Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique

Nature Protocols

Volumn 3, Issue 9, 2008, Pages 1501-1509

  Gharaibeh, Burhan ^a,b   Lu, Aiping ^a   Tebbets, Jessica ^a   Zheng, Bo ^a   Feduska, Joe ^a   Crisan, Mihaela ^a   Péault, Bruno ^a,c   Cummins, James ^a   Huard, Johnny ^a,b,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b Department of Orthopaedic Surgery ^*  (United States)

^c CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; COLLAGENASE; COLLAGENASE XI; DISPASE; TRYPSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL ADHESION; CELL FRACTIONATION; CELL ISOLATION; CELL POPULATION; CONTROLLED STUDY; CULTURE TECHNIQUE; ENRICHMENT CULTURE; ENZYME MECHANISM; ENZYME METABOLISM; ISOLATION PROCEDURE; MATERIAL COATING; MICROTITER PLATE ASSAY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE; STEM CELL;

ANIMALS; CELL ADHESION; CELL SEPARATION; MICE; MUSCLE, SKELETAL; STEM CELLS;

MURINAE;

EID: 51649123800     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2008.142     Document Type: Article

References (82)

1. Kessler, P.D. & Byrne, B.J. Myoblast cell grafting into heart muscle: cellular biology and potential applications. Annu. Rev. Physiol. 61, 219-242 (1999).
2. Marelli, D., Desrosiers, C., el-Alfy, M., Kao, R.L. & Chiu, R.C. Cell transplantation for myocardial repair: An experimental approach. Cell Transplant. 1, 383-390 (1992).
3. Reinecke, H., Poppa, V. & Murry, C.E. Skeletal muscle stem cells do not transdifferentiate into cardiomyocytes after cardiac grafting. J. Mol. Cell Cardiol. 34, 241-249 (2002).
4. Suzuki, K. et al. Development of a novel method for cell transplantation through the coronary artery. Circulation 102 III359-III364 (2000).
5. Taylor, D.A. et al. Regenerating functional myocardium: Improved performance after skeletal myoblast transplantation. Nat. Med. 4, 929-933 (1998).
6. Dib, N. et al. Feasibility and safety of autologous myoblast transplantation in patients with ischemic cardiomyopathy. Cell Transplant. 14, 11-19 (2005).
7. Dib, N. et al. Safety and feasibility of autologous myoblast transplantation in patients with ischemic cardiomyopathy: Four-year follow-up. Circulation 112, 1748-1755 (2005).
8. Herreros, J. et al. Autologous intramyocardial injection of cultured skeletal muscle-derived stem cells in patients with non-acute myocardial infarction. Eur. Heart J. 24, 2012-2020 (2003).
9. Ince, H., Petzsch, M., Rehders, T.C., Chatterjee, T. & Nienaber, C.A. Transcatheter transplantation of autologous skeletal myoblasts in postinfarction patients with severe left ventricular dysfunction. J. Endovasc. Ther. 11, 695-704 (2004).
10. Menasche, P. Cellular transplantation: Hurdles remaining before widespread clinical use. Curr. Opin. Cardiol. 19, 154-161 (2004).
11. Menasche, P. Myoblast transfer in heart failure. Surg. Clin. North Am. 84, 125-139 (2004).
12. Menasche, P. Skeletal myoblast for cell therapy. Coron. Artery Dis. 16, 105-110 (2005).
13. Menasche, P. et al. Myoblast transplantation for heart failure. Lancet 357, 279-280 (2001).
14. Menasche, P. et al. Autologous skeletal myoblast transplantation for severe postinfarction left ventricular dysfunction. J. Am. Coll. Cardiol. 41, 1078-1083 (2003).
15. Pagani, F.D. et al. Autologous skeletal myoblasts transplanted to ischemia-damaged myocardium in humans. Histological analysis of cell survival and differentiation. J. Am. Coll. Cardiol. 41, 879-888 (2003).
16. Smits, P.C. et al. Catheter-based intramyocardial injection of autologous skeletal myoblasts as a primary treatment of ischemic heart failure: Clinical experience with six-month follow-up. J. Am. Coll. Cardiol. 42, 2063-2069 (2003).
