SpringerLink
Log in

Overview of Cell Types Capable of Contributing to Skeletal Muscle Repair and Regeneration

  • Living reference work entry
  • First Online:
Cell Engineering and Regeneration

Part of the book series: Reference Series in Biomedical Engineering ((TIENRE))

  • 253 Accesses

Abstract

Skeletal muscle is the most abundant tissue in the human body, accounting for more than 30% of body weight, and is vital for the maintenance of posture, locomotion, and breathing. Skeletal muscle possesses a high intrinsic regenerative ability due to its resident stem cell, the satellite cell. However, muscle repair can fail in muscular dystrophies, during aging or after extensive trauma. A multitude of cell types are currently under investigation for their ability to support muscle regeneration in pathologies that induce tissue damage beyond the capacity of physiological regeneration. Even if the satellite cell is the most potent myogenic cell, factors including limited availability, difficulty of isolation, and in vitro expansion potential need to be addressed, and unorthodox cell types investigated, to develop the optimal cell type for a given therapeutic application. This chapter gives an overview of the advantages and disadvantages of cell types with myogenic capacity, focusing primarily on satellite cells, bone marrow-derived cells, muscle interstitial cells, and pluripotent stem cells.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

Similar content being viewed by others

References

  • Acharyya S, Butchbach MER, Sahenk Z, Wang H, Saji M, Carathers M, Ringel MD, Skipworth RJE, Fearon KCH, Hollingsworth MA et al (2005) Dystrophin glycoprotein complex dysfunction: a regulatory link between muscular dystrophy and cancer cachexia. Cancer Cell 8:421–432

    Article  Google Scholar 

  • Agley CC, Rowlerson AM, Velloso CP, Lazarus NL, Harridge SDR (2015) Isolation and quantitative immunocytochemical characterization of primary myogenic cells and fibroblasts from human skeletal muscle. J Vis Exp 95:e52049

    Google Scholar 

  • Aguennouz M, Vita GL, Messina S, Cama A, Lanzano N, Ciranni A, Rodolico C, Di Giorgio RM, Vita G (2011) Telomere shortening is associated to TRF1 and PARP1 overexpression in Duchenne muscular dystrophy. Neurobiol Aging 32:2190–2197

    Article  Google Scholar 

  • Allouh MZ, Yablonka-Reuveni Z, Rosser BWC (2008) Pax7 reveals a greater frequency and concentration of satellite cells at the ends of growing skeletal muscle fibers. J Histochem Cytochem 56:77–87

    Article  Google Scholar 

  • Asakura A, Seale P, Girgis-Gabardo A, Rudnicki MA (2002) Myogenic specification of side population cells in skeletal muscle. J Cell Biol 159:123–134

    Article  Google Scholar 

  • Baker JH, Poindextor CE (1991) Muscle regeneration following segmental necrosis in tenotomized muscle fibers. Muscle Nerve 14:348–357

    Article  Google Scholar 

  • Barberi T, Willis LM, Socci ND, Studer L (2005) Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med 2:e161

    Article  Google Scholar 

  • Bareja A, Holt JA, Luo G, Chang C, Lin J, Hinken AC, Freudenberg JM, Kraus WE, Evans WJ, Billin AN (2014) Human and mouse skeletal muscle stem cells: convergent and divergent mechanisms of myogenesis. PLoS One 9:e90398

    Article  Google Scholar 

  • Baroffio A, Aubry JP, Kaelin A, Krause RM, Hamann M, Bader CR (1993) Purification of human muscle satellite cells by flow cytometry. Muscle Nerve 16:498–505

    Article  Google Scholar 

  • Beauchamp JR, Heslop L, Yu DS, Tajbakhsh S, Kelly RG, Wernig A, Buckingham ME, Partridge TA, Zammit PS (2000) Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151:1221–1234

    Article  Google Scholar 

  • Benchaouir R, Meregalli M, Farini A, D’Antona G, Belicchi M, Goyenvalle A, Battistelli M, Bresolin N, Bottinelli R, Garcia L et al (2007) Restoration of human dystrophin following transplantation of exon-skip**-engineered DMD patient stem cells into dystrophic mice. Cell Stem Cell 1:646–657

    Article  Google Scholar 

  • Berry SE, Liu J, Chaney EJ, Kaufman SJ (2007) Multipotential mesoangioblast stem cell therapy in the mdx/utrn-/- mouse model for Duchenne muscular dystrophy. Regen Med 2:275–288

    Article  Google Scholar 

  • Besson V, Smeriglio P, Wegener A, Relaix F, Nait Oumesmar B, Sassoon DA, Marazzi G (2011) PW1 gene/paternally expressed gene 3 (PW1/Peg3) identifies multiple adult stem and progenitor cell populations. Proc Natl Acad Sci USA 108:11470–11475

    Article  Google Scholar 

  • Betsholtz C (2004) Insight into the physiological functions of PDGF through genetic studies in mice. Cytokine Growth Factor Rev 15:215–228

    Article  Google Scholar 

  • Bharathy N, Ling BMT, Taneja R (2013) Epigenetic regulation of skeletal muscle development and differentiation. Subcell Biochem 61:139–150

    Article  Google Scholar 

  • Birbrair A, Zhang T, Wang Z-M, Messi ML, Enikolopov GN, Mintz A, Delbono O (2013a) Role of pericytes in skeletal muscle regeneration and fat accumulation. Stem Cells Dev 22:2298–2314

    Article  Google Scholar 

  • Birbrair A, Zhang T, Wang Z-M, Messi ML, Mintz A, Delbono O (2013b) Type-1 pericytes participate in fibrous tissue deposition in aged skeletal muscle. Am J Physiol Cell Physiol 305:C1098–C1113

    Article  Google Scholar 

  • Biressi S, Rando TA (2010) Heterogeneity in the muscle satellite cell population. Semin Cell Dev Biol 21:845–854

    Article  Google Scholar 

  • Biressi S, Tagliafico E, Lamorte G, Monteverde S, Tenedini E, Roncaglia E, Ferrari S, Ferrari S, Cusella-De Angelis MG, Tajbakhsh S et al (2007) Intrinsic phenotypic diversity of embryonic and fetal myoblasts is revealed by genome-wide gene expression analysis on purified cells. Dev Biol 304:633–651

    Article  Google Scholar 

  • Blanco-Bose WE, Yao CC, Kramer RH, Blau HM (2001) Purification of mouse primary myoblasts based on alpha 7 integrin expression. Exp Cell Res 265:212–220

    Article  Google Scholar 

  • Blau HM, Webster C (1981) Isolation and characterization of human muscle cells. Proc Natl Acad Sci USA 78:5623–5627

    Article  Google Scholar 

  • Blau HM, Webster C, Pavlath GK (1983) Defective myoblasts identified in Duchenne muscular dystrophy. Proc Natl Acad Sci USA 80:4856–4860

    Article  Google Scholar 

  • Boldrin L, Morgan JE (2012) Human satellite cells: identification on human muscle fibres. PLoS Curr 3:RRN1294

