Scilight Press

Author Information

Received: 29 Jul 2024 | Revised: 30 Sep 2024 | Accepted: 20 Oct 2024 | Published: 30 Oct 2024

Abstract

Graphical Abstract

Image Viewer

Open in new tab

Download Image

Keywords

Satellite Cells | Asymmetric Division | Skeletal Muscle Regeneration | Muscle Aging

References 

• 1.
  Relaix, F.; Bencze, M.; Borok, M.J.; Der Vartanian, A.; Gattazzo, F.; Mademtzoglou, D.; Perez-Diaz, S.; Prola, A.; Reyes-Fernandez, P.C.; Rotini, A.; et al. Perspectives on Skeletal Muscle Stem Cells. Nat. Commun. 2021, 12, 692. https://doi.org/10.1038/s41467-020-20760-6.
• 2.
  Fu, X.; Zhuang, C.; Hu, P. Regulation of Muscle Stem Cell Fate. Cell Regen. 2022, 11, 40. https://doi.org/10.1186/s13619-022-00142-7.
• 3.
  Sousa-Victor, P.; García-Prat, L.; Muñoz-Cánoves, P. Control of Satellite Cell Function in Muscle Regeneration and Its Disruption in Ageing. Nat. Rev. Mol. Cell Biol. 2022, 23, 204–226. https://doi.org/10.1038/s41580-021-00421-2.
• 4.
  Peng, J.; Han, L.; Liu, B.; Song, J.; Wang, Y.; Wang, K.; Guo, Q.; Liu, X.; Li, Y.; Zhang, J.; et al. Gli1 Marks a Sentinel Muscle Stem Cell Population for Muscle Regeneration. Nat. Commun. 2023, 14, 6993. https://doi.org/10.1038/s41467-023-42837-8.
• 5.
  AMPKα2 Is a Skeletal Muscle Stem Cell Intrinsic Regulator of Myonuclear Accretion–PubMed. Available online: https://pubmed.ncbi.nlm.nih.gov/38077152/ (accessed on 19 March 2024).
• 6.
  Hong, X.; Isern, J.; Campanario, S.; Perdiguero, E.; Ramírez-Pardo, I.; Segalés, J.; Hernansanz-Agustín, P.; Curtabbi, A.; Deryagin, O.; Pollán, A.; et al. Mitochondrial Dynamics Maintain Muscle Stem Cell Regenerative Competence throughout Adult Life by Regulating Metabolism and Mitophagy. Cell Stem Cell 2022, 29, 1298–1314.e10. https://doi.org/10.1016/j.stem.2022.07.009.
• 7.
  Sastourné-Arrey, Q.; Mathieu, M.; Contreras, X.; Monferran, S.; Bourlier, V.; Gil-Ortega, M.; Murphy, E.; Laurens, C.; Varin, A.; Guissard, C.; et al. Adipose Tissue Is a Source of Regenerative Cells That Augment the Repair of Skeletal Muscle after Injury. Nat. Commun. 2023, 14, 80. https://doi.org/10.1038/s41467-022-35524-7.
• 8.
  Wosczyna, M.N.; Konishi, C.T.; Perez Carbajal, E.E.; Wang, T.T.; Walsh, R.A.; Gan, Q.; Wagner, M.W.; Rando, T.A. Mesenchymal Stromal Cells Are Required for Regeneration and Homeostatic Maintenance of Skeletal Muscle. Cell Rep. 2019, 27, 2029–2035.e5. https://doi.org/10.1016/j.celrep.2019.04.074.
• 9.
  Lukjanenko, L.; Karaz, S.; Stuelsatz, P.; Gurriaran-Rodriguez, U.; Michaud, J.; Dammone, G.; Sizzano, F.; Mashinchian, O.; Ancel, S.; Migliavacca, E.; et al. Aging Disrupts Muscle Stem Cell Function by Impairing Matricellular WISP1 Secretion from Fibro-Adipogenic Progenitors. Cell Stem Cell 2019, 24, 433–446.e7. https://doi.org/10.1016/j.stem.2018.12.014.
• 10.
  Shang, M.; Cappellesso, F.; Amorim, R.; Serneels, J.; Virga, F.; Eelen, G.; Mazzone, M. Macrophage-derived glutamine boosts satellite cells and muscle regeneration. Nature 2020, 587, 626–631.
• 11.