17. Beauchamp, J.R., Morgan, J.E., Pagel, C.N. & Partridge, LA. 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 (1999).
18. Fan, Y., Maley, M., Beilharz, M. & Grounds, M. Rapid death of injected myoblasts in myoblast transfer therapy. Muscle Nerve 29, 853-860 (1996).
19. Guerette, B., Asselin, I., Skuk, D., Entman, M. & Tremblay, J.P. Control of inflammatory damage by anti-LFA-1: Increase success of myoblast transplantation. Cell Transplant. 6, 101-107 (1997).
20. Gussoni, E., Blau, H.M. & Kunkel, L.M. The fate of individual myoblasts after transplantation into muscles of DMD patients. Nat. Med. 3 970-977 (1997).
21. Gussoni, E. et al. Normal dystrophin transcripts detected in Duchenne muscular dystrophy patients after myoblast transplantation. Nature 356, 435-438 (1992).
22. Huard, J., Acsadi, G., Jani, A., Massie, B. & Karpati, G. Gene transfer into skeletal muscles by isogenic myoblasts. Hum. Gene Ther. 5 949-958 (1994).
23. Huard, J. et al. Myoblast transplantation produced dystrophin-positive muscle fibres in a 16-year-old patient with Duchenne muscular dystrophy. Clin. Sci. 81, 287-288 (1991).
24. Huard, J. et al. Human myoblast transplantation: Preliminary results of 4 cases. Muscle Nerve 15, 550-560 (1992).
25. Huard, J. et al. Human myoblast transplantation between immunohisto-compatible donors and recipients produces immune reactions. Transplant. Proc. 24, 3049-3051 (1992).
26. Huard, J. et al. Human myoblast transplantation in immunodeficient and immunosuppressed mice: Evidence of rejection. Muscle Nerve 17, 224-234 (1994).
27. Huard, J., Verreault, S., Roy, R., Tremblay, M. & Tremblay, J.P. High efficiency of muscle regeneration after human myoblast clone transplantation in SCID mice. J. Clin. Invest. 93, 586-599 (1994).
28. Karpati, G. et al. Dystrophin is expressed in mdx skeletal muscle fibers after normal myoblast implantation. Am. J. Pathol. 135 27-32 (1989).
29. Kinoshita, I. et al. Very efficient myoblast allotransplantation in mice under FK506 immunosuppression. Muscle Nerve 17, 1407-1415 (1994).
30. Mendell, J.R. et al. Myoblast transfer in the treatment of Duchenne's muscular dystrophy. N. Engl. J. Med. 333, 832-838 (1995).
31. Morgan, J.E., Hoffman, E.P. & Partridge, T.A. Normal myogenic cells from newborn mice restore normal histology to degenerating muscles of the mdx mouse. J. Cell Biol. 111, 2437-2449 (1990).
32. Morgan, J.E., Pagel, C.N., Sherratt, T. & Partridge, T.A. Long-term persistence and migration of myogenic cells injected into pre-irradiated muscles of mdx mice. J. Neurol. Sci. 115, 191-200 (1993).
33. Morgan, J.E., Watt, D.J., Sloper, J.C. & Partridge, T.A. Partial correction of an inherited biochemical defect of skeletal muscle by grafts of normal muscle precursor cells. J. Neurol. Sci. 86, 137-147 (1988).
34. Partridge, LA. Invited review: Myoblast transfer a possible therapy for inherited myopathies? Muscle Nerve 14, 197-212 (1991).
35. Petersen, Z.Q. & Huard, J. The influence of muscle fiber type in myoblast-mediated gene transfer to skeletal muscles. Cell Transplant. 9, 503-517 (2000).
36. Clu, Z. et al. Development of approaches to improve cell survival in myoblast transfer therapy. J. Cell Biol. 142, 1257-1267 (1998).
37. Qu, Z. & Huard, J. Matching host muscle and donor myoblasts for myosin heavy chain improves myoblast transfer therapy. Gene Ther. 7 428-437 (2000).
38. Tremblay, J.P. et al. 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 (1993).
