Recent progress in satellite cell/myoblast engraftment - Relevance for therapy

FEBS Journal

Volumn 280, Issue 17, 2013, Pages 4281-4293

  Briggs, Deborah ^a   Morgan, Jennifer E ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

cell therapy; Duchenne muscular dystrophy; mdx mouse; muscular dystrophy; myoblasts; satellite cells; skeletal muscle regeneration

Indexed keywords

DYSTROPHIN;

CELL FATE; CELL THERAPY; CELL TRANSPLANTATION; DUCHENNE MUSCULAR DYSTROPHY; ENGRAFTMENT; HUMAN; MUSCLE ATROPHY; MUSCLE INJURY; MYOBLAST; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; REVIEW; SATELLITE CELL;

CELL THERAPY; DUCHENNE MUSCULAR DYSTROPHY; MDX MOUSE; MUSCULAR DYSTROPHY; MYOBLASTS; SATELLITE CELLS; SKELETAL MUSCLE REGENERATION;

ANIMALS; GRAFT SURVIVAL; HUMANS; MUSCULAR DYSTROPHIES; MYOBLASTS; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84882707945     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12273     Document Type: Review

References (115)

1. Emery AE, (2002) The muscular dystrophies. Lancet 359, 687-695.
2. Hoffman EP, Brown RH Jr, &, Kunkel LM, (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51, 919-928.
3. Bonilla E, Samitt CE, Miranda AF, Hays AP, Salviati G, DiMauro S, Kunkel LM, Hoffman EP, &, Rowland LP,. (1988) Duchenne muscular dystrophy: deficiency of dystrophin at the muscle cell surface. Cell 54, 447-452.
4. Ervasti JM, (2007) Dystrophin, its interactions with other proteins, and implications for muscular dystrophy. Biochim Biophys Acta 1772, 108-117.
5. Morgan JE, &, Zammit PS, (2010) Direct effects of the pathogenic mutation on satellite cell function in muscular dystrophy. Exp Cell Res 316, 3100-3108.
6. 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.
7. 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.
8. Sacco A, Doyonnas R, Kraft P, Vitorovic S, &, Blau HM, (2008) Self-renewal and expansion of single transplanted muscle stem cells. Nature 456, 502-506.
9. Neal A, Boldrin L, &, Morgan JE, (2012) The satellite cell in male and female, developing and adult mouse muscle: distinct stem cells for growth and regeneration. PLoS One 7, e37950.
10. Rocheteau P, Gayraud-Morel B, Siegl-Cachedenier I, Blasco MA, &, Tajbakhsh S, (2012) A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell 148, 112-125.
11. 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.
12. Negroni E, Vallese D, Vilquin J-T, Butler-Browne G, Mouly V, &, Trollet C, (2011) Current advances in cell therapy strategies for muscular dystrophies. Expert Opin Biol Ther 11, 157-176.
13. Sampaolesi M, Torrente Y, Innocenzi A, Tonlorenzi R, D'Antona G, Pellegrino MA, Barresi R, Bresolin N, De Angelis MG, Campbell KP, et al,. (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301, 487-492.
14. Sampaolesi M, Blot S, D'Antona G, Granger N, Tonlorenzi R, Innocenzi A, Mognol P, Thibaud JL, Galvez BG, Barthélémy I, et al,. (2006) Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444, 574-579.
15. 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.
16. Dellavalle A, Maroli G, Covarello D, Azzoni E, Innocenzi A, Perani L, Antonini S, Sambasivan R, Brunelli S, Tajbakhsh S, &, Cossu G, (2011) Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat Commun 2, 499.
17. 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.
18. Torrente Y, Belicchi M, Marchesi C, Dantona 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.
19. 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.
20. 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.
21. De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, Mostoslavsky G, Serre AC, Snyder EY, Yoo JJ, et al,. (2007) Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 25, 100-106.
22. Ma X, Zhang S, Zhou J, Chen B, Shang Y, Gao T, Wang X, Xie H, &, Chen F, (2012) Clone-derived human AF-amniotic fluid stem cells are capable of skeletal myogenic differentiation in vitro and in vivo. J Tissue Eng Regen Med 6, 598-613.
