Satellite Cell Heterogeneity in Skeletal Muscle Homeostasis

Tierney, Matthew T.; Sacco, Alessandra

doi:10.1016/j.tcb.2016.02.004

Cited by 151Muscle Physiology and DisordersMuscle metabolism and nutritionAdipose Tissue and Metabolism

Satellite Cell Heterogeneity in Skeletal Muscle Homeostasis

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Tierney, Matthew T., Sacco, Alessandra·2016·Trends in Cell Biology

DOI 10.1016/j.tcb.2016.02.004PMC PMC4877266

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Abstract

The cellular turnover required for skeletal muscle maintenance and repair is mediated by resident stem cells, also termed satellite cells. Satellite cells normally reside in a quiescent state, intermittently entering the cell cycle to fuse with neighboring myofibers and replenish the stem cell pool. However, the mechanisms by which satellite cells maintain the precise balance between self-renewal and differentiation necessary for long-term homeostasis remain unclear. Recent work has supported a previously unappreciated heterogeneity in the satellite cell compartment that may underlie the observed variability in cell fate and function. In this review, we examine the work supporting this notion as well as the potential governing principles, developmental origins, and principal determinants of satellite cell heterogeneity.

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Transcription factors like Pax7 governing satellite cell activation exhibit differential expression, affecting individual muscle adaptation to caloric surplus.
“Additionally, transcription factors like Pax7 that govern satellite cell activation exhibit differential expression, affecting individual muscle adaptation to caloric surplus [60].”
From Beyond Calories: Individual Metabolic and Hormonal Adaptations Driving Variability in Weight Management—A State-of-the-Art Narrative Review (2024) · cites this paper as [60]
Variability in satellite cell activation and fusion capacity impacts muscle growth potential.
“Variability in satellite cell activation and fusion capacity impacts muscle growth potential.”
From Beyond Calories: Individual Metabolic and Hormonal Adaptations Driving Variability in Weight Management—A State-of-the-Art Narrative Review (2024) · cites this paper as [60]
Satellite cells are crucial for muscle hypertrophy, as they fuse to existing muscle fibers, increasing muscle mass.
“Satellite cells, which are muscle stem cells, are crucial for muscle hypertrophy, as they fuse to existing muscle fibers, increasing muscle mass.”
From Beyond Calories: Individual Metabolic and Hormonal Adaptations Driving Variability in Weight Management—A State-of-the-Art Narrative Review (2024) · cites this paper as [60]

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Background
TNF/p38α/Polycomb Signaling to Pax7 Locus in Satellite Cells Links Inflammation to the Epigenetic Control of Muscle Regeneration
Palacios, D., Mozzetta, C., Consalvi, S., Caretti, G., Saccone, V., Proserpio, V., Marquez, V. E., Valente, S., Mai, A., Forcales, S. V., et al. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.08.013 · Cited by 392 · see citing works
Fibronectin Regulates Wnt7a Signaling and Satellite Cell Expansion
Bentzinger, C. F., Wang, Y. X., von Maltzahn, J., Soleimani, V. D., Yin, H., & Rudnicki, M. A. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2012.09.015 · Cited by 386 · cited 1× · see citing works
“Paracrine secretion of the extracellular matrix (ECM) molecule fibronectin may allow for communication between satellite cell subsets themselves in the context of asymmetric division [82].”
Background
Live imaging of stem cell and progeny behaviour in physiological hair-follicle regeneration
Rompolas, P., Deschene, E. R., Zito, G., Gonzalez, D. G., Saotome, I., Haberman, A. M., & Greco, V. (2012) · Nature · doi:10.1038/nature11218 · Cited by 379 · see citing works
Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration
Shea, K. L., Xiang, W., LaPorta, V. S., Licht, J. D., Keller, C., Basson, M. A., & Brack, A. S. (2010) · Cell stem cell · doi:10.1016/j.stem.2009.12.015 · Cited by 351 · cited 1× · see citing works
“Sprouty-1 (Spry1), an inhibitor of FGF signaling, can overcome this defect [97]; however, its expression is only retained in the LRC fraction.”
Background
Muscle Satellite Cells Are Primed for Myogenesis but Maintain Quiescence with Sequestration of Myf5 mRNA Targeted by microRNA-31 in mRNP Granules
Crist, C. G., Montarras, D., & Buckingham, M. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2012.03.011 · Cited by 346 · see citing works
p53-Mediated Hematopoietic Stem and Progenitor Cell Competition
Bondar, T., & Medzhitov, R. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.03.002 · Cited by 342 · see citing works
A Population of Myogenic Stem Cells That Survives Skeletal Muscle Aging
Collins, C. A., Zammit, P. S., Ruiz, A. P., Morgan, J. E., & Partridge, T. A. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0372 · Cited by 320 · see citing works
Myogenin is required for late but not early aspects of myogenesis during mouse development.
Venuti, J. M., Morris, J., Vivian, J. L., Olson, E. N., & Klein, W. H. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.128.4.563 · Cited by 316 · cited 1× · see citing works
“Myogenin works downstream to trigger advancement to the myocyte stage and subsequent terminal differentiation [9].”
Background
Mouse Spermatogenic Stem Cells Continually Interconvert between Equipotent Singly Isolated and Syncytial States
Hara, K., Nakagawa, T., Enomoto, H., Suzuki, M., Yamamoto, M. P., Simons, B. D., & Yoshida, S. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.01.019 · Cited by 313 · see citing works
Reciprocal inhibition between Pax7 and muscle regulatory factors modulates myogenic cell fate determination
Olguín, H. C., Yang, Z., Tapscott, S. J., & Olwin, B. B. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200608122 · Cited by 311 · cited 4× · see citing works
“Myogenin works downstream to trigger advancement to the myocyte stage and subsequent terminal differentiation [9].”
BackgroundInfluential
MicroRNA-133 Controls Brown Adipose Determination in Skeletal Muscle Satellite Cells by Targeting Prdm16
Yin, H., Pasut, A., Soleimani, V. D., Bentzinger, C. F., Antoun, G., Thorn, S., Seale, P., Fernando, P., van IJcken, W., Grosveld, F., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.01.004 · Cited by 293 · cited 1× · see citing works
“Although transdifferentiation to fibrogenic and adipogenic fates has been described in satellite cells [67,68], here we focus on plasticity within the myogenic lineage.”
Background
High Incidence of Non-Random Template Strand Segregation and Asymmetric Fate Determination In Dividing Stem Cells and their Progeny
Conboy, M. J., Karasov, A. O., & Rando, T. A. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050102 · Cited by 287 · cited 1× · see citing works
“Cell adhesion regulates DNA segregation and satellite cell fate during asymmetric division in situ and in vitro [35,51,52]; thus, monitoring satellite cell division dynamics within their native microenvironment is of critical importance.”
Background
Myf5-Positive Satellite Cells Contribute to Pax7-Dependent Long-Term Maintenance of Adult Muscle Stem Cells
Günther, S., Kim, J., Kostin, S., Lepper, C., Fan, C.-M., & Braun, T. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2013.07.016 · Cited by 280 · see citing works
Constitutive Notch Activation Upregulates Pax7 and Promotes the Self-Renewal of Skeletal Muscle Satellite Cells
Wen, Y., Bi, P., Liu, W., Asakura, A., Keller, C., & Kuang, S. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.06753-11 · Cited by 271 · cited 1× · see citing works
“The Notch signaling pathway integrates juxtacrine, or contact-dependent, information to promote satellite cell self-renewal [33].”
