., Nakamori, M., Wang, E. T., & Swanson, M. S. (2017) · Genes & Development · doi:10.1101/gad.300590.117 · Cited by 94 · see citing works
Tierney, M. T., Stec, M. J., Rulands, S., Simons, B. D., & Sacco, A. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2017.11.009 · Cited by 92 · see citing works
“Prior efforts have demonstrated a significant accumulation of MuSC fusion to myofibers with age absent injury (Keefe et al., 2015; Pawlikowski et al., 2015).”
BackgroundMurach, K. A., Mobley, C. B., Zdunek, C. J., Frick, K. K., Jones, S. R., McCarthy, J. J., Peterson, C. A., & Dungan, C. M. (2020) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12617 · Cited by 93 · see citing works
“Our laboratory and others report that depletion of satellite cells, the primary contributors of myonuclei, in adult sedentary mice generally does not result in a catastrophic nor appreciable loss of myonuclei across multiple muscles throughout the lifespan.(42,49,51,52) While alternative stem cell populations may cont…”
BackgroundFusion-independent satellite cell communication to muscle fibers during load-induced hypertrophy
Murach, K. A., Vechetti, I. J., Van Pelt, D. W., Crow, S. E., Dungan, C. M., Figueiredo, V. C., Kosmac, K., Fu, X., Richards, C. I., Fry, C. S., et al. (2020) · Function · doi:10.1093/function/zqaa009 · Cited by 94 · see citing works
“caution for accurately determining the contribution of satellite cell fusion to muscle fibers (21, 59, 73, 93, 114).”
BackgroundMethodInfluentialNeelakantan, H., Brightwell, C. R., Graber, T. G., Maroto, R., Wang, H.-Y. L., McHardy, S. F., Papaconstantinou, J., Fry, C. S., & Watowich, S. J. (2019) · Biochemical Pharmacology · doi:10.1016/j.bcp.2019.02.008 · Cited by 88 · see citing works
“, gastrocnemius, soleus) experience age-related declines in muSC abundance [21].”
Musculoskeletal senescence: a moving target ready to be eliminated
Baar, M. P., Perdiguero, E., Muñoz-Cánoves, P., & de Keizer, P. L. (2018) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2018.05.007 · Cited by 83 · see citing works
“Furthermore, several studies show that sarcopenic muscle has a reduced ability to recover after injury, which is dependent on satellite cell function [5,21 ,35,36].”
BackgroundExercise promotes satellite cell contribution to myofibers in a load-dependent manner
Masschelein, E., D’Hulst, G., Zvick, J., Hinte, L. C., Soro-Arnáiz, I., Gorski, T., von Meyenn, F., Bar‐Nur, O., & Bock, K. D. (2020) · Skeletal Muscle · doi:10.1186/s13395-020-00237-2 · Cited by 82 · see citing works
“Genetic lineage experiments, in which Pax7 cells and their derived fibers are fluorescently labeled, have recently shown that there is a considerable (up to 30%) contribution of SCs to uninjured adult mouse skeletal muscle fibers (Keefe et al., 2015; Pawlikowski et al., 2015).”
BackgroundMethodResultInfluentialMitochondria and cellular senescence: Implications for musculoskeletal ageing
Habiballa, L., Salmonowicz, H., & Passos, J. F. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.10.417 · Cited by 82 · see citing works
Alternative polyadenylation of Pax3 controls muscle stem cell fate and muscle function
de Morree, A., Klein, J. D. D., Gan, Q., Farup, J., Urtasun, A., Kanugovi, A., Bilen, B., van Velthoven, C. T. J., Quarta, M., & Rando, T. A. (2019) · Science · doi:10.1126/science.aax1694 · Cited by 81 · see citing works
Porpiglia, E., Mai, T., Kraft, P. E., Holbrook, C. A., de Morrée, A., Gonzalez, V. D., Hilgendorf, K. I., Frésard, L., Trejo, A., Bhimaraju, S., et al. (2022) · Cell stem cell · doi:10.1016/j.stem.2022.10.009 · Cited by 81 · see citing works
Mixing it up: the biological significance of hybrid skeletal muscle fibers
Medler, S. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.200832 · Cited by 80 · see citing works
“In addition, myonuclei from satellite cells may continually join with uninjured adult muscle fibers throughout life, especially in certain muscles including the diaphragm and extraocular muscles (Keefe et al., 2015; McLoon and Wirtschafter, 2002, 2003; McLoon et al., 2004; Pawlikowski et al., 2015).”