23. Piccoli M, Franzin C, Bertin E, Urbani L, Blaauw B, Repele A, Taschin E, Cenedese A, Zanon GF, André-Schmutz I, et al,. (2012) Amniotic fluid stem cells restore the muscle cell niche in a HSA-Cre, Smn(F7/F7) mouse model. Stem Cells 30, 1675-1684.
24. 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.
25. Murphy MM, Lawson JA, Mathew SJ, Hutcheson DA, &, Kardon G, (2011) Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 138, 3625-3637.
26. Sambasivan R, Yao R, Kissenpfennig A, Van Wittenberghe L, Paldi A, Gayraud-Morel B, Guenou H, Malissen B, Tajbakhsh S, &, Galy A, (2011) Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 138, 3647-3656.
27. Relaix F, &, Zammit PS, (2012) Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 139, 2845-2856.
28. Partridge TA, Grounds M, &, Sloper JC, (1978) Evidence of fusion between host and donor myoblasts in skeletal muscle grafts. Nature 273, 306-308.
29. 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.
30. Partridge T, (2000) The current status of myoblast transfer. Neurol Sci 21, S939-S942.
31. 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.
32. Huard J, Roy R, Bouchard JP, Malouin F, Richards CL, &, Tremblay JP, (1992) Human myoblast transplantation between immunohistocompatible donors and recipients produces immune reactions. Transplant Proc 24, 3049-3051.
33. 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.
34. Tremblay JP, Bouchard JP, Malouin F, Théau D, Cottrell F, Collin H, Rouche A, Gilgenkrantz S, Abbadi N, Tremblay M, et al,. (1993) Myoblast transplantation between monozygotic twin girl carriers of Duchenne muscular dystrophy. Neuromuscul Disord 3, 583-592.
35. Tremblay JP, Malouin F, Roy R, Huard J, Bouchard JP, Satoh A, &, Richards CL, (1993) Results of a triple blind clinical study of myoblast transplantations without immunosuppressive treatment in young boys with Duchenne muscular dystrophy. Cell Transplant 2, 99-112.
36. Mendell JR, Kissel JT, Amato AA, King W, Signore L, Prior TW, Sahenk Z, Benson S, McAndrew PE, Rice R, et al,. (1995) Myoblast transfer in the treatment of Duchenne's muscular dystrophy. N Engl J Med 333, 832-838.
37. Morandi L, Bernasconi P, Gebbia M, Mora M, Crosti F, Mantegazza R, &, Cornelio F, (1995) Lack of mRNA and dystrophin expression in DMD patients three months after myoblast transfer. Neuromuscul Disord 5, 291-295.
38. Miller RG, Sharma KR, Pavlath GK, Gussoni E, Mynhier M, Lanctot AM, Greco CM, Steinman L, &, Blau HM, (1997) Myoblast implantation in Duchenne muscular dystrophy: the San Francisco study. Muscle Nerve 20, 469-478.
39. 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.
40. Skuk D, &, Tremblay JP, (2011) Intramuscular cell transplantation as a potential treatment of myopathies: clinical and preclinical relevant data. Expert Opin Biol Ther 11, 359-374.
41. Skuk D, Goulet M, Roy B, Chapdelaine P, Bouchard JP, Roy R, Dugré FJ, Sylvain M, Lachance JG, Deschênes L, et al,. (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.
42. Skuk D, Goulet M, Roy B, Piette V, Côté CH, Chapdelaine P, Hogrel JY, Paradis M, Bouchard JP, Sylvain M, et al,. (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.
43. Vilquin J-T, Catelain C, &, Vauchez K, (2011) Cell therapy for muscular dystrophies: advances and challenges. Curr Opin Organ Transplant 16, 640-649.
44. Périé 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.
45. Li S, Kimura E, Fall BM, Reyes M, Angello JC, Welikson R, Hauschka SD, &, Chamberlain JS, (2005) Stable transduction of myogenic cells with lentiviral vectors expressing a minidystrophin. Gene Ther 12, 1099-1108.