Background
Coordination of Satellite Cell Activation and Self-Renewal by Par-Complex-Dependent Asymmetric Activation of p38α/β MAPK
Troy, A., Cadwallader, A. B., Fedorov, Y., Tyner, K., Tanaka, K. K., & Olwin, B. B. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2012.05.025 · Cited by 268 · see citing works
Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants
Schuster-Gossler, K., Cordes, R., & Gossler, A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608281104 · Cited by 262 · cited 1× · see citing works
“The Notch ligand Delta is also present on the myofiber surface and positively regulates this transition [93].”
Background
Intravital Imaging Reveals Ghost Fibers as Architectural Units Guiding Myogenic Progenitors during Regeneration
Webster, M. T., Manor, U., Lippincott‐Schwartz, J., & Fan, C. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.11.005 · Cited by 248 · cited 2× · see citing works
“Reorienting the remaining basal lamina by surgical manipulation increased the rate of apical-basal division but led to disorganized tissue repair, indicating that this 3D architecture favors planar division for proper regeneration [53].”
Background
Phosphorylation of eIF2α Is a Translational Control Mechanism Regulating Muscle Stem Cell Quiescence and Self-Renewal
Zismanov, V., Chichkov, V., Colangelo, V., Jamet, S., Wang, S., Syme, A., Koromilas, A. E., & Crist, C. G. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.09.020 · Cited by 247 · see citing works
Evidence that hematopoiesis may be a stochastic process in vivo
Abkowitz, J. L., Catlin, S. N., & Guttorp, P. M. (1996) · Nature Medicine · doi:10.1038/nm0296-190 · Cited by 246 · cited 1× · see citing works
“Evidence of the Markov assumption, stating the stochastic nature of cell fate adoption is primarily influenced by the present state, has been found in hematopoietic and cancer stem cells [77,78].”
Background
Mouse Germ Line Stem Cells Undergo Rapid and Stochastic Turnover
Klein, A. M., Nakagawa, T., Ichikawa, R., Yoshida, S., & Simons, B. D. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.05.017 · Cited by 246 · see citing works
Autocrine and Paracrine Angiopoietin 1/Tie-2 Signaling Promotes Muscle Satellite Cell Self-Renewal
Abou-Khalil, R., Grand, F. L., Pallafacchina, G., Valable, S., Authier, F., Rudnicki, M. A., Gherardi, R. K., Germain, S., Chrétien, F. C., Sotiropoulos, A., et al. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.06.001 · Cited by 236 · cited 1× · see citing works
“Angiopoietin-1/Tie2/TEK signaling and ERK1/2 pathway activation promote satellite cell quiescence [99].”
Background
The Ordered Architecture of Murine Ear Epidermis Is Maintained by Progenitor Cells with Random Fate
Doupé, D. P., Klein, A. M., Simons, B. D., & Jones, P. H. (2010) · Developmental Cell · doi:10.1016/j.devcel.2009.12.016 · Cited by 224 · see citing works
Colonization of the Satellite Cell Niche by Skeletal Muscle Progenitor Cells Depends on Notch Signals
Bröhl, D., Vasyutina, E. L., Czajkowski, M. T., Griger, J., Raßek, C., Rahn, H.-P., Purfürst, B., Wende, H., & Birchmeier, C. (2012) · Developmental Cell · doi:10.1016/j.devcel.2012.07.014 · Cited by 214 · cited 1× · see citing works
“Notably, Rbpj-mediated Notch activity in satellite cell precursors themselves is required for niche colonization [92].”
Background
Muscle fiber pattern is independent of cell lineage in postnatal rodent development
Hughes, S. M., & Blau, H. M. (1992) · Cell · doi:10.1016/0092-8674(92)90142-y · Cited by 198 · cited 1× · see citing works
“Although several studies have described behavioral diversity on the basis of myofiber type association [28,29] or embryological origin, including those derived from craniofacial and extraocular muscles [30,31], we focus on satellite cells of somitic origin that reside in the limb.”
Background
Ex Vivo Expansion and In Vivo Self-Renewal of Human Muscle Stem Cells
Charville, G. W., Cheung, T. H., Yoo, B., Santos, P. J. F., Lee, G., Shrager, J. B., & Rando, T. A. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.08.004 · Cited by 196 · see citing works
Progenitors of skeletal muscle satellite cells express the muscle determination gene, MyoD
Kanisicak, O., Mendez, J. J., Yamamoto, S., Yamamoto, M., & Goldhamer, D. J. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.05.554 · Cited by 192 · see citing works
Evidence of fusion between host and donor myoblasts in skeletal muscle grafts
Partridge, T. A., Grounds, M. D., & Sloper, J. C. (1978) · Nature · doi:10.1038/273306a0 · Cited by 190 · cited 1× · see citing works
“Grafting experiments demonstrated that endogenous myogenic cells directly participate in myofiber repair [2], but direct evidence identifying satellite cells as the resident stem cell population remained elusive for several years.”
Background
Early forming label-retaining muscle stem cells require p27kip1 for maintenance of the primitive state
Chakkalakal, J. V., Christensen, J., Xiang, W., Tierney, M. T., Boscolo, F. S., Sacco, A., & Brack, A. S. (2014) · Development · doi:10.1242/dev.100842 · Cited by 148 · cited 2× · see citing works
“LRCs more efficiently contribute to muscle repair and stem cell pool repopulation following transplantation from healthy, aged, and dystrophic muscle [61,64].”
BackgroundSelf-citation
Two Cell Lineages, myf5 and myf5-Independent, Participate in Mouse Skeletal Myogenesis
Haldar, M., Karan, G., Tvrdík, P., & Capecchi, M. R. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.01.002 · Cited by 142 · cited 1× · see citing works
“The ablation of Myf5+ cells only temporarily delays myogenesis before full recovery during the late fetal stages [86,87], consistent with the possible satellite stem cell reserve having never expressed Myf5 [32].”
Background
Human Satellite Cell Transplantation and Regeneration from Diverse Skeletal Muscles
Xu, X., Wilschut, K. J., Kouklis, G. K., Tian, H., Hesse, R., Garland, C. B., Sbitany, H., Hansen, S. L., Seth, R., Knott, P. D., et al. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.07.016 · Cited by 140 · see citing works
Biomarker system for studying muscle, stem cells, and cancer in vivo
Nishijo, K., Hosoyama, T., Bjornson, C. R. R., Schaffer, B. S., Prajapati, S. I., Bahadur, A. N., Hansen, M. S. T., Blandford, M. C., McCleish, A. T., Rubin, B. P., et al. (2009) · The FASEB Journal · doi:10.1096/fj.08-128116 · Cited by 132 · see citing works
Cell-autonomous Notch activity maintains the temporal specification potential of skeletal muscle stem cells
Mourikis, P., Gopalakrishnan, S., Sambasivan, R., & Tajbakhsh, S. (2012) · Development · doi:10.1242/dev.084756 · Cited by 132 · cited 1× · see citing works
“Active Notch signaling is required for the maintenance of quiescence [95,96] but is antagonized by excessive levels of TGFβdependent pSmad3 activity [48].”
