Muscle Satellite Cells Are Primed for Myogenesis but Maintain Quiescence with Sequestration of Myf5 mRNA Targeted by microRNA-31 in mRNP Granules
Open accessAbstract
Regeneration of adult tissues depends on stem cells that are primed to enter a differentiation program, while remaining quiescent. How these two characteristics can be reconciled is exemplified by skeletal muscle in which the majority of quiescent satellite cells transcribe the myogenic determination gene Myf5, without activating the myogenic program. We show that Myf5 mRNA, together with microRNA-31, which regulates its translation, is sequestered in mRNP granules present in the quiescent satellite cell. In activated satellite cells, mRNP granules are dissociated, relative levels of miR-31 are reduced, and Myf5 protein accumulates, which initially requires translation, but not transcription. Conditions that promote the continued presence of mRNP granules delay the onset of myogenesis. Manipulation of miR-31 levels affects satellite cell differentiation ex vivo and muscle regeneration in vivo. We therefore propose a model in which posttranscriptional mechanisms hold quiescent stem cells poised to enter a tissue-specific differentiation program.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Myf5 mRNA and its regulatory miRNA miR-31 are sequestered in mRNP granules in quiescent MuSCs.
“the Myf5 (myogenic factor 5) mRNA and its regulatory miRNA miR-31 were found to be sequestered in mRNA ribonucleoprotein particle (mRNP) granules in quiescent MuSCs91.”
From Molecular regulation of stem cell quiescence (2013) · cites this paper as [91]
Cites
Silencing of microRNAs in vivo with ‘antagomirs’
Krützfeldt, J., Rajewsky, N., Braich, R., Rajeev, K. G., Tuschl, T., Manoharan, M., & Stoffel, M. (2005) · Nature · doi:10.1038/nature04303 · Cited by 3,949 · see citing works
Pax7 Is Required for the Specification of Myogenic Satellite Cells
Seale, P., Sabourin, L. A., Girgis-Gabardo, A., Mansouri, A., Gruß, P., & Rudnicki, M. A. (2000) · Cell · doi:10.1016/s0092-8674(00)00066-0 · Cited by 2,345 · see citing works
Eukaryotic stress granules: the ins and outs of translation.
Buchan, J., & Parker, R. (2009) · Molecules and Cells · doi:10.1016/j.molcel.2009.11.020 · Cited by 1,517 · see citing works
Asymmetric self-renewal and commitment of satellite stem cells in muscle
Kuang, S., Kuroda, K., Le Grand, F., & Rudnicki, M. A. (2007) · Cell · doi:10.1016/j.cell.2007.03.044 · Cited by 1,449 · cited 1× · see citing works
“, 2006); however, unlike their embryonic counterparts, more than 95% have already activated the Myf5 gene in the course of their history (Kuang et al., 2007), indicating that they had entered the myogenic program.”
BackgroundRelief of microRNA-Mediated Translational Repression in Human Cells Subjected to Stress
Bhattacharyya, S. N., Habermacher, R., Martiné, U., Closs, E. I., & Filipowicz, W. (2006) · Cell · doi:10.1016/j.cell.2006.04.031 · Cited by 1,332 · see citing works
MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies
Liu, J., Valencia-Sanchez, M. A., Hannon, G. J., & Parker, R. (2005) · Nature Cell Biology · doi:10.1038/ncb1274 · Cited by 1,234 · see citing works
A Pax3/Pax7-dependent population of skeletal muscle progenitor cells
Relaix, F., Rocancourt, D., Mansouri, A., & BUCKINGHAM, M. E. (2005) · Nature · doi:10.1038/nature03594 · Cited by 1,167 · see citing works
Self-citationDirect Isolation of Satellite Cells for Skeletal Muscle Regeneration
Montarras, D., Morgan, J., Collins, C., Relaix, F., Zaffran, S., Cumano, A., Partridge, T., & Buckingham, M. (2005) · Science · doi:10.1126/science.1114758 · Cited by 1,100 · see citing works
Self-citationExpression of Cd34 and Myf5 Defines the Majority of Quiescent Adult Skeletal Muscle Satellite Cells
Beauchamp, J. R., Heslop, L., Yu, D. S., Tajbakhsh, S., Kelly, R. G., Wernig, A., BUCKINGHAM, M. E., Partridge, T. A., & Zammit, P. S. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.6.1221 · Cited by 917 · see citing works