BackgroundDissecting Murine Muscle Stem Cell Aging through Regeneration Using Integrative Genomic Analysis
Shcherbina, A., Larouche, J., Fraczek, P., Yang, B. A., Brown, L. A., Markworth, J. F., Chung, C. H., Khaliq, M., de Silva, K., Choi, J. J., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107964 · Cited by 76 · see citing works
“hindlimb muscles of transgenic mice harboring a Cre/LoxP-based system for MuSC lineage tracing Pax7CreERT2/+; Rosa26TdTomato (P7TdT) (Keefe et al., 2015).”
BackgroundEarly satellite cell communication creates a permissive environment for long-term muscle growth
Murach, K. A., Peck, B. D., Policastro, R. A., Vechetti, I. J., Van Pelt, D. W., Dungan, C. M., Denes, L. T., Fu, X., Brightwell, C. R., Zentner, G. E., et al. (2021) · iScience · doi:10.1016/j.isci.2021.102372 · Cited by 75 · see citing works
Contribution of muscle satellite cells to sarcopenia
Huo, F., Liu, Q., & Liu, H. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.892749 · Cited by 74 · see citing works
“Although the role of MuSCs in sarcopenia is questionable, maintaining the integrity of MuSC number and function is indispensable for muscle health (Keefe et al., 2015).”
BackgroundThe roles of muscle stem cells in muscle injury, atrophy and hypertrophy
Fukada, S. (2018) · The Journal of Biochemistry · doi:10.1093/jb/mvy019 · Cited by 74 · see citing works
Becker, M., Joseph, S. S., García‐Carrizo, F., Tom, R. Z., Opaleva, D., Serr, I., Tschöp, M. H., Schulz, T. J., Hofmann, S. M., & Daniel, C. (2023) · Cell Metabolism · doi:10.1016/j.cmet.2023.08.010 · Cited by 73 · see citing works
Changes in Redox Signaling in the Skeletal Muscle with Aging
Szentesi, P., Csernoch, L., Dux, L., & Keller-Pintér, A. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/4617801 · Cited by 71 · see citing works
Furuichi, Y., Kawabata, Y., Aoki, M., Mita, Y., FUJII, N. L., & Manabe, Y. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.640399 · Cited by 69 · see citing works
“Primary cultures of satellite cells have widely been used to study the myogenesis, metabolism, myokine secretion, and contractile capacity of muscle cells (Lecompte et al., 2017; Sanchez et al., 2018; Chen et al., 2019).”
MethodKeep Your Friends Close: Cell–Cell Contact and Skeletal MyogenesisPreprint
Krauss, R. S., Joseph, G. A., & Goel, A. J. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a029298 · Cited by 68 · see citing works
“Unlike tissues such as the epidermis or hematopoietic system, myofibers are not replenished homeostatically, and as such, satellite cells do not play a major role in maintenance of adult skeletal muscle (Fry et al. 2015; Keefe et al. 2015).”
BackgroundCho, D. S., & Doles, J. D. (2017) · Gene · doi:10.1016/j.gene.2017.09.014 · Cited by 64 · see citing works
“Furthermore, our data only represent basal (uninjured) SC activation dynamics in adult mice (Pawlikowski et al., 2015; Keefe et al., 2015) and do not represent injury, age, or disease-associated cell/tissue activation states.”
