Macrophages Improve Survival, Proliferation and Migration of Engrafted Myogenic Precursor Cells into MDX Skeletal Muscle

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Lesault, Pierre François ^b,c   Theret, Marine ^d,e,f   Magnan, Mélanie ^d,e,f   Cuvellier, Sylvain ^d,e,f   Niu, Yiming ^b,c   Gherardi, Romain K ^b,c   Tremblay, Jacques P ^a   Hittinger, Luc ^b,c   Chazaud, Bénédicte ^d,e,f  

^a University Laval   (Canada)

^b INSERM U955   (France)

^c UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^d INSTITUT COCHIN   (France)

^e CNRS   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PHAGOCYTOSIS; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MOUSE; MUSCLE CELL; MUSCLE REGENERATION; MYOBLAST; MYOGENIC PRECURSOR CELL; MYOPATHY; NONHUMAN; SKELETAL MUSCLE; STEM CELL EXPANSION; STEM CELL TRANSPLANTATION;

ANIMALS; BLOTTING, WESTERN; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; MACROPHAGES; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES; MYOBLASTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84867090688     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046698     Document Type: Article

References (53)

1. Kuang S, Rudnicki MA, (2008) The emerging biology of satellite cells and their therapeutic potential. Trends in Molecular Medicine 14: 82-91.
2. Wallace GQ, McNally EM, (2009) Mechanisms of muscle degeneration, regeneration, and repair in the muscular dystrophies. Annu Rev Physiol 71: 37-57.
3. Cossu G, Sampaolesi M, (2007) New therapies for Duchenne muscular dystrophy: challenges, prospects and clinical trials. Trends Mol Med 13: 520-526.
4. Negroni E, Butler-Browne GS, Mouly V, (2006) Myogenic stem cells: regeneration and cell therapy in human skeletal muscle. Pathol Biol (Paris) 54: 100-108.
5. 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.
6. Karpati G, Pouliot Y, Zubrzycka-Gaarn E, Carpenter S, Ray PN, et al. (1989) Dystrophin is expressed in mdx skeletal muscle fibers after normal myoblast implantation. Am J Pathol 135: 27-32.
7. Peault B, Rudnicki M, Torrente Y, Cossu G, Tremblay JP, et al. (2007) Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 15: 867-877.
8. 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.
9. Fan Y, Maley M, Beilharz M, Grounds M, (1996) Rapid death of injected myoblasts in myoblast transfer therapy. Muscle Nerve 19: 853-860.
10. Guerette B, Skuk D, Celestin F, Huard C, Tardif F, et al. (1997) Prevention by anti-LFA-1 of acute myoblast death following transplantation. J Immunol 159: 2522-2531.
11. Moens PD, Van-Schoor MC, Marechal G, (1996) Lack of myoblasts migration between transplanted and host muscles of mdx and normal mice. J Muscle Res Cell Motil 17: 37-43.
12. Kinoshita I, Vilquin JT, Asselin I, Chamberlain J, Tremblay JP, (1998) Transplantation of myoblasts from a transgenic mouse overexpressing dystrophin produced only a relatively small increase of dystrophin-positive membrane. Muscle Nerve 21: 91-103.
13. Bouchentouf M, Benabdallah BF, Bigey P, Yau TM, Scherman D, et al. (2008) Vascular endothelial growth factor reduced hypoxia-induced death of human myoblasts and improved their engraftment in mouse muscles. Gene Ther 15: 404-414.
14. Bouchentouf M, Benabdallah BF, Rousseau J, Schwartz LM, Tremblay JP, (2007) Induction of Anoikis Following Myoblast Transplantation into SCID Mouse Muscles Requires the Bit1 and FADD Pathways. Am J Transplant 7: 1491-1505.
15. Smythe GM, Fan Y, Grounds MD, (2000) Enhanced migration and fusion of donor myoblasts in dystrophic and normal host muscle. Muscle Nerve 23: 560-574.
16. Hodgetts SI, Spencer MJ, Grounds MD, (2003) A role for natural killer cells in the rapid death of cultured donor myoblasts after transplantation. Transplantation 75: 863-871.
17. Sammels LM, Bosio E, Fragall CT, Grounds MD, van Rooijen N, et al. (2004) Innate inflammatory cells are not responsible for early death of donor myoblasts after myoblast transfer therapy. Transplantation 77: 1790-1797.
18. Merly F, Huard C, Asselin I, Robbins PD, Tremblay JP, (1998) Anti-inflammatory effect of transforming growth factor-beta1 in myoblast transplantation. Transplantation 65: 793-799.
19. Torrente Y, El Fahime E, Caron NJ, Bresolin N, Tremblay JP, (2000) Intramuscular migration of myoblasts transplanted after muscle pretreatment with metalloproteinases. Cell Transplant 9: 539-549.
20. 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.
21. 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.
22. Riederer I, Negroni E, Bigot A, Bencze M, Di Santo J, et al. (2008) Heat shock treatment increases engraftment of transplanted human myoblasts into immunodeficient mice. Transplant Proc 40: 624-630.
23. 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.
24. Benabdallah BF, Bouchentouf M, Tremblay JP, (2005) Improved success of myoblast transplantation in mdx mice by blocking the myostatin signal. Transplantation 79: 1696-1702.
25. Lafreniere JF, Mills P, Bouchentouf M, Tremblay JP, (2006) Interleukin-4 improves the migration of human myogenic precursor cells in vitro and in vivo. Exp Cell Res 312: 1127-1141.
