Generation of skeletal muscle cells from embryonic and induced pluripotent stem cells as an in vitro model and for therapy of muscular dystrophies

Journal of Cellular and Molecular Medicine

Volumn 16, Issue 7, 2012, Pages 1353-1364

  Salani, Sabrina ^a   Donadoni, Chiara ^a   Rizzo, Federica ^a   Bresolin, Nereo ^a,b   Comi, Giacomo P ^a   Corti, Stefania ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b SCIENTIFIC INSTITUTE   (Italy)

Author keywords

Embryonic stem cell; Induced pluripotent stem cell; Muscular dystrophy; Myoblast; Protocol

Indexed keywords

ANIMAL; CELL DIFFERENTIATION; CULTURE TECHNIQUE; CYTOLOGY; DISEASE MODEL; EMBRYONIC STEM CELL; HUMAN; MUSCULAR DYSTROPHY; PLURIPOTENT STEM CELL; REGENERATION; REVIEW; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; STEM CELL TRANSPLANTATION; TRANSPLANTATION;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; EMBRYONIC STEM CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MUSCLE FIBERS, SKELETAL; MUSCULAR DYSTROPHIES; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE; STEM CELL TRANSPLANTATION;

MURINAE;

EID: 84863089743     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2011.01498.x     Document Type: Review

References (81)