  Zhang, C.; Cheng, N.; Qiao, B.; Zhang, F.; Wu, J.; Liu, C.; Li, Y.; Du, J. Age-related Decline of Interferon-gamma Responses in Macrophage Impairs Satellite Cell Proliferation and Regeneration. J. Cachexia Sarcopenia Muscle 2020, 11, 1291–1305. https://doi.org/10.1002/jcsm.12584.
• 12.
  Southerland, K.W.; Xu, Y.; Peters, D.T.; Lin, X.; Wei, X.; Xiang, Y.; Fei, K.; Olivere, L.A.; Morowitz, J.M.; Otto, J.; et al. Skeletal Muscle Regeneration Failure in Ischemic-Damaged Limbs Is Associated with pro-Inflammatory Macrophages and Premature Differentiation of Satellite Cells. Genome Med. 2023, 15, 95. https://doi.org/10.1186/s13073-023-01250-y.
• 13.
  Burzyn, D.; Kuswanto, W.; Kolodin, D.; Shadrach, J.L.; Cerletti, M.; Jang, Y.; Sefik, E.; Tan, T.G.; Wagers, A.J.; Benoist, C.; et al. A Special Population of Regulatory T Cells Potentiates Muscle Repair. Cell 2013, 155, 1282–1295. https://doi.org/10.1016/j.cell.2013.10.054.
• 14.
  Becker, M.; Joseph, S.S.; Garcia-Carrizo, F.; Tom, R.Z.; Opaleva, D.; Serr, I.; Tschöp, M.H.; Schulz, T.J.; Hofmann, S.M.; Daniel, C. Regulatory T Cells Require IL6 Receptor Alpha Signaling to Control Skeletal Muscle Function and Regeneration. Cell Metab. 2023, 35, 1736–1751.e7. https://doi.org/10.1016/j.cmet.2023.08.010.
• 15.
  Seale, P.; Sabourin, L.A.; Girgis-Gabardo, A.; Mansouri, A.; Gruss, P.; Rudnicki, M.A. Pax7 Is Required for the Specification of Myogenic Satellite Cells. Cell 2000, 102, 777–786. https://doi.org/10.1016/S0092-8674(00)00066-0.
• 16.
  Sambasivan, R.; Yao, R.; Kissenpfennig, A.; Van Wittenberghe, L.; Paldi, A.; Gayraud-Morel, B.; Guenou, H.; Malissen, B.; Tajbakhsh, S.; Galy, A. Pax7-Expressing Satellite Cells Are Indispensable for Adult Skeletal Muscle Regeneration. Development 2011, 138, 4333–4333. https://doi.org/10.1242/dev.073601.
• 17.
  Saber, J.; Rudnicki, M.A. Carm1 and the Epigenetic Control of Stem Cell Function. Stem Cells Transl. Med. 2022, 11, 1143–1150. https://doi.org/10.1093/stcltm/szac068.
• 18.
  Davis, R.L.; Weintraub, H.; Lassar, A.B. Expression of a Single Transfected cDNA Converts Fibmblasts to Myoblasts. Cell 1987, 51, 987–1000.
• 19.
  Weintraub, H.; Tapscott, S.J.; Davis, R.L.; Thayer, M.J.; Adam, M.A.; Lassar, A.B.; Miller, A.D. Activation of Muscle-Specific Genes in Pigment, Nerve, Fat, Liver, and Fibroblast Cell Lines by Forced Expression of MyoD. Proc. Natl. Acad. Sci. USA 1989, 86, 5434–5438. https://doi.org/10.1073/pnas.86.14.5434.
• 20.
  Megeney, L.A.; Kablar, B.; Garrett, K.; Anderson, J.E.; Rudnicki, M.A. MyoD Is Required for Myogenic Stem Cell Function in Adult Skeletal Muscle. Genes. Dev. 1996, 10, 1173–1183. https://doi.org/10.1101/gad.10.10.1173.
• 21.
  Sabourin, L.A.; Girgis-Gabardo, A.; Seale, P.; Asakura, A.; Rudnicki, M.A. Reduced Differentiation Potential of Primary MyoD−/− Myogenic Cells Derived from Adult Skeletal Muscle. J. Cell Biol. 1999, 144, 631–643.
• 22.
