Isolation and characterization of porcine adult muscle-derived progenitor cells

Journal of Cellular Biochemistry

Volumn 105, Issue 5, 2008, Pages 1228-1239

  Wilschut, Karlijn J ^a   Jaksani, Sridevi ^a   Van Den Dolder, Juliette ^a   Haagsman, Henk P ^a   Roelen, Bernard A J ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Adult stem cells; Muscle; Pig

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; CD31 ANTIGEN; DESMIN; MYOGENIC FACTOR 5; OCTAMER TRANSCRIPTION FACTOR 4; SMOOTH MUSCLE ACTIN; THY 1 ANTIGEN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR PAX3; VIMENTIN;

ADIPOGENESIS; ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL EXPANSION; CELL ISOLATION; CELL LINEAGE; CELL MIGRATION; COCULTURE; CONTROLLED STUDY; KARYOTYPE; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; STEM CELL; SWINE;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; FLOW CYTOMETRY; MICE; MUSCLE FIBERS, SKELETAL; MYOBLASTS; STEM CELLS; SWINE;

MURINAE; SUIDAE; SUS;

EID: 57149106731     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21921     Document Type: Article

References (74)

1. Akune T, Ohba S, Kamekura S, Yamaguchi M, Chung UI, Kubota N, Terauchi Y, Harada Y, Azuma Y, Nakamura K, Kadowaki T, Kawaguchi H. 2004. PPARgamma insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors. J Clin Invest 113:846-855.
2. Asakura A, Komaki M, Rudnicki M. 2001. Muscle satellite cells are multi-potential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation 68:245-253.
3. Asakura A, Seale P, Girgis-Gabardo A, Rudnicki MA. 2002. Myogenic specification of side population cells in skeletal muscle. J Cell Biol 159:123-134.
4. Blanton JR Jr, Bidwell CA, Sanders DA, Sharkey CM, McFarland DC, Gerrard DE, Grant AL. 2000. Plasmid transfection and retroviral transduction of porcine muscle cells for cell-mediated gene transfer. J Anim Sci 78:909-918.
5. Blanton JR Jr, Grant AL, McFarland DC, Robinson JP, Bidwell CA. 1999. Isolation of two populations of myoblasts from porcine skeletal muscle. Muscle Nerve 22:43-50.
6. Bosch P, Pratt SL, Stice SL. 2006. Isolation, characterization, gene modification, and nuclear reprogramming of porcine mesenchymal stem cells. Biol Reprod 74:46-57.
7. Buckingham M. 2007. Skeletal muscle progenitor cells and the role of Pax genes. CR Biol 330:530-533.
8. Cao B, Zheng B, Jankowski RJ, Kimura S, Ikezawa M, Deasy B, Cummins J, Epperly M, Qu-Petersen Z, Huard J. 2003. Muscle stem cells differentiate into haematopoietic lineages but retain myogenic potential. Nat Cell Biol 5:640-646.
9. Carlin R, Davis D, Weiss M, Schultz B, Troyer D. 2006. Expression of early transcription factors Oct4, Sox2 and Nanog by porcine umbilical cord (PUC) matrix cells. Reprod Biol Endocrinol 4:8.
10. Chambers I, Smith A. 2004. Self-renewal of teratocarcinoma and embryonic stem cells. Oncogene 23:7150-7160.
11. Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA, Morgan JE. 2005. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122:289-301.
12. Cossu G, Bianco P. 2003. Mesoangioblasts-vascular progenitors for extravascular mesodermal tissues. Curr Opin Genet Dev 13:537-542.
13. Cui Q, Wang GJ, Balian G. 1997. Steroid-induced adipogenesis in a pluripotential cell line from bone marrow. J Bone Joint Surg Am 79:1054-1063.
14. Darabi R, Gehlbach K, Bachoo RM, Kamath S, Osawa M, Kamm KE, Kyba M, Perlingeiro RC. 2008. Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nat Med 14:134-143.
15. Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L, Innocenzi A, Galvez BG, Messina G, Morosetti R, Li S, Belicchi M, Peretti G, Chamberlain JS, Wright WE, Torrente Y, Ferrari S, Bianco P, Cossu G. 2007. Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9:255-267.
