Slowing down differentiation of engrafted human myoblasts into immunodeficient mice correlates with increased proliferation and migration

Molecular Therapy

Volumn 20, Issue 1, 2012, Pages 146-154

  Riederer, Ingo ^a,b   Negroni, Elisa ^a   Bencze, Maximilien ^a   Wolff, Annie ^a   Aamiri, Ahmed ^c   Di Santo, James P ^d   Silva Barbosa, Suse D ^b,e   Butler Browne, Gillian ^a   Savino, Wilson ^a,b   Mouly, Vincent ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c FACULTÉ DES SCIENCES   (Morocco)

^d INSTITUT PASTEUR   (France)

^e INSTITUTO NACIONAL DE CÂNCER   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL TRANSPLANTATION; CONTROLLED STUDY; ENGRAFTMENT; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; INFANT; MOUSE; MUSCLE DEVELOPMENT; MUSCLE INJURY; MUSCLE MASS; MUSCLE REGENERATION; MYOBLAST; NONHUMAN; TIBIALIS ANTERIOR MUSCLE; XENOTRANSPLANTATION;

MUS;

EID: 84856949330     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2011.193     Document Type: Article

References (50)

1. Mauro, A (1961). Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9: 493-495.
2. Negroni, E, Vallese, D, Vilquin, JT, Butler-Browne, G, Mouly, V and Trollet, C (2011). Current advances in cell therapy strategies for muscular dystrophies. Expert Opin Biol Ther 11: 157-176.
3. Cooper, RN, Tajbakhsh, S, Mouly, V, Cossu, G, Buckingham, M and 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. (Pubitemid 29430035)
4. Guo, K, Wang, J, Andrés, V, Smith, RC and Walsh, K (1995). MyoD-induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation. Mol Cell Biol 15: 3823-3829.
5. Brunetti, A and Goldfine, ID (1990). Role of myogenin in myoblast differentiation and its regulation by fibroblast growth factor. J Biol Chem 265: 5960-5963.
6. Morgan, JE and Partridge, TA (2003). Muscle satellite cells. Int J Biochem Cell Biol 35: 1151-1156. (Pubitemid 36577304)
7. Watt, DJ, Lambert, K, Morgan, JE, Partridge, TA and Sloper, JC (1982). Incorporation of donor muscle precursor cells into an area of muscle regeneration in the host mouse. J Neurol Sci 57: 319-331. (Pubitemid 13212268)
8. Partridge, TA, Morgan, JE, Coulton, GR, Hoffman, EP and Kunkel, LM (1989). Conversion of mdx myofibres from dystrophin-negative to-positive by injection of normal myoblasts. Nature 337: 176-179. (Pubitemid 19025378)
9. Asselin, I, Tremblay, M, Vilquin, JT, Guérette, B, Roy, R and Tremblay, JP (1995). Quantification of normal dystrophin mRNA following myoblast transplantation in mdx mice. Muscle Nerve 18: 980-986.
10. Huard, J, Bouchard, JP, Roy, R, Labrecque, C, Dansereau, G, Lemieux, B et al. (1991). Myoblast transplantation produced dystrophin-positive muscle fibres in a 16-year-old patient with Duchenne muscular dystrophy. Clin Sci 81: 287-288.
11. Gussoni, E, Pavlath, GK, Lanctot, AM, Sharma, KR, Miller, RG, Steinman, L et al. (1992). Normal dystrophin transcripts detected in Duchenne muscular dystrophy patients after myoblast transplantation. Nature 356: 435-438.
12. Tremblay, JP, Malouin, F, Roy, R, Huard, J, Bouchard, JP, Satoh, A et al. (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. (Pubitemid 23134486)
13. Skuk, D, Goulet, M, Roy, B, Chapdelaine, P, Bouchard, JP, Roy, R 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. (Pubitemid 44264834)