  Chen, Y.-H.; Wang, Y.-H.; Chang, M.-Y.; Lin, C.-Y.; Weng, C.-W.; Westerfield, M.; Tsai, H.-J. Multiple Upstream Modules Regulate Zebrafish Myf5expression. BMC Dev. Biol. 2007, 7, 1. https://doi.org/10.1186/1471-213X-7-1.
• 23.
  Zhang, P.; Li, W.; Wang, L.; Liu, H.; Gong, J.; Wang, F.; Chen, X. Salidroside Inhibits Myogenesis by Modulating P-Smad3-Induced Myf5 Transcription. Front. Pharmacol. 2018, 9, 209. https://doi.org/10.3389/fphar.2018.00209.
• 24.
  Sato, T.; Rocancourt, D.; Marques, L.; Thorsteinsdóttir, S.; Buckingham, M. A Pax3/Dmrt2/Myf5 Regulatory Cascade Functions at the Onset of Myogenesis. PLoS Genet. 2010, 6, e1000897. https://doi.org/10.1371/journal.pgen.1000897.
• 25.
  Li, Q.; Zhu, X.; Yu, C.; Shang, L.; Li, R.; Wang, X.; Yang, Y.; Meng, J.; Kong, X. Case Report: A Novel Homozygous Mutation in MYF5 Due to Paternal Uniparental Isodisomy of Chromosome 12 in a Case of External Ophthalmoplegia With Rib and Vertebral Anomalies. Front. Genet. 2022, 12, 780363. https://doi.org/10.3389/fgene.2021.780363.
• 26.
  Doucet, C.; Gutierrez, G.J.; Lindon, C.; Lorca, T.; Lledo, G.; Pinset, C.; Coux, O. Multiple Phosphorylation Events Control Mitotic Degradation of the Muscle Transcription Factor Myf5. BMC Biochem. 2005, 6, 27. https://doi.org/10.1186/1471-2091-6-27.
• 27.
  Hadchouel, J.; Tajbakhsh, S.; Primig, M.; Chang, T.H.-T.; Daubas, P.; Rocancourt, D.; Buckingham, M. Modular Long-Range Regulation of Myf5 Reveals Unexpected Heterogeneity between Skeletal Muscles in the Mouse Embryo. Development 2000, 127, 4455–4467. https://doi.org/10.1242/dev.127.20.4455.
• 28.
  Ganassi, M.; Badodi, S.; Wanders, K.; Zammit, P.S.; Hughes, S.M. Myogenin Is an Essential Regulator of Adult Myofibre Growth and Muscle Stem Cell Homeostasis. eLife 2020, 9, e60445. https://doi.org/10.7554/eLife.60445.
• 29.
  Benavente-Diaz, M.; Comai, G.; Di Girolamo, D.; Langa, F.; Tajbakhsh, S. Dynamics of Myogenic Differentiation Using a Novel Myogenin Knock-in Reporter Mouse. Skelet. Muscle 2021, 11, 5. https://doi.org/10.1186/s13395-021-00260-x.
• 30.
  Lazure, F.; Blackburn, D.M.; Corchado, A.H.; Sahinyan, K.; Karam, N.; Sharanek, A.; Nguyen, D.; Lepper, C.; Najafabadi, H.S.; Perkins, T.J.; et al. Myf6/MRF4 Is a Myogenic Niche Regulator Required for the Maintenance of the Muscle Stem Cell Pool. EMBO Rep. 2020, 21, e49499. https://doi.org/10.15252/embr.201949499.
• 31.
  Shea, K.L.; Xiang, W.; LaPorta, V.S.; Licht, J.D.; Keller, C.; Basson, M.A.; Brack, A.S. Sprouty1 Regulates Reversible Quiescence of a Self-Renewing Adult Muscle Stem Cell Pool during Regeneration. Cell Stem Cell 2010, 6, 117–129. https://doi.org/10.1016/j.stem.2009.12.015.
• 32.
  Chakkalakal, J.V.; Jones, K.M.; Basson, M.A.; Brack, A.S. The Aged Niche Disrupts Muscle Stem Cell Quiescence. Nature 2012, 490, 355–360. https://doi.org/10.1038/nature11438.
• 33.
  Bigot, A.; Duddy, W.J.; Ouandaogo, Z.G.; Negroni, E.; Mariot, V.; Ghimbovschi, S.; Harmon, B.; Wielgosik, A.; Loiseau, C.; Devaney, J.; et al. Age-Associated Methylation Suppresses SPRY1, Leading to a Failure of Re-Quiescence and Loss of the Reserve Stem Cell Pool in Elderly Muscle. Cell Rep. 2015, 13, 1172–1182. https://doi.org/10.1016/j.celrep.2015.09.067.