    Article  Google Scholar 

  • Borchin B, Chen J, Barberi T (2013) Derivation and FACS-mediated purification of PAX3+/PAX7+ skeletal muscle precursors from human pluripotent stem cells. Stem Cell Reports 1:620–631

    Article  Google Scholar 

  • Bosnakovski D, Xu Z, Li W, Thet S, Cleaver O, Perlingeiro RCR, Kyba M (2008) Prospective isolation of skeletal muscle stem cells with a Pax7 reporter. Stem Cells 26:3194–3204

    Article  Google Scholar 

  • Brazelton TR, Nystrom M, Blau HM (2003) Significant differences among skeletal muscles in the incorporation of bone marrow-derived cells. Dev Biol 262:64–74

    Article  Google Scholar 

  • Briggs D, Morgan JE (2013) Recent progress in satellite cell/myoblast engraftment - relevance for therapy. FEBS J 280:4281–4293

    Article  Google Scholar 

  • Cacchiarelli D, Qiu X, Srivatsan S, Manfredi A, Ziller M, Overbey E, Grimaldi A, Grimsby J, Pokharel P, Livak KJ et al (2018) Aligning single-cell developmental and reprogramming trajectories identifies molecular determinants of myogenic reprogramming outcome. Cell Syst 7:258–268.e3

    Article  Google Scholar 

  • Calhabeu F, Hayashi S, Morgan JE, Relaix F, Zammit PS (2013) Alveolar rhabdomyosarcoma-associated proteins PAX3/FOXO1A and PAX7/FOXO1A suppress the transcriptional activity of MyoD-target genes in muscle stem cells. Oncogene 32:651–662

    Article  Google Scholar 

  • Cantini M, Giurisato E, Radu C, Tiozzo S, Pampinella F, Senigaglia D, Zaniolo G, Mazzoleni F, Vitiello L (2002) Macrophage-secreted myogenic factors: a promising tool for greatly enhancing the proliferative capacity of myoblasts in vitro and in vivo. Neurol Sci 23:189–194

    Article  Google Scholar 

  • Caron L, Kher D, Lee KL, McKernan R, Dumevska B, Hidalgo A, Li J, Yang H, Main H, Ferri G et al (2016) A human pluripotent stem cell model of facioscapulohumeral muscular dystrophy-affected skeletal muscles. Stem Cells Transl Med 5:1145–1161

    Article  Google Scholar 

  • Ceafalan LC, Popescu BO, Hinescu ME (2014) Cellular players in skeletal muscle regeneration. Biomed Res Int 2014:957014

    Article  Google Scholar 

  • Chal J, Al Tanoury Z, Hestin M, Gobert B, Aivio S, Hick A, Cherrier T, Nesmith AP, Parker KK, Pourquié O (2016) Generation of human muscle fibers and satellite-like cells from human pluripotent stem cells in vitro. Nat Protoc 11:1833–1850

    Article  Google Scholar 

  • Chargé SBP, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84:209–238

    Article  Google Scholar 

  • Chazaud B, Brigitte M, Yacoub-Youssef H, Arnold L, Gherardi R, Sonnet C, Lafuste P, Chretien F (2009) Dual and beneficial roles of macrophages during skeletal muscle regeneration. Exerc Sport Sci Rev 37:18–22

    Article  Google Scholar 

  • Cho DS, Doles JD (2017) Single cell transcriptome analysis of muscle satellite cells reveals widespread transcriptional heterogeneity. Gene 636:54–63

    Article  Google Scholar 

  • Ciciliot S, Schiaffino S (2010) Regeneration of mammalian skeletal muscle. Basic mechanisms and clinical implications. Curr Pharm Des 16:906–914

    Article  Google Scholar 

  • Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA, Morgan JE (2005) Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122:289–301

    Article  Google Scholar 

  • Conrad MF, Crawford RS, Hackney LA, Paruchuri V, Abularrage CJ, Patel VI, Lamuraglia GM, Cambria RP (2011) Endovascular management of patients with critical limb ischemia. J Vasc Surg 53:1020–1025

    Article  Google Scholar 

  • Cornelison DD, Wold BJ (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191:270–283

    Article  Google Scholar 

  • Cornelison DD, Filla MS, Stanley HM, Rapraeger AC, Olwin BB (2001) Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev Biol 239:79–94

    Article  Google Scholar 

  • Cosgrove BD, Gilbert PM, Porpiglia E, Mourkioti F, Lee SP, Corbel SY, Llewellyn ME, Delp SL, Blau HM (2014) Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat Med 20:255–264

    Article  Google Scholar 

  • Cossu G, Bianco P (2003) Mesoangioblasts – vascular progenitors for extravascular mesodermal tissues. Curr Opin Genet Dev 13:537–542

    Article  Google Scholar 

  • Cossu G, Previtali SC, Napolitano S, Cicalese MP, Tedesco FS, Nicastro F, Noviello M, Roostalu U, Natali Sora MG, Scarlato M et al (2015) Intra-arterial transplantation of HLA-matched donor mesoangioblasts in Duchenne muscular dystrophy. EMBO Mol Med 7:1513–1528

    Article  Google Scholar 

  • Cottle BJ, Lewis FC, Shone V, Ellison-Hughes GM (2017) Skeletal muscle-derived interstitial progenitor cells (PICs) display stem cell properties, being clonogenic, self-renewing, and multi-potent in vitro and in vivo. Stem Cell Res Ther 8:158

    Google Scholar 

  • Crisan M, Yap S, Casteilla L, Chen C-W, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313

    Article  Google Scholar 

  • Darabi R, Arpke RW, Irion S, Dimos JT, Grskovic M, Kyba M, Perlingeiro RCR (2012) Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell 10:610–619

    Article  Google Scholar 

  • Daubas P, Tajbakhsh S, Hadchouel J, Primig M, Buckingham M (2000) Myf5 is a novel early axonal marker in the mouse brain and is subjected to post-transcriptional regulation in neurons. Development 127:319–331

    Google Scholar 

  • Day K, Shefer G, Richardson JB, Enikolopov G, Yablonka-Reuveni Z (2007) Nestin-GFP reporter expression defines the quiescent state of skeletal muscle satellite cells. Dev Biol 304:246–259

    Article  Google Scholar 

  • De Angelis L, Berghella L, Coletta M, Lattanzi L, Zanchi M, Cusella-De Angelis MG, Ponzetto C, Cossu G (1999) Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. J Cell Biol 147:869–878

    Article  Google Scholar 

  • Delbono O (2011) Expression and regulation of excitation-contraction coupling proteins in aging skeletal muscle. Curr Aging Sci 4:248–259

    Article  Google Scholar 

  • Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L, Innocenzi A, Galvez BG, Messina G, Morosetti R et al (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9:255–267

    Article  Google Scholar 

  • Dellavalle A, Maroli G, Covarello D, Azzoni E, Innocenzi A, Perani L, Antonini S, Sambasivan R, Brunelli S, Tajbakhsh S et al (2011) Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat Commun 2:499

    Article  Google Scholar 

  • Diaz-Flores L, Gutierrez R, Varela H (1992) Behavior of postcapillary venule pericytes during postnatal angiogenesis. J Morphol 213:33–45