46. Wilson CA, &, Cichutek K, (2009) The US and EU regulatory perspectives on the clinical use of hematopoietic stem/progenitor cells genetically modified ex vivo by retroviral vectors. Methods Mol Biol 506, 477-488.
47. Ciuffi A, (2008) Mechanisms governing lentivirus integration site selection. Curr Gene Ther 8, 419-429.
48. Bokhoven M, Stephen SL, Knight S, Gevers EF, Robinson IC, Takeuchi Y, &, Collins MK, (2009) Insertional gene activation by lentiviral and gammaretroviral vectors. J Virol 83, 283-294.
49. Zhang F, Thornhill SI, Howe SJ, Ulaganathan M, Schambach A, Sinclair J, Kinnon C, Gaspar HB, Antoniou M, &, Thrasher AJ, (2007) Lentiviral vectors containing an enhancer-less ubiquitously acting chromatin opening element (UCOE) provide highly reproducible and stable transgene expression in hematopoietic cells. Blood 110, 1448-1457.
50. Rahim AA, Wong AM, Howe SJ, Buckley SM, Acosta-Saltos AD, Elston KE, Ward NJ, Philpott NJ, Cooper JD, Anderson PN, et al,. (2009) Efficient gene delivery to the adult and fetal CNS using pseudotyped non-integrating lentiviral vectors. Gene Ther 16, 509-520.
51. Montini E, Cesana D, Schmidt M, Sanvito F, Ponzoni M, Bartholomae C, SergiSergi L, Benedicenti F, Ambrosi A, Di Serio C, et al,. (2006) Hematopoietic stem cell gene transfer in a tumor-prone mouse model uncovers low genotoxicity of lentiviral vector integration. Nat Biotechnol 24, 687-696.
52. Kumar M, Keller B, Makalou N, &, Sutton RE, (2001) Systematic determination of the packaging limit of lentiviral vectors. Hum Gene Ther 12, 1893-1905.
53. Kimura E, Li S, Gregorevic P, Fall BM, &, Chamberlain JS, (2010) Dystrophin delivery to muscles of mdx mice using lentiviral vectors leads to myogenic progenitor targeting and stable gene expression. Mol Ther 18, 206-213.
54. 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.
55. Lai Y, Thomas GD, Yue Y, Yang HT, Li D, Long C, Judge L, Bostick B, Chamberlain JS, Terjung RL, &, Duan D, (2009) Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J Clin Invest 119, 624-635.
56. 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.
57. Ono Y, Masuda S, Nam H, Benezra R, Miyagoe-Suzuki Y, &, Takeda S, (2012) Slow-dividing satellite cells retain long-term self-renewal ability in adult muscle. J Cell Sci 125, 1309-1317.
58. Collins CA, Zammit PS, Ruiz AP, Morgan JE, &, Partridge TA, (2007) A population of myogenic stem cells that survives skeletal muscle aging. Stem Cells 25, 885-894.
59. Fukada S, Uezumi A, Ikemoto M, Masuda S, Segawa M, Tanimura N, Yamamoto H, Miyagoe-Suzuki Y, &, Takeda S, (2007) Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25, 2448-2459.
60. Gilbert PM, &, Blau HM, (2011) Engineering a stem cell house into a home. Stem Cell Res Ther 2, 3.
61. Csete M, (2005) Oxygen in the cultivation of stem cells. Ann N Y Acad Sci 1049, 1-8.
62. Brahimi-Horn MC, &, Pouysségur J, (2007) Oxygen, a source of life and stress. FEBS Lett 581, 3582-3591.
63. Simon MC, &, Keith B, (2008) The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 9, 285-296.
64. Mohyeldin A, Garzon-Muvdi T, &, Quinones-Hinojosa A, (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7, 150-161.
65. Duguez S, Duddy WJ, Gnocchi V, Bowe J, Dadgar S, &, Partridge TA, (2012) Atmospheric oxygen tension slows myoblast proliferation via mitochondrial activation. PLoS One 7, e43853.
66. Liu W, Wen Y, Bi P, Lai X, Liu XS, Liu X, &, Kuang S, (2012) Hypoxia promotes satellite cell self-renewal and enhances the efficiency of myoblast transplantation. Development 139, 2857-2865.
67. Gilbert PM, Havenstrite KL, Magnusson KE, 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.
68. Gilbert PM, Corbel S, Doyonnas R, Havenstrite K, Magnusson KEG, &, Blau HM, (2012) A single cell bioengineering approach to elucidate mechanisms of adult stem cell self-renewal. Integr Biol 4, 360-367.
69. 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.