14. Skuk D, Goulet M, Roy B, Piette V, Cote CH, Chapdelaine P 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. (Pubitemid 46188617)
15. Beauchamp, JR, Morgan, JE, Pagel, CN and 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.
16. Skuk, D, Caron, NJ, Goulet, M, Roy, B and 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. (Pubitemid 37159035)
17. Guérette, B, Skuk, D, Célestin, F, Huard, C, Tardif, F, Asselin, I et al. (1997). Prevention by anti-LFA-1 of acute myoblast death following transplantation. J Immunol 159: 2522-2531. (Pubitemid 127681048)
18. Satoh, A, Huard, J, Labrecque, C and Tremblay, JP (1993). Use of fluorescent latex microspheres (FLMs) to follow the fate of transplanted myoblasts. J Histochem Cytochem 41: 1579-1582. (Pubitemid 23275261)
19. Skuk, D, Roy, B, Goulet, M and 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. (Pubitemid 29072601)
20. Montarras, D, Morgan, J, Collins, C, Relaix, F, Zaffran, S, Cumano, A et al. (2005). Direct isolation of satellite cells for skeletal muscle regeneration. Science 309: 2064-2067. (Pubitemid 41362326)
21. Cooper, RN, Thiesson, D, Furling, D, Di Santo, JP, Butler-Browne, GS and 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. (Pubitemid 36930406)
22. Zammit, PS, Heslop, L, Hudon, V, Rosenblatt, JD, Tajbakhsh, S, Buckingham, ME et al. (2002). Kinetics of myoblast proliferation show that resident satellite cells are competent to fully regenerate skeletal muscle fibers. Exp Cell Res 281: 39-49. (Pubitemid 35373781)
23. Gerdes, J, Schwab, U, Lemke, H and Stein, H (1983). Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation. Int J Cancer 31: 13-20. (Pubitemid 13179545)
24. Hendzel, MJ, Wei, Y, Mancini, MA, Van Hooser, A, Ranalli, T, Brinkley, BR et al. (1997). Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106: 348-360. (Pubitemid 27510848)
25. Bigot, A, Jacquemin, V, Debacq-Chainiaux, F, Butler-Browne, GS, Toussaint, O, Furling, D et al. (2008). Replicative aging down-regulates the myogenic regulatory factors in human myoblasts. Biol Cell 100: 189-199. (Pubitemid 351372677)
26. Hilfer, SR, Searls, RL and Fonte, VG (1973). An ultrastructural study of early myogenesis in the chick wing bud. Dev Biol 30: 374-391.
27. Francis-West, PH, Antoni, L and Anakwe, K (2003). Regulation of myogenic differentiation in the developing limb bud. J Anat 202: 69-81. (Pubitemid 36503970)
28. Edom, F, Mouly, V, Barbet, JP, Fiszman, MY and Butler-Browne, GS (1994). Clones of human satellite cells can express in vitro both fast and slow myosin heavy chains. Dev Biol 164: 219-229. (Pubitemid 24234348)
29. Dhawan, J and Rando, TA (2005). Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol 15: 666-673. (Pubitemid 41713968)
30. Cooper, RN, Irintchev, A, Di Santo, JP, Zweyer, M, Morgan, JE, Partridge, TA et al. (2001). A new immunodeficient mouse model for human myoblast transplantation. Hum Gene Ther 12: 823-831. (Pubitemid 32692347)
31. Silva-Barbosa, SD, Butler-Browne, GS, Di Santo, JP and Mouly, V (2005). Comparative analysis of genetically engineered immunodeficient mouse strains as recipients for human myoblast transplantation. Cell Transplant 14: 457-467. (Pubitemid 41566352)
32. Kinoshita, I, Roy, R, Dugré, FJ, Gravel, C, Roy, B, Goulet, M et al. (1996). Myoblast transplantation in monkeys: control of immune response by FK506. J Neuropathol Exp Neurol 55: 687-697. (Pubitemid 26187395)