    Article  Google Scholar 

  • Dinsmore J, Ratliff J, Deacon T, Pakzaban P, Jacoby D, Galpern W, Isacson O (1996) Embryonic stem cells differentiated in vitro as a novel source of cells for transplantation. Cell Transplant 5:131–143

    Article  Google Scholar 

  • Dreyfus PA, Chretien F, Chazaud B, Kirova Y, Caramelle P, Garcia L, Butler-Browne G, Gherardi RK (2004) Adult bone marrow-derived stem cells in muscle connective tissue and satellite cell niches. Am J Pathol 164:773–779

    Article  Google Scholar 

  • Dulauroy S, Di Carlo SE, Langa F, Eberl G, Peduto L (2012) Lineage tracing and genetic ablation of ADAM12(+) perivascular cells identify a major source of profibrotic cells during acute tissue injury. Nat Med 18:1262–1270

    Article  Google Scholar 

  • Enge M, Bjarnegård M, Gerhardt H, Gustafsson E, Kalén M, Asker N, Hammes H-P, Shani M, Fässler R, Betsholtz C (2002) Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J 21:4307–4316

    Article  Google Scholar 

  • Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F (1998) Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279:1528–1530

    Article  Google Scholar 

  • Fiore D, Judson RN, Low M, Lee S, Zhang E, Hopkins C, Xu P, Lenzi A, Rossi FMV, Lemos DR (2016) Pharmacological blockage of fibro/adipogenic progenitor expansion and suppression of regenerative fibrogenesis is associated with impaired skeletal muscle regeneration. Stem Cell Res 17:161–169

    Article  Google Scholar 

  • Fukada S, Higuchi S, Segawa M, Koda K, Yamamoto Y, Tsujikawa K, Kohama Y, Uezumi A, Imamura M, Miyagoe-Suzuki Y et al (2004) Purification and cell-surface marker characterization of quiescent satellite cells from murine skeletal muscle by a novel monoclonal antibody. Exp Cell Res 296:245–255

    Article  Google Scholar 

  • Fukada S, Uezumi A, Ikemoto M, Masuda S, Segawa M, Tanimura N, Yamamoto H, Miyagoe-Suzuki Y, Takeda S’i (2007) Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25:2448–2459

    Article  Google Scholar 

  • Fukada S, Ma Y, Ohtani T, Watanabe Y, Murakami S, Yamaguchi M (2013) Isolation, characterization, and molecular regulation of muscle stem cells. Front Physiol 4:317

    Article  Google Scholar 

  • Fukushima K, Badlani N, Usas A, Riano F, Fu F, Huard J (2001) The use of an antifibrosis agent to improve muscle recovery after laceration. Am J Sports Med 29:394–402

    Article  Google Scholar 

  • Fuoco C, Sangalli E, Vono R, Testa S, Sacchetti B, Latronico MVG, Bernardini S, Madeddu P, Cesareni G, Seliktar D et al (2014) 3D hydrogel environment rejuvenates aged pericytes for skeletal muscle tissue engineering. Front Physiol 5:203

    Article  Google Scholar 

  • Fuoco C, Rizzi R, Biondo A, Longa E, Mascaro A, Shapira-Schweitzer K, Kossovar O, Benedetti S, Salvatori ML, Santoleri S et al (2015) In vivo generation of a mature and functional artificial skeletal muscle. EMBO Mol Med 7:411–422

    Article  Google Scholar 

  • Galvez BG, Sampaolesi M, Brunelli S, Covarello D, Gavina M, Rossi B, Constantin G, Torrente Y, Cossu G (2006) Complete repair of dystrophic skeletal muscle by mesoangioblasts with enhanced migration ability. J Cell Biol 174:231–243

    Article  Google Scholar 

  • Garry DJ, Meeson A, Elterman J, Zhao Y, Yang P, Bassel-Duby R, Williams RS (2000) Myogenic stem cell function is impaired in mice lacking the forkhead/winged helix protein MNF. Proc Natl Acad Sci USA 97:5416–5421

    Article  Google Scholar 

  • Gerli MFM, Moyle LA, Benedetti S, Ferrari G, Ucuncu E, Ragazzi M, Constantinou C, Louca I, Sakai H, Ala P et al (2019) Combined notch and PDGF signaling enhances migration and expression of stem cell markers while inducing perivascular cell features in muscle satellite cells. Stem Cell Reports 12:461–473

    Article  Google Scholar 

  • Gilbert PM, Havenstrite KL, Magnusson KEG, Sacco A, Leonardi NA, Kraft P, Nguyen NK, Thrun S, Lutolf MP, Blau HM (2010) Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329:1078–1081

    Article  Google Scholar 

  • Giordani L, He GJ, Negroni E, Sakai H, Law JYC, Siu MM, Wan R, Corneau A, Tajbakhsh S, Cheung TH et al (2019) High-dimensional single-cell cartography reveals novel skeletal muscle-resident cell populations. Molecular Cell 74:609–621.e6

    Article  Google Scholar 

  • Glass DJ (2010) Signaling pathways perturbing muscle mass. Curr Opin Clin Nutr Metab Care 13:225–229

    Article  Google Scholar 

  • Gnocchi VF, White RB, Ono Y, Ellis JA, Zammit PS (2009) Further characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells. PLoS One 4:e5205

    Article  Google Scholar 

  • Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183:1797–1806

    Article  Google Scholar 

  • Goupille O, Pallafacchina G, Relaix F, Conway SJ, Cumano A, Robert B, Montarras D, Buckingham M (2011) Characterization of Pax3-expressing cells from adult blood vessels. J Cell Sci 124:3980–3988

    Article  Google Scholar 

  • Greising SM, Gransee HM, Mantilla CB, Sieck GC (2012) Systems biology of skeletal muscle: fiber type as an organizing principle. Wiley Interdiscip Rev Syst Biol Med 4:457–473

    Article  Google Scholar 

  • Guimarães-Camboa N, Cattaneo P, Sun Y, Moore-Morris T, Gu Y, Dalton ND, Rockenstein E, Masliah E, Peterson KL, Stallcup WB et al (2017) Pericytes of multiple organs do not behave as mesenchymal stem cells In Vivo. Cell Stem Cell 20:345–359.e5

    Article  Google Scholar 

  • Gussoni E, Soneoka Y, Strickland CD, Buzney EA, Khan MK, Flint AF, Kunkel LM, Mulligan RC (1999) Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401:390–394

    Google Scholar 

  • Gussoni E, Bennett RR, Muskiewicz KR, Meyerrose T, Nolta JA, Gilgoff I, Stein J, Chan Y, Lidov HG, Bönnemann CG et al (2002) Long-term persistence of donor nuclei in a Duchenne muscular dystrophy patient receiving bone marrow transplantation. J Clin Invest 110:807–814

    Article  Google Scholar 

  • Hanson J, Huxley HE (1953) Structural basis of the cross-striations in muscle. Nature 172:530–532

    Article  Google Scholar 

  • Helal MAM, Shaheen NEM, Abu Zahra FA (2016) Immunomodulatory capacity of the local mesenchymal stem cells transplantation after severe skeletal muscle injury in female rats. Immunopharmacol Immunotoxicol 38:414–422