• 34.
  Xie, L.; Yin, A.; Nichenko, A.S.; Beedle, A.M.; Call, J.A.; Yin, H. Transient HIF2A Inhibition Promotes Satellite Cell Proliferation and Muscle Regeneration. J. Clin. Investig. 2018, 128, 2339–2355. https://doi.org/10.1172/JCI96208.
• 35.
  Meng, J.; Lv, Z.; Chen, X.; Sun, C.; Jin, C.; Ding, K.; Chen, C. LBP1C-2 from Lycium Barbarum Maintains Skeletal Muscle Satellite Cell Pool by Interaction with FGFR1. iScience 2023, 26, 106573. https://doi.org/10.1016/j.isci.2023.106573.
• 36.
  Dumont, N.A.; Wang, Y.X.; Von Maltzahn, J.; Pasut, A.; Bentzinger, C.F.; Brun, C.E.; Rudnicki, M.A. Dystrophin expression in muscle stem cells regulates their polarity and asymmetric division. Nat. Med. 2015, 21, 1455–1463.
• 37.
  Conboy, I.M.; Rando, T.A. The Regulation of Notch Signaling Controls Satellite Cell Activation and Cell Fate Determination in Postnatal Myogenesis. Developmental Cell 2002, 3, 397–409.
• 38.
  Conboy, I.M.; Conboy, M.J.; Wagers, A.J.; Girma, E.R.; Weissman, I.L.; Rando, T.A. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005, 433, 760–764.
• 39.
  Servián-Morilla, E.; Takeuchi, H.; Lee, T.V.; Clarimon, J.; Mavillard, F.; Area-Gómez, E.; Rivas, E.; Nieto-González, J.L.; Rivero, M.C.; Cabrera, M.; et al. A POGLUT1 Mutation Causes a Muscular Dystrophy with Reduced Notch Signaling and Satellite Cell Loss. EMBO Mol. Med. 2016, 8, 1289–1309.
• 40.
  Baghdadi, M.B.; Firmino, J.; Soni, K.; Evano, B.; Di Girolamo, D.; Mourikis, P.; Tajbakhsh, S. Notch-induced miR-708 antagonizes satellite cell migration and maintains quiescence. Cell Stem Cell 2018, 23, 859–868. e5.
• 41.
  Wei, X.; Rigopoulos, A.; Lienhard, M.; Pöhle-Kronawitter, S.; Kotsaris, G.; Franke, J.; Stricker, S. Neurofibromin 1 controls metabolic balance and Notch-dependent quiescence of murine juvenile myogenic progenitors. Nat. Commun. 2024, 15, 1393.
• 42.
  Brack, A.S.; Conboy, M.J.; Roy, S.; Lee, M.; Kuo, C.J.; Keller, C.; Rando, T.A. Increased Wnt Signaling during Aging Alters Muscle Stem Cell Fate and Increases Fibrosis. Science 2007, 317, 807–810. https://doi.org/10.1126/science.1144090.
• 43.
  Brack, A.S.; Conboy, I.M.; Conboy, M.J.; Shen, J.; Rando, T.A. A Temporal Switch from Notch to Wnt Signaling in Muscle Stem Cells Is Necessary for Normal Adult Myogenesis. Cell Stem Cell 2008, 2, 50–59. https://doi.org/10.1016/j.stem.2007.10.006.
• 44.
  Le Grand, F.; Jones, A.E.; Seale, V.; Scimè, A.; Rudnicki, M.A. Wnt7a Activates the Planar Cell Polarity Pathway to Drive the Symmetric Expansion of Satellite Stem Cells. Cell Stem Cell 2009, 4, 535–547. https://doi.org/10.1016/j.stem.2009.03.013.
• 45.
  Carlson, M.E.; Hsu, M.; Conboy, I.M. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 2008, 454, 528–532.
• 46.
  Ge, X.; McFarlane, C.; Vajjala, A.; Lokireddy, S.; Ng, Z.H.; Tan, C.K.; Kambadur, R. Smad3 signaling is required for satellite cell function and myogenic differentiation of myoblasts. Cell Res. 2011, 21, 1591–1604.
• 47.