39. Vilquin, J.T., Wagner, E., Kinoshita, I., Roy, R. & Tremblay, J.P. Successful histocompatible myoblast transplantation in dystrophin-deficient mdx mouse despite the production of antibodies against dystrophin. J. Cell Biol. 131, 975-988 (1995).
40. Lee, J.Y. et al. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J. Cell Biol. 150, 1085-1100 (2000).
41. Qu-Petersen, Z. et al. Identification of a novel population of muscle stem cells in mice: Potential for muscle regeneration. J. Cell Biol. 157, 851-864 (2002).
42. Deasy, B.M., Schugar, R.C. & Huard, J. Sex differences in muscle-derived stem cells and skeletal muscle. Crit. Rev. Eukaryot. Gene Expr. 18, 173-188 (2008).
43. Payne, T.R. et al. A relationship between vascular endothelial growth factor, angiogenesis, and cardiac repair after muscle stem cell transplantation into ischemic hearts. J. Am. Coll. Cardiol. 50 1677-1684 (2007).
44. Cursi, K.A. et al. Osteogenic potential of postnatal skeletal muscle-derived stem cells is influenced by donor sex. J. Bone Miner Res. 22, 1592-1602 (2007).
45. Lee, P.Y., Cobain, E., Huard, J. & Huang, L. Thermosensitive hydrogel PEG-PLGA-PEG enhances engraftment of muscle-derived stem cells and promotes healing in diabetic wound. Mol. Ther. 15, 1189-1194 (2007).
46. Kwon, D. et al. Periurethral cellular injection: Comparison of muscle-derived progenitor cells and fibroblasts with regard to efficacy and tissue contractility in an animal model of stress urinary incontinence. Urology 68, 449-454 (2006).
47. Oshima, H. et al. Differential myocardial infarct repair with muscle stem cells compared to myoblasts. Mol. Ther. 12, 1130-1141 (2005).
48. Chermansky, C.J. et al. Intraurethral muscle-derived cell injections increase leak point pressure in a rat model of intrinsic sphincter deficiency. Urology 63, 780-785 (2004).
49. Cannon, T.W. et al. Improved sphincter contractility after allogenic muscle-derived progenitor cell injection into the denervated rat urethra. Urology 62, 958-963 (2003).
50. Cao, B. et al. Muscle stem cells differentiate into haematopoietic lineages but retain myogenic potential. Nat Cell Biol. 5, 640-646 (2003).
51. Li, Y. & Huard, J. Differentiation of muscle-derived cells into myofibroblasts in injured skeletal muscle. Am. J. Pathol. 161 895-907 (2002).
52. Kuroda, R. et al. Cartilage repair using bone morphogenetic protein 4 and muscle-derived stem cells. Arthritis Rheum. 54 433-442 (2006).
53. Lee, J.Y. et al. Enhancement of bone healing based on ex vivo gene therapy using human muscle-derived cells expressing bone morphogenetic protein 2. Hum. Gene Ther. 13, 1201-1211 (2002).
54. Payne, T.R. et al. Regeneration of dystrophin-expressing myocytes in the mdx heart by skeletal muscle stem cells. Gene Ther. 12 1264-1274 (2005).
55. Deasy, B.M. et al. A role for cell sex in stem cell-mediated skeletal muscle regeneration: Female cells have higher muscle regeneration efficiency. J. Cell Biol. 177, 73-86 (2007).
56. Jankowski, R.J., Haluszczak, C., Trucco, M. & Huard, J. Flow cytometric characterization of myogenic cell populations obtained via the preplate technique: Potential for rapid isolation of muscle-derived stem cells. Hum. Gene Ther. 12, 619-628 (2001).
57. Asakura, A., Seale, P., Girgis-Gabardo, A. & Rudnicki, M.A. Myogenic specification of side population cells in skeletal muscle. J. Cell Biol. 159, 123-134 (2002).
58. Crisan, M. et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell (in the press).
59. Zheng, B. et al. Prospective identification of myogenic endothelial cells in human skeletal muscle. Nat. Biotechnol. 25 1025-1034 (2007).
