Abstract
Stem cell therapy has been envisaged for treating disorders affecting skeletal muscle tissue. Several cell types have been identified for exerting a myogenic potential in certain conditions. In order to efficiently regenerate injured muscles while remaining safe for patients, these myogenic progenitors should present characteristics such as their availability to be isolated from patients, their growth and commitment performances and, if necessary, their capacity to be genetically corrected. Here, we present an overview of the main myogenic cell candidates that have been identified and tested in vivo, classifying them by their route of delivery (intra-muscular and systemic delivery), and focusing our attention on their regenerative capacity in animal models of Duchenne muscular dystrophy.
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References
Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495
Christov C, Chretien F, Abou-Khalil R, Bassez G, Vallet G, Authier FJ, Bassaglia Y, Shinin V, Tajbakhsh S, Chazaud B, Gherardi RK (2007) Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol Biol Cell 18:1397–1409
Edom-Vovard F, Mouly V, Barbet JP, Butler-Browne GS (1999) The four populations of myoblasts involved in human limb muscle formation are present from the onset of primary myotube formation. J Cell Sci 112(Pt 2):191–199
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
Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91:534–551
Zammit PS, Partridge TA, Yablonka-Reuveni Z (2006) The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histochem Cytochem 54:1177–1191
Peault B, Rudnicki M, Torrente Y, Cossu G, Tremblay JP, Partridge T, Gussoni E, Kunkel LM, Huard J (2007) Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 15:867–877
Rudnicki MA, Le Grand F, McKinnell I, Kuang S (2008) The molecular regulation of muscle stem cell function. Cold Spring Harb Symp Quant Biol 73:323–331
Kuang S, Rudnicki MA (2008) The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med 14:82–91
Asakura A, Komaki M, Rudnicki M (2001) Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation 68:245–253
Shinin V, Gayraud-Morel B, Gomes D, Tajbakhsh S (2006) Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8:677–687
Decary S, Mouly V, Hamida CB, Sautet A, Barbet JP, Butler-Browne GS (1997) Replicative potential and telomere length in human skeletal muscle: implications for satellite cell-mediated gene therapy. Hum Gene Ther 8:1429–1438
Charge SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84:209–238
Schultz E, Jaryszak DL, Valliere CR (1985) Response of satellite cells to focal skeletal muscle injury. Muscle Nerve 8:217–222
Cooper RN, Tajbakhsh S, Mouly V, Cossu G, Buckingham M, Butler-Browne GS (1999) In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J Cell Sci 112(Pt 17):2895–2901
Cornelison DD, Olwin BB, Rudnicki MA, Wold BJ (2000) MyoD(−/−) satellite cells in single-fiber culture are differentiation defective and MRF4 deficient. Dev Biol 224:122–137
Fuchtbauer EM, Westphal H (1992) MyoD and myogenin are coexpressed in regenerating skeletal muscle of the mouse. Dev Dyn 193:34–39
Megeney LA, Kablar B, Garrett K, Anderson JE, Rudnicki MA (1996) MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev 10:1173–1183
Smythe GM, Grounds MD (2001) Absence of MyoD increases donor myoblast migration into host muscle. Exp Cell Res 267:267–274
Rhodes SJ, Konieczny SF (1989) Identification of MRF4: a new member of the muscle regulatory factor gene family. Genes Dev 3:2050–2061
Wright WE, Sassoon DA, Lin VK (1989) Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56:607–617
Hasty P, Bradley A, Morris JH, Edmondson DG, Venuti JM, Olson EN, Klein WH (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364:501–506
Nabeshima Y, Hanaoka K, Hayasaka M, Esumi E, Li S, Nonaka I, Nabeshima Y (1993) Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364:532–535
Villalta SA, Deng B, Rinaldi C, Wehling-Henricks M, Tidball JG (2011) IFN-gamma promotes muscle damage in the mdx mouse model of Duchenne muscular dystrophy by suppressing M2 macrophage activation and inhibiting muscle cell proliferation. J Immunol 187:5419–5428
Serrano AL, Munoz-Canoves P (2010) Regulation and dysregulation of fibrosis in skeletal muscle. Exp Cell Res 316:3050–3058
Manzur AY, Kuntzer T, Pike M, Swan A (2008) Glucocorticoid corticosteroids for Duchenne muscular dystrophy. Cochrane Database Syst Rev CD003725
