Defining the heterogeneity of skeletal muscle-derived side and main population cells isolated immediately ex vivo

Journal of Cellular Physiology

Volumn 222, Issue 3, 2010, Pages 676-684

  Kallestad, Kristen M ^a   McLoon, Linda K ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 1; CADHERIN; CD34 ANTIBODY; CELL ANTIGEN; CELL MARKER; HOE 33342; M CADHERIN; TRANSCRIPTION FACTOR PAX7; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL POPULATION; CELL SELECTION; CELL SUBPOPULATION; CELL TRANSPLANTATION; CONTROLLED STUDY; EX VIVO STUDY; FLOW CYTOMETRY; MEDICAL LITERATURE; MORTALITY; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; SPECIES; STEM CELL;

ANIMALS; ANTIGENS, CD34; ANTIGENS, CD45; ANTIGENS, LY; BENZIMIDAZOLES; BIOLOGICAL MARKERS; CADHERINS; CELL DIFFERENTIATION; CELL LINEAGE; CELL SEPARATION; CELL SURVIVAL; FLOW CYTOMETRY; FLUORESCENT DYES; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MULTIPOTENT STEM CELLS; MUSCLE, SKELETAL; PAX7 TRANSCRIPTION FACTOR; PHENOTYPE; RABBITS; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 73649109893     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21989     Document Type: Article

References (77)

1. Asakura A, Komaki M, Rudnicki MA. 2001. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation 68:245-253.
2. 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.
3. Beauchamp JR, Heslop L, Yu DS, Tajbakhsh S, Kelly RG, Wernig A, Buckingham ME, Partridge TA, Zammit PS. 2000. Expression of CD34 andMyf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151:1221-1234.
4. Blaveri K, Heslop L, YuDS, Rosenblatt JD, Gross JG, Partridge TA, Morgan JE. 1999. Patterns of repair of dystrophic mouse muscle: Studies on isolated fibers. Dev Dyn 216:244-256.
5. Case J, Horvath TL, Ballas CB, March KL, Srour EF. 2008. In vitro clonal analysis of murine pluripotent stem cells isolated from skeletal muscle and adipose stromal cells. Exp Hematol 36:224-234.
6. Caiozzo VJ, Baker MJ, Huang K, Chou H, Wu YZ, Baldwin KM. 2003. Single-fiber myosin heavy chain polymorphism: How many patterns and what proportions? AmJ Physiol Regul Integr Comp Physiol 285:R570-R580.
7. Camargo FD, Chambers SM, Drew E, McNagny KM, Goodell MA. 2006. Hematopoietic stem cells do not engraft with absolute efficiencies. Blood 107:501-507.
8. Challen GA, Bertoncello I, Deane JA, Ricardo SD, Little MH. 2006. Kidney side population reveals multilineage potential and renal functional capacity but also cellular heterogeneity. J Am Soc Nephrol 17:1896-1912.
9. Ciancio G, Pollack A, Taupier MA, Block NL, Irvin GL III. 1988. Measurement of cell-cycle phase-specific cell death using Hoechst 33342 and propidium iodide: Preservation by ethanol fixation. J Histochem Cytochem 36:1147-1152.
10. 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.
11. Cornelison DD, Wold BJ. 1997. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191:270-283.
12. De Bari C, Dell'Accio F, Vandenabeele F, Vermeesch JR, Raymackers JM, Luyten FP. 2003. Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J Cell Biol 160:909-918.
13. Decary S, Mouly V, Hamida CB, Sautet A, Barbet JP, 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.
14. Decary S, Ben Hamida C, Mouly V, Barbet JP, Hentati F, Butler-Browne GS. 2000. Shorter telomeres in dystrophic muscle consistent with extensive regeneration in young children. Neuromuscul Disord 10:113-120.
15. Dell'Agnola C, Rabascio C, Mancuso P, Capillo M, Pruneri G, Gobbi A, Minucci S, Ronzoni S, Volorio S, Calabrese L, Tradati N, Martinelli G, Shultz L, Bertolini F. 2002. In vitro and in vivo hematopoietic potential of human stem cells residing in muscle tissue. Exp Hematol 30:905-914.
16. Durand RE, Olive PL. 1982. Cytotoxicity, mutagenicity and DNA damage by Hoechst 33342. J Histochem Cytochem 30:111-116.