60. Jankowski, R.J., Deasy, B.M. & Huard, J. Muscle-derived stem cells. Gene Ther. 9, 642-647 (2002).
61. Rando, LA. & Blau, H.M. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J. Cell Biol. 125, 1275-1287 (1994).
62. Richler, C. & Yaffe, D. The in vitro cultivation and differentiation capacities of myogenic cell lines. Dev. Biol. 23, 1-22 (1970).
63. Alessandri, G. et al. Isolation and culture of human muscle-derived stem cells able to differentiate into myogenic and neurogenic cell lineages. Lancet 364, 1872-1883 (2004).
64. Epperly, M.W. et al. Bone roarrow origin of cells with capacity for homing and differentiation to esophageal squamous epithelium. Radiat Res. 162, 233-240 (2004).
65. Hwang, J.H. et al. Isolation of muscle derived stem cells from rat and its smooth muscle differentiation [corrected]. Mol. Cells 19, 57-61 (2004).
66. Machida, S., Spangenburg, E.E. & Booth, F.W. Primary rat muscle progenitor cells have decreased proliferation and myotube formation during passages. Cell Prolif. 37, 267-277 (2004).
67. Rouger, K. et al. Progenitor cell isolation from muscle-derived cells based on adhesion properties. J. Histochem Cytochem. 55 607-618 (2007).
68. Sun, J.S., Wu, S.Y. & Lin, F.H. The role of muscle-derived stem cells in bone tissue engineering. Biomaterials 26, 3953-3960 (2005).
69. Huard, J., Cao, B. & Qu-Petersen, Z. Muscle-derived stem cells: potential for muscle regeneration. Birth Defects Res. 69, 230-237 (2003).
70. Peault, B. et al. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol. Ther. 15, 867-877 (2007).
71. Carr, L.K. et al. 1-year follow-up of autologous muscle-derived stem cell injection pilot study to treat stress urinary incontinence. Int. Urogynecol. J. Pelvic. Floor Dysfunct. 19, 881-883 (2008).
72. Deasy, B.M., Jankowski, R.J. & Huard, J. Muscle-derived stem cells: characterization and potential for cell-mediated therapy. Blood Cells Mol. Dis. 27, 924-933 (2001).
73. Tavian, M. et al. The vascular wall as a source of stem cells. Ann. N Y Acad. Sci. 1044, 41-50 (2005).
74. Sarig, R., Baruchi, Z., Fuchs, O., Nudel, U. & Yaffe, D. Regeneration and transdifferentiation potential of muscle-derived stem cells propagated as myospheres. Stem Cells 24, 1769-1778 (2006).
75. Lu, A. et al. Isolation of myogenic progenitor populations from PaX7 deficient skeletal muscle based on adhesion characteristics. Gene Ther. (in the press).
76. Strober, W. Trypan blue exclusion test of cell viability. Curr. Protoc. Immunol. Appendix 3, Appendix 3B (2001).
77. Deasy, B.M. et al. Long-term self-renewal of postnatal muscle-derived stem cells. Mol. Biol. Cell 16, 3323-3333 (2005).
78. Romero-Ramos, M. et al. Neuronal differentiation of stem cells isolated from adult muscle. J. Neurosci. Res. 69, 894-907 (2002).
79. Winitsky S.O. et al. Adult muride skeletal muscle contains cells that can differentiate into beating cardiomyocytes in vitro. PLoS Biol. 3, e87 (2005).
80. Tamaki, T. et al. Cardiomyocyte formation by skeletal muscle-derived multi-myogenic stem cells after transplantation into infarcted myocardium. PloS ONE 3, e1789 (2008).
81. Arsic, N., Mamaeva, D., Lamb, N.J. & Fernandez, A. Muscle-derived stem cells isolated as non-adherent population give rise to cardiac, skeletal muscle and neural lineages. Exp. Cell Res. 314, 1266-1280 (2008).
82. Nolazco, G. et al. Effect of muscle-derived stem cells on the restoration of corpora cavemosa smooth muscle and erectile function in the aged rat. BJU Int. 101, 1156-1164 (2008).