  Teng, H.; Zheng, J.; Liang, Y.; Zhao, J.; Yan, Y.; Li, S.; Tong, H. Podocan promoting skeletal muscle post‐injury regeneration by inhibiting TGF‐β signaling pathway. FASEB J. 2024, 38, e23502.
• 48.
  Rozo, M.; Li, L.; Fan, C.-M. Targeting Β1-Integrin Signaling Enhances Regeneration in Aged and Dystrophic Muscle in Mice. Nat. Med. 2016, 22, 889–896.
• 49.
  Feige, P.; Brun, C.E.; Ritso, M.; Rudnicki, M.A. Orienting muscle stem cells for regeneration in homeostasis, aging, and disease. Cell Stem Cell 2018, 23, 653–664.
• 50.
  Troy, A.; Cadwallader, A.B.; Fedorov, Y.; Tyner, K.; Tanaka, K.K.; Olwin, B.B. Coordination of Satellite Cell Activation and Self-Renewal by Par-Complex-Dependent Asymmetric Activation of P38α/β MAPK. Cell Stem Cell 2012, 11, 541–553. https://doi.org/10.1016/j.stem.2012.05.025.
• 51.
  Bernet, J.D.; Doles, J.D.; Hall, J.K.; Kelly Tanaka, K.; Carter, T.A.; Olwin, B.B. P38 MAPK Signaling Underlies a Cell-Autonomous Loss of Stem Cell Self-Renewal in Skeletal Muscle of Aged Mice. Nat. Med. 2014, 20, 265–271. https://doi.org/10.1038/nm.3465.
• 52.
  Reano, S.; Angelino, E.; Ferrara, M.; Malacarne, V.; Sustova, H.; Sabry, O.; Filigheddu, N. Unacylated ghrelin enhances satellite cell function and relieves the dystrophic phenotype in duchenne muscular dystrophy mdx model. Stem Cells 2017, 35, 1733–1746.
• 53.
  Massenet, J.; Gardner, E.; Chazaud, B.; Dilworth, F.J. Epigenetic Regulation of Satellite Cell Fate during Skeletal Muscle Regeneration. Skeletal Muscle 2021, 11, 4. https://doi.org/10.1186/s13395-020-00259-w.
• 54.
  Liu, L.; Cheung, T.H.; Charville, G.W.; Hurgo, B.M.C.; Leavitt, T.; Shih, J.; Brunet, A.; Rando, T.A. Chromatin Modifications as Determinants of Muscle Stem Cell Quiescence and Chronological Aging. Cell Rep. 2013, 4, 189–204. https://doi.org/10.1016/j.celrep.2013.05.043.
• 55.
  Naito, M.; Mori, M.; Inagawa, M.; Miyata, K.; Hashimoto, N.; Tanaka, S.; Asahara, H. Dnmt3a Regulates Proliferation of Muscle Satellite Cells via p57Kip2. PLoS Genet. 2016, 12, e1006167. https://doi.org/10.1371/journal.pgen.1006167.
• 56.
  Marroncelli, N.; Bianchi, M.; Bertin, M.; Consalvi, S.; Saccone, V.; De Bardi, M.; Puri, P.L.; Palacios, D.; Adamo, S.; Moresi, V. HDAC4 Regulates Satellite Cell Proliferation and Differentiation by Targeting P21 and Sharp1 Genes. Sci. Rep. 2018, 8, 3448. https://doi.org/10.1038/s41598-018-21835-7.
• 57.
  Zhang, N.; Mendieta-Esteban, J.; Magli, A.; Lilja, K.C.; Perlingeiro, R.C.R.; Marti-Renom, M.A.; Tsirigos, A.; Dynlacht, B.D. Muscle Progenitor Specification and Myogenic Differentiation Are Associated with Changes in Chromatin Topology. Nat. Commun. 2020, 11, 6222. https://doi.org/10.1038/s41467-020-19999-w.
• 58.
  Liu, N.; Williams, A.H.; Kim, Y.; McAnally, J.; Bezprozvannaya, S.; Sutherland, L.B.; Olson, E.N. An intragenic MEF2-dependent enhancer directs muscle-specific expression of microRNAs 1 and 133. Proc. Natl. Acad. Sci. USA 2007, 104, 20844–20849.
• 59.
  Liu, N.; Bezprozvannaya, S.; Shelton, J.M.; Frisard, M.I.; Hulver, M.W.; McMillan, R.P.; Olson, E.N. Mice lacking microRNA 133a develop dynamin 2–dependent centronuclear myopathy. J. Clin. Investig. 2011, 121, 3258–3268.