Background
Chromosome-specific nonrandom sister chromatid segregation during stem-cell division
Yadlapalli, S., & Yamashita, Y. M. (2013) · Nature · doi:10.1038/nature12106 · Cited by 131 · cited 1× · see citing works
“While Pax7HI satellite cells performing TDSS may represent an enduring stem cell subpopulation, work in the male germline shows that non-random sister chromatid segregation is often interrupted and without a clear proliferative or differentiation phenotype, questioning its ability to truly protect against errors in DN…”
Background
Calcitonin Receptor Signaling Inhibits Muscle Stem Cells from Escaping the Quiescent State and the Niche
Yamaguchi, M., Watanabe, Y., Ohtani, T., Uezumi, A., Mikami, N., Nakamura, M., Sato, T., Ikawa, M., Hoshino, M., Tsuchida, K., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.08.083 · Cited by 124 · cited 1× · see citing works
“Calcitonin receptor, a G-protein-coupled receptor (GPCR), suppressed emergence from the niche in a cAMP-dependent manner [98].”
Background
Prevention of Muscle Aging by Myofiber-Associated Satellite Cell Transplantation
Hall, J. K., Banks, G. B., Chamberlain, J. S., & Olwin, B. B. (2010) · Science Translational Medicine · doi:10.1126/scitranslmed.3001081 · Cited by 116 · cited 1× · see citing works
“Functional repopulation assays verified the capacity of satellite cells for long-term self-renewal over serial rounds of regeneration but also observed disparity with regard to repopulation efficiency [26,27].”
Background
Different autonomous myogenic cell populations revealed by ablation of Myf5-expressing cells during mouse embryogenesis
Gensch, N., Borchardt, T., Schneider, A., Riethmacher, D., & Braun, T. W. (2008) · Development · doi:10.1242/dev.019331 · Cited by 113 · see citing works
Slow-dividing satellite cells retain long-term self-renewal ability in adult muscle
Ono, Y., Masuda, S., Nam, H.-S., Benezra, R., Miyagoe‐Suzuki, Y., & Takeda, S. (2012) · Journal of Cell Science · doi:10.1242/jcs.096198 · Cited by 109 · cited 1× · see citing works
“The functional implications are significant, as cycling activity is inversely correlated to long-term self-renewal potential with age and through telomere shortening [60,90,91].”
Background
Myoblasts transferred to the limbs of embryos are committed to specific fibre fates
DiMario, J. X., Fernyak, S. E., & Stockdale, F. E. (1993) · Nature · doi:10.1038/362165a0 · Cited by 106 · cited 1× · see citing works
“Although several studies have described behavioral diversity on the basis of myofiber type association [28,29] or embryological origin, including those derived from craniofacial and extraocular muscles [30,31], we focus on satellite cells of somitic origin that reside in the limb.”
Background
Autonomous Extracellular Matrix Remodeling Controls a Progressive Adaptation in Muscle Stem Cell Regenerative Capacity during Development
Tierney, M. T., Gromova, A., Sesillo, F. B., Sala, D., Spenlé, C., Orend, G., & Sacco, A. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.072 · Cited by 98 · cited 1× · see citing works
“Autonomous ECM remodeling underlies distinct stem cell functionalities observed between fetal satellite cell precursors and their adult counterparts, regulating their regenerative potential in a stage-specific manner [94].”
BackgroundSelf-citation
Muscle satellite cell proliferation and association: new insights from myofiber time-lapse imaging
Siegel, A. L., Kuhlmann, P., & Cornelison, D. (2011) · Skeletal Muscle · doi:10.1186/2044-5040-1-7 · Cited by 82 · cited 1× · see citing works
“Intravital imaging experiments have observed apical-basal division events in vivo less frequently than has been reported on isolated single myofibers [22,53].”
Background
Numb is required to prevent p53-dependent senescence following skeletal muscle injury
Le Roux, I., Konge, J., Le Cam, L., Flamant, P., & Tajbakhsh, S. (2015) · Nature Communications · doi:10.1038/ncomms9528 · Cited by 81 · cited 1× · see citing works
“Although Numb-deficient satellite cells exhibit myostatin-dependent proliferative defects [36], Numb is also able to prevent p53-dependent senescence during muscle repair [37].”
Background
Cell Adhesion Geometry Regulates Non-Random DNA Segregation and Asymmetric Cell Fates in Mouse Skeletal Muscle Stem Cells
Yennek, S., Burute, M., Théry, M., & Tajbakhsh, S. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.04.016 · Cited by 81 · cited 1× · see citing works
“Cell adhesion regulates DNA segregation and satellite cell fate during asymmetric division in situ and in vitro [35,51,52]; thus, monitoring satellite cell division dynamics within their native microenvironment is of critical importance.”
Background
Extraocular muscle satellite cells are high performance myo-engines retaining efficient regenerative capacity in dystrophin deficiency
Stuelsatz, P., Shearer, A. M., Li, Y., Muir, L. A., Ieronimakis, N. M., Shen, Q. W., Kirillova, I., & Yablonka‐Reuveni, Z. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.08.035 · Cited by 79 · cited 1× · see citing works
“Although several studies have described behavioral diversity on the basis of myofiber type association [28,29] or embryological origin, including those derived from craniofacial and extraocular muscles [30,31], we focus on satellite cells of somitic origin that reside in the limb.”
Background
Cell Competition Modifies Adult Stem Cell and Tissue Population Dynamics in a JAK-STAT-Dependent Manner
Kolahgar, G., Suijkerbuijk, S. J. E., Kuciński, I., Poirier, E. Z., Mansour, S., Simons, B. D., & Piddini, E. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.06.010 · Cited by 76 · cited 1× · see citing works
“These findings do not rule out intrinsic factors as a contributing variable, especially in pathological circumstances, as genetic perturbations and environmental disruption can lead to non-neutral competition and altered fitness [58,59].”
Background
MyoD-expressing progenitors are essential for skeletal myogenesis and satellite cell development
Wood, W. M., Etemad, S. A., Yamamoto, M., & Goldhamer, D. J. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.09.012 · Cited by 71 · cited 1× · see citing works
“Ablation of Myod1+ cells abruptly halts myofiber formation during primary myogenesis and eliminates Pax7+ cells by fetal stages [89].”
Background
Muscle Stem Cell Fate Is Controlled by the Cell-Polarity Protein Scrib
Ono, Y., Urata, Y., Goto, S., Nakagawa, S., Humbert, P. O., Li, T., & Zammit, P. S. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.01.045 · Cited by 59 · cited 1× · see citing works
“Another member of the cell polarity complex, Scrib, is upregulated during satellite cell activation and also asymmetrically distributed to the progenitor-like daughter cell [41].”
Background
Numb-deficient satellite cells have regeneration and proliferation defects
George, R. M., Biressi, S., Beres, B. J., Rogers, E., Mulia, A. K., Allen, R. E., Rawls, A., Rando, T. A., & Wilson‐Rawls, J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1311628110 · Cited by 55 · cited 1× · see citing works
“Although Numb-deficient satellite cells exhibit myostatin-dependent proliferative defects [36], Numb is also able to prevent p53-dependent senescence during muscle repair [37].”