    Article  Google Scholar 

  • Hellström M, Gerhardt H, Kalén M, Li X, Eriksson U, Wolburg H, Betsholtz C (2001) Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 153:543–553

    Article  Google Scholar 

  • Hernández-Hernández JM, García-González EG, Brun CE, Rudnicki MA (2017) The myogenic regulatory factors, determinants of muscle development, cell identity and regeneration. Semin Cell Dev Biol 72:10–18

    Article  Google Scholar 

  • Heslop L, Morgan JE, Partridge TA (2000) Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J Cell Sci 113(Pt 12):2299–2308

    Google Scholar 

  • Hicks MR, Hiserodt J, Paras K, Fujiwara W, Eskin A, Jan M, ** H, Young CS, Evseenko D, Nelson SF et al (2018) ERBB3 and NGFR mark a distinct skeletal muscle progenitor cell in human development and hPSCs. Nat Cell Biol 20:46–57

    Article  Google Scholar 

  • Ho ATV, Palla AR, Blake MR, Yucel ND, Wang YX, Magnusson KEG, Holbrook CA, Kraft PE, Delp SL, Blau HM (2017) Prostaglandin E2 is essential for efficacious skeletal muscle stem-cell function, augmenting regeneration and strength. Proc Natl Acad Sci 114(26):6675–6684

    Google Scholar 

  • Hogendoorn S, Duijnisveld BJ, van Duinen SG, Stoel BC, van Dijk JG, Fibbe WE, Nelissen RGHH (2014) Local injection of autologous bone marrow cells to regenerate muscle in patients with traumatic brachial plexus injury: a pilot study. Bone Joint Res 3:38–47

    Article  Google Scholar 

  • Ikemoto M, Fukada S-I, Uezumi A, Masuda S, Miyoshi H, Yamamoto H, Wada MR, Masubuchi N, Miyagoe-Suzuki Y, Takeda S’i (2007) Autologous transplantation of SM/C-2.6(+) satellite cells transduced with micro-dystrophin CS1 cDNA by lentiviral vector into mdx mice. Mol Ther 15:2178–2185

    Article  Google Scholar 

  • Incitti T, Magli A, Darabi R, Yuan C, Lin K, Arpke RW, Azzag K, Yamamoto A, Stewart R, Thomson JA, et al (2019) Pluripotent stem cell-derived myogenic progenitors remodel their molecular signature upon in vivo engraftment. Proc Natl Acad Sci 116(10):4346–4351

    Article  Google Scholar 

  • Irintchev A, Zeschnigk M, Starzinski-Powitz A, Wernig A (1994) Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev Dyn 199:326–337

    Article  Google Scholar 

  • Jackson KA, Mi T, Goodell MA (1999) Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc Natl Acad Sci USA 96:14482–14486

    Article  Google Scholar 

  • Janssen I, Heymsfield SB, Wang ZM, Ross R (2000) Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol (1985) 89:81–88

    Article  Google Scholar 

  • Järvinen TAH, Järvinen TLN, Kääriäinen M, Kalimo H, Järvinen M (2005) Muscle injuries: biology and treatment. Am J Sports Med 33:745–764

    Article  Google Scholar 

  • Joe AWB, Yi L, Natarajan A, Le Grand F, So L, Wang J, Rudnicki MA, Rossi FMV (2010) Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol 12:153–163

    Article  Google Scholar 

  • Jørgensen LH, Jensen CH, Wewer UM, Schrøder HD (2007) Transgenic overexpression of ADAM12 suppresses muscle regeneration and aggravates dystrophy in aged mdx mice. Am J Pathol 171:1599–1607

    Article  Google Scholar 

  • Kakulas BA, Papadimitriou JM, Knight JO, Mastaglia FL (1968) Normal and abnormal human muscle in tissue culture. Proc Aust Assoc Neurol 5:79–85

    Google Scholar 

  • Kale S, Hanai J, Chan B, Karihaloo A, Grotendorst G, Cantley L, Sukhatme VP (2005) Microarray analysis of in vitro pericyte differentiation reveals an angiogenic program of gene expression. FASEB J 19:270–271

    Article  Google Scholar 

  • Katz B (1961) The termination of the afferent nerve fibre in the muscle spindle of the frog. Philos Trans R Soc Lond Ser B Biol Sci 243:221–240

    Article  Google Scholar 

  • Klinger F-G, Scaldaferri M-L, Di Carlo A, Baiocchi M, Coletta M, Cossu G, De Felici M (2003) Myogenic potential of mouse primordial germ cells. Int J Dev Biol 47:303–305

    Google Scholar 

  • Kobari L, Giarratana MC, Pflumio F, Izac B, Coulombel L, Douay L (2001) CD133+ cell selection is an alternative to CD34+ cell selection for ex vivo expansion of hematopoietic stem cells. J Hematother Stem Cell Res 10:273–281

    Article  Google Scholar 

  • Kostallari E, Baba-Amer Y, Alonso-Martin S, Ngoh P, Relaix F, Lafuste P, Gherardi RK (2015) Pericytes in the myovascular niche promote post-natal myofiber growth and satellite cell quiescence. Development 142:1242–1253

    Article  Google Scholar 

  • Kowalski K, Dos Santos M, Maire P, Ciemerych MA, Brzoska E (2018) Induction of bone marrow-derived cells myogenic identity by their interactions with the satellite cell niche. Stem Cell Res Ther 9:258

    Article  Google Scholar 

  • Kuang S, Kuroda K, Le Grand F, Rudnicki MA (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129:999–1010

    Article  Google Scholar 

  • LaBarge MA, Blau HM (2002) Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell 111:589–601

    Article  Google Scholar 

  • Labbe R, Lindsay T, Walker PM (1987) The extent and distribution of skeletal muscle necrosis after graded periods of complete ischemia. J Vasc Surg 6:152–157

    Article  Google Scholar 

  • Lapidos KA, Chen YE, Earley JU, Heydemann A, Huber JM, Chien M, Ma A, McNally EM (2004) Transplanted hematopoietic stem cells demonstrate impaired sarcoglycan expression after engraftment into cardiac and skeletal muscle. J Clin Invest 114:1577–1585

    Article  Google Scholar 

  • Latil M, Rocheteau P, Châtre L, Sanulli S, Mémet S, Ricchetti M, Tajbakhsh S, Chrétien F (2012) Skeletal muscle stem cells adopt a dormant cell state post mortem and retain regenerative capacity. Nat Commun 3:903

    Article  Google Scholar 

  • Lepper C, Partridge TA, Fan C-M (2011) An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138:3639–3646

    Article  Google Scholar 

  • Linard C, Brachet M, L’homme B, Strup-Perrot C, Busson E, Bonneau M, Lataillade J-J, Bey E, Benderitter M (2018) Long-term effectiveness of local BM-MSCs for skeletal muscle regeneration: a proof of concept obtained on a pig model of severe radiation burn. Stem Cell Res Ther 9:299

    Article  Google Scholar 

  • Lindström M, Thornell L-E (2009) New multiple labelling method for improved satellite cell identification in human muscle: application to a cohort of power-lifters and sedentary men. Histochem Cell Biol 132:141–157