Partridge TA, Morgan JE, Coulton GR, Hoffman EP, Kunkel LM (1989) Conversion of mdx myofibres from dystrophin-negative to -positive by injection of normal myoblasts. Nature 337:176–179
Fanin M, Hoffman EP, Saad FA, Martinuzzi A, Danieli GA, Angelini C (1993) Dystrophin-positive myotubes in innervated muscle cultures from Duchenne and Becker muscular dystrophy patients. Neuromuscul Disord 3:119–127
Partridge T (2000) The current status of myoblast transfer. Neurol Sci 21:S939–S942
Cossu G, Sampaolesi M (2007) New therapies for Duchenne muscular dystrophy: challenges, prospects and clinical trials. Trends Mol Med 13:520–526
Gussoni E, Pavlath GK, Lanctot AM, Sharma KR, Miller RG, Steinman L, Blau HM (1992) Normal dystrophin transcripts detected in Duchenne muscular dystrophy patients after myoblast transplantation. Nature 356:435–438
Karpati G, Ajdukovic D, Arnold D, Gledhill RB, Guttmann R, Holland P, Koch PA, Shoubridge E, Spence D, Vanasse M et al (1993) Myoblast transfer in Duchenne muscular dystrophy. Ann Neurol 34:8–17
Fan Y, Maley M, Beilharz M, Grounds M (1996) Rapid death of injected myoblasts in myoblast transfer therapy. Muscle Nerve 19:853–860
Beauchamp JR, Morgan JE, Pagel CN, Partridge TA (1999) Dynamics of myoblast transplantation reveal a discrete minority of precursors with stem cell-like properties as the myogenic source. J Cell Biol 144:1113–1122
Guerette B, Skuk D, Celestin F, Huard C, Tardif F, Asselin I, Roy B, Goulet M, Roy R, Entman M, Tremblay JP (1997) Prevention by anti-LFA-1 of acute myoblast death following transplantation. J Immunol 159:2522–2531
Sammels LM, Bosio E, Fragall CT, Grounds MD, van Rooijen N, Beilharz MW (2004) Innate inflammatory cells are not responsible for early death of donor myoblasts after myoblast transfer therapy. Transplantation 77:1790–1797
Skuk D, Caron NJ, Goulet M, Roy B, Tremblay JP (2003) Resetting the problem of cell death following muscle-derived cell transplantation: detection, dynamics and mechanisms. J Neuropathol Exp Neurol 62:951–967
Cooper RN, Thiesson D, Furling D, Di Santo JP, Butler-Browne GS, Mouly V (2003) Extended amplification in vitro and replicative senescence: key factors implicated in the success of human myoblast transplantation. Hum Gene Ther 14:1169–1179
Hayflick L (1965) The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 37:614–636
Riederer I, Negroni E, Bencze M, Wolff A, Aamiri A, Di Santo JP, Silva-Barbosa SD, Butler-Browne G, Savino W, Mouly V (2012) Slowing down differentiation of engrafted human myoblasts into immunodeficient mice correlates with increased proliferation and migration. Mol Ther 20:146–154
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
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
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
Lipton BH, Schultz E (1979) Developmental fate of skeletal muscle satellite cells. Science 205:1292–1294
Rando TA, Pavlath GK, Blau HM (1995) The fate of myoblasts following transplantation into mature muscle. Exp Cell Res 220:383–389
Skuk D, Roy B, Goulet M, Tremblay JP (1999) Successful myoblast transplantation in primates depends on appropriate cell delivery and induction of regeneration in the host muscle. Exp Neurol 155:22–30
Quenneville SP, Chapdelaine P, Skuk D, Paradis M, Goulet M, Rousseau J, Xiao X, Garcia L, Tremblay JP (2007) Autologous transplantation of muscle precursor cells modified with a lentivirus for muscular dystrophy: human cells and primate models. Mol Ther 15:431–438
Morgan JE, Pagel CN, Sherratt T, Partridge TA (1993) Long-term persistence and migration of myogenic cells injected into pre-irradiated muscles of mdx mice. J Neurol Sci 115:191–200
Silva-Barbosa SD, Butler-Browne GS, de Mello W, Riederer I, Di Santo JP, Savino W, Mouly V (2008) Human myoblast engraftment is improved in laminin-enriched microenvironment. Transplantation 85:566–575
El Fahime E, Mills P, Lafreniere JF, Torrente Y, Tremblay JP (2002) The urokinase plasminogen activator: an interesting way to improve myoblast migration following their transplantation. Exp Cell Res 280:169–178
Morgan J, Rouche A, Bausero P, Houssaini A, Gross J, Fiszman MY, Alameddine HS (2010) MMP-9 overexpression improves myogenic cell migration and engraftment. Muscle Nerve 42:584–595