Self-citationMovement of Eukaryotic mRNAs Between Polysomes and Cytoplasmic Processing Bodies
Brengues, M., Teixeira, D., & Parker, R. (2005) · Science · doi:10.1126/science.1115791 · Cited by 796 · see citing works
Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells
Relaix, F., Montarras, D., Zaffran, S., Gayraud-Morel, B., Rocancourt, D., Tajbakhsh, S., Mansouri, A., Cumano, A., & BUCKINGHAM, M. E. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200508044 · Cited by 736 · see citing works
Self-citationMammalian Stress Granules and Processing Bodies
Kedersha, N., & Anderson, P. (2007) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(07)31005-7 · Cited by 664 · see citing works
Translation Repression in Human Cells by MicroRNA-Induced Gene Silencing Requires RCK/p54
Chu, C., & Rana, T. M. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040210 · Cited by 521 · see citing works
Muddashetty, R. S., Nalavadi, V. C., Gross, C., Yao, X., Xing, L., Laur, O., Warren, S. T., & Bassell, G. J. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.05.006 · Cited by 364 · see citing works
MicroRNA control of muscle development and disease
Williams, A. H., Liu, N., van Rooij, E., & Olson, E. N. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.01.029 · Cited by 347 · see citing works
Muscle stem cell behavior is modified by microRNA-27 regulation of Pax3 expression
Crist, C. G., Montarras, D., Pallafacchina, G., Rocancourt, D., Cumano, A., Conway, S. J., & BUCKINGHAM, M. E. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900210106 · Cited by 298 · see citing works
Self-citationmiRNA in situ hybridization in formaldehyde and EDC–fixed tissues
Pena, J., Sohn-Lee, C., Rouhanifard, S. H., Ludwig, J., Hafner, M., Mihailovic, A., Lim, C., Holoch, D., Berninger, P., Zavolan, M., et al. (2009) · Nature Methods · doi:10.1038/nmeth.1294 · Cited by 292 · see citing works
Pallafacchina, G., François, S., Regnault, B., Czarny, B., Dive, V., Cumano, A., Montarras, D., & BUCKINGHAM, M. E. (2009) · Stem Cell Research · doi:10.1016/j.scr.2009.10.003 · Cited by 278 · see citing works
Self-citationIn vivo degradation of RNA polymerase II largest subunit triggered by alpha-amanitin
Nguyen, V. T. (1996) · Nucleic Acids Research · doi:10.1093/nar/24.15.2924 · Cited by 257 · see citing works
A role for the myogenic determination gene Myf5 in adult regenerative myogenesis
Gayraud-Morel, B., Chrétien, F. C., Flamant, P., Gomès, D., Zammit, P. S., & Tajbakhsh, S. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.08.059 · Cited by 240 · see citing works
Immunoprecipitation of mRNA-protein complexes
Peritz, T., Zeng, F., Kannanayakal, T. J., Kilk, K., Eiríksdóttir, E., Langel, Ü., & Eberwine, J. H. (2006) · Nature Protocols · doi:10.1038/nprot.2006.82 · Cited by 240 · see citing works
Ustanina, S., Carvajal, J. J., Rigby, P. W. J., & Braun, T. W. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0736 · Cited by 160 · see citing works
miR‐31 modulates dystrophin expression: new implications for Duchenne muscular dystrophy therapy
Cacchiarelli, D., Incitti, T., Martone, J., Cesana, M., Cazzella, V., Santini, T., Sthandier, O., & Bozzoni, I. (2011) · EMBO Reports · doi:10.1038/embor.2010.208 · Cited by 151 · see citing works
A C-terminal silencing domain in GW182 is essential for miRNA function
Eulálio, A., Helms, S., Fritzsch, C., Fauser, M., & Izaurralde, E. (2009) · RNA · doi:10.1261/rna.1605509 · Cited by 130 · see citing works
BUCKINGHAM, M. E., & Montarras, D. (2008) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2008.06.005 · Cited by 115 · see citing works
Self-citationCultured myf5 null and myoD null muscle precursor cells display distinct growth defects
Montarras, D., Lindon, C., Pinset, C., & Domeyne, P. (2000) · Biology of the Cell · doi:10.1016/s0248-4900(00)01110-2 · Cited by 72 · see citing works