70. 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.
71. 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.
72. 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.
73. Shireman PK, Contreras-Shannon V, Ochoa O, Karia BP, Michalek JE, &, McManus LM, (2007) MCP-1 deficiency causes altered inflammation with impaired skeletal muscle regeneration. J Leukoc Biol 81, 775-785.
74. Tidball JG, &, Wehling-Henricks M, (2007) Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo. J Physiol 578, 327-336.
75. Lescaudron L, Peltékian E, Fontaine-Pérus J, Paulin D, Zampieri M, Garcia L, &, Parrish E, (1999) Blood borne macrophages are essential for the triggering of muscle regeneration following muscle transplant. Neuromuscul Disord 9, 72-80.
76. Bencze M, Negroni E, Vallese D, Yacoub-Youssef H, Chaouch S, Wolff A, Aamiri A, Di Santo JP, Chazaud B, Butler-Browne G, et al,. (2012) Proinflammatory macrophages enhance the regenerative capacity of human myoblasts by modifying their kinetics of proliferation and differentiation. Mol Ther 20, 2168-2179.
77. Lesault PF, Theret M, Magnan M, Cuvellier S, Niu Y, Gherardi RK, Tremblay JP, Hittinger L, &, Chazaud B, (2012) Macrophages improve survival, proliferation and migration of engrafted myogenic precursor cells into MDX skeletal muscle. PLoS One 7, e46698.
78. Moyer AL, &, Wagner KR, (2011) Regeneration versus fibrosis in skeletal muscle. Curr Opin Rheumatol 23, 568-573.
79. Mathew SJ, Hansen JM, Merrell AJ, Murphy MM, Lawson JA, Hutcheson DA, Hansen MS, Angus-Hill M, &, Kardon G, (2010) Connective tissue fibroblasts and Tcf4 regulate myogenesis. Development 138, 371-384.
80. Joe AW, Yi L, Natarajan A, Le Grand F, So L, Wang J, Rudnicki MA, &, Rossi FM, (2010) Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol 12, 153-163.
81. Chakkalakal JV, Jones KM, Basson MA, &, Brack AS, (2012) The aged niche disrupts muscle stem cell quiescence. Nature 490, 355-360.
82. 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.
83. Boldrin L, Zammit PS, Muntoni F, &, Morgan JE, (2009) Mature adult dystrophic mouse muscle environment does not impede efficient engrafted satellite cell regeneration and self-renewal. Stem Cells 27, 2478-2487.
84. Boldrin L, Neal A, Zammit PS, Muntoni F, &, Morgan JE, (2012) Donor satellite cell engraftment is significantly augmented when the host niche is preserved and endogenous satellite cells are incapacitated. Stem Cells 30, 1971-1984.
85. Bouchentouf M, Benabdallah BF, &, Tremblay JP, (2004) Myoblast survival enhancement and transplantation success improvement by heat-shock treatment in mdx mice. Transplantation 77, 1349-1356.
86. 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.
87. Bouchentouf M, Benabdallah BF, Bigey P, Yau TM, Scherman D, &, Tremblay JP, (2008) Vascular endothelial growth factor reduced hypoxia-induced death of human myoblasts and improved their engraftment in mouse muscles. Gene Ther 15, 404-414.
88. Morgan J, Rouche A, Bausero P, Houssaïni A, Gross J, Fiszman MY, &, Alameddine HS, (2010) MMP-9 overexpression improves myogenic cell migration and engraftment. Muscle Nerve 42, 584-595.
89. Cohn RD, van Erp C, Habashi JP, Soleimani AA, Klein EC, Lisi MT, Gamradt M, ap Rhys CM, Holm TM, Loeys BL, Ramirez F, Judge DP, Ward CW, &, Dietz HC, (2007) Angiotensin II type 1 receptor blockade attenuates TGF-β-induced failure of muscle regeneration in multiple myopathic states. Nat Med 13, 204.
90. Fakhfakh R, Lamarre Y, Skuk D, &, Tremblay JP, (2012) Losartan enhances the success of myoblast transplantation. Cell Transplant 21, 139-152.
91. Fakhfakh R, Michaud A, &, Tremblay JP, (2011) Blocking the myostatin signal with a dominant negative receptor improves the success of human myoblast transplantation in dystrophic mice. Mol Ther 19, 204-210.
92. 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.