Background
Two distinct muscle progenitor populations coexist throughout amniote development
Picard, C. A., & Marcelle, C. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.10.018 · Cited by 36 · cited 1× · see citing works
“Behavioral heterogeneity emerges quickly in satellite cell precursors, given the differences in proliferative rate observed during embryonic myogenesis [84].”
Background
Slow-dividing satellite cells retain long-term self-renewal ability in adult muscle
Ono, Y., Masuda, S., Nam, H.-S., Benezra, R., Miyagoe‐Suzuki, Y., & Takeda, S. (2012) · Development · doi:10.1242/dev.080978 · Cited by 26 · see citing works

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Sorted by citations

Single-cell sequencing reveals dissociation-induced gene expression in tissue subpopulations
van den Brink, S. C., Sage, F., Vértesy, Á., Spanjaard, B., Peterson-Maduro, J., Baron, C. S., Robin, C., & van Oudenaarden, A. (2017) · Nature Methods · doi:10.1038/nmeth.4437 · Cited by 1,072 · see citing works
Function of the myogenic regulatory factors Myf5, MyoD, Myogenin and MRF4 in skeletal muscle, satellite cells and regenerative myogenesis
Zammit, P. S. (2017) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2017.11.011 · Cited by 887 · see citing works
Control of satellite cell function in muscle regeneration and its disruption in ageing
Sousa-Victor, P., García-Prat, L., & Muñoz-Cánoves, P. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00421-2 · Cited by 476 · see citing works
Perspectives on skeletal muscle stem cells
Relaix, F., Bencze, M., Borok, M. J., Vartanian, A. D., Gattazzo, F., Mademtzoglou, D., Perez-Diaz, S., Prola, A., Fernandez, P. C. R., Rotini, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20760-6 · Cited by 389 · see citing works
Single-cell analysis of the muscle stem cell hierarchy identifies heterotypic communication signals involved in skeletal muscle regeneration
De Micheli, A. J., Laurilliard, E. J., Heinke, C. L., Ravichandran, H., Fraczek, P., Soueid-Baumgarten, S., De Vlaminck, I., Elemento, O., & Cosgrove, B. D. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.067 · Cited by 373 · see citing works
ERBB3 and NGFR mark a distinct skeletal muscle progenitor cell in human development and hPSCs
Hicks, M. R., Hiserodt, J., Paras, K. I., Fujiwara, W., Eskin, A., Jan, M., Xi, H., Young, C. S., Evseenko, D. A., Nelson, S. F., et al. (2017) · Nature Cell Biology · doi:10.1038/s41556-017-0010-2 · Cited by 194 · see citing works
Tumor cell dormancy
Gomis, R. R., & Gawrzak, S. (2016) · Molecular Oncology · doi:10.1016/j.molonc.2016.09.009 · Cited by 190 · see citing works
A Human Skeletal Muscle Atlas Identifies the Trajectories of Stem and Progenitor Cells across Development and from Human Pluripotent Stem Cells
Xi, H., Langerman, J., Sabri, S., Chien, P., Young, C. S., Younesi, S., Hicks, M. R., Gonzalez, K. M., Fujiwara, W., Marzi, J., et al. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.04.017 · Cited by 156 · see citing works
“In vivo, mouse SMPCs contribute to muscle establishment and growth, whereas SCs in mature muscles are typically quiescent and enter the cell cycle in the event of injury (Tierney and Sacco, 2016).”
Crosstalk between YAP/TAZ and Notch Signaling
Totaro, A., Castellan, M., Biagio, D. D., & Piccolo, S. (2018) · Trends in Cell Biology · doi:10.1016/j.tcb.2018.03.001 · Cited by 163 · see citing works
“differentiate to fuse with each other or to pre-existing myofibers, as such those regenerating the muscle or mediating hypertrophy [70].”
Background
Functionally heterogeneous human satellite cells identified by single cell RNA sequencing
Barruet, E., Garcia, S. M., Striedinger, K., Wu, J., Lee, S., Byrnes, L. E., Wong, A., Sun, X., Tamaki, S. J., Brack, A. S., et al. (2020) · eLife · doi:10.7554/elife.51576 · Cited by 137 · see citing works
Notch1 and Notch2 Coordinately Regulate Stem Cell Function in the Quiescent and Activated States of Muscle Satellite Cells
Fujimaki, S., Seko, D., Kitajima, Y., Yoshioka, K., Tsuchiya, Y., Masuda, S., & Ono, Y. (2017) · Stem Cells · doi:10.1002/stem.2743 · Cited by 112 · see citing works
Satellite cells in ageing: use it or lose it
Chen, W., Datzkiw, D., & Rudnicki, M. A. (2020) · Open Biology · doi:10.1098/rsob.200048 · Cited by 116 · see citing works
“The satellite cell population maintains a level of functional heterogeneity, with subpopulations of satellite cells mounting differential responses depending on environmental stimuli [113,114].”
Background
Short‐term disuse promotes fatty acid infiltration into skeletal muscle
Pagano, A. F., Brioche, T., Arc-Chagnaud, C., Demangel, R., Chopard, A., & Py, G. (2017) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1002/jcsm.12259 · Cited by 99 · see citing works
Gasdermin D-mediated metabolic crosstalk promotes tissue repair
Chi, Z., Chen, S., Yang, D., Cui, W., Lu, Y., Wang, Z., Li, M., Yu, W., Zhang, J., Jiang, Y., et al. (2024) · Nature · doi:10.1038/s41586-024-08022-7 · Cited by 116 · see citing works
Induction of muscle stem cell quiescence by the secreted niche factor Oncostatin M
Sampath, S. C., Sampath, S. C., Ho, A. T. V., Corbel, S. Y., Millstone, J. D., Lamb, J. R., Walker, J. R., Kinzel, B., Schmedt, C., & Blau, H. M. (2018) · Nature Communications · doi:10.1038/s41467-018-03876-8 · Cited by 105 · see citing works
“2b), and adds to our knowledge of heterogeneity within the stem cell pool 43, 44 .”
Background
Estrogen Receptor β Controls Muscle Growth and Regeneration in Young Female Mice
Seko, D., Fujita, R., Kitajima, Y., Nakamura, K., Imai, Y., & Ono, Y. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.07.017 · Cited by 104 · see citing works
“With aging, the ability and the number of satellite cells to repair injured muscles is progressively impaired due to the alterations in both niche environment and cell-intrinsic mechanisms, which ultimately hinder skeletal muscle homeostasis (Kuang and Rudnicki, 2008; Tierney and Sacco, 2016).”
Background
The cell biology of quiescent yeast – a diversity of individual scenarios
Sagot, I., & Laporte, D. (2019) · Journal of Cell Science · doi:10.1242/jcs.213025 · Cited by 86 · see citing works
“This heterogeneity is markedly exemplified by muscle (Sutcu and Ricchetti, 2018; Tierney and Sacco, 2016) and hematopoietic (Nakamura-Ishizu et al.”