    Article  Google Scholar 

  • Liu N, Garry GA, Li S, Bezprozvannaya S, Sanchez-Ortiz E, Chen B, Shelton JM, Jaichander P, Bassel-Duby R, Olson EN (2017) A Twist2-dependent progenitor cell contributes to adult skeletal muscle. Nat Cell Biol 19:202–213

    Article  Google Scholar 

  • Luth ES, Jun SJ, Wessen MK, Liadaki K, Gussoni E, Kunkel LM (2008) Bone marrow side population cells are enriched for progenitors capable of myogenic differentiation. J Cell Sci 121:1426–1434

    Article  Google Scholar 

  • Luz MAM, Marques MJ, Santo Neto H (2002) Impaired regeneration of dystrophin-deficient muscle fibers is caused by exhaustion of myogenic cells. Braz J Med Biol Res 35:691

    Article  Google Scholar 

  • Machado L, Esteves de Lima J, Fabre O, Proux C, Legendre R, Szegedi A, Varet H, Ingerslev LR, Barrès R, Relaix F et al (2017) In situ fixation redefines quiescence and early activation of skeletal muscle stem cells. Cell Rep 21:1982–1993

    Article  Google Scholar 

  • Maffioletti SM, Gerli MFM, Ragazzi M, Dastidar S, Benedetti S, Loperfido M, VandenDriessche T, Chuah MK, Tedesco FS (2015) Efficient derivation and inducible differentiation of expandable skeletal myogenic cells from human ES and patient-specific iPS cells. Nat Protoc 10:941–958

    Article  Google Scholar 

  • Maffioletti SM, Sarcar S, Henderson ABH, Mannhardt I, Pinton L, Moyle LA, Steele-Stallard H, Cappellari O, Wells KE, Ferrari G et al (2018) Three-dimensional human iPSC-derived artificial skeletal muscles model muscular dystrophies and enable multilineage tissue engineering. Cell Rep 23:899–908

    Article  Google Scholar 

  • Marg A, Escobar H, Gloy S, Kufeld M, Zacher J, Spuler A, Birchmeier C, Izsvák Z, Spuler S (2014) Human satellite cells have regenerative capacity and are genetically manipulable. J Clin Invest 124:4257–4265

    Article  Google Scholar 

  • Massagué J (2012) TGFβ signalling in context. Nat Rev Mol Cell Biol 13:616–630

    Article  Google Scholar 

  • Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495

    Article  Google Scholar 

  • McCarthy JJ, Mula J, Miyazaki M, Erfani R, Garrison K, Farooqui AB, Srikuea R, Lawson BA, Grimes B, Keller C et al (2011) Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development 138:3657–3666

    Article  Google Scholar 

  • Meng J, Muntoni F, Morgan JE (2011) Stem cells to treat muscular dystrophies – Where are we? Neuromuscul Disord 21:4–12

    Article  Google Scholar 

  • Meng J, Chun S, Asfahani R, Lochmüller H, Muntoni F, Morgan J (2014) Human skeletal muscle-derived CD133(+) cells form functional satellite cells after intramuscular transplantation in immunodeficient host mice. Mol Ther 22:1008–1017

    Article  Google Scholar 

  • Meng J, Muntoni F, Morgan J (2018) CD133+ cells derived from skeletal muscles of Duchenne muscular dystrophy patients have a compromised myogenic and muscle regenerative capability. Stem Cell Res 30:43–52

    Article  Google Scholar 

  • Minasi MG, Riminucci M, De Angelis L, Borello U, Berarducci B, Innocenzi A, Caprioli A, Sirabella D, Baiocchi M, De Maria R et al (2002) The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 129:2773–2783

    Google Scholar 

  • Mintz B, Baker WW (1967) Normal mammalian muscle differentiation and gene control of isocitrate dehydrogenase synthesis. Proc Natl Acad Sci USA 58:592–598

    Article  Google Scholar 

  • Mitchell KJ, Pannérec A, Cadot B, Parlakian A, Besson V, Gomes ER, Marazzi G, Sassoon DA (2010) Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat Cell Biol 12:257–266

    Article  Google Scholar 

  • Moncaut N, Rigby PWJ, Carvajal JJ (2013) Dial M(RF) for myogenesis. FEBS J 280:3980–3990

    Article  Google Scholar 

  • Montanaro F, Liadaki K, Schienda J, Flint A, Gussoni E, Kunkel LM (2004) Demystifying SP cell purification: viability, yield, and phenotype are defined by isolation parameters. Exp Cell Res 298:144–154

    Article  Google Scholar 

  • Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A, Partridge T, Buckingham M (2005) Direct isolation of satellite cells for skeletal muscle regeneration. Science 309:2064–2067

    Article  Google Scholar 

  • Morosetti R, Mirabella M, Gliubizzi C, Broccolini A, De Angelis L, Tagliafico E, Sampaolesi M, Gidaro T, Papacci M, Roncaglia E et al (2006) MyoD expression restores defective myogenic differentiation of human mesoangioblasts from inclusion-body myositis muscle. Proc Natl Acad Sci USA 103:16995–17000

    Article  Google Scholar 

  • Morosetti R, Mirabella M, Gliubizzi C, Broccolini A, Sancricca C, Pescatori M, Gidaro T, Tasca G, Frusciante R, Tonali PA et al (2007) Isolation and characterization of mesoangioblasts from facioscapulohumeral muscular dystrophy muscle biopsies. Stem Cells 25:3173–3182

    Article  Google Scholar 

  • Morosetti R, Gidaro T, Broccolini A, Gliubizzi C, Sancricca C, Tonali PA, Ricci E, Mirabella M (2011) Mesoangioblasts from facioscapulohumeral muscular dystrophy display in vivo a variable myogenic ability predictable by their in vitro behavior. Cell Transplant 20:1299–1313

    Article  Google Scholar 

  • Motohashi N, Asakura Y, Asakura A (2014) Isolation, culture, and transplantation of muscle satellite cells. J Vis Exp e50846. https://doi.org/10.3791/50846

  • Moyle LA, Zammit PS (2014) Isolation, culture and immunostaining of skeletal muscle fibres to study myogenic progression in satellite cells. Methods Mol Biol 1210:63–78

    Article  Google Scholar 

  • Naldaiz-Gastesi N, Goicoechea M, Alonso-Martín S, Aiastui A, López-Mayorga M, García-Belda P, Lacalle J, San José C, Araúzo-Bravo MJ, Trouilh L et al (2016) Identification and characterization of the dermal panniculus carnosus muscle stem cells. Stem Cell Reports 7:411–424

    Article  Google Scholar 

  • Negroni E, Riederer I, Chaouch S, Belicchi M, Razini P, Di Santo J, Torrente Y, Butler-Browne GS, Mouly V (2009) In vivo myogenic potential of human CD133+ muscle-derived stem cells: a quantitative study. Mol Ther 17:1771–1778

    Article  Google Scholar 

  • Negroni E, Bigot A, Butler-Browne GS, Trollet C, Mouly V (2016) Cellular therapies for muscular dystrophies: frustrations and clinical successes. Hum Gene Ther 27:117–126

