Transplanted myoblasts can migrate several millimeters to fuse with damaged myofibers in nonhuman primate skeletal muscle

Journal of Neuropathology and Experimental Neurology

Volumn 70, Issue 9, 2011, Pages 770-778

  Skuk, Daniel ^a   Goulet, Marlyne ^a   Tremblay, Jacques P ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

Cell migration; Myogenic cell transplantation,Myoblasts; Nonhuman primates; Skeletal muscle

Indexed keywords

BETA GALACTOSIDASE;

ANIMAL EXPERIMENT; ARTICLE; CELL DAMAGE; CELL FUNCTION; CELL FUSION; CELL MIGRATION; CELL SUSPENSION; CELL TRANSPLANTATION; CONTROLLED STUDY; FEMALE; MACACA FASCICULARIS; MALE; MYOBLAST; NONHUMAN; PERIMYSIUM; PRIORITY JOURNAL; SKELETAL MUSCLE;

EID: 80052171183     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e31822a6baa     Document Type: Article

References (42)

1. Skuk D, Tremblay JP. Intramuscular cell transplantation as a potential treatment of myopathies: Clinical and preclinical relevant data. Expert Opin Biol Ther 2011;11:359-74
2. 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
3. Partridge TA, Grounds M, Sloper JC. Evidence of fusion between host and donor myoblasts in skeletal muscle grafts. Nature 1978;273:306-8 (Pubitemid 8332886)
4. Konigsberg IR. The differentiation of cross-striated myofibrils in short term cell culture. Exp Cell Res 1960;21:414-20
5. Watt DJ, Morgan JE, Partridge TA. Use of mononuclear precursor cells to insert allogeneic genes into growing mouse muscles. Muscle Nerve 1984;7:741-50 (Pubitemid 15209290)
6. Bartlett RJ, Sharp NJ, Hung WY, et al. Molecular markers for myoblast transplantation in GRMD. Adv Exp Med Biol 1990;280:273-78 (Pubitemid 20330852)
7. Kinoshita I, Vilquin JT, Gravel C, et al. Myoblast allotransplantation in primates. Muscle Nerve 1995;18:1217-18
8. Boubaker el Andalousi R, Daussin PA, Micallef JP, et al. Changes in mass and performance in rabbit muscles after muscle damage with or without transplantation of primary satellite cells. Cell Transplant 2002; 11:169-80
9. Holzer N, Hogendoorn S, Zurcher L, et al. Autologous transplantation of porcine myogenic precursor cells in skeletal muscle. Neuromuscul Disord 2005;15:237-44 (Pubitemid 40255779)
10. Skuk D. Myoblast transplantation for inherited myopathies: A clinical approach. Expert Opin Biol Ther 2004;4:1871-85 (Pubitemid 39627139)
11. Skuk D, Goulet M, Roy B, et al. Dystrophin expression in muscles of Duchenne muscular dystrophy patients after high-density injections of normal myogenic cells. J Neuropathol Exp Neurol 2006;65:371-86 (Pubitemid 44264834)
12. Skuk D, Goulet M, Roy B, et al. 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 2007;17:38-46 (Pubitemid 46188617)
13. Skuk D, Roy B, Goulet M, et al. Dystrophin expression in myofibers of Duchenne muscular dystrophy patients following intramuscular injections of normal myogenic cells. Mol Ther 2004;9:475-82 (Pubitemid 38404538)
14. Skuk D, Goulet M, Roy B, et al. Efficacy of myoblast transplantation in nonhuman primates following simple intramuscular cell injections: Toward defining strategies applicable to humans. Exp Neurol 2002;175:112-26 (Pubitemid 34507914)
15. Skuk D, Goulet M, Tremblay JP. Use of repeating dispensers to increase the efficiency of the intramuscular myogenic cell injection procedure. Cell Transplant 2006;15:659-63 (Pubitemid 44904677)
16. Quenneville SP, Chapdelaine P, Skuk D, et al. Autologous transplantation of muscle precursor cells modified with a lentivirus for muscular dystrophy: Human cells and primate models. Mol Ther 2007;15: 431-38 (Pubitemid 46111895)
17. El Fahime E, Torrente Y, Caron NJ, et al. In vivo migration of transplanted myoblasts requires matrix metalloproteinase activity. Exp Cell Res 2000;258:279-87 (Pubitemid 30483506)
18. El Fahime E, Mills P, Lafreniere JF, et al. The urokinase plasminogen activator: An interesting way to improve myoblast migration following their transplantation. Exp Cell Res 2002;280:169-78 (Pubitemid 35333759)
19. Caron NJ, Asselin I, Morel G, et al. Increased myogenic potential and fusion of matrilysin-expressing myoblasts transplanted in mice. Cell Transplant 1999;8:465-76