33. Skuk, D, Goulet, M, Roy, B and Tremblay, JP (2000). Myoblast transplantation in whole muscle of nonhuman primates. J Neuropathol Exp Neurol 59: 197-206. (Pubitemid 30143878)
34. Decary, S, Mouly, V and Butler-Browne, GS (1996). Telomere length as a tool to monitor satellite cell amplification for cell-mediated gene therapy. Hum Gene Ther 7: 1347-1350. (Pubitemid 26318674)
35. Tidball, JG (2005). Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288: R345-R353. (Pubitemid 40129595)
36. Karalaki, M, Fili, S, Philippou, A and Koutsilieris, M (2009). Muscle regeneration: cellular and molecular events. In Vivo 23: 779-796.
37. Stamenkovic, I (2003). Extracellular matrix remodelling: the role of matrix metalloproteinases. J Pathol 200: 448-464.
38. El Fahime, E, Torrente, Y, Caron, NJ, Bresolin, MD and Tremblay, JP (2000). In vivo migration of transplanted myoblasts requires matrix metalloproteinase activity. Exp Cell Res 258: 279-287. (Pubitemid 30483506)
39. Goetzl, EJ, Banda, MJ and Leppert, D (1996). Matrix metalloproteinases in immunity. J Immunol 156: 1-4. (Pubitemid 26006939)
40. Silva-Barbosa, SD, Butler-Browne, GS, de Mello, W, Riederer, I, Di Santo, JP, Savino, W et al. (2008). Human myoblast engraftment is improved in laminin-enriched microenvironment. Transplantation 85: 566-575.
41. Goudenege, S, Lamarre, Y, Dumont, N, Rousseau, J, Frenette, J, Skuk, D et al. (2010). Laminin-111: a potential therapeutic agent for Duchenne muscular dystrophy. Mol Ther 18: 2155-2163.
42. Lafreniere, JF, Mills, P, Tremblay, JP and 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. (Pubitemid 38780543)
43. de Mello Coelho, V, Villa-Verde, DM, Farias-de-Oliveira, DA, de Brito, JM, Dardenne, M and Savino, W (2002). Functional insulin-like growth factor-1/insulin-like growth factor-1 receptor-mediated circuit in human and murine thymic epithelial cells. Neuroendocrinology 75: 139-150. (Pubitemid 34195774)
44. Sorokin, LM, Maley, MA, Moch, H, von der Mark, H, von der Mark, K, Cadalbert, L et al. (2000). Laminin α4 and integrin α6 are upregulated in regenerating dy/dy skeletal muscle: comparative expression of laminin and integrin isoforms in muscles regenerating after crush injury. Exp Cell Res 256: 500-514. (Pubitemid 30244208)
45. Arnold, L, Henry, A, Poron, F, Baba-Amer, Y, van Rooijen, N, Plonquet, A et al. (2007). Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204: 1057-1069. (Pubitemid 46798150)
46. Neville, C, Rosenthal, N, McGrew, M, Bogdanova, N and Hauschka, S (1997). Skeletal muscle cultures. Methods Cell Biol 52: 85-116. (Pubitemid 128787390)
47. Negroni, E, Riederer, I, Chaouch, S, Belicchi, M, Razini, P, Di Santo, J et al. (2009). In vivo myogenic potential of human CD133+ muscle-derived stem cells: a quantitative study. Mol Ther 17: 1771-1778.
48. Kaufman, SJ and Foster, RF (1988). Replicating myoblasts express a muscle-specific phenotype. Proc Natl Acad Sci USA 85: 9606-9610. (Pubitemid 19027175)
49. Decary, S, Mouly, V, Hamida, CB, Sautet, A, Barbet, JP and 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. (Pubitemid 27393998)
50. Irintchev, A, Langer, M, Zweyer, M, Theisen, R and Wernig, A (1997). Functional improvement of damaged adult mouse muscle by implantation of primary myoblasts. J Physiol (Lond) 500 (Pt 3): 775-785. (Pubitemid 27207834)