Skuk D, Goulet M, Roy B, Chapdelaine P, Bouchard JP, Roy R, Dugre FJ, Sylvain M, Lachance JG, Deschenes L, Senay H, Tremblay JP (2006) Dystrophin expression in muscles of duchenne muscular dystrophy patients after high-density injections of normal myogenic cells. J Neuropathol Exp Neurol 65:371–386
Skuk D, Goulet M, Roy B, Piette V, Cote CH, Chapdelaine P, Hogrel JY, Paradis M, Bouchard JP, Sylvain M, Lachance JG, Tremblay JP (2007) First test of a "high-density injection" protocol for myogenic cell transplantation throughout large volumes of muscles in a Duchenne muscular dystrophy patient: eighteen months follow-up. Neuromuscul Disord 17:38–46
Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L, Innocenzi A, Galvez BG, Messina G, Morosetti R, Li S, Belicchi M, Peretti G, Chamberlain JS, Wright WE, Torrente Y, Ferrari S, Bianco P, Cossu G (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9:255–267
Gentry T, Foster S, Winstead L, Deibert E, Fiordalisi M, Balber A (2007) Simultaneous isolation of human BM hematopoietic, endothelial and mesenchymal progenitor cells by flow sorting based on aldehyde dehydrogenase activity: implications for cell therapy. Cytotherapy 9:259–274
Mitchell JB, McIntosh K, Zvonic S, Garrett S, Floyd ZE, Kloster A, Di Halvorsen Y, Storms RW, Goh B, Kilroy G, Wu X, Gimble JM (2006) Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 24:376–385
Vauchez K, Marolleau JP, Schmid M, Khattar P, Chapel A, Catelain C, Lecourt S, Larghero J, Fiszman M, Vilquin JT (2009) Aldehyde dehydrogenase activity identifies a population of human skeletal muscle cells with high myogenic capacities. Mol Ther 17:1948–1958
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
Xynos A, Corbella P, Belmonte N, Zini R, Manfredini R (2010) Ferrari G Bone marrow-derived hematopoietic cells undergo myogenic differentiation following a Pax-7 independent pathway. Stem Cells 28:965–973
Ferrari G, Stornaiuolo A, Mavilio F (2001) Failure to correct murine muscular dystrophy. Nature 411:1014–1015
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
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
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
Gavina M, Belicchi M, Rossi B, Ottoboni L, Colombo F, Meregalli M, Battistelli M, Forzenigo L, Biondetti P, Pisati F, Parolini D, Farini A, Issekutz AC, Bresolin N, Rustichelli F, Constantin G, Torrente Y (2006) VCAM-1 expression on dystrophic muscle vessels has a critical role in the recruitment of human blood-derived CD133+ stem cells after intra-arterial transplantation. Blood 108:2857–2866
Torrente Y, Tremblay JP, Pisati F, Belicchi M, Rossi B, Sironi M, Fortunato F, El Fahime M, D'Angelo MG, Caron NJ, Constantin G, Paulin D, Scarlato G, Bresolin N (2001) Intraarterial injection of muscle-derived CD34(+)Sca-1(+) stem cells restores dystrophin in mdx mice. J Cell Biol 152:335–348
Bachrach E, Perez AL, Choi YH, Illigens BM, Jun SJ, del Nido P, McGowan FX, Li S, Flint A, Chamberlain J, Kunkel LM (2006) Muscle engraftment of myogenic progenitor cells following intraarterial transplantation. Muscle Nerve 34:44–52
Motohashi N, Uezumi A, Yada E, Fukada S, Fukushima K, Imaizumi K, Miyagoe-Suzuki Y, Takeda S (2008) Muscle CD31(−) CD45(−) side population cells promote muscle regeneration by stimulating proliferation and migration of myoblasts. Am J Pathol 173:781–791
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
Minasi MG, Riminucci M, De Angelis L, Borello U, Berarducci B, Innocenzi A, Caprioli A, Sirabella D, Baiocchi M, De Maria R, Boratto R, Jaffredo T, Broccoli V, Bianco P, Cossu G (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
Cossu G, Bianco P (2003) Mesoangioblasts–vascular progenitors for extravascular mesodermal tissues. Curr Opin Genet Dev 13:537–542
Sampaolesi M, Torrente Y, Innocenzi A, Tonlorenzi R, D'Antona G, Pellegrino MA, Barresi R, Bresolin N, De Angelis MG, Campbell KP, Bottinelli R, Cossu G (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301:487–492
Sampaolesi M, Blot S, D'Antona G, Granger N, Tonlorenzi R, Innocenzi A, Mognol P, Thibaud JL, Galvez BG, Barthelemy I, Perani L, Mantero S, Guttinger M, Pansarasa O, Rinaldi C, Cusella De Angelis MG, Torrente Y, Bordignon C, Bottinelli R, Cossu G (2006) Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444:574–579
Torrente Y, Belicchi M, Sampaolesi M, Pisati F, Meregalli M, D'Antona G, Tonlorenzi R, Porretti L, Gavina M, Mamchaoui K, Pellegrino MA, Furling D, Mouly V, Butler-Browne GS, Bottinelli R, Cossu G, Bresolin N (2004) Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest 114:182–195