• 60.
  Horak, M.; Novak, J.; Bienertova-Vasku, J. Muscle-Specific microRNAs in Skeletal Muscle Development. Dev. Biol. 2016, 410, 1–13. https://doi.org/10.1016/j.ydbio.2015.12.013.
• 61.
  Kuang, S.; Kuroda, K.; Le Grand, F.; Rudnicki, M.A. Asymmetric Self-Renewal and Commitment of Satellite Stem Cells in Muscle. Cell 2007, 129, 999–1010. https://doi.org/10.1016/j.cell.2007.03.044.
• 62.
  Chang, N.C.; Sincennes, M.-C.; Chevalier, F.P.; Brun, C.E.; Lacaria, M.; Segalés, J.; Muñoz-Cánoves, P.; Ming, H.; Rudnicki, M.A. The Dystrophin Glycoprotein Complex Regulates the Epigenetic Activation of Muscle Stem Cell Commitment. Cell Stem Cell 2018, 22, 755–768.e6. https://doi.org/10.1016/j.stem.2018.03.022.
• 63.
  Dumont, N.A.; Rudnicki, M.A. Targeting Muscle Stem Cell Intrinsic Defects to Treat Duchenne Muscular Dystrophy. NPJ Regen. Med. 2016, 1, 16006–. https://doi.org/10.1038/npjregenmed.2016.6.
• 64.
  Wang, Y.X.; Feige, P.; Brun, C.E.; Hekmatnejad, B.; Dumont, N.A.; Renaud, J.-M.; Faulkes, S.; Guindon, D.E.; Rudnicki, M.A. EGFR-Aurka Signaling Rescues Polarity and Regeneration Defects in Dystrophin-Deficient Muscle Stem Cells by Increasing Asymmetric Divisions. Cell Stem Cell 2019, 24, 419–432.e6. https://doi.org/10.1016/j.stem.2019.01.002.
• 65.
  Kim, K.M.; Yoo, G.D.; Heo, W.; Oh, H.T.; Park, J.; Shin, S.; Do, Y.; Jeong, M.G.; Hwang, E.S.; Hong, J. TAZ Stimulates Exercise-induced Muscle Satellite Cell Activation via Pard3–P38 MAPK–TAZ Signalling Axis. J. Cachexia Sarcopenia Muscle 2023, 14, 2733–2746. https://doi.org/10.1002/jcsm.13348.
• 66.
  Dewey, E.; Taylor, D.; Johnston, C. Cell Fate Decision Making through Oriented Cell Division. JDB 2015, 3, 129–157. https://doi.org/10.3390/jdb3040129.
• 67.
  Sunchu, B.; Cabernard, C. Principles and mechanisms of asymmetric cell division. Development 2020, 147, dev167650.
• 68.
  Shinin, V.; Gayraud-Morel, B.; Gomès, D.; Tajbakhsh, S. Asymmetric Division and Cosegregation of Template DNA Strands in Adult Muscle Satellite Cells. Nat. Cell Biol. 2006, 8, 677–682. https://doi.org/10.1038/ncb1425.
• 69.
  Rocheteau, P.; Gayraud-Morel, B.; Siegl-Cachedenier, I.; Blasco, M.A.; Tajbakhsh, S. A Subpopulation of Adult Skeletal Muscle Stem Cells Retains All Template DNA Strands after Cell Division. Cell 2012, 148, 112–125. https://doi.org/10.1016/j.cell.2011.11.049.
• 70.
  Cheung, T.H.; Quach, N.L.; Charville, G.W.; Liu, L.; Park, L.; Edalati, A.; Yoo, B.; Hoang, P.; Rando, T.A. Maintenance of Muscle Stem-Cell Quiescence by microRNA-489. Nature 2012, 482, 524–528. https://doi.org/10.1038/nature10834.
• 71.
  Welle, S. Cellular and Molecular Basis of Age-Related Sarcopenia. Can. J. Appl. Physiol. 2002, 27. https://doi.org/10.1139/h02-002.
• 72.
  Jejurikar, S.S.; Henkelman, E.A.; Cederna, P.S.; Marcelo, C.L.; Urbanchek, M.G.; Kuzon, W.M. Aging Increases the Susceptibility of Skeletal Muscle Derived Satellite Cells to Apoptosis. Exp. Gerontol. 2006, 41, 828–836. https://doi.org/10.1016/j.exger.2006.06.053.