BackgroundFukada, S., Akimoto, T., & Sotiropoulos, A. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2020.118742 · Cited by 65 · see citing works
Systemic Problems: A perspective on stem cell aging and rejuvenation
Conboy, I. M., Conboy, M. J., & Rebo, J. (2015) · Aging · doi:10.18632/aging.100819 · Cited by 65 · see citing works
“Despite semantics, this does not exclude contribution of muscle stem cells to this tissue even in sedentary mice [84] or the effects of their functional decline with aging particularly when muscle needs rebuilding upon exercise or attrition [85, 86].”
BackgroundRandolph, M. E., & Pavlath, G. K. (2015) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2015.00190 · Cited by 63 · see citing works
“In vivo lineage tracing studies examining the contribution of diaphragmatic satellite cells to uninjured diaphragm muscles revealed continued addition of new myonuclei with age, yet myofiber size was not affected with satellite cell ablation (Keefe et al., 2015).”
BackgroundFochi, S., Giuriato, G., Simone, T. D., Gomez‐Lira, M., Tamburin, S., Piccolo, L. D., Schena, F. F., Venturelli, M., & Romanelli, M. G. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186732 · Cited by 63 · see citing works
“St y in ice have e onstrate that re ction of satellite cells affects scle rege erative ca acity it o t affecti g sarco e ia, a oes ot co trib te to t e ai te a ce of scle size ri g agi g, o e er i se e tary a lt ice, i t e absence of injury, satellite cells may contribute to myfibers at different extent between muscle…”
BackgroundInsights into muscle stem cell dynamics during postnatal development
Bachman, J. F., & Chakkalakal, J. V. (2021) · FEBS Journal · doi:10.1111/febs.15856 · Cited by 61 · see citing works
Kwon, J. B., Ettyreddy, A. R., Vankara, A., Bohning, J. D., Devlin, G. W., Hauschka, S. D., Asokan, A., & Gersbach, C. A. (2020) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2020.09.016 · Cited by 61 · see citing works
“The diaphragm has the highest satellite cell contribution to myofiber generation due to the constant activation of this muscle to drive ventilation.(32) Furthermore, diaphragm satellite cells are molecularly unique from limb muscles in their expression of Pax3.”
BackgroundJackson, J. R., Kirby, T. J., Fry, C. S., Cooper, R. L., McCarthy, J. J., Peterson, C. A., & Dupont‐Versteegden, E. E. (2015) · Skeletal Muscle · doi:10.1186/s13395-015-0065-3 · Cited by 60 · see citing works
“Furthermore, recent work from our laboratory [27] and others [28] demonstrated that despite living most of their adult life without satellite cells, there was no observable phenotypic change in aged Pax7/DTA mice that were satellite cell depleted at 4 months of age leading to the conclusion that satellite cells are no…”
Twist1 Activation in Muscle Progenitor Cells Causes Muscle Loss Akin to Cancer Cachexia
Parajuli, P., Kumar, S., Loumaye, A., Singh, P., Eragamreddy, S., Nguyen, T. L., Ozkan, S., Razzaque, M. S., Prunier, C., Thissen, J.-P., et al. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.05.026 · Cited by 58 · see citing works
“Congruently, we detected a small fraction of myofibers in TA muscle that express exogenous 6xMyc-Twist1 (Figure S2F), supporting the inability of Twist1 to block myoblast differentiation, and further confirming previous studies that adult satellite cells can differentiate into myofibers under homeostatic conditions (K…”
ResultContreras, O., Córdova-Casanova, A., & Brandan, E. (2021) · Cellular Signalling · doi:10.1016/j.cellsig.2021.110036 · Cited by 57 · see citing works
Mademtzoglou, D., Asakura, Y., Borok, M. J., Alonso‐Martín, S., Mourikis, P., Kodaka, Y., Mohan, A., Asakura, A., & Relaix, F. (2018) · eLife · doi:10.7554/elife.33337 · Cited by 57 · see citing works
Differentiation of the human PAX7-positive myogenic precursors/satellite cell lineage in vitro
Tanoury, Z. A., Rao, J., Tassy, O., Gobert, B., Gapon, S., Garnier, J., Wagner, E. K., Hick, A., Hall, A. J., Gussoni, E., et al. (2020) · Development · doi:10.1242/dev.187344 · Cited by 55 · see citing works
The Composition, Development, and Regeneration of Neuromuscular Junctions
Liu, W., & Chakkalakal, J. V. (2017) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2017.08.005 · Cited by 52 · see citing works
Redelsperger, F., Raddi, N., Bacquin, A., Vernochet, C., Mariot, V., Gache, V., Blanchard‐Gutton, N., Charrin, S., Tiret, L., Dumonceaux, J., et al. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006289 · Cited by 51 · see citing works
“As variations in nuclear size and shape may affect myonuclear count [19], we measured the nuclear length of myonuclei on longitudinal sections.”