Self-citationDaubas, P., Crist, C. G., Bajard, L., Relaix, F., Pecnard, E., Rocancourt, D., & BUCKINGHAM, M. E. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.11.031 · Cited by 24 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Sarcopenia: Aging-Related Loss of Muscle Mass and Function
Larsson, L., Degens, H., Li, M., Salviati, L., Lee, Y. I., Thompson, W., Kirkland, J. L., & Sandri, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00061.2017 · Cited by 1,797 · see citing works
Molecular regulation of stem cell quiescence
Cheung, T. H., & Rando, T. A. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3591 · Cited by 1,148 · see citing works
Zammit, P. S. (2017) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2017.11.011 · Cited by 887 · see citing works
Satellite Cells and Skeletal Muscle Regeneration
Dumont, N. A., Bentzinger, C. F., Sincennes, M., & Rudnicki, M. A. (2015) · Comprehensive Physiology · doi:10.1002/cphy.c140068 · Cited by 719 · see citing works
The myogenic regulatory factors, determinants of muscle development, cell identity and regeneration
Hernández‐Hernández, J. M., García-González, E. G., Brun, C. E., & Rudnicki, M. A. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.11.010 · Cited by 669 · see citing works
Gene Regulatory Networks and Transcriptional Mechanisms that Control Myogenesis
BUCKINGHAM, M. E., & Rigby, P. W. J. (2014) · Developmental Cell · doi:10.1016/j.devcel.2013.12.020 · Cited by 662 · see citing works
Self-citationRyall, J. G., Dell’Orso, S., Derfoul, A., Juan, A., Zare, H., Feng, X., Clermont, D., Koulnis, M., Gutierrez-Cruz, G., Fulco, M., et al. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2014.12.004 · Cited by 575 · see citing works
Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging
Liu, L., Cheung, T. H., Charville, G. W., Hurgo, B. M. C., Leavitt, T., Shih, J., Brunet, A., & Rando, T. A. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.05.043 · Cited by 544 · see citing works
Intrinsic and extrinsic mechanisms regulating satellite cell function
Dumont, N. A., Wang, Y. X., & Rudnicki, M. A. (2015) · Development · doi:10.1242/dev.114223 · Cited by 491 · 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
Muscle-specific microRNAs in skeletal muscle development
Horak, M., Novák, J., & Vašků, J. B. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.12.013 · 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
Zanou, N., & Gailly, P. L. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1330-4 · Cited by 361 · see citing works
Adult-specific functions of animal microRNAs
Sun, K., & Lai, E. C. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3471 · Cited by 333 · see citing works
Molecular circuitry of stem cell fate in skeletal muscle regeneration, ageing and disease
Almada, A. E., & Wagers, A. J. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.7 · Cited by 315 · see citing works
Stem Cell Quiescence: Dynamism, Restraint, and Cellular Idling
van Velthoven, C. T. J., & Rando, T. A. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.01.001 · Cited by 313 · see citing works
Adult stem cells at work: regenerating skeletal muscle
Schmidt, M., Schüler, S. C., Hüttner, S. S., von Eyß, B., & von Maltzahn, J. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03093-6 · Cited by 313 · see citing works
Cellular Mechanisms and Regulation of Quiescence
Marescal, O., & Cheeseman, I. M. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.09.029 · Cited by 284 · see citing works
Myogenic regulatory factors: The orchestrators of myogenesis after 30 years of discovery
Asfour, H. A., Allouh, M. Z., & Said, R. S. (2018) · Experimental Biology and Medicine · doi:10.1177/1535370217749494 · Cited by 257 · see citing works
Muscle satellite cell heterogeneity and self-renewal
Motohashi, N., & Asakura, A. (2014) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2014.00001 · Cited by 251 · see citing works
PAX3 and PAX7 as upstream regulators of myogenesis
BUCKINGHAM, M. E., & Relaix, F. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.09.017 · Cited by 247 · see citing works
