Myogenesis pp 21-52

Part of the Methods in Molecular Biology book series (MIMB, volume 798)

Skeletal Muscle Satellite Cells: Background and Methods for Isolation and Analysis in a Primary Culture System

Protocol

Abstract

Repair of adult skeletal muscle depends on satellite cells, myogenic stem cells located between the basal lamina and the plasmalemma of the myofiber. Standardized protocols for the isolation and culture of satellite cells are key tools for understanding cell autonomous and extrinsic factors that regulate their performance. Knowledge gained from such studies can contribute important insights to developing strategies for the improvement of muscle repair following trauma and in muscle wasting disorders. This chapter provides an introduction to satellite cell biology and further describes the basic protocol used in our laboratory to isolate and culture satellite cells from adult skeletal muscle. The cell culture conditions detailed herein support proliferation and differentiation of satellite cell progeny and the development of reserve cells, which are thought to reflect the in vivo self-renewal ability of satellite cells. Additionally, this chapter describes our standard immunostaining protocol that allows the characterization of satellite cell progeny by the temporal expression of characteristic transcription factors and structural proteins associated with different stages of myogenic progression. Although emphasis is given here to the isolation and characterization of satellite cells from mouse hindlimb muscles, the protocols are suitable for other muscle types (such as diaphragm and extraocular muscles) and for muscles from other species, including chicken and rat. Altogether, the basic protocols described are straightforward and facilitate the study of diverse aspects of skeletal muscle stem cells.

Key words

Skeletal muscle Satellite cell Stem cell Myogenesis Pronase Gelatin Matrigel Pax7 MyoD Myogenin 