Background
Influence of Platelet-Rich and Platelet-Poor Plasma on Endogenous Mechanisms of Skeletal Muscle Repair/Regeneration
Chellini, F., Tani, A., Zecchi‐Orlandini, S., & Sassoli, C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030683 · Cited by 87 · see citing works
“There is evidence indicating that a small percentage of satellite cells are true stem cells, capable of self-renewal, thereby ensuring the replenishment of the basal pool of resident satellite cells that are recruitable in the case of muscle re-injury [16,23,24].”
Background
Exercise protects proliferative muscle satellite cells against exhaustion via the Igfbp7-Akt-mTOR axis
Chen, Z., Li, L., Wu, W., Liu, Z., Huang, Y., Yang, L., Luo, Q., Chen, J., Hou, Y., & Song, G. (2020) · Theranostics · doi:10.7150/thno.43577 · Cited by 85 · see citing works
“Additionally, we induced repeated muscle injuries in mice and observed the preserved number of Pax7+ cells in myofibers in exercise mice compared with their counterparts (Figure S2D, E).”
BackgroundMethodInfluential
Bioprocessing technology of muscle stem cells: implications for cultured meat
Guan, X., Zhou, J., Du, G., & Chen, J. (2021) · Trends in biotechnology · doi:10.1016/j.tibtech.2021.11.004 · Cited by 84 · see citing works
Exercise 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
Long acting GLP-1 analog liraglutide ameliorates skeletal muscle atrophy in rodents
Gurjar, A. A., Kushwaha, S., Chattopadhyay, S., Das, N., Pal, S., China, S. P., Kumar, H., Trivedi, A. K., Guha, R., Chattopadhyay, N., et al. (2020) · Metabolism · doi:10.1016/j.metabol.2019.154044 · Cited by 79 · see citing works
Defining and identifying satellite cell-opathies within muscular dystrophies and myopathies
Ganassi, M., Francesco Muntoni, A., & Zammit, P. S. (2021) · Experimental Cell Research · doi:10.1016/j.yexcr.2021.112906 · Cited by 80 · see citing works
Combined use of bone marrow-derived mesenchymal stromal cells (BM-MSCs) and platelet rich plasma (PRP) stimulates proliferation and differentiation of myoblasts in vitro: new therapeutic perspectives for skeletal muscle repair/regeneration
Sassoli, C., Vallone, L., Tani, A., Chellini, F., Nosi, D., & Zecchi‐Orlandini, S. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2792-3 · Cited by 70 · see citing works
Telocytes: An Emerging Component of Stem Cell Niche Microenvironment
Rosa, I., Marini, M., & Manetti, M. (2021) · Journal of Histochemistry & Cytochemistry · doi:10.1369/00221554211025489 · Cited by 69 · see citing works
Abnormalities in Skeletal Muscle Myogenesis, Growth, and Regeneration in Myotonic Dystrophy
André, L. M., Ausems, C. R. M., Wansink, D. G., & Wieringa, B. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00368 · Cited by 68 · see citing works
“This seemingly stochastic nature of fate adoption, which is associated with a high-degree of heterogeneity and plasticity of the satellite cell population in the natural environment of the muscle (203), is a complicating factor during the period that they regain proliferative activity as myoblasts.”
Single‐cell RNA‐seq reveals novel interaction between muscle satellite cells and fibro‐adipogenic progenitors mediated with FGF7 signalling
Ma, L., Meng, Y., An, Y., Han, P., Zhang, C., Yue, Y., Wen, C., Shi, X., Jin, J., Yang, G., et al. (2024) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13484 · Cited by 64 · see citing works
Mechanisms of muscle cells alterations and regeneration decline during aging
Chinvattanachot, G., Rivas, D., & Duque, G. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102589 · Cited by 59 · see citing works
“Furthermore, recent studies have described the heterogeneity within SC populations (Collins et al., 2005; Biressi and Rando, 2010; Tierney and Sacco, 2016).”
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 mouse Pax7 population is heterogeneous, with different populations of cells exhibiting different regenerative capacities (Cornelison, 2018; Tierney and Sacco, 2016).”
Background
Mechanisms of cooperative cell-cell interactions in skeletal muscle regeneration
Koike, H., Manabe, I., & Oishi, Y. (2022) · Inflammation and Regeneration · doi:10.1186/s41232-022-00234-6 · Cited by 55 · see citing works
“Muscle regeneration is achieved via the coordinated regulation of activation, proliferation, and differentiation of MuSCs [19, 20].”
Background
Inferring cell state by quantitative motility analysis reveals a dynamic state system and broken detailed balance
Kimmel, J. C., Chang, A. Y., Brack, A. S., & Marshall, W. F. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005927 · Cited by 54 · see citing works
“Heterogeneity within the MuSC population is well appreciated [11], suggesting that motility behavior may also be heterogenous during activation.”
Background
Sphingosine 1-Phosphate (S1P)/ S1P Receptor Signaling and Mechanotransduction: Implications for Intrinsic Tissue Repair/Regeneration
Sassoli, C., Pierucci, F., Zecchi‐Orlandini, S., & Meacci, E. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20225545 · Cited by 53 · see citing works
“There is evidence suggesting that, in parallel, a small percentage of satellite cells undergo to self-renewal thereby ensuring the replenishment of the basal pool of resident satellite cells, ready for responding to future demands [175].”
Background
Single cell sequencing maps skeletal muscle cellular diversity as disease severity increases in dystrophic mouse models
Saleh, K. K., Xi, H., Switzler, C., Skuratovsky, E., Romero, M. A., Chien, P., Gibbs, D. E., Gane, L., Hicks, M. R., Spencer, M. J., et al. (2022) · iScience · doi:10.1016/j.isci.2022.105415 · Cited by 51 · see citing works
“MuSC has been demonstrated to be a heterogeneous population influenced by microenvironment signaling (Motohashi and Asakura, 2014; Tierney and Sacco, 2016).”
Background
Morphological evidence for telocytes as stromal cells supporting satellite cell activation in eccentric contraction-induced skeletal muscle injury
Manetti, M., Tani, A., Rosa, I., Chellini, F., Squecco, R., Idrizaj, E., Zecchi‐Orlandini, S., Ibba‐Manneschi, L., & Sassoli, C. (2019) · Scientific Reports · doi:10.1038/s41598-019-51078-z · Cited by 52 · see citing works
Key concepts in muscle regeneration: muscle “cellular ecology” integrates a gestalt of cellular cross-talk, motility, and activity to remodel structure and restore function
Anderson, J. E. (2021) · European Journal of Applied Physiology · doi:10.1007/s00421-021-04865-4 · Cited by 52 · see citing works
“It is well established that muscle satellite cells are a heterogeneous population (Tierney and Sacco 2016) that is regulated to maintain quiescence (Subramaniam et al.”
Background
The application of bone marrow mesenchymal stem cells and biomaterials in skeletal muscle regeneration
Wang, Y., Wang, D., Guo, Y.-C., Liu, J., & Pan, J. (2020) · Regenerative Therapy · doi:10.1016/j.reth.2020.11.002 · Cited by 50 · see citing works
“Although some scholars have believed that satellite cells were able to replace the injured skeletal muscle fibers and keep cell pools in stable states [35], whether satellite cells have enough ability to promote skeletal muscle regeneration is not clear.”