1. Emery AE. The muscular dystrophies. Lancet. 2002; 359: 687-95.
2. Palmieri B, Tremblay JP. Myoblast transplantation: a possible surgical treatment for a severe pediatric disease. Surg Today. 2010; 40: 902-8.
3. Hoffman EP, Brown RH Jr, Kunkel LM. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell. 1987; 51: 919-28.
4. Durbeej M, Campbell KP. Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr Opin Genet Dev. 2002; 12: 349-61.
5. Broglio L, Tentorio M, Cotelli MS, et al. Limb-girdle muscular dystrophy-associated protein diseases. Neurologist. 2010; 16: 340-52.
6. Wein N, Avril A, Bartoli M, et al. Efficient bypass of mutations in dysferlin deficient patient cells by antisense-induced exon skipping. Hum Mutat. 2010; 31: 136-42.
7. Urtizberea JA, Bassez G, Leturcq F, et al. Dysferlinopathies. Neurol India. 2008; 56: 289-97.
8. Gallardo E, Saenz A, Illa I. Limb-girdle muscular dystrophy 2A. Handb Clin Neurol. 2011; 101: 97-110.
9. McArdle A, Edwards RH, Jackson MJ. How does dystrophin deficiency lead to muscle degeneration?- evidence from the mdx mouse. Neuromuscul Disord. 1995; 5: 445-56.
10. Tanabe Y, Esaki K, Nomura T. Skeletal muscle pathology in X chromosome-linked muscular dystrophy (mdx) mouse. Acta Neuropathol. 1986; 69: 91-5.
11. Watkins SC, Cullen MJ. A quantitative study of myonuclear and satellite cell nuclear size in Duchenne's muscular dystrophy, polymyositis and normal human skeletal muscle. Anat Rec. 1988; 222: 6-11.
12. Matsumura K, Campbell KP. Deficiency of dystrophin-associated proteins: a common mechanism leading to muscle cell necrosis in severe childhood muscular dystrophies. Neuromuscul Disord. 1993; 3: 109-18.
13. Negroni E, Vallese D, Vilquin JT, et al. Current advances in cell therapy strategies for muscular dystrophies. Expert Opin Biol Ther. 2011; 11: 157-76.
14. Péault B, Rudnicki M, Torrente Y, et al. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther. 2007; 15: 867-77.
15. Meregalli M, Farini A, Belicchi M, et al. CD133(+) cells isolated from various sources and their role in future clinical perspectives. Expert Opin Biol Ther. 2010; 10: 1521-8.
16. Torrente Y, Belicchi M, Sampaolesi M, et al. Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest. 2004; 114: 182-95.
17. Luth ES, Jun SJ, Wessen MK, et al. Bone marrow side population cells are enriched for progenitors capable of myogenic differentiation. J Cell Sci. 2008; 121: 1426-34.
18. Otto A, Collins-Hooper H, Patel K. The origin, molecular regulation and therapeutic potential of myogenic stem cell populations. J Anat. 2009; 215: 477-97.
19. Vilquin JT. Myoblast transplantation: clinical trials and perspectives. Acta Myol. 2005; 24: 119-27.
20. Collins CA, Olsen I, Zammit PS, et al. Stem cell function, selfrenewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell. 2005; 122: 289-301.
21. Hyser CL, Mendell JR. Recent advances in Duchenne and Becker muscular dystrophy. Neurol Clin. 1988; 6: 429-53.
22. Biggar WD, Harris VA, Eliasoph L, et al. Long-term benefits of deflazacort treatment for boys with Duchenne muscular dystrophy in their second decade. Neuromuscul Disord. 2006; 16: 249-55.
23. Forrest S, Meloni PL, Muntoni F, et al. Personalized exon skipping strategies to address clustered non-deletion dystrophin mutations. Neuromuscul Disord. 2010; 20: 810-6.
24. Hoffman EP, Bronson A, Levin AA, et al. Restoring dystrophin expression in Duchenne muscular dystrophy muscle progress in exon skipping and stop codon read through. Am J Pathol. 2011; 179: 12-22.
25. Finkel RS. Read-through strategies for suppression of nonsense mutations in Duchenne/Becker muscular dystrophy: aminoglycosides and ataluren (PTC124). J Child Neurol. 2010; 25: 1158-64.
26. Malik V, Rodino-Klapac LR, Viollet L, et al. Gentamicin-induced readthrough of stop codons in Duchenne muscular dystrophy. Ann Neurol. 2010; 67: 771-80.
27. Brussee V, Tardif F, Roy B, et al. Successful myoblast transplantation in fibrotic muscles: no increased impairment by the connective tissue. Transplantation. 1999; 67: 1618-22.
28. Choi J, Costa ML, Mermelstein CS, et al. MyoD converts primary dermal fibroblasts, chondroblasts, smooth muscle, and retinal pigmented epithelial cells into striated mononucleated myoblasts and multinucleated myotubes. Proc Natl Acad Sci USA. 1990; 87: 7988-92.