MethodSatellite cell activation and apoptosis in skeletal muscle from severely burned children
Fry, C. S., Porter, C. C., Sidossis, L. S., Nieten, C., Reidy, P. T., Hundeshagen, G., Mlcak, R. P., Rasmussen, B. B., Lee, J. O., Suman-Vejas, O. E., et al. (2016) · The Journal of Physiology · doi:10.1113/jp272520 · Cited by 50 · see citing works
“Proper maintenance and homeostasis of skeletal muscle involve the fusion of satellite cells (Keefe et al. 2015; Pawlikowski et al. 2015), and long term skeletal muscle hypertrophy is attenuated in their absence (Fry et al.”
BackgroundTakeshita, H., Yamamoto, K. I., Nozato, S., Takeda, M., Fukada, S., Inagaki, T., Tsuchimochi, H., Shirai, M., Nozato, Y., Fujimoto, T., et al. (2018) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12334 · Cited by 48 · see citing works
Osteogenic potential of alpha smooth muscle actin expressing muscle resident progenitor cells
Matthews, B. G., Torreggiani, E., Roeder, E., Matić, I., Grčević, D., & Kalajzić, I. (2015) · Bone · doi:10.1016/j.bone.2015.12.010 · Cited by 45 · see citing works
“that demonstrated contribution of satellite cells to muscle fibers of 6month-old animals over the following 6 months or more[31].”
BackgroundResultInfluentialMcKenna, C. F., & Fry, C. S. (2017) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000409 · Cited by 45 · see citing works
Extraocular Muscle Repair and Regeneration
Verma, M., Fitzpatrick, K. R., & McLoon, L. K. (2017) · Current Ophthalmology Reports · doi:10.1007/s40135-017-0141-4 · Cited by 44 · see citing works
Post-Transcriptional Regulation in Skeletal Muscle Development, Repair, and Disease
Weskamp, K., Olwin, B. B., & Parker, R. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2020.12.002 · Cited by 45 · see citing works
Immunometabolism of macrophages regulates skeletal muscle regeneration
Chen, Y.-F., Lee, C., Wu, H.-H., Lin, W., & Lee, O. K. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.948819 · Cited by 43 · see citing works
“Although ablation of MuSCs in adult mice impaired skeletal muscle regenerative capacity, it did not cause a reduction in the cross-sectional area of uninjured adult muscle regardless of myofiber types (Fry et al., 2015; Keefe et al., 2015).”
BackgroundSkeletal Muscle Nuclei in Mice are not Post-mitotic
Borowik, A., Davidyan, A., Peelor, F. F., Volovičeva, E., Doidge, S. M., Bubak, M. P., Mobley, C. B., McCarthy, J. J., Dupont‐Versteegden, E. E., & Miller, B. F. (2022) · Function · doi:10.1093/function/zqac059 · Cited by 41 · see citing works
Larouche, J. A., Mohiuddin, M., Choi, J. J., Ulintz, P., Fraczek, P. M., Sabin, K., Pitchiaya, S., Kurpiers, S. J., Castor‐Macias, J. A., Liu, W., et al. (2021) · eLife · doi:10.7554/elife.66749 · Cited by 40 · see citing works
Kozakowska, M., Pietraszek‐Gremplewicz, K., Cieśla, M., Seczyńska, M., Bronisz-Budzyńska, I., Podkalicka, P., Bukowska-Straková, K., Łoboda, A., Józkowicz, A., & Dulak, J. (2017) · American Journal Of Pathology · doi:10.1016/j.ajpath.2017.10.017 · Cited by 41 · see citing works
Myotonic Dystrophy and Developmental Regulation of RNA Processing
Thomas, J. D., Oliveira, R., Sznajder, Ł. J., & Swanson, M. S. (2018) · Comprehensive physiology · doi:10.1002/cphy.c170002 · Cited by 47 · see citing works
Butchart, L., Fox, A. H., Shavlakadze, T., & Grounds, M. D. (2016) · Differentiation · doi:10.1016/j.diff.2016.05.003 · Cited by 39 · see citing works
“Differentiation (201 2002), and some low-level incorporation of satellite cells into myofibres has been reported in varying degrees (dependent on the muscle) well into adulthood (Keefe et al., 2015).”