Background
Deep Convolutional and Recurrent Neural Networks for Cell Motility Discrimination and Prediction
Kimmel, J. C., Brack, A. S., & Marshall, W. F. (2019) · IEEE Transactions on Computational Biology and Bioinformatics · doi:10.1109/tcbb.2019.2919307 · Cited by 49 · see citing works
“Heterogeneous ﬁtness for regeneration within the MuSC pool is well appreciated [16], and analysis of heterogeneous motility behaviors may provide an additional lens through which to decompose different MuSC phenotypes.”
Background
Single Stem Cell Imaging and Analysis Reveals Telomere Length Differences in Diseased Human and Mouse Skeletal Muscles
Tichy, E. D., Sidibe, D. K., Tierney, M. T., Stec, M. J., Sharifi‐Sanjani, M., Hosalkar, H. S., Mubarak, S. J., Johnson, F. B., Sacco, A., & Mourkioti, F. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.08.003 · Cited by 48 · see citing works
“Over the last few years it became widely accepted that MuSCs are a heterogeneous population (Ono et al., 2010; Tierney and Sacco, 2016).”
BackgroundSelf-citation
The mechanosensitive ion channel PIEZO1 promotes satellite cell function in muscle regeneration
Hirano, K., Tsuchiya, M., Shiomi, A., Takabayashi, S., Suzuki, M., Ishikawa, Y., Kawano, Y., Takabayashi, Y., Nishikawa, K., Nagao, K., et al. (2022) · Life Science Alliance · doi:10.26508/lsa.202201783 · Cited by 47 · see citing works
“The importance of MuSCs is further demonstrated by the fact that their impaired function is closely associated with sarcopenia and a class ofmuscle diseases (i.e., muscular dystrophy) (Dumont et al, 2015; Tierney & Sacco, 2016; Feige et al, 2018).”
Background
Transcriptional reprogramming of skeletal muscle stem cells by the niche environment
Lazure, F., Farouni, R., Sahinyan, K., Blackburn, D. M., Hernández-Corchado, A., Perron, G., Lu, T., Osakwe, A., Ragoussis, J., Crist, C. G., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36265-x · Cited by 50 · see citing works
Macrophage Involvement in Aging-Associated Skeletal Muscle Regeneration
Cui, C., Ferrucci, L., & Gorospe, M. (2023) · Cells · doi:10.3390/cells12091214 · Cited by 47 · see citing works
“SCs are the sole myogenic adult stem cells in skeletal muscle [25,26] and they are located between the sarcolemma and the basal lamina in each myofiber [27].”
Background
Timing Is Everything—The High Sensitivity of Avian Satellite Cells to Thermal Conditions During Embryonic and Posthatch Periods
Halevy, O. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00235 · Cited by 46 · see citing works
Technical requirements for cultured meat production: a review
Ramani, S., Ko, D., Kim, B., Cho, C., Kim, W., Jo, C., Lee, C., Kang, J., Hur, S. J., & Park, S. (2021) · Journal of Animal Science and Technology · doi:10.5187/jast.2021.e45 · Cited by 45 · see citing works
Beyond Calories: Individual Metabolic and Hormonal Adaptations Driving Variability in Weight Management—A State-of-the-Art Narrative Review
Theodorakis, N., Kreouzi, M., Pappas, A., & Nikolaou, M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252413438 · Cited by 43 · see citing works
Murine muscle stem cell response to perturbations of the neuromuscular junction are attenuated with aging
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
A novel approach for the isolation and long-term expansion of pure satellite cells based on ice-cold treatment
Benedetti, A., Cera, G., Meo, D. D., Villani, C., Bouché, M., & Lozanoska‐Ochser, B. (2021) · Skeletal Muscle · doi:10.1186/s13395-021-00261-w · Cited by 41 · see citing works
“Unlike the fast-dividing SCs, which have a limited ability to form secondary myogenic colonies after passage and instead undergo differentiation, the slow dividing SCs form secondary myogenic colonies when passaged (23,24).”
Background
Satellite cell‐specific ablation of Cdon impairs integrin activation, FGF signalling, and muscle regeneration
Bae, J., Hong, M., Jeong, H., Kim, H., Lee, S., Ryu, D., Bae, G., Cho, S. C., Lee, Y., Krauss, R. S., et al. (2020) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12563 · Cited by 39 · see citing works
“This is followed by expansion and differentiation of progenitor cells, coinciding with decreased Pax7 and increased Myogenin expression.(3) The ability of satellite cells to proliferate and return to quiescence is critical for the maintenance of the stem cell population.”
Background
Empowering Muscle Stem Cells for the Treatment of Duchenne Muscular Dystrophy
Filippelli, R. L., & Chang, N. C. (2021) · Cells Tissues Organs · doi:10.1159/000514305 · Cited by 35 · see citing works
“…muscle is dependent on a heterogenous population of satellite cells consisting of satellite stem cells and committed progenitor cells, with distinct functional roles and varied cell fate potential for self-renewal and commitment to differentiation [Biressi and Rando, 2010; Tierney and Sacco, 2016].”
BackgroundInfluential
Rejuvenating 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
A robust Pax7EGFP mouse that enables the visualization of dynamic behaviors of muscle stem cells
Tichy, E. D., Sidibe, D. K., Greer, C. D., Oyster, N. M., Rompolas, P., Rosenthal, N. A., Blau, H. M., & Mourkioti, F. (2018) · Skeletal Muscle · doi:10.1186/s13395-018-0169-7 · Cited by 33 · see citing works
Visualization of PAX7 protein dynamics in muscle satellite cells in a YFP knock-in-mouse line
Kitajima, Y., & Ono, Y. (2018) · Skeletal Muscle · doi:10.1186/s13395-018-0174-x · Cited by 32 · see citing works
FNDC1 is a myokine that promotes myogenesis and muscle regeneration
Zhang, R. X., Zhai, Y. Y., Ding, R., Huang, J. H., Shi, X., Liu, H., Liu, X. P., Zhang, J. F., Lu, J. F., Zhang, Z., et al. (2024) · The EMBO Journal · doi:10.1038/s44318-024-00285-0 · Cited by 28 · see citing works
“…an ordered series of cellular events including satellite cell activation, migration, alignment, adhesion, and membrane fusion, generating new multinucleated myo ﬁ bers or fusing with existing ones, which is critical for the repair of damaged myo ﬁ bres (Park et al, 2016; Tierney and Sacco, 2016).”
Loss of heterogeneity, quiescence, and differentiation in muscle stem cells
Sutcu, H. H., & Ricchetti, M. (2018) · Stem Cell Investigation · doi:10.21037/sci.2018.03.02 · Cited by 28 · see citing works
“The origins and the function of this heterogeneity are not clear, but it is believed that it endows satellite cells with a level of plasticity that is necessary to adapt to different needs of skeletal muscle growth, homeostasis, regeneration (3), and resistance to unfavorable conditions.”
Background
Current Understanding of the Pathways Involved in Adult Stem and Progenitor Cell Migration for Tissue Homeostasis and Repair
Goichberg, P. (2016) · Stem Cell Reviews and Reports · doi:10.1007/s12015-016-9663-7 · Cited by 26 · see citing works
Muscle Stem Cells Give Rise to Rhabdomyosarcomas in a Severe Mouse Model of Duchenne Muscular Dystrophy
Sesillo, F. B., Fox, D. J., & Sacco, A. (2019) · Cell Reports · doi:10.1016/j.celrep.2018.12.089 · Cited by 26 · see citing works
“Skeletal muscle is a low-turnover tissue maintained by muscle stem cells (MuSCs), which are required for tissue growth and repair (Brack and Rando, 2012; Tierney and Sacco, 2016).”