17. Epting CL, Lopez JE, Shen X, Liu L, Bristow J, Bernstein HS. 2004. Stem cell antigen-1 is necessary for cell-cycle withdrawal and myoblast differentiation in C2C12 cells. J Cell Sci 117:6185-6195.
18. Fukada S, Higuchi S, Segawa M, Koda K, Yamamoto Y, Tsujikawa K, Kohama Y, Uezumi A, imamura M, Miyagoe-Suzuki Y, Takeda S, Yamamoto H. 2004. Purification and cell-surface marker characterization of quiescent satellite cells from murine skeletal muscle by a novel monoclonal antibody. Exp Cell Res 296:245-255.
19. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. 1996. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183:1797-1806.
20. Goodell MA, Rosenzweig M, Kim H, Marks DF, DeMaria M, Paradis G, Grupp SA, Sieff CA, Mulligan RC, Johnson RP. 1997. Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat Med 3:1337-1345.
21. Gussoni E, Blau HM, Kunkel LM. 1997. The fate of individual myoblasts after transplantation into muscles of DMD patients. Nat Med 3:970-977.
22. Gussoni E, Soneoka Y, Strickland CD, Buzney EA, Khan MK, Flint AF, Kunkel LM, Mulligan RC. 1999. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401:390-394.
23. Hardin JA, Sherr DH, DeMaria M, Lopez PA. 1992. A simple fluorescence method for surface antigen phenotyping of lymphocytes undergoing DNA fragmentation. J Immunol Methods 154:99-107.
24. Heslop L, Beauchamp JR, Tajbakhsh S, Buckingham ME, Partridge TA, Zammit PS. 2001. Transplanted primary neonatal myoblasts can give rise to functional satellite cells as identified using the Myf5nlacZl+ mouse. Gene Ther 8:778-783.
25. Hoh JF, Hughes S. 1988. Myogenic and neurogenic regulation ofmyosin gene expression in cat jaw-closing muscles regenerating in fast and slow limb muscle beds. J Muscle Res Cell Motil 9:59-72.
26. Howell JC, Yoder MC, Srour EF. 2002. Hematopoietic potential of murine skeletal muscle-derived CD45(-)Sca-1(+)c-kit(-) cells. Exp Hematol 30:915-924.
27. Huard J, Acsadi G, Jani A, Massie B, Karpati G. 1994. Gene transfer into skeletal muscles by isogenic myoblasts. Hum Gene Ther 5:949-958.
28. Jackson KA, Mi T, Goodell MA. 1999. Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc Natl Acad Sci USA 96:14482-14486.
29. Jankowski RJ, Deasy BM, Cao B, Gates C, Huard J. 2002. The role of CD34 expression and cellular fusion in the regeneration capacity of myogenic progenitor cells. J Cell Sci 115:4361-4374.
30. 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.
31. Kadi F, Charifi N, Denic C, Lexell J. 2004. Satellite cells and myonuclei in young and elderly women and men. Muscle Nerve 29:120-127.
32. Karpati G, Ajdukovic D, Arnold D,Gledhill RB, Guttmann R, Holland P, Koch PA, Shoubridge E, Spence D, Vanasse M, Watters GV, Abrahamowicz M, Duff C, Worton RG. 1993. Myoblast transfer in Duchenne muscular dystrophy. Ann Neurol 34:8-17.
33. Khoruts A, Mondino A, Pape KA, Reiner SL, Jenkins MK. 1998. A natural immunological adjuvant enhances T cell clonal expansion through a CD28-dependent, interleukin (IL)-2-independent mechanism. J Exp Med 187:225-236.
34. KomuroH, Saihara R, Shinya M, Takita J, Kaneko S, Kaneko M, Hayashi Y. 2007. Identification of side population cells (stem-like cell population) in pediatric solid tumor cell lines. J Pediatr Surg 42:2040-2045.
35. Kondo T, Case J, Srour EF, Hashino E. 2006. Skeletal muscle-derived progenitor cells exhibit neural competence. Neuroreport 17:1-4.
36. Lindstrom M, Thornell LE. 2009. New multiple labelling method for improved satellite cell identification in human muscle: Application to a cohort of power-lifters and sedentary men. Histochem Cell Biol 132:141-157.