20. Lafreniere JF, Mills P, Tremblay JP, et al. Growth factors improve the in vivo migration of human skeletal myoblasts by modulating their endogenous proteolytic activity. Transplant 2004;77:1741-7 (Pubitemid 38780543)
21. Geluk A, Elferink DG, Slierendregt BL, et al. Evolutionary conservation of major histocompatibility complexYDR/peptide/T cell interactions in primates. J Exp Med 1993;177:979-87 (Pubitemid 23097387)
22. Jaeger EE, Bontrop RE, Lanchbury JS. Structure, diversity, and evolution of the T-cell receptor VB gene repertoire in primates. Immunogenetics 1994;40:184-91 (Pubitemid 24217860)
23. Rose SM, Blustein N, Rotrosen D. Recommendations of the expert panel on ethical issues in clinical trials of transplant tolerance. National Institute of Allergy and Infectious Diseases of the National Institutes of Health. Transplantation 1998;66:1123-25 (Pubitemid 28530311)
24. Kirk AD. Transplantation tolerance: A look at the nonhuman primate literature in the light of modern tolerance theories. Crit Rev Immunol 1999;19:349-88 (Pubitemid 30053171)
25. Kirk AD. Crossing the bridge: Large animal models in translational transplantation research. Immunol Rev 2003;196:176-96 (Pubitemid 37468111)
26. Borisov AB. Regeneration of skeletal and cardiac muscle in mammals: Do nonprimate models resemble human pathology? Wound Repair Regen 1999;7:26-35 (Pubitemid 29159038)
27. Skuk D, Roy B, Goulet M, et al. Successful myoblast transplantation in primates depends on appropriate cell delivery and induction of regeneration in the host muscle. Exp Neurol 1999;155:22-30 (Pubitemid 29072601)
28. Skuk D, Goulet M, Roy B, et al. Myoblast transplantation in whole muscle of nonhuman primates. J Neuropathol Exp Neurol 2000;59:197-206 (Pubitemid 30143878)
29. Richard PL, Gosselin C, Laliberte T, et al. A first semimanual device for clinical intramuscular repetitive cell injections. Cell Transplant 2010;19: 67-78
30. Moens PD, Van-Schoor MC, Marechal G. Lack of myoblasts migration between transplanted and host muscles of mdx and normal mice. J Muscle Res Cell Motil 1996;17:37-43 (Pubitemid 26157740)
31. Robertson TA, Maley MA, Grounds MD, et al. The role of macrophages in skeletal muscle regeneration with particular reference to chemotaxis. Exp Cell Res 1993;207:321-31 (Pubitemid 23246804)
32. Bischoff R. Chemotaxis of skeletal muscle satellite cells. Dev Dyn 1997; 208:505-15 (Pubitemid 27152842)
33. Tokura Y, Nakayama Y, Fukada S, et al. Muscle injuryYinduced thymosin beta4 acts as a chemoattractant for myoblasts. J Biochem 2011; 149:43-48
34. Siegel AL, Atchison K, Fisher KE, et al. 3D timelapse analysis of muscle satellite cell motility. Stem Cells 2009;27:2527-38
35. Skuk D, Paradis M, Goulet M, et al. Ischemic central necrosis in pockets of transplanted myoblasts in nonhuman primates: Implications for celltransplantation strategies. Transplantation 2007;84:1307-15 (Pubitemid 351339319)
36. Watt DJ, Karasinski J, Moss J, et al. Migration of muscle cells. Nature 1994;368:406-7
37. Meng J, Muntoni F, Morgan JE. Stem cells to treat muscular dystrophiesVWhere are we? Neuromuscul Disord 2011;21:4-12
38. Skuk D, Tremblay JP. Myoblast transplantation: The current status of a potential therapeutic tool for myopathies. J Muscle Res Cell Motil 2003; 24:285-300 (Pubitemid 37323636)
39. Lafreniere JF, Mills P, Bouchentouf M, et al. Interleukin-4 improves the migration of human myogenic precursor cells in vitro and in vivo. Exp Cell Res 2006;312:1127-41
40. Mills P, Dominique JC, Lafreniere JF, et al. A synthetic mechano growth factor E peptide enhances myogenic precursor cell transplantation success. Am J Transplant 2007;7:2247-59 (Pubitemid 47347850)
41. Mills P, Lafreniere JF, Benabdallah BF, et al. A new pro-migratory activity on human myogenic precursor cells for a synthetic peptide within the E domain of the mechano growth factor. Exp Cell Res 2007;313:527-37 (Pubitemid 46186304)
42. Lafreniere JF, Caron MC, Skuk D, et al. Growth factor co-injection improves the migration potential of monkey myogenic precursors without affecting cell transplantation success. Cell Transplant 2009;18:719-30