Self-citationZismanov, 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
Self-citationDell'Orso, S., Juan, A. H., Ko, K.-D., Naz, F., Perovanovic, J., Gutierrez-Cruz, G., Feng, X., & Sartorelli, V. (2019) · Development · doi:10.1242/dev.174177 · Cited by 243 · see citing works
Regulation of adult stem cell quiescence and its functions in the maintenance of tissue integrity
de Morrée, A., & Rando, T. A. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00568-6 · Cited by 243 · see citing works
Transcriptional profiling of quiescent muscle stem cells in vivo
van Velthoven, C. T. J., de Morree, A., Egner, I. M., Brett, J. O., & Rando, T. A. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.037 · Cited by 235 · see citing works
Orienting Muscle Stem Cells for Regeneration in Homeostasis, Aging, and Disease
Feige, P., Brun, C. E., Ritso, M., & Rudnicki, M. A. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.10.006 · Cited by 227 · see citing works
Oki, T., Nishimura, K., Kitaura, J., Togami, K., Maehara, A., Izawa, K., Sakaue-Sawano, A., Niida, A., Miyano, S., Aburatani, H., et al. (2014) · Scientific Reports · doi:10.1038/srep04012 · Cited by 216 · see citing works
Regulation of Muscle Stem Cell Functions: A Focus on the p38 MAPK Signaling Pathway
Segalés, J., Perdiguero, E., & Muñoz‐Cánoves, P. (2016) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2016.00091 · Cited by 209 · see citing works
Lying low but ready for action: the quiescent muscle satellite cell
Montarras, D., L’honoré, A., & BUCKINGHAM, M. E. (2013) · FEBS Journal · doi:10.1111/febs.12372 · Cited by 199 · see citing works
Self-citationCombination of inflammation-related cytokines promotes long-term muscle stem cell expansion
Fu, X., Xiao, J., Wei, Y., Li, S., Liu, Y., Yin, J., Sun, K., Sun, H., Wang, H., Zhang, Z., et al. (2015) · Cell Research · doi:10.1038/cr.2015.58 · Cited by 196 · see citing works
Stem cell activation in skeletal muscle regeneration
Fu, X., Wang, H.-T., & Hu, P. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1819-5 · Cited by 161 · see citing works
Singh, K., & Dilworth, F. J. (2013) · FEBS Journal · doi:10.1111/febs.12188 · Cited by 186 · see citing works
Lv, C., Li, F., Li, X., Tian, Y., Zhang, Y., Sheng, X., Song, Y., Meng, Q., Yuan, S., Luan, L., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01059-5 · Cited by 182 · see citing works
Chang, N. C., & Rudnicki, M. A. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416022-4.00006-8 · Cited by 180 · see citing works
Wnt4 from the Niche Controls the Mechano-Properties and Quiescent State of Muscle Stem Cells
Eliazer, S., Muncie, J. M., Christensen, J., Sun, X., D’Urso, R. S., Weaver, V. M., & Brack, A. S. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.08.007 · Cited by 171 · see citing works
“To confirm that niche-derived Wnt4 regulated SC quiescence, we stained muscle sections with DDX6, a marker of mRNP granules, that is lost when SCs break quiescence (Crist et al., 2012; Goel et al., 2017).”
BackgroundRoles of nonmyogenic mesenchymal progenitors in pathogenesis and regeneration of skeletal muscle
Uezumi, A., Ikemoto‐Uezumi, M., & Tsuchida, K. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00068 · Cited by 163 · see citing works
Mechanisms, Hallmarks, and Implications of Stem Cell Quiescence
Cho, I., Lui, P. P., Obajdin, J., Riccio, F., Stroukov, W., Willis, T. L., Spagnoli, F. M., & Watt, F. M. (2019) · Stem Cell Reports · doi:10.1016/j.stemcr.2019.05.012 · Cited by 163 · see citing works
MicroRNA in myogenesis and muscle atrophy
Wang, X. H. (2013) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32835f81b9 · Cited by 157 · see citing works
Chang, N. C., Sincennes, M., Chevalier, F. P., Brun, C. E., Lacaria, M., Segalés, J., Muñoz‐Cánoves, P., Ming, H., & Rudnicki, M. A. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.03.022 · Cited by 154 · see citing works
Stem cell quiescence: the challenging path to activation