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
Benchaouir R, Meregalli M, Farini A, D'Antona G, Belicchi M, Goyenvalle A, Battistelli M, Bresolin N, Bottinelli R, Garcia L, Torrente Y (2007) Restoration of human dystrophin following transplantation of exon-skipping-engineered DMD patient stem cells into dystrophic mice. Cell Stem Cell 1:646–657
Shi M, Ishikawa M, Kamei N, Nakasa T, Adachi N, Deie M, Asahara T, Ochi M (2009) Acceleration of skeletal muscle regeneration in a rat skeletal muscle injury model by local injection of human peripheral blood-derived CD133-positive cells. Stem Cells 27:949–960
Torrente Y, Belicchi M, Marchesi C, Dantona G, Cogiamanian F, Pisati F, Gavina M, Giordano R, Tonlorenzi R, Fagiolari G, Lamperti C, Porretti L, Lopa R, Sampaolesi M, Vicentini L, Grimoldi N, Tiberio F, Songa V, Baratta P, Prelle A, Forzenigo L, Guglieri M, Pansarasa O, Rinaldi C, Mouly V, Butler-Browne GS, Comi GP, Biondetti P, Moggio M, Gaini SM, Stocchetti N, Priori A, D'Angelo MG, Turconi A, Bottinelli R, Cossu G, Rebulla P, Bresolin N (2007) Autologous transplantation of muscle-derived CD133+ stem cells in Duchenne muscle patients. Cell Transplant 16:563–577
Perie S, Mamchaoui K, Mouly V, Blot S, Bouazza B, Thornell LE, St Guily JL, Butler-Browne G (2006) Premature proliferative arrest of cricopharyngeal myoblasts in oculo-pharyngeal muscular dystrophy: therapeutic perspectives of autologous myoblast transplantation. Neuromuscul Disord 16:770–781
Riederer I, Negroni E, Bigot A, Bencze M, Di Santo J, Aamiri A, Butler-Browne G, Mouly V (2008) Heat shock treatment increases engraftment of transplanted human myoblasts into immunodeficient mice. Transplant Proc 40:624–630
Goudenege S, Pisani DF, Wdziekonski B, Di Santo JP, Bagnis C, Dani C, Dechesne CA (2009) Enhancement of myogenic and muscle repair capacities of human adipose-derived stem cells with forced expression of MyoD. Mol Ther 17:1064–1072
Jackson WM, Nesti LJ, Tuan RS (2010) Potential therapeutic applications of muscle-derived mesenchymal stem and progenitor cells. Expert Opin Biol Ther 10:505–517
Arnold L, Henry A, Poron F, Baba-Amer Y, van Rooijen N, Plonquet A, Gherardi RK, Chazaud B (2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204:1057–1069
Bencze M, Negroni E, Vallese D, Yacoub–Youssef H, Chaouch S, Wolff A, Aamiri A, Di Santo JP, Chazaud B, Butler-Browne G, Savino W, Mouly V, Riederer I (2012) Proinflammatory macrophages enhance the regenerative capacity of human myoblasts by modifying their kinetics of proliferation and differentiation. Mol Ther 20(11):2168–2179
Rossi CA, Flaibani M, Blaauw B, Pozzobon M, Figallo E, Reggiani C, Vitiello L, Elvassore N, De Coppi P (2011) In vivo tissue engineering of functional skeletal muscle by freshly isolated satellite cells embedded in a photopolymerizable hydrogel. FASEB J 25:2296–2304
Borselli C, Storrie H, Benesch-Lee F, Shvartsman D, Cezar C, Lichtman JW, Vandenburgh HH, Mooney DJ (2010) Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. Proc Natl Acad Sci U S A 107:3287–3292
Bodnar MS, Meneses JJ, Rodriguez RT, Firpo MT (2004) Propagation and maintenance of undifferentiated human embryonic stem cells. Stem Cells Dev 13:243–253
Barberi T, Bradbury M, Dincer Z, Panagiotakos G, Socci ND, Studer L (2007) Derivation of engraftable skeletal myoblasts from human embryonic stem cells. Nat Med 13:642–648
Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872
Darabi R, Arpke RW, Irion S, Dimos JT, Grskovic M, Kyba M, Perlingeiro RC (2012) Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell 10:610–619
Acknowledgements
The research conducted by the authors in the field of cell transplantation is supported by Association Française contre les Myopathies (AFM) and Association Institut de Myologie (AIM), Université Pierre et Marie Curie (UPMC), INSERM, CNRS, PHRC, ANR Genopath In-A-Fib, DPP-Nl and EC contract MYOAGE (contract HEALTH-F2-2009-223576) from the seventh FP.
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Bencze, M., Riederer, I., Butler-Browne, G.S., Savino, W., Mouly, V. (2013). Myogenic Potential of Stem Cells: In Vivo Assessment. In: Turksen, K. (eds) Stem Cells: Current Challenges and New Directions. Stem Cell Biology and Regenerative Medicine. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4614-8066-2_1
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