16. Dhawan J, Rando TA. 2005. Stem cells in postnatal myogenesis: Molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol 15:666-673.
17. Dodson MV, McFarland DC, Grant AL, Doumit ME, Velleman SG. 1996. Extrinsic regulation of domestic animal-derived satellite cells. Domest Anim Endocrinol 13:107-126.
18. Doumit ME, Merkel RA. 1992. Conditions for isolation and culture of porcine myogenic satellite cells. Tissue Cell 24:253-262.
19. Feldman JL, Stockdale FE. 1991. Skeletalmuscle satellite cell diversity: Satellite cells form fibers of different types in cell culture. Dev Biol 143:320-334.
20. Fiegel HC, Gluer S, Roth B, Rischewski J, von Schweinitz D, Ure B, Lambrecht W, Kluth D. 2004. Stem-like cells in human hepatoblastoma. J Histochem Cytochem 52:1495-1501.
21. Fligger JM, Malven PV, Doumit ME, Merkel RA, Grant AL. 1998. Increases in insulin-like growth factor binding protein-2 accompany decreases in proliferation and differentiation when porcine muscle satellite cells undergo multiple passages. J Anim Sci 76:2086-2093.
22. Grassi F, Pagani F, Spinelli G, De Angelis L, Cossu G, Eusebi F. 2004. Fusion-independent expression of functional ACh receptors in mouse mesoangioblast stem cells contacting muscle cells. J Physiol 560:479-489.
23. Grefte S, Kuijpers-Jagtman AM, Torensma R, Von den Hoff JW. 2007. Skeletal muscle development and regeneration. Stem Cells Dev 16:857-868.
24. Hasegawa T, Oizumi K, Yoshiko Y, Tanne K, Maeda N, Aubin JE. 2008. The PPARgamma-selective ligand BRL-49653 differentially regulates the fate choices of rat calvaria versus rat bone marrow stromal cell populations. BMC Dev Biol 8:71.
25. Hashimoto N, Kiyono T, Wada MR, Umeda R, Goto YI, Nonaka I, Shimizu S, Yasumoto S, Inagawa-Ogashiwa M. 2008. Osteogenic properties of human myogenic progenitor cells. Mech Dev 125:257-269.
26. Hawke TJ, Garry DJ. 2001. Myogenic satellite cells: Physiology to molecular biology. J Appl Physiol 91:534-551.
27. Holterman CE, Rudnicki MA. 2005. Molecular regulation of satellite cell function. Semin Cell Dev Biol 16:575-584.
28. Holzer N, Hogendoorn S, Zurcher L, Garavaglia G, Yang S, Konig S, Laumonier T, Menetrey J. 2005. Autologous transplantation of porcinemyogenic precursor cells in skeletal muscle. Neuromuscul Disord 15:237-244.
29. Hwang YS, Polak JM, Mantalaris A. 2008. In vitro direct osteogenesis of murine embryonic stem cells without embryoid body formation. Stem Cells Dev June 18 [Epub ahead of print].
30. Iohara K, Zheng L, Ito M, Tomokiyo A, Matsushita K, Nakashima M. 2006. Side population cells isolated from porcine dental pulp tissue with self-renewal and multipotency for dentinogenesis, chondrogenesis, adipogenesis, and neurogenesis. Stem Cells 24:2493-2503.
31. Jacquemin V, Furling D, Bigot A, Butler-Browne GS, Mouly V. 2004. IGF-1 induces human myotube hypertrophy by increasing cell recruitment. Exp Cell Res 299:148-158.
32. Jiang Y, Vaessen B, Lenvik T, Blackstad M, Reyes M, Verfaillie CM. 2002. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp Hematol 30:896-904.
33. Kassar-Duchossoy L, Gayraud-Morel B, Gomes D, Rocancourt D, Buckingham M, Shinin V, Tajbakhsh S. 2004. Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice. Nature 431:466-471.
34. Kassar-Duchossoy L, Giacone E, Gayraud-Morel B, Jory A, Gomes D, Tajbakhsh S. 2005. Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev 19:1426-1431.
35. Kim J, Seandel M, Falciatori I, Wen D, Rafii S. 2008. CD34+ testicular stromal cells support long-term expansion of embryonic and adult stem and progenitor cells. Stem Cells July 31 [Epub ahead of print].