29. Anastasia L, Sampaolesi M, Papini N, et al. Reversine-treated fibroblasts acquire myogenic competence in vitro and in regenerating skeletal muscle. Cell Death Differ. 2006; 13: 2042-51.
30. Lattanzi L, Salvatori G, Coletta M, et al. High efficiency myogenic conversion of human fibroblasts by adenoviral vector-mediated MyoD gene transfer. An alternative strategy for ex vivo genetherapy of primary myopathies. J Clin Invest. 1998; 101: 2119-28.
31. Del Bo R, Torrente Y, Corti S, et al. In vitro and in vivo tetracycline-controlled myogenic conversion of NIH-3T3 cells: evidence of programmed cell death after muscle cell transplantation. Cell Transplant. 2001; 10: 209-21.
32. Meng J, Muntoni F, Morgan JE. Stem cells to treat muscular dystrophies - where are we?Neuromuscul Disord. 2011; 21: 4-12.
33. Tomaskovic-Crook E, Crook JM. Human embryonic stem cell therapies for neurodegenerative diseases. CNS Neurol Disord Drug Targets. 2011; 10: 440-8.
34. Lowry WE, Richter L, Yachechko R, et al. Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc Natl Acad Sci. 2008; 105: 2883-8.
35. Meissner A, Wernig M, Jaenisch R. Direct reprogramming of genetically unmodified fibroblasts into pluripotent stem cells. Nat Biotechnol. 2007; 25: 1177-81.
36. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by definedfactors. Cell. 2007; 131: 861-72.
37. Park IH, Zhao R, West JA, et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature. 2008; 451: 141-6.
38. Park IH, Lerou PH, Zhao R, et al. Generation of human-induced pluripotent stem cells. Nat Protoc. 2008; 3: 1180-6.
39. Pang ZP, Yang N, Vierbuchen T, et al. Induction of human neuronal cells by defined transcription factors. Nature. 2011; doi:10.1038/nature10202.
40. Davis RL, Weintraub H, Lassar AB. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell. 1987; 51: 987-1000.
41. Tapscott SJ, Davis RL, Thayer MJ, et al. MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts. Science. 1988; 242: 405-11.
42. Weintraub H, Tapscott SJ, Davis RL, et al. Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc Natl Acad Sci USA. 1989; 86: 5434-38.
43. Sakurai H, Inami Y, Tamamura Y, et al. Bidirectional induction toward paraxial mesodermal derivatives from mouse ES cells in chemically defined medium. Stem Cell Res. 2009; 3: 157-69.
44. Johansson BM, Wiles MV. Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development. Mol. Cell. Biol. 1995; 15: 141-51.
45. Ng ES, Azzola L, Sourris K, et al. The primitive streak gene Mixl1 is required for efficient haematopoiesis and BMP4-induced ventral mesoderm patterning in differentiating ES cells. Development. 2005; 132: 873-84.
46. Era T, Izumi N, Hayashi M, et al. Multiple mesoderm subsets give rise to endothelial cells, whereas hematopoietic cells are differentiated only from a restricted subset in embryonic stem cell differentiation culture. Stem Cells. 2008; 26: 401-11.
47. Pick M, Azzola L, Mossman A, et al. Differentiation of human embryonic stem cells in serumfree medium reveals distinct roles for bone morphogenetic protein 4, vascular endothelial growth factor, stem cell factor, and fibroblast growth factor 2 in hematopoiesis. Stem Cells. 2007; 25: 2206-14.
48. Park C, Afrikanova I, Chung YS, et al. A hierarchical order of factors in the generation of FLK1- and SCL-expressing hematopoietic and endothelial progenitors from embryonic stem cells. Development. 2004; 131: 2749-62.
49. Honda M, Kurisaki A, Ohnuma K, et al. N-cadherin is a useful marker for the progenitor of cardiomyocytes differentiated from mouse ES cells in serum-free condition. Biochem Biophys Res Commun. 2006; 351: 877-82.
50. Bruce SJ, Rea RW, Steptoe AL, et al. In vitro differentiation of murine embryonic stem cells toward a renal lineage. Differentiation. 2007; 75: 337-49.
51. Barberi T, Willis LM, Socci ND, et al. Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med. 2005; 2: 161.
52. Barberi T, Bradbury M, Dincer Z, et al. Derivation of engraftable skeletal myoblasts from human embryonic stem cells. Nat Med. 2007; 13: 642-8.
53. Firth AL, Yao W, Ogawa A, et al. Multipotent mesenchymal progenitor cells are present in endarterectomized tissues from patients with chronic thromboembolic pulmonary hypertension. Am J Physiol Cell Physiol. 2010; 298: 1217-25.
54. Van der Velden JL, Langen RC, Kelders MC, et al. Inhibition of glycogen synthase kinase-3beta activity is sufficient to stimulate myogenic differentiation. Am J Physiol Cell Physiol. 2006; 290: 453-62.