• 73.
  Hwang, A.B.; Brack, A.S. Muscle Stem Cells and Aging. Curr. Top. Dev. Biol. 2018, 126, 299–322. https://doi.org/10.1016/bs.ctdb.2017.08.008.
• 74.
  Cosgrove, B.D.; Gilbert, P.M.; Porpiglia, E.; Mourkioti, F.; Lee, S.P.; Corbel, S.Y.; Llewellyn, M.E.; Delp, S.L.; Blau, H.M. Rejuvenation of the Muscle Stem Cell Population Restores Strength to Injured Aged Muscles. Nat. Med. 2014, 20, 255–264. https://doi.org/10.1038/nm.3464.
• 75.
  Benjamin, D.I.; Brett, J.O.; Both, P.; Benjamin, J.S.; Ishak, H.L.; Kang, J.; Kim, S.; Chung, M.; Arjona, M.; Nutter, C.W.; et al. Multiomics Reveals Glutathione Metabolism as a Driver of Bimodality during Stem Cell Aging. Cell Metabolism 2023, 35, 472–486.e6. https://doi.org/10.1016/j.cmet.2023.02.001.
• 76.
  Forcina, L.; Musarò, A. Rejuvenating muscle stem cells with the glutathione system. Cell Metab. 2023, 35, 379–381.
• 77.
  Cardone, N.; Taglietti, V.; Baratto, S.; Kefi, K.; Periou, B.; Gitiaux, C.; Barnerias, C.; Lafuste, P.; Pharm, F.L.; Pharm, J.N.; et al. Myopathologic Trajectory in Duchenne Muscular Dystrophy (DMD) Reveals Lack of Regeneration Due to Senescence in Satellite Cells. Acta Neuropathol. Commun. 2023, 11, 167. https://doi.org/10.1186/s40478-023-01657-z.
• 78.
  Tichy, E.D.; Sidibe, D.K.; Tierney, M.T.; Stec, M.J.; Sharifi-Sanjani, M.; Hosalkar, H.; Mubarak, S.; Johnson, F.B.; Sacco, A.; Mourkioti, F. Single Stem Cell Imaging and Analysis Reveals Telomere Length Differences in Diseased Human and Mouse Skeletal Muscles. Stem Cell Rep. 2017, 9, 1328–1341. https://doi.org/10.1016/j.stemcr.2017.08.003.
• 79.
  Sandonà; M; Esposito, F.; Cargnoni, A.; Silini, A.; Romele, P.; Parolini, O.; Saccone, V. Amniotic membrane-derived stromal cells release extracellular vesicles that favor regeneration of dystrophic skeletal muscles. Int. J. Mol. Sci. 2023, 24, 12457.
• 80.
  Su, Y.; Cao, Y.; Liu, C.; Xu, Q.; Li, N.; Lan, M.; Li, L.; Wang, K.; Zhang, Z.; Meng, Q. Inactivating IL34 Promotes Regenerating Muscle Stem Cell Expansion and Attenuates Duchenne Muscular Dystrophy in Mouse Models. Theranostics 2023, 13, 2588–2604. https://doi.org/10.7150/thno.83817.
• 81.
  Taglietti, V.; Kefi, K.; Rivera, L.; Bergiers, O.; Cardone, N.; Coulpier, F.; Gioftsidi, S.; Drayton-Libotte, B.; Hou, C.; Authier, F.-J.; et al. Thyroid-Stimulating Hormone Receptor Signaling Restores Skeletal Muscle Stem Cell Regeneration in Rats with Muscular Dystrophy. Sci. Transl. Med. 2023, 15, eadd5275. https://doi.org/10.1126/scitranslmed.add5275.
• 82.
  Nance, M.E.; Shi, R.; Hakim, C.H.; Wasala, N.B.; Yue, Y.; Pan, X.; Zhang, T.; Robinson, C.A.; Duan, S.X.; Yao, G.; et al. AAV9 Edits Muscle Stem Cells in Normal and Dystrophic Adult Mice. Molecular Therapy 2019, 27, 1568–1585. https://doi.org/10.1016/j.ymthe.2019.06.012.
• 83.
  Chen, S.; Zhang, P.; Duan, H.; Wang, J.; Qiu, Y.; Cui, Z.; Xie, L. Gut microbiota in muscular atrophy development, progression and treatment: New therapeutic targets and opportunities. Innovation 2023, 4, 100479.