    Article  Google Scholar 

  • Negroni E, Vallese D, Vilquin JT, Butler-Browne G, Mouly V, Trollet C (2011) Current advances in cell therapy strategies for muscular dystrophies. Expert Opin Biol Ther 11:157–76

    Article  Google Scholar 

  • Nehls V, Denzer K, Drenckhahn D (1992) Pericyte involvement in capillary sprouting during angiogenesis in situ. Cell Tissue Res 270:469–474

    Article  Google Scholar 

  • Ontell M, Hughes D, Bourke D (1982) Secondary myogenesis of normal muscle produces abnormal myotubes. Anat Rec 204:199–207

    Article  Google Scholar 

  • Ortuste Quiroga HP, Goto K, Zammit PS (2016) Isolation, cryosection and immunostaining of skeletal muscle. Methods Mol Biol 1460:85–100

    Article  Google Scholar 

  • Ozerdem U, Stallcup WB (2003) Early contribution of pericytes to angiogenic sprouting and tube formation. Angiogenesis 6:241–249

    Article  Google Scholar 

  • Pannerec A, Formicola L, Besson V, Marazzi G, Sassoon DA (2013) Defining skeletal muscle resident progenitors and their cell fate potentials. Development 140:2879–2891

    Article  Google Scholar 

  • Pawlikowski B, Lee L, Zuo J, Kramer RH (2009) Analysis of human muscle stem cells reveals a differentiation-resistant progenitor cell population expressing Pax7 capable of self-renewal. Dev Dyn 238:138–149

    Article  Google Scholar 

  • Pelagiadis I, Relakis K, Kalmanti L, Dimitriou H (2012) CD133 immunomagnetic separation: effectiveness of the method for CD133(+) isolation from umbilical cord blood. Cytotherapy 14:701–706

    Article  Google Scholar 

  • Périé S, Trollet C, Mouly V, Vanneaux V, Mamchaoui K, Bouazza B, Marolleau JP, Laforêt P, Chapon F, Eymard B et al (2014) Autologous myoblast transplantation for oculopharyngeal muscular dystrophy: a phase I/IIa clinical study. Mol Ther 22:219–225

    Article  Google Scholar 

  • Pette D, Spamer C (1986) Metabolic properties of muscle fibers. Fed Proc 45:2910–2914

    Google Scholar 

  • Pisani DF, Clement N, Loubat A, Plaisant M, Sacconi S, Kurzenne J-Y, Desnuelle C, Dani C, Dechesne CA (2010) Hierarchization of myogenic and adipogenic progenitors within human skeletal muscle. Stem Cells 28:2182–2194

    Article  Google Scholar 

  • Pisconti A, Bernet JD, Olwin BB (2012) Syndecans in skeletal muscle development, regeneration and homeostasis. Muscles Ligaments Tendons J 2:1–9

    Google Scholar 

  • Pogogeff IA, Murray MR (1946) Form and behavior of adult mammalian skeletal muscle in vitro. Anat Rec 95:321–335

    Article  Google Scholar 

  • Porpiglia E, Samusik N, Van Ho AT, Cosgrove BD, Mai T, Davis KL, Jager A, Nolan GP, Bendall SC, Fantl WJ et al (2017) High-resolution myogenic lineage map** by single-cell mass cytometry. Nat Cell Biol 19:558–567

    Article  Google Scholar 

  • Quarta M, Brett JO, DiMarco R, De Morree A, Boutet SC, Chacon R, Gibbons MC, Garcia VA, Su J, Shrager JB et al (2016) An artificial niche preserves the quiescence of muscle stem cells and enhances their therapeutic efficacy. Nat Biotechnol 34:752–759

    Article  Google Scholar 

  • Rao L, Qian Y, Khodabukus A, Ribar T, Bursac N (2018) Engineering human pluripotent stem cells into a functional skeletal muscle tissue. Nat Commun 9:126

    Article  Google Scholar 

  • Reimann J, Brimah K, Schroder R, Wernig A, Beauchamp JR, Partridge TA (2004) Pax7 distribution in human skeletal muscle biopsies and myogenic tissue cultures. Cell Tissue Res 315:233–242

    Article  Google Scholar 

  • Relaix F, Zammit PS (2012) Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Develepment 139:2845–2856

    Google Scholar 

  • Relaix F, Montarras D, Zaffran S, Gayraud-Morel B, Rocancourt D, Tajbakhsh S, Mansouri A, Cumano A, Buckingham M (2006) Pax3 and Pax7 have distinct and overlap** functions in adult muscle progenitor cells. J Cell Biol 172:91–102

    Article  Google Scholar 

  • Richler C, Yaffe D (1970) The in vitro cultivation and differentiation capacities of myogenic cell lines. Dev Biol 23:1–22

    Article  Google Scholar 

  • Rivier F (2004) Role of bone marrow cell trafficking in replenishing skeletal muscle SP and MP cell populations. J Cell Sci 117:1979–1988

    Article  Google Scholar 

  • Rosen GD, Sanes JR, LaChance R, Cunningham JM, Roman J, Dean DC (1992) Roles for the integrin VLA-4 and its counter receptor VCAM-1 in myogenesis. Cell 69:1107–1119

    Article  Google Scholar 

  • Rosenblatt JD (1992) A time course study of the isometric contractile properties of rat extensor digitorum longus muscle injected with bupivacaine. Comp Biochem Physiol Comp Physiol 101:361–367

    Article  Google Scholar 

  • Saini J, McPhee JS, Al-Dabbagh S, Stewart CE, Al-Shanti N (2016) Regenerative function of immune system: Modulation of muscle stem cells. Ageing Res Rev 27:67–76

    Article  Google Scholar 

  • Sambasivan R, Gayraud-Morel B, Dumas G, Cimper C, Paisant S, Kelly RG, Tajbakhsh S (2009) Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Dev Cell 16:810–821

    Article  Google Scholar 

  • Sampaolesi M, Torrente Y, Innocenzi A, Tonlorenzi R, D’Antona G, Pellegrino MA, Barresi R, Bresolin N, De Angelis MGC, Campbell KP et al (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301:487–492

    Article  Google Scholar 

  • Sancricca C (2010) Vessel-associated stem cells from skeletal muscle: from biology to future uses in cell therapy. World J Stem Cells 2:39

    Article  Google Scholar 

  • Scharner J, Zammit PS (2011) The muscle satellite cell at 50: the formative years. Skelet Muscle 1:28

    Article  Google Scholar 

  • Schmalbruch H (1976) The morphology of regeneration of skeletal muscles in the rat. Tissue Cell 8:673–692

    Article  Google Scholar 

  • Schultz E, Gibson MC, Champion T (1978) Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J Exp Zool 206:451–456

    Article  Google Scholar 

  • Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–786

    Article  Google Scholar 

  • Serena E, Zatti S, Zoso A, Lo Verso F, Tedesco FS, Cossu G, Elvassore N (2016) Skeletal muscle differentiation on a chip shows human donor mesoangioblasts’ efficiency in restoring dystrophin in a duchenne muscular dystrophy model. Stem Cells Transl Med 5:1676