BackgroundTissue cross talks governing limb muscle development and regeneration
Helmbacher, F., & Stricker, S. (2020) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2020.05.005 · Cited by 39 · see citing works
“Nevertheless, a small fraction of satellite cells participates in active turnover all during life [176-178].”
BackgroundZhang, X., Wang, L., Qiu, K., Xu, D., & Yin, J. (2019) · The FASEB Journal · doi:10.1096/fj.201801907r · Cited by 38 · see citing works
Regenerating Myofibers after an Acute Muscle Injury: What Do We Really Know about Them?
Pizza, F. X., & Buckley, K. H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241612545 · Cited by 37 · see citing works
Collins, B. C., & Kardon, G. (2021) · Development · doi:10.1242/dev.199861 · Cited by 35 · see citing works
“…continuously contribute to uninjured myofibers, but the degree of contribution varies between slow and fast myofibers and in different anatomical muscles (Keefe et al., 2015), potentially reflecting cell-intrinsic differences among satellite cells in different muscles (de Morree et al., 2019).”
BackgroundSorensen, J. R., Kaluhiokalani, J. P., Hafen, P. S., Deyhle, M. R., Parcell, A. C., & Hyldahl, R. D. (2019) · The FASEB Journal · doi:10.1096/fj.201900519r · Cited by 35 · see citing works
Wang, Q.-Q., Jing, X.-M., Bi, Y., Cao, X., Wang, Y., Li, Y., Qiao, B., Chen, Y., Hao, Y., & Hu, J. (2018) · Medical Science Monitor · doi:10.12659/msm.913362 · Cited by 34 · see citing works
“Nowadays, it remains controversial that whether a decrease in the number or regenerative capacity of SCs contributes to sarcopenia [8,9], but studies suggest depressed and blunted recovery of muscle after HS in aged rats [25,29] and SCs are indispensable for myogenesis and muscular recovery.”
Adipose tissue in older individuals: a contributing factor to sarcopenia
Wang, T., Zhou, D., & Hong, Z. (2024) · Metabolism · doi:10.1016/j.metabol.2024.155998 · Cited by 35 · see citing works
Anderson, J. E., Do, M. Q., Daneshvar, N., Suzuki, T., Dort, J., Mizunoya, W., & Tatsumi, R. (2016) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12286 · Cited by 33 · see citing works
“Importantly, satellite cells contribute to muscle fibres through adult life, even without proliferation (Keefe et al., 2015; Pawlikowski et al., 2015).”
BackgroundRejuvenating stem cells to restore muscle regeneration in aging
Bengal, E., Perdiguero, E., Serrano, A. L., & Muñoz‐Cánoves, P. (2017) · F1000Research · doi:10.12688/f1000research.9846.1 · Cited by 30 · see citing works
Tissue Engineering for Musculoskeletal Regeneration and Disease Modeling
Li, Z. A., Xiang, S., Li, E. N., Fritch, M. R., Alexander, P. G., Lin, H., & Tuan, R. S. (2020) · Handbook of experimental pharmacology · doi:10.1007/164_2020_377 · Cited by 34 · see citing works
Choo, H. J., Canner, J. P., Vest, K. E., Thompson, Z., & Pavlath, G. K. (2017) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00119.2017 · Cited by 33 · see citing works
“Recent reports indicate a basal level of SC fusion with myofibers occurs in uninjured muscle (26, 40).”