93. Gérard C, Dufour C, Goudenege S, Skuk D, &, Tremblay JP, (2012) AG490 improves the survival of human myoblasts in vitro and in vivo. Cell Transplant 21, 2665-2676.
94. Lafreniere JF, Mills P, Tremblay JP, &, El Fahime E, (2004) Growth factors improve the in vivo migration of human skeletal myoblasts by modulating their endogenous proteolytic activity. Transplantation 77, 1741-1747.
95. Lafreniere JF, Caron MC, Skuk D, Goulet M, Cheikh AR, &, Tremblay JP, (2009) Growth factor coinjection improves the migration potential of monkey myogenic precursors without affecting cell transplantation success. Cell Transplant 18, 719-730.
96. Brimah K, Ehrhardt J, Mouly V, Butler-Browne GS, Partridge TA, &, Morgan JE, (2004) Human muscle precursor cell regeneration in the mouse host is enhanced by growth factors. Hum Gene Ther 15, 1109-1124.
97. Morgan JE, Hoffman EP, &, Partridge TA, (1990) Normal myogenic cells from newborn mice restore normal histology to degenerating muscles of the mdx mouse. J Cell Biol 111, 2437-2449.
98. Morgan JE, Pagel CN, Sherrratt 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.
99. Harris JB, (2003) Myotoxic phospholipases A2 and the regeneration of skeletal muscles. Toxicon 42, 933-945.
100. Morgan JE, Coulton GR, &, Partridge TA, (1987) Muscle precursor cells invade and repopulate freeze-killed muscles. J Muscle Res Cell Motil 8, 386-396.
101. Gross JG, Bou-Gharios G, &, Morgan JE, (1999) Potentiation of myoblast transplantation by host muscle irradiation is dependent on the rate of radiation delivery. Cell Tissue Res 298, 371-375.
102. Grounds MD, &, Yablonka-Reuveni Z, (1993) Molecular and cell biology of skeletal muscle regeneration. Mol Cell Biol Hum Dis Ser 3, 210-256.
103. Ehrhardt J, Brimah K, Adkin C, Partridge T, &, Morgan J, (2007) Human muscle precursor cells give rise to functional satellite cells in vivo. Neuromuscul Disord 17, 631-638.
104. Bouchentouf M, Benabdallah BF, Mills P, &, Tremblay JP, (2006) Exercise improves the success of myoblast transplantation in mdx mice. Neuromuscul Disord 16, 518-529.
105. Takahashi K, &, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676.
106. 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.
107. Goudenege S, Lebel C, Huot NB, Dufour C, Fujii I, Gekas J, Rousseau J, &, Tremblay JP, (2012) Myoblasts derived from normal hESCs and dystrophic hiPSCs efficiently fuse with existing muscle fibers following transplantation. Mol Ther 20, 2153-2167.
108. Wu SM, &, Hochedlinger K, (2011) Harnessing the potential of induced pluripotent stem cells for regenerative medicine. Nat Cell Biol 13, 497-505.
109. Chang H, Yoshimoto M, Umeda K, Iwasa T, Mizuno Y, Fukada S, Yamamoto H, Motohashi N, Miyagoe-Suzuki Y, Takeda S, et al,. (2009) Generation of transplantable, functional satellite-like cells from mouse embryonic stem cells. FASEB J 23, 1907-1919.
110. Mizuno Y, Chang H, Umeda K, Niwa A, Iwasa T, Awaya T, Fukada S, Yamamoto H, Yamanaka S, Nakahata T, &, Heike T, (2010) Generation of skeletal muscle stem/progenitor cells from murine induced pluripotent stem cells. FASEB J 24, 2245-2253.
111. Darabi R, Pan W, Bosnakovski D, Baik J, Kyba M, &, Perlingeiro RCR, (2011) Functional myogenic engraftment from mouse iPS cells. Stem Cell Rev 7, 948-957.
112. 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.
113. Tedesco FS, Gerli MF, 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.
114. Hussein SMI, Elbaz J, &, Nagy AA, (2013) Genome damage in induced pluripotent stem cells: assessing the mechanisms and their consequences. BioEssays 35, 152-162.
115. Patel K, &, Morgan J, (2012) 185th ENMC International Workshop: stem/precursor cells as a therapeutic strategy for muscular dystrophies 3-5 June 2011, Naarden, The Netherlands. Neuromuscul Disord 22, 447-452.