    Article  Google Scholar 

  • Shefer G, Van de Mark DP, Richardson JB, Yablonka-Reuveni Z (2006) Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev Biol 294:50–66

    Article  Google Scholar 

  • Shefer G, Rauner G, Yablonka-Reuveni Z, Benayahu D (2010) Reduced satellite cell numbers and myogenic capacity in aging can be alleviated by endurance exercise. PLoS One 5:e13307

    Article  Google Scholar 

  • Shelton M, Metz J, Liu J, Carpenedo RL, Demers S-P, Stanford WL, Skerjanc IS (2014) Derivation and expansion of PAX7-positive muscle progenitors from human and mouse embryonic stem cells. Stem Cell Reports 3:516–529

    Article  Google Scholar 

  • Shelton M, Kocharyan A, Liu J, Skerjanc IS, Stanford WL (2016) Robust generation and expansion of skeletal muscle progenitors and myocytes from human pluripotent stem cells. Methods 101:73–84

    Article  Google Scholar 

  • Shen W, Li Y, Tang Y, Cummins J, Huard J (2005) NS-398, a cyclooxygenase-2-specific inhibitor, delays skeletal muscle healing by decreasing regeneration and promoting fibrosis. Am J Pathol 167:1105–1117

    Article  Google Scholar 

  • Sherwood RI, Christensen JL, Conboy IM, Conboy MJ, Rando TA, Weissman IL, Wagers AJ (2004) Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle. Cell 119:543–554

    Article  Google Scholar 

  • Sinha-Hikim I, Taylor WE, Gonzalez-Cadavid NF, Zheng W, Bhasin S (2004) Androgen receptor in human skeletal muscle and cultured muscle satellite cells: up-regulation by androgen treatment. J Clin Endocrinol Metab 89:5245–5255

    Article  Google Scholar 

  • Smith AST, Davis J, Lee G, Mack DL, Kim D-H (2016) Muscular dystrophy in a dish: engineered human skeletal muscle mimetics for disease modeling and drug discovery. Drug Discov Today 21:1387

    Article  Google Scholar 

  • Springer ML, Ozawa CR, Blau HM (2002) Transient production of ?-smooth muscle actin by skeletal myoblasts during differentiation in culture and following intramuscular implantation. Cell Motil Cytoskeleton 51:177–186

    Article  Google Scholar 

  • Steele-Stallard HB, Pinton L, Sarcar S, Ozdemir T, Maffioletti SM, Zammit PS, Tedesco FS (2018) Modeling skeletal muscle laminopathies using human induced pluripotent stem cells carrying pathogenic LMNA mutations. Front Physiol 9:1332

    Article  Google Scholar 

  • Strömberg A, Jansson M, Fischer H, Rullman E, Hägglund H, Gustafsson T (2013) Bone marrow derived cells in adult skeletal muscle tissue in humans. Skelet Muscle 3:12

    Article  Google Scholar 

  • Stumm J, Vallecillo-García P, Vom Hofe-Schneider S, Ollitrault D, Schrewe H, Economides AN, Marazzi G, Sassoon DA, Stricker S (2018) Odd skipped-related 1 (Osr1) identifies muscle-interstitial fibro-adipogenic progenitors (FAPs) activated by acute injury. Stem Cell Res 32:8–16

    Article  Google Scholar 

  • Swartz EW, Baek J, Pribadi M, Wojta KJ, Almeida S, Karydas A, Gao F-B, Miller BL, Coppola G (2016) A novel protocol for directed differentiation of C9orf72-associated human induced pluripotent stem cells into contractile skeletal myotubes. Stem Cells Transl Med 5:1461

    Article  Google Scholar 

  • Tajbakhsh S, Bober E, Babinet C, Pournin S, Arnold H, Buckingham M (1996) Gene targeting the myf-5 locus with nlacZ reveals expression of this myogenic factor in mature skeletal muscle fibres as well as early embryonic muscle. Dev Dyn 206:291–300

    Article  Google Scholar 

  • Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676

    Article  Google Scholar 

  • Takano H, Komuro I, Oka T, Shiojima I, Hiroi Y, Mizuno T, Yazaki Y (1998) The Rho family G proteins play a critical role in muscle differentiation. Mol Cell Biol 18:1580–1589

    Article  Google Scholar 

  • Tamaki T, Akatsuka A, Yoshimura S, Roy RR, Edgerton VR (2002) New fiber formation in the interstitial spaces of rat skeletal muscle during postnatal growth. J Histochem Cytochem 50:1097–1111

    Article  Google Scholar 

  • Tamaki T, Akatsuka A, Okada Y, Matsuzaki Y, Okano H, Kimura M (2003) Growth and differentiation potential of main- and side-population cells derived from murine skeletal muscle. Exp Cell Res 291:83–90

    Article  Google Scholar 

  • Tanaka KK, Hall JK, Troy AA, Cornelison DDW, Majka SM, Olwin BB (2009) Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration. Cell Stem Cell 4:217–225

    Article  Google Scholar 

  • Tedesco FS, Dellavalle A, Diaz-Manera J, Messina G, Cossu G (2010) Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J Clin Invest 120:11–19

    Article  Google Scholar 

  • Tedesco FS, Gerli MFM, Perani L, Benedetti S, Ungaro F, Cassano M, Antonini S, Tagliafico E, Artusi V, Longa E et al (2012) Transplantation of genetically corrected human iPSC-derived progenitors in mice with limb-girdle muscular dystrophy. Sci Transl Med 4:140ra89–140ra89

    Article  Google Scholar 

  • Tierney MT, Sacco A (2016) Satellite cell heterogeneity in skeletal muscle homeostasis. Trends Cell Biol 26:434–444

    Article  Google Scholar 

  • Torrente Y, Belicchi M, Sampaolesi M, Pisati F, Meregalli M, D’Antona G, Tonlorenzi R, Porretti L, Gavina M, Mamchaoui K et al (2004) Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest 114:182–195

    Article  Google Scholar 

  • Torrente Y, Belicchi M, Marchesi C, D’Antona G, Cogiamanian F, Pisati F, Gavina M, Giordano R, Tonlorenzi R, Fagiolari G et al (2007) Autologous transplantation of muscle-derived CD133+ stem cells in Duchenne muscle patients. Cell Transplant 16:563–577

    Article  Google Scholar 

  • Uezumi A, Fukada S, Yamamoto N, Takeda S’i, Tsuchida K (2010) Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol 12:143–152

    Article  Google Scholar 

  • Uezumi A, Ito T, Morikawa D, Shimizu N, Yoneda T, Segawa M, Yamaguchi M, Ogawa R, Matev MM, Miyagoe-Suzuki Y et al (2011) Fibrosis and adipogenesis originate from a common mesenchymal progenitor in skeletal muscle. J Cell Sci 124:3654–3664

    Article  Google Scholar 

  • van Velthoven CTJ, de Morree A, Egner IM, Brett JO, Rando TA (2017) Transcriptional profiling of quiescent muscle stem cells in vivo. Cell Rep 21:1994–2004

    Article  Google Scholar 

  • Vilquin J-T, Catelain C, Vauchez K (2011) Cell therapy for muscular dystrophies: advances and challenges. Curr Opin Organ Transplant 16:640–649