36. Kolf CM, Cho E, Tuan RS. 2007. Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: Regulation of niche, self-renewal and differentiation. Arthritis Res Ther 9:204.
37. Kues WA, Petersen B, Mysegades W, Carnwath JW, Niemann H. 2005. Isolation of murine and porcine fetal stem cells from somatic tissue. Biol Reprod 72:1020-1108.
38. Kuijk EW, Du Puy L, Van Tol HT, Haagsman HP, Colenbrander B, Roelen BA. 2007. Validation of reference genes for quantitative RT-PCR studies in porcine oocytes and preimplantation embryos. BMC Dev Biol 7:58.
39. Kuijk EW, Du Puy L, Van Tol HT, Oei CH, Haagsman HP, Colenbrander B, Roelen BA. 2008. Differences in early lineage segregation between mammals. Dev Dyn 237:918-927.
40. Leclerc N, Noh T, Khokhar A, Smith E, Frenkel B. 2005. Glucocorticoids inhibit osteocalcin transcription in osteoblasts by suppressing Egr2/Krox20-binding enhancer. Arthritis Rheum 52:929-939.
41. Lee JY, Qu-Petersen Z, Cao B, Kimura S, Jankowski R, Cummins J, Usas A, Gates C, Robbins P, Wernig A, Huard J. 2000. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol 150:1085-1100.
42. Li CD, Zhang WY, Li HL, Jiang XX, Zhang Y, Tang P, Mao N. 2005. Isolation and identification of a multilineage potential mesenchymal cell from human placenta. Placenta Sep. 17 [Epub ahead of print].
43. Ludwig TE, Levenstein ME, Jones JM, Berggren WT, Mitchen ER, Frane JL, Crandall LJ, Daigh CA, Conard KR, Piekarczyk MS, Llanas RA, Thomson JA. 2006. Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 24:185-187.
44. Mauro A. 1961. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493-495.
45. McKinnell IW, Ishibashi J, Le Grand F, Punch VG, Addicks GC, Greenblatt JF, Dilworth FJ, Rudnicki MA. 2007. Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex. Nat Cell Biol. 10:77-84.
46. Meeson AP, Hawke TJ, Graham S, Jiang N, Elterman J, Hutcheson K, Dimaio JM, Gallardo TD, Garry DJ. 2004. Cellular and molecular regulation of skeletal muscle side population cells. Stem Cells 22:1305-1320.
47. Mesires NT, Doumit ME. 2002. Satellite cell proliferation and differentiation during postnatal growth of porcine skeletal muscle. Am J Physiol Cell Physiol 282:C899-906.
48. Montanaro F, Liadaki K, Schienda J, Flint A, Gussoni E, Kunkel LM. 2004. Demystifying SP cell purification: Viability, yield, and phenotype are defined by isolation parameters. Exp Cell Res 298:144-154.
49. Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A, Partridge T, Buckingham M. 2005. Direct isolation of satellite cells for skeletal muscle regeneration. Science 309:2064-2067.
50. Peault B, Rudnicki M, Torrente Y, Cossu G, Tremblay JP, Partridge T, Gussoni E, Kunkel LM, Huard J. 2007. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 15:867-877.
51. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
52. Pownall ME, Gustafsson MK, Emerson CP Jr. 2002. Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu Rev Cell Dev Biol 18:747-783.
53. Qu-Petersen Z, Deasy B, Jankowski R, Ikezawa M, Cummins J, Pruchnic R, Mytinger J, Cao B, Gates C, Wernig A, Huard J. 2002. Identification of a novel population of muscle stem cells in mice: Potential for muscle regeneration. J Cell Biol 157:851-864.
54. Qu Z, Balkir L, van Deutekom JC, Robbins PD, Pruchnic R, Huard J. 1998. Development of approaches to improve cell survival in myoblast transfer therapy. J Cell Biol 142:1257-1267.
55. Rajkumar VS, Howell K, Csiszar K, Denton CP, Black CM, Abraham DJ. 2005. Shared expression of phenotypic markers in systemic sclerosis indicates a convergence of pericytes and fibroblasts to a myofibroblast lineage in fibrosis. Arthritis Res Ther 7:R1113-1123.
56. Relaix F, Rocancourt D, Mansouri A, Buckingham M. 2005. A Pax3/Pax7-dependent population of skeletalmuscle progenitor cells. Nature 435:948-953.