BackgroundSrikuea, R., Hirunsai, M., & Charoenphandhu, N. (2020) · Scientific Reports · doi:10.1038/s41598-020-65067-0 · Cited by 32 · see citing works
Linc‐MYH configures INO80 to regulate muscle stem cell numbers and skeletal muscle hypertrophy
Schutt, C., Hallmann, A., Hachim, S., Klockner, I., Valussi, M., Atzberger, A., Graumann, J., Braun, T. W., & Boettger, T. (2020) · The EMBO Journal · doi:10.15252/embj.2020105098 · Cited by 32 · see citing works
“The definitive amount of MuSCs is determined during postnatal development in individual skeletal muscles and remains stable after reaching adulthood, even after multiple rounds of tissue regeneration (White et al , 2010; Keefe et al , 2015).”
Fukada, S., & Ito, N. (2021) · Experimental Cell Research · doi:10.1016/j.yexcr.2021.112907 · Cited by 31 · see citing works
All for One and One for All: Regenerating Skeletal MusclePreprint
Hindi, S. M., & Millay, D. P. (2021) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a040824 · Cited by 32 · see citing works
Skeletal muscle aging – Stem cells in the spotlight
Henze, H., Jung, M. J., Ahrens, H. E., Steiner, S., & von Maltzahn, J. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111283 · Cited by 28 · see citing works
“mice by long-term labeling experiments, this contribution is highly dependent on muscle type and age (Keefe et al., 2015).”
Myogenic Cell Transplantation in Genetic and Acquired Diseases of Skeletal Muscle
Boyer, O., Butler-Browne, G. S., Chinoy, H., Cossu, G., Galli, F., Lilleker, J. B., Magli, A., Mouly, V., Perlingeiro, R. C. R., Previtali, S. C., et al. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.702547 · Cited by 28 · see citing works
“Although lineage tracing studies show that satellite cells fuse into myofibers in sedentary mice throughout the lifespan (Keefe et al., 2015), loss of function experiments provide evidence that lifelong genetic depletion of satellite cells in transgenic mice did not increase the severity of sarcopenia (Fry et al.”
BackgroundMitochondrial-derived vesicles in skeletal muscle remodeling and adaptation
Picca, A., Guerra, F., Calvani, R., Romanò, R., Coelho‐Júnior, H. J., Bucci, C., Leeuwenburgh, C., & Marzetti, E. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.03.023 · Cited by 28 · see citing works
- Authors
- Keefe, A. C., Lawson, J. A., Flygare, S. D., Fox, Z. D., Colasanto, M. P., Mathew, S. J., Yandell, M., & Kardon, G.
- Affiliations
- University of Utah (US)
- Corresponding author
- Kardon, Gabrielle
- Venue
- Nature Communications
- Published
- 2015-05-14
- Volume
- 6
- Issue
- 1
- Pages
- 7087-7087
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC4435732
- OpenAlex
- W244232182
- Cited by
- 279
- References
- 56
- Citations by year
- 2026: 14 · 2025: 11 · 2024: 31 · 2023: 34 · 2022: 20 · 2021: 27 · 2020: 31 · 2019: 25 · 2018: 27 · 2017: 32 · 2016: 14 · 2015: 13
- FWCI
- 12.44
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Nature Communications (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health (NIH-R01)
- National Institute of General Medical Sciences (R01GM088269)
- National Institute of Diabetes and Digestive and Kidney Diseases (T32DK007115)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD07491, R01HD053728, T32HD007491)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- satellite cells, muscle stem cells, sarcopenia, muscle aging, sedentary mice
- MeSH terms
- Alleles, Animals, Crosses, Genetic, Homeostasis, Male, Mice, Inbred C57BL, Regeneration, Time Factors, Muscle Fibers, Skeletal, Satellite Cells, Skeletal Muscle, Green Fluorescent Proteins, Mice, PAX7 Transcription Factor, Sarcopenia
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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