Urbán, N., & Cheung, T. H. (2021) · Development · doi:10.1242/dev.165084 · Cited by 154 · see citing works
Satellite Cell Heterogeneity in Skeletal Muscle Homeostasis
Tierney, M. T., & Sacco, A. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.02.004 · Cited by 151 · see citing works
Niche Cadherins Control the Quiescence-to-Activation Transition in Muscle Stem Cells
Goel, A. J., Rieder, M.-K., Arnold, H.-H., Radice, G. L., & Krauss, R. S. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.102 · Cited by 146 · see citing works
Post-transcriptional regulation of satellite cell quiescence by TTP-mediated mRNA decay
Hausburg, M. A., Doles, J. D., Clement, S. L., Cadwallader, A. B., Hall, M. N., Blackshear, P. J., Lykke‐Andersen, J., & Olwin, B. B. (2015) · eLife · doi:10.7554/elife.03390 · Cited by 136 · see citing works
Wang, Y. X., Dumont, N. A., & Rudnicki, M. A. (2014) · Journal of Cell Science · doi:10.1242/jcs.151209 · Cited by 125 · see citing works
MicroRNAs in skeletal muscle biology and exercise adaptation
Kirby, T. J., & McCarthy, J. J. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.07.004 · Cited by 123 · see citing works
Proteostatic and Metabolic Control of Stemness
García‐Prat, L., Sousa‐Victor, P., & Muñoz‐Cánoves, P. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.04.011 · Cited by 123 · see citing works
Distinct contextual roles for Notch signalling in skeletal muscle stem cells
Mourikis, P., & Tajbakhsh, S. (2014) · BMC Developmental Biology · doi:10.1186/1471-213x-14-2 · Cited by 120 · see citing works
Molecular mechanisms of skeletal muscle development, regeneration, and osteogenic conversion
Endo, T. (2015) · Bone · doi:10.1016/j.bone.2015.02.028 · Cited by 117 · see citing works
Engineered skeletal muscles for disease modeling and drug discovery
Wang, J., Khodabukus, A., Rao, L., VanDusen, K. W., Abutaleb, N. O., & Bursac, N. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.119416 · Cited by 117 · 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
Dek Modulates Global Intron Retention during Muscle Stem Cells Quiescence Exit
Yue, L., Wan, R., Luan, S., Zeng, W., & Cheung, T. H. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.05.006 · Cited by 115 · see citing works
Concise Review: Epigenetic Regulation of Myogenesis in Health and Disease
Sincennes, M., Brun, C. E., & Rudnicki, M. A. (2016) · Stem Cells Translational Medicine · doi:10.5966/sctm.2015-0266 · Cited by 114 · see citing works
microRNAs in skeletal muscle development
Mok, G. F., Lozano-Velasco, E., & Münsterberg, A. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.10.032 · Cited by 111 · see citing works
Moncaut, N., Rigby, P. W. J., & Carvajal, J. J. (2013) · FEBS Journal · doi:10.1111/febs.12379 · Cited by 110 · see citing works
Non-coding RNAs in muscle differentiation and musculoskeletal disease
Ballarino, M., Morlando, M., Fatica, A., & Bozzoni, I. (2016) · Journal of Clinical Investigation · doi:10.1172/jci84419 · Cited by 110 · see citing works
Rong, S., Wang, L., Peng, Z., Liao, Y., Li, D., Yang, X., Nussler, A. K., Liu, L., Bao, W., & Yang, W. Q. (2020) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12536 · Cited by 104 · see citing works
Function and regulation of microRNA‐31 in development and disease
Stepicheva, N. A., & Song, J. L. (2016) · Molecular Reproduction and Development · doi:10.1002/mrd.22678 · Cited by 103 · see citing works
Noncoding RNAs, Emerging Regulators of Skeletal Muscle Development and Diseases
Nie, M., Deng, Z., Liu, J., & Wang, D. (2015) · BioMed Research International · doi:10.1155/2015/676575 · Cited by 102 · see citing works
miR-195/497 induce postnatal quiescence of skeletal muscle stem cells
Sato, T., Yamamoto, T., & Sehara‐Fujisawa, A. (2014) · Nature Communications · doi:10.1038/ncomms5597 · Cited by 101 · see citing works
MicroRNA Profile and Adaptive Response to Exercise Training: A Review