37. Lipton BH, Schultz E. 1979. Developmental fate of skeletal muscle satellite cells. Science 205:1292-1294.
38. Majka SM, Jackson KA, Kienstra KA, Majesky MW, Goodell MA, Hirschi KK. 2003. Distinct progenitor populations in skeletal muscle are bone marrow derived and exhibit different cell fates during vascular regeneration. J Clin Invest 111:71-79.
39. Mauro A. 1961. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493-495.
40. McKinney-Freeman SL, Jackson KA, Camargo FD, Ferrari G, Mavilio F, Goodell MA. 2002. Muscle-derived hematopoietic stem cells are hematopoietic in origin. Proc Natl Acad Sci USA 99:1341-1346.
41. McKinney-Freeman SL, Majka SM, Jackson KA, Norwood K, Hirschi KK, Goodell MA. 2003. Altered phenotype and reduced function of muscle-derived hematopoietic stem cells. Exp Hematol 31:806-814.
42. McLoon LK, Thorstenson KM, Solomon A, Lewis MP. 2007. Myogenic precursor cells in craniofacial muscles. Oral Sci 13:134-140.
43. Meeson AP, Hawke TJ, Graham S, JiangN, 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.
44. Miller RG, Sharma KR, Pavlath GK, Gussoni E, Mynhier M, Lanctot AM, Greco CM, Steinman L, Blau HM. 1997. Myoblast implantation in Duchenne muscular dystrophy: The San Francisco study. Muscle Nerve 20:469-478.
45. Mitchell PO, Mills T,O'Connor RS, Kline ER, Graubert T,Dzierzak E, Pavlath GK. 2005. Sca-1 negatively regulates proliferation and differentiation of muscle cells. Dev Biol 283:240-252.
46. 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.
47. Morgan JE, Coulton GR, Partridge TA. 1987. Muscle precursor cells invade and repopulate freeze-killed muscles. J Muscle Res Cell Motil 8:386-396.
48. Motohashi N, Uezumi A, Yada E, Fukada S, Fukushima K, Imaizumi K, Miyagoe-Suzuki Y, Takeda S. 2008. Muscle CD31(-) CD45(-) side population cells promote muscle regeneration by stimulating proliferation and migration of myoblasts.AmJ Pathol 173:781-791.
49. Muskiewicz KR, Frank NY, Flint AF, Gussoni E. 2005. Myogenic potential of muscle side and main population cells after intravenous injection into sub-lethally irradiated mdx mice. J Histochem Cytochem 53:861-873.
50. Naylor CS, Jaworska E, Branson K, Embleton MJ, Chopra R. 2005. Side population/ABCG2-positive cells represent a heterogeneous group of haemopoietic cells: Implications for the use of adult stem cells in transplantation and plasticity protocols. Bone Marrow Transplant 35:353-360.
51. Porter JD, Khanna S, Kaminski HJ, Rao JS, Merriam AP, Richmonds CR, Leahy P, Li J, Andrade FH. 2001. Extraocular muscle is defined by a fundamentally distinct gene expression profile. Proc Natl Acad Sci USA 98:12062-12067.
52. 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.
53. Rando TA, Blau HM. 1994. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J Cell Biol 125:1275-1287.
54. Redvers RP, Li A, Kaur P. 2006. Side population in adult murine epidermis exhibits phenotypic and functional characteristics of keratinocyte stem cells. Proc Natl Acad Sci USA 103:13168-13173.
55. Reimann J, Brimah K, Schroder R, Wernig A, Beauchamp JR, Partridge TA. 2004. Pax7 distribution in human skeletal muscle biopsies and myogenic tissue cultures. Cell Tissue Res 315:233-242.
56. Renault V, Piron-Hamelin G, Forestier C, DiDona S, Decary S, Hentati F, Saillant G, Butler-Browne GS, Mouly V. 2000. Skeletal muscle regeneration and the mitotic clock. Exp Gerontol 35:711-719.
57. Rivier F, Alkan O, Flint AF, Muskiewicz K, Allen PD, Leboulch P, Gussoni E. 2004. Role of bone marrow cell trafficking in replenishing skeletal muscle SP and MP cell populations. J Cell Sci 117:1979-1988.
58. Sacco A, Doyonnas R, Kraft P, Vitorovic S, Blau HM. 2008. Self-renewal and expansion of single transplanted muscle stem cells. Nature 456:502-506.