• 84.
  Lahiri, S.; Kim, H.; Garcia-Perez, I.; Reza, M.M.; Martin, K.A.; Kundu, P.; Cox, L.M.; Selkrig, J.; Posma, J.M.; Zhang, H.; et al. The Gut Microbiota Influences Skeletal Muscle Mass and Function in Mice. Sci. Transl. Med. 2019, 11, eaan5662. https://doi.org/10.1126/scitranslmed.aan5662.
• 85.
  Chen, S.; Huang, L.; Liu, B.; Duan, H.; Li, Z.; Liu, Y.; Li, H.; Fu, X.; Lin, J.; Xu, Y.; et al. Dynamic Changes in Butyrate Levels Regulate Satellite Cell Homeostasis by Preventing Spontaneous Activation during Aging. Sci. China Life Sci. 2023. https://doi.org/10.1007/s11427-023-2400-3.
• 86.
  Hanna, B.S.; Wang, G.; Galván-Peña, S.; Mann, A.O.; Ramirez, R.N.; Muñoz-Rojas, A.R.; Smith, K.; Wan, M.; Benoist, C.; Mathis, D. The Gut Microbiota Promotes Distal Tissue Regeneration via RORγ+ Regulatory T Cell Emissaries. Immunity 2023, 56, 829–846.e8. https://doi.org/10.1016/j.immuni.2023.01.033.
• 87.
  Jollet, M.; Mariadassou, M.; Rué, O.; Pessemesse, L.; Ollendorff, V.; Ramdani, S.; Vernus, B.; Bonnieu, A.; Bertrand-Gaday, C.; Goustard, B.; et al. Insight into the Role of Gut Microbiota in Duchenne Muscular Dystrophy. Am. J. Pathol. 2024, 194, 264–279. https://doi.org/10.1016/j.ajpath.2023.10.010.
• 88.
  Kalkan, H.; Pagano, E.; Paris, D.; Panza, E.; Cuozzo, M.; Moriello, C.; Piscitelli, F.; Abolghasemi, A.; Gazzerro, E.; Silvestri, C.; et al. Targeting Gut Dysbiosis against Inflammation and Impaired Autophagy in Duchenne Muscular Dystrophy. EMBO Mol. Med. 2023, 15, e16225. https://doi.org/10.15252/emmm.202216225.
• 89.
  Guo, Q.; Luo, Q.; Song, G. Control of Muscle Satellite Cell Function by Specific Exercise-induced Cytokines and Their Applications in Muscle Maintenance. J. Cachexia Sarcopenia Muscle 2024, 15, 466–476. https://doi.org/10.1002/jcsm.13440.
• 90.
  Kang, X.; Qian, J.; Shi, Y.X.; Bian, X.T.; Zhang, L.D.; Li, G.M.; Miao, H.M. Exercise-induced Musclin determines the fate of fibro-adipogenic progenitors to control muscle homeostasis. Cell Stem Cell 2024, 31, 212–226.e7.
• 91.
  Qaisar, R.; Bhaskaran, S.; Van Remmen, H. Muscle Fiber Type Diversification during Exercise and Regeneration. Free. Radic. Biol. Med. 2016, 98, 56–67. https://doi.org/10.1016/j.freeradbiomed.2016.03.025.
• 92.
  Distefano, G.; Goodpaster, B.H. Effects of Exercise and Aging on Skeletal Muscle. Cold Spring Harb. Perspect. Med. 2018, 8, a029785. https://doi.org/10.1101/cshperspect.a029785.
• 93.
  McKendry, J.; Stokes, T.; Mcleod, J.C.; Phillips, S.M. Resistance Exercise, Aging, Disuse, and Muscle Protein Metabolism. In Comprehensive Physiology; Terjung, R., Ed.; Wiley: Hoboken, NJ, USA, 2021; pp. 2249–2278. ISBN 978-0-470-65071-4.
• 94.
  Hurst, C.; Robinson, S.M.; Witham, M.D.; Dodds, R.M.; Granic, A.; Buckland, C.; De Biase, S.; Finnegan, S.; Rochester, L.; Skelton, D.A.; et al. Resistance Exercise as a Treatment for Sarcopenia: Prescription and Delivery. Age Ageing 2022, 51, afac003. https://doi.org/10.1093/ageing/afac003.