BackgroundSelf-citation
Muscle Satellite Cell Heterogeneity: Does Embryonic Origin Matter?
Rodríguez-Outeiriño, L., Hernández‐Torres, F., Acuña, F. R.-D., Matías-Valiente, L., Sánchez–Fernández, C., Franco, D., & Aránega, A. E. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.750534 · Cited by 26 · see citing works
“The process by which SCs emerge from their quiescent status and enter the myogenic program is well established; however, several studies have highlighted the existence of different SC responses related to their performance during the muscle repair process (Tierney and Sacco, 2016; Cornelison, 2018).”
Background
Thermal stress affects proliferation and differentiation of turkey satellite cells through the mTOR/S6K pathway in a growth-dependent manner
Xu, J., Strasburg, G., Reed, K., & Velleman, S. G. (2022) · PLoS ONE · doi:10.1371/journal.pone.0262576 · Cited by 24 · see citing works
Nitric oxide treatment attenuates muscle atrophy during hind limb suspension in mice
Anderson, J. E., Zhu, A., & Mizuno, T. M. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2017.12.021 · Cited by 25 · see citing works
Quiescence, an individual journey
Sagot, I., & Laporte, D. (2019) · Current Genetics · doi:10.1007/s00294-018-00928-w · Cited by 24 · see citing works
Separation of functionally divergent muscle precursor cell populations from porcine juvenile muscles by discontinuous Percoll density gradient centrifugation
Miersch, C., Stange, K., & Röntgen, M. (2018) · BMC Cell Biology · doi:10.1186/s12860-018-0156-1 · Cited by 24 · see citing works
“These cells are pre-quiescent and pass through distinct cell states during myogenic commitment accompanied by a characteristic time-dependent myogenic marker expression profile [36, 59, 60].”
Background
Recovery in the Myogenic Program of Congenital Myotonic Dystrophy Myoblasts after Excision of the Expanded (CTG)n Repeat
André, L. M., van Cruchten, R. T. P., Willemse, M. P., Bezstarosti, K., Demmers, J., van Agtmaal, E. L., Wansink, D. G., & Wieringa, B. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20225685 · Cited by 22 · see citing works
“The onset of differentiation and gradual transition of muscle progenitor cells and the subsequent fusion for the formation of terminally differentiated myofibers is controlled by an intricate network of factors and machinery for the control of transcription, RNA processing and translation [2], and the turnover of gene…”
Background
Muscle stem cells get a new look: Dynamic cellular projections as sensors of the stem cell niche
Krauss, R. S., & Kann, A. P. (2023) · BioEssays · doi:10.1002/bies.202200249 · Cited by 20 · see citing works
“In homeostatic adult muscle, MuSCs comprise a functionally heterogeneous population.[18,19] Various means have been used to purify MuSC subpopulations with stem cell activity which exceeds that of the remaining MuSC population (this is generally assessed by ability to engraft into injured muscle and repopulate the ste…”
BackgroundMethod
Sexual dimorphisms in skeletal muscle: current concepts and research horizons
Emmert, M. E., Emmert, A. S., Goh, Q., & Cornwall, R. (2024) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00529.2023 · Cited by 22 · see citing works
Sestrins regulate muscle stem cell metabolic homeostasis
Yang, B. A., Castor‐Macias, J. A., Fraczek, P. M., Cornett, A. M., Brown, L. A., Kim, M., Brooks, S. V., Lombaert, I. M. A., Lee, J. H., & Aguilar, C. A. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.07.014 · Cited by 20 · see citing works
“After activation, myogenic progenitors (myoblasts) fusewiththemselvesandexistingmyofibers to regenerate and repair damaged tissue (Tierney and Sacco, 2016).”
Background
Improved Satellite Cell Proliferation Induced by L-Carnosine Benefits Muscle Growth of Pigs in Part through Activation of the Akt/mTOR/S6K Signaling Pathway
Liu, Y., Shen, W., Liu, T., Mosenthin, R., Bao, Y., Chen, P., Hao, W., Zhao, L., Zhang, J., Ji, C., et al. (2022) · Agriculture · doi:10.3390/agriculture12070988 · Cited by 20 · see citing works
Avian Satellite Cell Plasticity
Jankowski, M., Mozdziak, P. E., Petitte, J. N., Kulus, M., & Kempisty, B. (2020) · Animals · doi:10.3390/ani10081322 · Cited by 19 · see citing works
“Furthermore, they consist of cells that only react in the need of muscle remodeling or reconstruction of significant scale [6].”
Background
Effect of Temperature and Selection for Growth on Intracellular Lipid Accumulation and Adipogenic Gene Expression in Turkey Pectoralis Major Muscle Satellite Cells
Xu, J., Strasburg, G. M., Reed, K. M., & Velleman, S. G. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.667814 · Cited by 18 · see citing works
“Satellite cells (SCs) are a heterogenous stem cell population (Schultz, 1974; Kuang et al., 2007; Biressi and Rando, 2010; Smith et al., 2013; Tierney and Sacco, 2016), functioning in hypertrophic growth of post-hatch muscle (Moss and Leblond, 1971; Cardiasis and Cooper, 1975).”
Background
Cell Therapy for Anal Sphincter Incontinence: Where Do We Stand?
Balaphas, A., Meyer, J., Meier, R. P. H., Liot, É., Buchs, N. C., Roche, B., Toso, C., Bühler, L. H., Gonelle‐Gispert, C., & Ris, F. (2021) · Cells · doi:10.3390/cells10082086 · Cited by 17 · see citing works
“Satellite cells have typical features such as the expression of the transcription factor PAX7 (Figure 1) [104] but there is currently a lack of standardization in the nomenclature and characterization of other myogenic cells [120].”
Background
Image Based Tumor Cells Identification Using Convolutional Neural Network and Auto Encoders
Wajeed, M. A., & Sreenivasulu, V. (2019) · Traitement du signal · doi:10.18280/ts.360510 · Cited by 16 · see citing works
“, the layers of AI models can locate an appropriate portrayal of info pictures as far as visual element maps [23, 24].”
Background
SIX1 and SIX4 homeoproteins regulate PAX7+ progenitor cell properties during fetal epaxial myogenesis
Wurmser, M., Chaverot, N., Madani, R., Sakai, H., Négroni, E., Demignon, J., Saintpierre, B., Mouly, V., Amthor, H., Tapscott, S. J., et al. (2020) · Development · doi:10.1242/dev.185975 · Cited by 16 · see citing works
“5) compared with adult activated (2-month-old) PAX7+ cells (Tierney and Sacco, 2016).”