55. Schatteman GC, Morrison-Graham K, van Koppen A, et al. Regulation and role of PDGF receptor alpha-subunit expression during embryogenesis. Development. 1992; 115: 123-31.
56. Chargé SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004; 84: 209-38.
57. Walsh FS, Ritter MA. Surface antigen differentiation during human myogenesis in culture. Nature. 1981; 289: 60-4.
58. Wang X, Yang P. In vitro differentiation of mouse embryonic stem (mES) cells using the hanging drop method. J Vis Exp. 2008; doi:10.3791/825.
59. Guan K, Rohwedel J, Wobus AM. Embryonic stem cell differentiation models: cardiogenesis, myogenesis, neurogenesis, epithelial and vascular smooth muscle cell differentiation in vitro. Cytotechnology. 1999; 30: 211-26.
60. Rohwedel J, Kleppisch T, Pich U, et al. Formation of postsynaptic-like membranes during differentiation of embryonic stem cells in vitro. Exp Cell Res. 1998; 239: 214-25.
61. Zheng JK, Wang Y, Karandikar A, et al. Skeletal myogenesis by human embryonic stem cells. Cell Res. 2006; 16: 713-22.
62. Darabi R, Gehlbach K, Bachoo RM, et al. Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nat Med. 2008; 14: 134-43.
63. Belanto JJ, Diaz-Perez SV, Magyar CE, et al. Dexamethasone induces dysferlin in myoblasts and enhances their myogenic differentiation. Neuromuscul Disord. 2010; 20: 111-21.
64. Konieczny SF, Emerson CP Jr. 5-Azacytidine induction of stable mesodermal stem cell lineages from 10T1/2 cells: evidence for regulatory genes controlling determination. Cell. 1984; 38: 791-800.
65. Bajard L, Relaix F, Lagha M, et al. A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes Dev. 2006; 20: 2450-64.
66. Ema M, Takahashi S, Rossant J. Deletion of the selection cassette, but not cis-acting elements, in targeted Flk1-lacZ allele reveals Flk1 expression in multipotent mesodermal progenitors. Blood. 2006; 107: 111-7.
67. Takakura N, Yoshida H, Ogura Y, et al. PDGFR alpha expression during mouse embryogenesis: immunolocalization analyzed by whole-mount immunohistostaining using the monoclonal anti-mouse PDGFR alpha antibody APA5. J Histochem Cytochem. 1997; 45: 883-93.
68. Maroto M, Reshef R, Münsterberg AE, et al. Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell. 1997; 89: 139-48.
69. Watanabe S, Hirai H, Asakura Y, et al. MyoD gene suppression by Oct4 is required for reprogramming in myoblasts to produce induced pluripotent stem cells. Stem Cells. 2011; 29: 505-16.
70. Ahmed RP, Haider HK, Buccini S, et al. Reprogramming of skeletal myoblasts for induction of pluripotency for tumour-free cardiomyogenesis in the infarcted heart. Circ Res. 2011; 109: 60-70.
71. Darabi R, Pan W, Bosnakovski D, et al. Functional myogenic engraftment from mouse iPS cells. Stem Cell Rev. 2011; doi:10.1007/s12015-011-9258-2.
72. Mizuno Y, Chang H, Umeda K, et al. Generation of skeletal muscle stem/progenitor cells from murine induced pluripotent stem cells. FASEB J. 2010; 24: 2245-53.
73. Tajbakhsh S. Stem cells to tissue: molecular, cellular and anatomical heterogeneity in skeletal muscle. Curr Opin Genet Dev. 2003; 13: 413-22.
74. Fukada S, Higuchi S, Segawa M, et al. Purification and cell-surface marker characterization of quiescent satellite cells from murine skeletal muscle by a novel monoclonal antibody. Exp Cell Res. 2004; 296: 245-55.
75. Quattrocelli M, Palazzolo G, Floris G, et al. Intrinsic cell memory reinforces myogenic commitment of pericyte-derived iPSCs. J Pathol. 2011; 223: 593-603.
76. Nizzardo M, Simone C, Falcone M, et al. Human motor neuron generation from embryonic stem cells and induced pluripotent stem cells. Cell Mol Life Sci. 2010; 67: 3837-47.
77. Chidgey AP, Boyd RL. Immune privilege for stem cells: not as simple as it looked. Cell Stem Cell. 2008; 3: 357-8.
78. Swijnenburg RJ, Tanaka M, Vogel H, et al. Embryonic stem cell immunogenicity increases upon differentiation after transplantation into ischemic myocardium. Circulation. 2005; 112: 166-72.
79. Moretti A, Bellin M, Welling A, et al. Patient-specific induced pluripotent stem-cell models for long-QT syndrome. N Engl J Med. 2010; 363: 1397-409.
80. Maehr R, Chen S, Snitow M, et al. Generation of pluripotent stem cells from patients with type 1 diabetes. Proc Natl Acad Sci USA. 2009; 106: 15768-73.
81. Kazuki Y, Hiratsuka M, Takiguchi M, et al. Complete genetic correction of iPS cells from Duchenne muscular dystrophy. Mol Ther. 2010; 18: 386-93.