26. Lavasani M, Lu A, Peng H, Cummins J, Huard J, (2006) Nerve growth factor improves the muscle regeneration capacity of muscle stem cells in dystrophic muscle. Hum Gene Ther 17: 180-192.
27. Riederer I, Negroni E, Bencze M, Wolff A, Aamiri A, et al. (2012) Slowing down differentiation of engrafted human myoblasts into immunodeficient mice correlates with increased proliferation and migration. Mol Ther 20: 146-154.
28. Lescaudron L, Peltekian E, Fontaine-Perus J, Paulin D, Zampieri M, et al. (1999) Blood borne macrophages are essential for the triggering of muscle regeneration following muscle transplant. Neuromuscul Disord 9: 72-80.
29. McLennan IS, (1996) Degenerating and regenerating skeletal muscles contain several subpopulations of macrophages with distinct spatial and temporal distributions. Journal of Anatomy 188: 17-28.
30. Pimorady-Esfahani A, Grounds MD, McMenamin PG, (1997) Macrophages and dendritic cells in normal and regenerating murine skeletal muscle. Muscle Nerve 20: 158-166.
31. Summan M, Warren GL, Mercer RR, Chapman R, Hulderman T, et al. (2006) Macrophages and skeletal muscle regeneration: a clodronate-containing liposome depletion study. Am J Physiol Regul Integr Comp Physiol 290: R1488-R1495.
32. Dipasquale DM, Cheng M, Billich W, Huang SA, van Rooijen N, et al. (2007) The urokinase-type plasminogen activator and macrophages are required for skeletal muscle hypertrophy in mice. Am J Physiol Cell Physiol 293: C1278-C1285.
33. Segawa M, Fukada S, Yamamoto Y, Yahagi H, Kanematsu M, et al. (2008) Suppression of macrophage functions impairs skeletal muscle regeneration with severe fibrosis. Exp Cell Res 314: 3232-3244.
34. Sun D, Martinez CO, Ochoa O, Ruiz-Willhite L, Bonilla JR, et al. (2009) Bone marrow-derived cell regulation of skeletal muscle regeneration. FASEB J 23: 382-395.
35. Arnold L, Henry A, Poron F, Baba-Amer Y, van Rooijen N, et al. (2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. Journal of Experimental Medicine 204: 1071-1081.
36. Massimino ML, Rapizzi E, Cantini M, Libera LD, Mazzoleni F, et al. (1997) ED2+ macrophages increase selectively myoblast proliferation in muscle cultures. Biochemical and Biophysical Research Communications 235: 754-759.
37. Robertson TA, Maley MAL, Grounds MD, Papadimitriou JM, (1993) The role of macrophages in skeletal muscle regeneration with particular reference to chemotaxis. Experimental Cell Research 207: 321-331.
38. Chazaud B, Sonnet C, Lafuste P, Bassez G, Rimaniol AC, et al. (2003) Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth. J Cell Biol 163: 1133-1143.
39. Sonnet C, Lafuste P, Arnold L, Brigitte M, Poron F, et al. (2006) Human macrophages rescue myoblasts and myotubes from apoptosis through a set of adhesion molecular systems. Journal of Cell Science 119: 2497-2507.
40. Malerba A, Vitiello L, Segat D, Dazzo E, Frigo M, et al. (2009) Selection of multipotent cells and enhanced muscle reconstruction by myogenic macrophage-secreted factors. Exp Cell Res 315: 915-927.
41. Vidal B, Serrano AL, Tjwa M, Suelves M, Ardite E, et al. (2008) Fibrinogen drives dystrophic muscle fibrosis via a TGFbeta/alternative macrophage activation pathway. Genes Dev 22: 1747-1752.
42. Villalta SA, Nguyen HX, Deng B, Gotoh T, Tidball JG, (2009) Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum Mol Genet 18: 482-496.
43. Martinez FO, Sica A, Mantovani A, Locati M, (2008) Macrophage activation and polarization. Front Biosci 13 453-61: 453-461.
44. 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. Journal of Cell Biology 144: 1113-1121.
45. Hodgetts SI, Grounds MD (2003) Irradiation of dystrophic host tissue prior to myoblast transfer therapy enhances initial (but not long-term) survival of donor myoblasts. J Cell Sci 116: 4131-4146. 10.1242/jcs.00721 [doi];116/20/4131 [pii].
46. Pellegrini KL, Beilharz MW, (2011) The survival of myoblasts after intramuscular transplantation is improved when fewer cells are injected. Transplantation 91: 522-526.
47. Hawke TJ, Garry DJ, (2001) Myogenic satellite cells: physiology to molecular biology. Journal of Applied Physiology 91: 534-551.
48. Motohashi N, Uezumi A, Yada E, Fukada S, Fukushima K, et al. (2008) Muscle CD31(-) CD45(-) side population cells promote muscle regeneration by stimulating proliferation and migration of myoblasts. Am J Pathol 173: 781-791.
49. Mills P, Lafreniere JF, Benabdallah BF, El Fahime M, Tremblay JP, (2007) 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 313: 527-537.
50. Bencze M, Negroni E, Vallese D, Yavoub-Youssef H, Chaouch S, et al. (2012) Pro-inflammatory macrophages enhance the regenerative capacity of human myoblasts by modifying their kinetics of proliferation and differentiation. Mol Ther. In press.
51. Montarras D, Lindon C, Pinset C, Domeyne P, (2000) Cultured myf5 null and myoD null muscle precursor cells display distinct growth defects. Biology of the Cell 92: 565-572.
52. Stanley ER, (1997) Murine bone marrow-derived macrophages. Methods Mol Biol 75: 301-304.
53. Schleicher U, Bogdan C, (2009) Generation, culture and flow-cytometric characterization of primary mouse macrophages. Methods Mol Biol 531: 203-224.