Background
Bioenergetics mechanisms regulating muscle stem cell self-renewal commitment and function
Abreu, P. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.04.036 · Cited by 16 · see citing works
Healthy skeletal muscle aging: The role of satellite cells, somatic mutations and exercise
Franco, I., Fernandez‐Gonzalo, R., Vrtačnik, P., Lundberg, T. R., Eriksson, M., & Gustafsson, T. P. (2019) · International review of cytology · doi:10.1016/bs.ircmb.2019.03.003 · Cited by 17 · see citing works
Metabolic regulation in adult and aging skeletal muscle stem cellsPreprint
Sartorelli, V., & Ciuffoli, V. (2024) · Genes & Development · doi:10.1101/gad.352277.124 · Cited by 18 · see citing works
“Several observations suggest that the heterogeneity of MuSCs and muscle progenitors (Tierney and Sacco 2016) may be linked to their metabolic states.”
Quality Control of Stem Cell-Based Cultured Meat According to Specific Differentiation Abilities
Naraoka, Y., Mabuchi, Y., Kiuchi, M., Kumagai, K., Hisamatsu, D., Yoneyama, Y., Takebe, T., & Akazawa, C. (2024) · Cells · doi:10.3390/cells13020135 · Cited by 14 · see citing works
“Understanding the characteristics of cells in bovine tissue and predicting their differentiation potential would help regulate meat quality and lead to sustainable meat production technology.”
Background
The Combination of Lactoferrin and Creatine Ameliorates Muscle Decay in a Sarcopenia Murine Model
Wu, W., Guo, X., Qu, T., Huang, Y., Tao, J., He, J., Wang, X., Luo, J., An, P., Zhu, Y., et al. (2024) · Nutrients · doi:10.3390/nu16121958 · Cited by 14 · see citing works
“The mTOR signaling pathway activates Mtor , which in turn activates its downstream e ﬀ ectors ribosomal protein S6 kinase (S6K) and eIF4E-binding proteins (4E-BPs) to enhance mRNA translation and protein synthesis. mTOR signaling pathway activates Mtor which in turn activates its downstream…”
BackgroundInfluential
Could we also be regenerative superheroes, like salamanders?
Dall’Agnese, A., & Puri, P. (2016) · BioEssays · doi:10.1002/bies.201600015 · Cited by 14 · see citing works
“Upon skeletal muscle injury, mice and humans share with axolotls and paedamorphic newts similar skeletal muscle regeneration mechanisms that rely on muscle stem cells, rather than myofiber de-differentiation, for repair [22, 24, 59].”
BackgroundInfluential
Stem cells in skeletal muscle growth and regeneration in amniotes and teleosts: Emerging themes
Ruparelia, A. A., Ratnayake, D., & Currie, P. D. (2019) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.365 · Cited by 15 · see citing works
“While the source of this inherent heterogeneity still remains elusive, it is suggested that it conveys satellite cells plasticity such that they are able to adapt to fulfill the varying needs that emerge during growth, homeostasis and repair (Tierney & Sacco, 2016).”
Background
From gut to glutes: The critical role of niche signals in the maintenance and renewal of adult stem cells
Trentesaux, C., Striedinger, K., Pomerantz, J. H., & Klein, O. D. (2020) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2020.01.004 · Cited by 15 · see citing works
Transcriptomics, regulatory syntax, and enhancer identification in mesoderm-induced ESCs at single-cell resolution
Khateb, M., Perovanović, J., Ko, K. D., Jiang, K., Feng, X., Acevedo-Luna, N., Chal, J., Ciuffoli, V., Genzor, P., Simone, J., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111219 · Cited by 14 · see citing works
“Muscle stem cells (MuSCs), which are required for muscle growth and regeneration (Brack and Rando, 2012; Yin et al., 2013; Tierney and Sacco, 2016; Evano and Tajbakhsh, 2018; Fuchs and Blau, 2020; Relaix et al., 2021), can be generated from mouse or human pluripotent stem cells by either treatment with defined molecul…”
Background
Myogenic Satellite Cells: Biological Milieu and Possible Clinical Applications
Said, R. S., Mustafa, A., Asfour, H. A., & Shaqour, E. I. (2016) · Pakistan Journal of Biological Sciences · doi:10.3923/pjbs.2017.1.11 · Cited by 13 · see citing works
In vitro-generated human muscle reserve cells are heterogeneous for Pax7 with distinct molecular states and metabolic profiles
Bouche, A., Borner, B., Richard, C., Grand, Y., Hannouche, D., & Laumonier, T. (2023) · Stem Cell Research & Therapy · doi:10.1186/s13287-023-03483-5 · Cited by 11 · see citing works
“Through RNA sequencing, it was described that quiescent murine MuSCs are molecularly and phenotypically heterogeneous [12, 13].”
Background
Human IL6 stimulates bovine satellite cell proliferation through a Signal transducer and activator of transcription 3 (STAT3)-dependent mechanism
Brandt, A. M., Kania, J., Reinholt, B. M., & Johnson, S. (2017) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2017.08.004 · Cited by 11 · see citing works
Temperature and Growth Selection Effects on Proliferation, Differentiation, and Adipogenic Potential of Turkey Myogenic Satellite Cells Through Frizzled-7-Mediated Wnt Planar Cell Polarity Pathway
Xu, J., Strasburg, G. M., Reed, K. M., & Velleman, S. G. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.892887 · Cited by 11 · see citing works
“Satellite cells comprise a heterogeneous population (Schultz, 1974; Kuang et al., 2007; Tierney and Sacco, 2016) of multipotential stem cells (Asakura et al.”
Background
Culture substrate stiffness impacts human myoblast contractility-dependent proliferation and nuclear envelope wrinkling
Nguyen, J., Wang, L., Lei, W., Hu, Y., Gulati, N., Chávez-Madero, C., Ahn, H., Ginsberg, H. J., Krawetz, R. J., Brandt, M., et al. (2024) · Journal of Cell Science · doi:10.1242/jcs.261666 · Cited by 10 · see citing works
SRSF1 Is Crucial for Maintaining Satellite Cell Homeostasis During Skeletal Muscle Growth and Regeneration
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Authors: Tierney, M. T., & Sacco, A.
Affiliations: Sanford Burnham Prebys Medical Discovery Institute (US)
Corresponding author: Sacco, Alessandra
ORCID: Tierney, Matthew T.
Sacco, Alessandra
Venue: Trends in Cell Biology
Publisher: Elsevier BV
Published: 2016-06
Volume: 26
Issue: 6
Pages: 434-444
ISSN: 0962-8924 (ISSN-L)
DOI: 10.1016/j.tcb.2016.02.004
PMC: PMC4877266
OpenAlex: W2291414087
Cited by: 151
References: 108
Citations by year: 2026: 13 · 2025: 12 · 2024: 16 · 2023: 9 · 2022: 12 · 2021: 18 · 2020: 21 · 2019: 13 · 2018: 18 · 2017: 13 · 2016: 6
FWCI: 1.50
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Trends in Cell Biology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Arthritis and Musculoskeletal and Skin Diseases (F31AR065923, R01AR064873, P30AR061303, R03AR063328)
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, cellular heterogeneity, skeletal muscle homeostasis, muscle stem cells, self-renewal, cell differentiation, quiescence, myofiber fusion, cell fate, developmental origins
MeSH terms: Cell Self Renewal, Animals, Cell Compartmentation, Homeostasis, Humans, Models, Biological, Muscle, Skeletal, Satellite Cells, Skeletal Muscle

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Satellite Cell Heterogeneity in Skeletal Muscle Homeostasis

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