Domańska-Senderowska, D., Laguette, M.-J. N., Jegier, A., Cięszczyk, P., September, A. V., & Brzeziańska‐Lasota, E. (2019) · International Journal of Sports Medicine · doi:10.1055/a-0824-4813 · Cited by 98 · see citing works
Skeletal muscle in health and disease
Morgan, J., & Partridge, T. (2020) · Disease Models & Mechanisms · doi:10.1242/dmm.042192 · Cited by 62 · see citing works
Li, N., Nakauka‐Ddamba, A., Tobias, J. W., Jensen, S. T., & Lengner, C. J. (2016) · Gastroenterology · doi:10.1053/j.gastro.2016.04.049 · Cited by 94 · see citing works
Ballarino, M., Cazzella, V., D’Andrea, D., Grassi, L., Bisceglie, L., Cipriano, A., Santini, T., Pinnarò, C., Morlando, M., Tramontano, A. L., et al. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.01394-14 · Cited by 93 · see citing works
Epigenetic regulation of satellite cell fate during skeletal muscle regeneration
Massenet, J., Gardner, E., Chazaud, B., & Dilworth, F. J. (2021) · Skeletal Muscle · doi:10.1186/s13395-020-00259-w · Cited by 94 · see citing works
The Many Roles of Macrophages in Skeletal Muscle Injury and Repair
Wang, X., & Zhou, L. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.952249 · Cited by 97 · see citing works
Staufen1 inhibits MyoD translation to actively maintain muscle stem cell quiescence
de Morrée, A., van Velthoven, C. T. J., Gan, Q., Salvi, J. S., Klein, J. D. D., Akimenko, I., Quarta, M., Biressi, S., & Rando, T. A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1708725114 · Cited by 91 · see citing works
Quiescence Entry, Maintenance, and Exit in Adult Stem Cells
Mohammad, K., Dakik, P., Medkour, Y., Mitrofanova, D., & Titorenko, V. I. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092158 · Cited by 90 · see citing works
Comparative myogenesis in teleosts and mammals
Rossi, G., & Messina, G. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1604-5 · Cited by 81 · see citing works
Mega roles of microRNAs in regulation of skeletal muscle health and disease
Sharma, M. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00239 · Cited by 87 · see citing works
Judson, R. N., Quarta, M., Oudhoff, M. J., Soliman, H. S., Yi, L., Chang, C. K., Loi, G., Werff, R. V., Cait, A., Hamer, M., et al. (2018) · Cell stem cell · doi:10.1016/j.stem.2017.12.010 · Cited by 86 · see citing works
Lovett, J. A. C., Durcan, P., & Myburgh, K. H. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01149 · Cited by 85 · see citing works
Joly, W., Chartier, A., Rojas‐Ríos, P., Busseau, I., & Simonelig, M. (2013) · Stem Cell Reports · doi:10.1016/j.stemcr.2013.09.007 · Cited by 82 · see citing works
Switching roles: the functional plasticity of adult tissue stem cells
Wabik, A., & Jones, P. H. (2015) · The EMBO Journal · doi:10.15252/embj.201490386 · Cited by 81 · see citing works
Hierarchy and Plasticity in the Intestinal Stem Cell Compartment
Yousefi, M., Li, L., & Lengner, C. J. (2017) · Trends in Cell Biology · doi:10.1016/j.tcb.2017.06.006 · Cited by 81 · see citing works
Transient HIF2A inhibition promotes satellite cell proliferation and muscle regeneration
Xie, L., Yin, A., Nichenko, A. S., Beedle, A. M., Call, J. A., & Yin, H. (2018) · Journal of Clinical Investigation · doi:10.1172/jci96208 · Cited by 81 · see citing works
Regulation of Skeletal Muscle by microRNAs
Diniz, G. P., & Wang, D. (2016) · Comprehensive physiology · doi:10.1002/cphy.c150041 · Cited by 81 · see citing works
Kann, A. P., Hung, M., Wang, W., Nguyen, J., Gilbert, P. M., Wu, Z., & Krauss, R. S. (2022) · Cell stem cell · doi:10.1016/j.stem.2022.04.016 · Cited by 78 · see citing works
Zhao, Y., Chen, M., Lian, D., Li, Y., Li, Y., Wang, J., Deng, S., Yu, K., & Lian, Z. (2019) · Cells · doi:10.3390/cells8090988 · Cited by 77 · see citing works
Muscle Stem Cell Quiescence: Controlling Stemness by Staying Asleep
Ancel, S., Stuelsatz, P., & Feige, J. N. (2021) · Trends in Cell Biology · doi:10.1016/j.tcb.2021.02.006 · Cited by 75 · see citing works
microRNAs: Modulators of the underlying pathophysiology of sarcopenia?