59. 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.
60. 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.
61. Sherwood RI, Christensen JL, Conboy IM, Conboy MJ, Rando RA, Weissman IL, Wagers AJ. 2004. Isolation of adult mouse myogenic progenitors: Functional heterogeneity of cells within and engrafting skeletal muscle. Cell 119:543-554.
62. Skuk D, Caron N, Goulet M, Roy B, Espinosa F, Tremblay JP. 2002. Dynamics of the early immune cellular reactions after myogenic cell transplantation. Cell Transplant 11:671-681.
63. Smythe GM, Grounds MD. 2000. Exposure to tissue culture conditions can adversely affect myoblast behavior in vivo in whole muscle grafts: Implications for myoblast transfer therapy. Cell Transplant 9:379-393.
64. Spangrude GJ, Heimfeld S, Weissman IL. 1988. Purification and characterization of mouse hematopoietic stem cells. Science 241:58-62.
65. Tamaki T, Akatsuka A, Okada Y, Matsuzaki Y, Okano H, Kimura M. 2003. Growth and differentiation potential of main- and side-population cells derived from murine skeletal muscle. Exp Cell Res 291:83-90.
66. Tanaka KK, Hall JK, Troy AA, Cornelison DD, Majka SM, Olwin BB. 2009. Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration. Cell Stem Cell 4:217-225.
67. Torrente Y, Tremblay JP, Pisati F, Belicchi M, Rossi B, Sironi M, Fortunato F, El Fahime M, D'Angelo MG, Caron NJ, Constantin G, Paulin D, Scarlato G, Bresolin N. 2001. Intraarterial injection of muscle-derived CD34(+)Sca-1(+) stem cells restores dystrophin in mdx mice. J Cell Biol 152:335-348.
68. Tremblay JP, Bouchard JP,Malouin F, TheauD, Cottrell F, Collin H, Rouche A, Gilgenkrantz S, Abbadi N, Tremblay M, Tomé FMS, Fardeau M. 1993. Myoblast transplantation between monozygotic twin girl carriers of Duchenne muscular dystrophy. Neuromuscul Disord 3:583-592.
69. Uezumi A, Ojima K, Fukada S, Ikemoto M, Masuda S, Miyagoe-Suzuki Y, Takeda S. 2006. Functional heterogeneity of side population cells in skeletal muscle. Biochem Biophys Res Commun 341:864-873.
70. Wallen CA, Higashikubo R, Roti Roti JL. 1983. Comparison of the cell kill measured by the Hoechst-propidium iodide flow cytometric assay and the colony formation assay. Cell Tissue Kinet 16:357-365.
71. Watt DJ. 1990. A comparison of long-term survival of muscle precursor cell suspensions and minced muscle allografts in the non-tolerant mouse. Adv Exp Med Biol 280:35-38.
72. Wolnicka-Glubisz A, King W, Noonan FP. 2005. SCA-1+ cells with an adipocyte phenotype in neonatal mouse skin. J Invest Dermatol 125:383-385.
73. Wozniak AC, Pilipowicz O, Yablonka-Reuveni Z, Greenway S, Craven S, Scott E, Anderson JE. 2003. C-met expression and mechanical activation of satellite cells on cultured muscle fibers. J Histochem Cytochem 51:1437-1445.
74. Yoshida N, Yoshida S, Koishi K, Masuda K, Nabeshima Y. 1998. Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf-5 generates "reserve cells". J Cell Sci 111:769-779.
75. Zammit PS, Heslop L, Hudon Rosenblatt JD, Tajbakhsh S, Buckingham ME, Beauchamp JR, Partridge TA. 2002. Kinetics of myoblast proliferation show that resident satellite cells are competent to fully regenerate skeletal muscle fibers. Exp Cell Res 281:39-49.
76. Zeng H, Park JW, Guo M, Lin G, Li XJ, Chen FP, Xu RH. 2009. Lack of ABCG2 expression and side population properties in human pluripotent stem cells. Stem Cells 27:2435-2445.
77. Zhang X, Chen J, Davis B, Kiechle F. 1999. Hoechst 33342 induces apoptosis in HL-60 cells and inhibits topoisomerase I in vivo. Arch Pathol Lab Med 123:921-927.