    Article  Google Scholar 

  • Volonte D, Liu Y, Galbiati F (2005) The modulation of caveolin-1 expression controls satellite cell activation during muscle repair. FASEB J 19:237–239

    Article  Google Scholar 

  • Walsh FS, Ritter MA (1981) Surface antigen differentiation during human myogenesis in culture. Nature 289:60–64

    Article  Google Scholar 

  • Weintraub H (1993) The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75:1241–1244

    Article  Google Scholar 

  • Wernig G, Janzen V, Schäfer R, Zweyer M, Knauf U, Hoegemeier O, Mundegar RR, Garbe S, Stier S, Franz T et al (2005) The vast majority of bone-marrow-derived cells integrated into mdx muscle fibers are silent despite long-term engraftment. Proc Natl Acad Sci USA 102:11852–11857

    Article  Google Scholar 

  • Whalen RG, Harris JB, Butler-Browne GS, Sesodia S (1990) Expression of myosin isoforms during notexin-induced regeneration of rat soleus muscles. Dev Biol 141:24–40

    Article  Google Scholar 

  • Xu X, Wilschut KJ, Kouklis G, Tian H, Hesse R, Garland C, Sbitany H, Hansen S, Seth R, Knott PD et al (2015) Human satellite cell transplantation and regeneration from diverse skeletal muscles. Stem Cell Reports 5:419–434

    Article  Google Scholar 

  • Xu C-Y, Liu S-Q, Qin M-B, Zhuge C-F, Qin L, Qin N, Lai M-Y, Huang J-A (2017) SphK1 modulates cell migration and EMT-related marker expression by regulating the expression of p-FAK in colorectal cancer cells. Int J Mol Med 39:1277–1284

    Article  Google Scholar 

  • Yablonka-Reuveni Z (2011) The skeletal muscle satellite cell: still young and fascinating at 50. J Histochem Cytochem 59:1041–1059

    Article  Google Scholar 

  • Yamaguchi M, Ogawa R, Watanabe Y, Uezumi A, Miyagoe-Suzuki Y, Tsujikawa K, Yamamoto H, Takeda S, Fukada S (2012) Calcitonin receptor and Odz4 are differently expressed in Pax7-positive cells during skeletal muscle regeneration. J Mol Histol 43:581–587

    Article  Google Scholar 

  • Yao Y, Norris EH, Mason EC, Strickland S (2016) Laminin regulates PDGFRβ+ cell stemness and muscle development. Nat Commun 7:11415

    Article  Google Scholar 

  • Yin H, Price F, Rudnicki MA (2013) Satellite cells and the muscle stem cell niche. Physiol Rev 93:23–67

    Article  Google Scholar 

  • Young CS, Hicks MR, Ermolova NV, Nakano H, Jan M, Younesi S, Karumbayaram S, Kumagai-Cresse C, Wang D, Zack JA, Kohn DB, Nakano A, Nelson SF, Miceli MC, Spencer MJ, Pyle AD (2016) A single CRISPR-cas9 deletion strategy that targets the majority of DMD patients restores dystrophin function in hiPSC-derived muscle cells. Cell Stem Cell 18:533–540

    Article  Google Scholar 

  • Zammit PS (2008) All muscle satellite cells are equal, but are some more equal than others? J Cell Sci 121:2975–2982

    Article  Google Scholar 

  • Zammit PS (2017) Function of the myogenic regulatory factors Myf5, MyoD, Myogenin and MRF4 in skeletal muscle, satellite cells and regenerative myogenesis. Semin Cell Dev Biol 72:19–32

    Article  Google Scholar 

  • Zammit PS, Heslop L, Hudon V, Rosenblatt JD, Tajbakhsh S, Buckingham ME, Beauchamp JR, Partridge TA (2002) Kinetics of myoblast proliferation show that resident satellite cells are competent to fully regenerate skeletal muscle fibers. Exp Cell Res 281:39–49

    Article  Google Scholar 

  • Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR (2004) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166:347–357

    Article  Google Scholar 

  • Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA, Partridge TA, Beauchamp JR (2006) Pax7 and myogenic progression in skeletal muscle satellite cells. J Cell Sci 119:1824–1832

    Article  Google Scholar 

  • Zeng W, Jiang S, Kong X, El-Ali N, Ball AR, Ma CI-H, Hashimoto N, Yokomori K, Mortazavi A (2016) Single-nucleus RNA-seq of differentiating human myoblasts reveals the extent of fate heterogeneity. Nucleic Acids Res 44:e158. gkw739

    Google Scholar 

  • Zheng B, Cao B, Crisan M, Sun B, Li G, Logar A, Yap S, Pollett JB, Drowley L, Cassino T et al (2007) Prospective identification of myogenic endothelial cells in human skeletal muscle. Nat Biotechnol 25:1025–1034

    Article  Google Scholar 

  • Zuba-Surma EK, Kucia M, Ratajczak J, Ratajczak MZ (2009) “Small stem cells” in adult tissues: very small embryonic-like stem cells stand up! Cytom Part A 75:4–13

    Article  Google Scholar 

Download references

Acknowledgment

JP is supported by a Wellcome Trust PhD Studentship [203949/Z/16/A]. The Zammit laboratory is supported by the Medical Research Council [MR/P023215/1 and MR/S002472/1], FSH Society Shack Family and Friends research grant [FSHS-82013-06], and Association Française contre les Myopathies [AFM 17865 and 20082].

Author information

Authors and Affiliations

  1. Randall Centre for Cell and Molecular Biophysics, King’s College London, London, UK

    Johanna Pruller & Peter S. Zammit

Authors
  1. Johanna Pruller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter S. Zammit
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Johanna Pruller or Peter S. Zammit .

Editor information

Editors and Affiliations

  1. Tulane Univ. Sch. of Medicine, New Orleans, LA, USA

    Jeffrey M. Gimble

  2. AUVA Center, Ludwig Boltzmann Institute for Experimen, Vienna, Austria

    Darja Marolt

  3. Human Development and Health, University of Southampton, Southampton, UK

    Richard Oreffo

  4. Experimental and Clinical Traumatol, Ludwig Boltzmann Institute for, Wien, Austria

    Heinz Redl

  5. AUVA Center, Ludwig Boltzmann Institute for Experimen, Vienna, Austria

    Susanne Wolbank

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this entry

Check for updates. Verify currency and authenticity via CrossMark

Cite this entry

Pruller, J., Zammit, P.S. (2019). Overview of Cell Types Capable of Contributing to Skeletal Muscle Repair and Regeneration. In: Gimble, J., Marolt, D., Oreffo, R., Redl, H., Wolbank, S. (eds) Cell Engineering and Regeneration. Reference Series in Biomedical Engineering(). Springer, Cham. https://doi.org/10.1007/978-3-319-37076-7_2-1

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-37076-7_2-1

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-37076-7

  • Online ISBN: 978-3-319-37076-7

  • eBook Packages: Springer Reference EngineeringReference Module Computer Science and Engineering

Publish with us

Policies and ethics

Search

Navigation