Brown, D. M., & Goljanek‐Whysall, K. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.08.007 · 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
Noncoding RNAs in the regulation of skeletal muscle biology in health and disease
Simionescu-Bankston, A., & Kumar, A. (2016) · Journal of Molecular Medicine · doi:10.1007/s00109-016-1443-y · Cited by 74 · see citing works
miR-186 Inhibits Muscle Cell Differentiation through Myogenin Regulation
Antoniou, A., Mastroyiannopoulos, N. P., Uney, J. B., & Phylactou, L. A. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.507343 · Cited by 74 · see citing works
The 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
Lin, Y.-F., Xiao, M.-H., Chen, H.-X., Meng, Y., Zhao, N., Yang, L., Tang, H., Wang, J.-L., Liu, X., Zhu, Y., et al. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1767-y · Cited by 73 · see citing works
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 · see citing works
Zhou, Z., Shirakawa, T., Ohbo, K., Sada, A., Wu, Q., Hasegawa, K., Saba, R., & Saga, Y. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.05.014 · Cited by 68 · see citing works
The role of microRNAs in skeletal muscle health and disease
McCarthy, J. J. (2015) · Frontiers in bioscience · doi:10.2741/4298 · Cited by 67 · see citing works
Regulation of myogenic gene expression
Vicente‐García, C., Hernández‐Camacho, J. D., & Carvajal, J. J. (2022) · Experimental Cell Research · doi:10.1016/j.yexcr.2022.113299 · Cited by 65 · see citing works
Novel RNA-binding activity of MYF5 enhancesCcnd1/Cyclin D1mRNA translation during myogenesis
Panda, A. C., Abdelmohsen, K., Martindale, J. L., Germanio, C. D., Yang, X., Grammatikakis, I., Noh, J. H., Zhang, Y., Lehrmann, E., Dudekula, D. B., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw023 · Cited by 65 · see citing works
Regulation of Muscle Growth in Early Postnatal Life in a Swine Model
Rudar, M., Fiorotto, M., & Davis, T. (2018) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-020518-115130 · Cited by 50 · see citing works
Cho, D. S., & Doles, J. D. (2017) · Gene · doi:10.1016/j.gene.2017.09.014 · Cited by 64 · see citing works
mTOR controls embryonic and adult myogenesis via mTORC1
Rion, N., Castets, P., Lin, S., Enderle, L., Reinhard, J. R., Eickhorst, C., & Rüegg, M. A. (2019) · Development · doi:10.1242/dev.172460 · Cited by 64 · see citing works
Fochi, 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
Moresi, V., Marroncelli, N., Coletti, D., & Adamo, S. (2015) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2015.01.002 · Cited by 63 · see citing works
Muscle Satellite Cells: Exploring the Basic Biology to Rule Them
de Almeida, C., Fernandes, S., Ribeiro, A. F., Okamoto, O. K., & Vainzof, M. (2016) · Stem Cells International · doi:10.1155/2016/1078686 · Cited by 62 · see citing works
Kearney, M., Cooper, P., Smith, A. J. F., & Duncan, H. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00311 · Cited by 59 · see citing works
Berti, F., Nogueira, J. M., Wöhrle, S., Sobreira, D. R., Hawrot, K., & Dietrich, S. (2015) · Journal of Anatomy · doi:10.1111/joa.12353 · Cited by 59 · see citing works
Shi, D., & Grifone, R. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.738978 · Cited by 58 · see citing works
Epigenetic modifications in muscle regeneration and progression of Duchenne muscular dystrophy
Rugowska, A., Starosta, A., & Konieczny, P. (2021) · Clinical Epigenetics · doi:10.1186/s13148-021-01001-z · Cited by 58 · see citing works
- Authors
- Crist, C. G., Montarras, D., & Buckingham, M.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Buckingham, Margaret
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2012-07
- Volume
- 11
- Issue
- 1
- Pages
- 118-126
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- OpenAlex
- W1993085259
- Cited by
- 346
- References
- 27
- Citations by year
- 2026: 13 · 2025: 16 · 2024: 19 · 2023: 16 · 2022: 28 · 2021: 26 · 2020: 26 · 2019: 30 · 2018: 28 · 2017: 28 · 2016: 31 · 2015: 38 · 2014: 18 · 2013: 21 · 2012: 6
- FWCI
- 10.66
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell stem cell (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- satellite cells, Myf5, miR-31, post-transcriptional regulation, stem cell quiescence, myogenesis, skeletal muscle regeneration, translation repression
- MeSH terms
- Animals, Cell Differentiation, Cytoplasmic Granules, Gene Expression Regulation, Regeneration, Ribonucleoproteins, RNA, Messenger, Muscle Development, Satellite Cells, Skeletal Muscle, MicroRNAs, Mice, Myogenic Regulatory Factor 5
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 ›
Are you an author, or do you see a problem with this page? Request a review