57. Sampaolesi M, Blot S, D'Antona G, Granger N, Tonlorenzi R, Innocenzi A, Mognol P, Thibaud JL, Galvez BG, Barthelemy I, Perani L, Mantero S, Guttinger M, Pansarasa O, Rinaldi C, Cusella De Angelis MG, Torrente Y, Bordignon C, Bottinelli R, Cossu G. 2006. Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444:574-579.
58. Schienda J, Engleka KA, Jun S, Hansen MS, Epstein JA, Tabin CJ, Kunkel LM, Kardon G. 2006. Somitic origin of limb muscle satellite and side population cells. Proc Natl Acad Sci USA 103:945-950.
59. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. 2000. Pax7 is required for the specification of myogenic satellite cells. Cell 102:777-786.
60. Shetty P, Bharucha K, Tanavde V. 2007. Human umbilical cord blood serum can replace fetal bovine serum in the culture of mesenchymal stem cells. Cell Biol Int 31:293-298.
61. Shi X, Garry DJ. 2006. Muscle stem cells in development, regeneration, and disease. Genes Dev 20:1692-1708.
62. Shockley KR, Rosen CJ, Churchill GA, Lecka-Czernik B. 2007. PPARgamma2 regulates a molecular signature of marrow mesenchymal stem cells. PPAR Res 2007:81219.
63. Suelves M, Lluis F, Ruiz V, Nebreda AR, Munoz-Canoves P. 2004. Phosphorylation of MRF4 transactivation domain by p38 mediates repression of specific myogenic genes. EMBO J 23:365-375.
64. Tamaki T, Okada Y, Uchiyama Y, Tono K, Masuda M, Wada M, Hoshi A, Ishikawa T, Akatsuka A. 2007. Clonal multipotency of skeletal muscle-derived stem cells between mesodermal and ectodermal lineage. Stem Cells 25:2283-2290.
65. Vacanti V, Kong E, Suzuki G, Sato K, Canty JM, Lee T. 2005. Phenotypic changes of adult porcine mesenchymal stem cells induced by prolonged passaging in culture. J Cell Physiol 205:194-201.
66. Vilquin JT, Marolleau JP, Sacconi S, Garcin I, Lacassagne MN, Robert I, Ternaux B, Bouazza B, Larghero J, Desnuelle C. 2005. Normal growth and regenerating ability of myoblasts from unaffected muscles of facioscapulohumeral muscular dystrophy patients. Gene Ther 12:1651-1662.
67. Xiao L, Yuan X, Sharkis SJ. 2006. Activin A maintains self-renewal and regulates fibroblast growth factor, Wnt, and bone morphogenic protein pathways in human embryonic stem cells. Stem Cells 24:1476-1486.
68. Zammit P, Beauchamp J. 2001. The skeletal muscle satellite cell: Stem cell or son of stem cell? Differentiation 68:193-204.
69. Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA, Partridge TA, Beauchamp JR. 2006. Pax7 and myogenic progression in skeletal muscle satellite cells. J Cell Sci 119:1824-1832.
70. Zeng L, Rahrmann E, Hu Q, Lund T, Sandquist L, Felten M, O'Brien TD, Zhang J, Verfaillie C. 2006. Multipotent adult progenitor cells from swine bone marrow. Stem Cells 24:2355-2366.
71. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, Ross J, Haug J, Johnson T, Feng JQ, Harris S, Wiedemann LM, Mishina Y, Li L. 2003. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425:836-841.
72. Zheng B, Cao B, Crisan M, Sun B, Li G, Logar A, Yap S, Pollett JB, Drowley L, Cassino T, Gharaibeh B, Deasy BM, Huard J, Peault B. 2007. Prospective identification of myogenic endothelial cells in human skeletal muscle. Nat Biotechnol 25:1025-1034.
73. Zou L, Zou X, Chen L, Li H, Mygind T, Kassem M, Bunger C. 2008. Multilineage differentiation of porcine bone marrow stromal cells associated with specific gene expression pattern. J Orthop Res 26:56-64.
74. Zuba-Surma EK, Kucia M, Dawn B, Guo Y, Ratajczak MZ, Bolli R. 2008. Bone marrow-derived pluripotent very small embryonic-like stem cells (VSELs) are mobilized after acute myocardial infarction. J Mol Cell Cardiol 44:865-873.