References

  1. 1.
    Hawke, TJ., and Garry, DJ. (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91, 534–551.PubMedGoogle Scholar
  2. 2.
    Zammit, PS., Partridge, TA., and Yablonka-Reuveni, Z. (2006) The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histochem Cytochem 54, 1177–1191.PubMedCrossRefGoogle Scholar
  3. 3.
    Yablonka-Reuveni, Z., and Day, K. (2011) Skeletal muscle stem cells in the spotlight: the satellite cell., in Regenerating the Heart: Stem Cells and the Cardiovascular System (Stem Cell Biology and Regenerative Medicine Series) (Cohen, I., and Gaudette, G., Eds.) Springer, Humana Press, Chapter 11, pp. 173–200.Google Scholar
  4. 4.
    Mauro, A. (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9, 493–495.PubMedCrossRefGoogle Scholar
  5. 5.
    Katz, B. (1961) The terminations of the afferent nerve fibre in the muscle spindle of the frog. Philos Trans Royal Soc Lond 243, 221–240.CrossRefGoogle Scholar
  6. 6.
    Bischoff, R. (1975) Regeneration of single skeletal muscle fibers in vitro. Anat Rec 182, 215–235.PubMedCrossRefGoogle Scholar
  7. 7.
    Konigsberg, U.R., Lipton, B.H., and Konigsberg, I.R. (1975) The regenerative response of single mature muscle fibers isolated in vitro. Dev Biol 45, 260–275.PubMedCrossRefGoogle Scholar
  8. 8.
    Yablonka-Reuveni, Z., and Rivera, A.J. (1994) Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev Biol 164, 588–603.PubMedCrossRefGoogle Scholar
  9. 9.
    Rosenblatt, J.D., Lunt, A.I., Parry, D.J., and Partridge, T.A. (1995) Culturing satellite cells from living single muscle fiber explants. In Vitro Cell Dev Biol Anim 31, 773–779.PubMedCrossRefGoogle Scholar
  10. 10.
    Zammit, P.S., Golding, J.P., Nagata, Y., Hudon, V., Partridge, T.A., and Beauchamp, J.R. (2004) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166, 347–357.PubMedCrossRefGoogle Scholar
  11. 11.
    Collins, C.A., Olsen, I., Zammit, P.S., Heslop, L., Petrie, A., Partridge, T.A., and Morgan, J.E. (2005) Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122, 289–301.PubMedCrossRefGoogle Scholar
  12. 12.
    Shefer, G., Van de Mark, D.P., Richardson, J.B., and Yablonka-Reuveni, Z. (2006) Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev Biol 294, 50–66.PubMedCrossRefGoogle Scholar
  13. 13.
    Day, K., Shefer, G., Richardson, J.B., Enikolopov, G., and Yablonka-Reuveni, Z. (2007) Nestin-GFP reporter expression defines the quiescent state of skeletal muscle satellite cells. Dev Biol 304, 246–259.PubMedCrossRefGoogle Scholar
  14. 14.
    Muir, A.R., Kanji, A.H., and Allbrook, D. (1965) The structure of the satellite cells in skeletal muscle. J Anat 99, 435–444.PubMedGoogle Scholar
  15. 15.
    Yablonka-Reuveni, Z. (1995) Development and postnatal regulation of adult myoblasts. Microsc Res Tech 30, 366–380.PubMedCrossRefGoogle Scholar
  16. 16.
    Boldrin, L., Muntoni, F., and Morgan, J.E. (2010) Are Human and Mouse Satellite Cells Really the Same? J Histochem Cytochem 58, 941–955.PubMedCrossRefGoogle Scholar
  17. 17.
    Biressi, S., and Rando, T.A. (2010) Heterogeneity in the muscle satellite cell population. Semin Cell Dev Biol 21, 845–854.PubMedCrossRefGoogle Scholar
  18. 18.
    Seale, P., Sabourin, L.A., Girgis-Gabardo, A., Mansouri, A., Gruss, P., and Rudnicki, M.A. (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102, 777–786.PubMedCrossRefGoogle Scholar
  19. 19.
    Day, K., Shefer, G., Shearer, A., and Yablonka-Reuveni, Z. (2010) The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny. Dev Biol 340, 330–343.PubMedCrossRefGoogle Scholar
  20. 20.
    Shefer, G., Rauner, G., Yablonka-Reuveni, Z., and Benayahu, D. (2010) Reduced satellite cell numbers and myogenic capacity in aging can be alleviated by endurance exercise. PLoS One. 5, e13307.PubMedCrossRefGoogle Scholar
  21. 21.
    Halevy, O., Piestun, Y., Allouh, M.Z., Rosser, B.W., Rinkevich, Y., Reshef, R., Rozenboim, I., Wleklinski-Lee, M., and Yablonka-Reuveni, Z. (2004) Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev Dyn 231, 489–502.PubMedCrossRefGoogle Scholar
  22. 22.
    Allouh, M.Z., Yablonka-Reuveni, Z., and Rosser, B.W. (2008) Pax7 reveals a greater frequency and concentration of satellite cells at the ends of growing skeletal muscle fibers. J Histochem Cytochem 56, 77–87.PubMedCrossRefGoogle Scholar
  23. 23.
    Lindstrom, M., and Thornell, L.E. (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.PubMedCrossRefGoogle Scholar
  24. 24.
    Lindstrom, M., Pedrosa-Domellof, F., and Thornell, L.E. (2010) Satellite cell heterogeneity with respect to expression of MyoD, myogenin, Dlk1 and c-Met in human skeletal muscle: application to a cohort of power lifters and sedentary men. Histochem Cell Biol 134, 371–385.PubMedCrossRefGoogle Scholar
  25. 25.
    Montarras, D., Morgan, J., Collins, C., Relaix, F., Zaffran, S., Cumano, A., Partridge, T., and Buckingham, M. (2005) Direct isolation of satellite cells for skeletal muscle regeneration. Science 309, 2064–2067.PubMedCrossRefGoogle Scholar
  26. 26.
    Beauchamp, J.R., Heslop, L., Yu, D.S., Tajbakhsh, S., Kelly, R.G., Wernig, A., Buckingham, M.E., Partridge, T.A., and Zammit, P.S. (2000) Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151, 1221–1234.PubMedCrossRefGoogle Scholar
  27. 27.
    Ono, Y., Boldrin, L., Knopp, P., Morgan, J.E., and Zammit, P.S. (2010) Muscle satellite cells are a functionally heterogeneous population in both somite-derived and branchiomeric muscles. Dev Biol 337, 29–41.PubMedCrossRefGoogle Scholar
  28. 28.
    Dellavalle, A., Sampaolesi, M., Tonlorenzi, R., Tagliafico, E., Sacchetti, B., Perani, L., Innocenzi, A., Galvez, B.G., Messina, G., Morosetti, R., Li, S., Belicchi, M., Peretti, G., Chamberlain, J.S., Wright, W.E., Torrente, Y., Ferrari, S., Bianco, P., and Cossu, G. (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9, 255–267.PubMedCrossRefGoogle Scholar
  29. 29.
    Zheng, B., Cao, B., Crisan, M., Sun, B., Li, G., Logar, A., Yap, S., Pollett, J.B., Drowley, L., Cassino, T., Gharaibeh, B., Deasy, B.M., Huard, J., and Peault, B. (2007) Prospective identification of myogenic endothelial cells in human skeletal muscle. Nat Biotechnol 25, 1025–1034.PubMedCrossRefGoogle Scholar
  30. 30.
    Tedesco, F.S., Dellavalle, A., Diaz-Manera, J., Messina, G., and Cossu, G. (2010) Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J Clin Invest 120, 11–19.PubMedCrossRefGoogle Scholar
  31. 31.
    Moss, F.P., and Leblond, C.P. (1971) Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec 170, 421–435.PubMedCrossRefGoogle Scholar
  32. 32.
    Campion, D.R. (1984) The muscle satellite cell: a review. Int Rev Cytol 87, 225–251.PubMedCrossRefGoogle Scholar
  33. 33.
    Schultz, E. (1996) Satellite cell proliferative compartments in growing skeletal muscles. Dev Biol 175, 84–94.PubMedCrossRefGoogle Scholar
  34. 34.
    White, R.B., Bierinx, A.S., Gnocchi, V.F., and Zammit, P.S. (2010) Dynamics of muscle fibre growth during postnatal mouse development. BMC Dev Biol 10, 21.PubMedCrossRefGoogle Scholar
  35. 35.
    Schultz, E., Gibson, M.C., and Champion, T. (1978) Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J Exp Zool 206, 451–456.PubMedCrossRefGoogle Scholar
  36. 36.
    Snow, M.H. (1978) An autoradiographic study of satellite cell differentiation into regenerating myotubes following transplantation of muscles in young rats. Cell Tissue Res 186, 535–540.PubMedCrossRefGoogle Scholar
  37. 37.
    Grounds, M.D., and Yablonka-Reuveni, Z. (1993) Molecular and cell biology of skeletal muscle regeneration. Mol Cell Biol Hum Dis Ser 3, 210–256.PubMedGoogle Scholar
  38. 38.
    Bischoff, R. (1989) Analysis of muscle regeneration using single myofibers in culture. Med Sci Sports Exerc 21, S164–172.PubMedGoogle Scholar
  39. 39.
    Yablonka-Reuveni, Z., Seger, R., and Rivera, A.J. (1999) Fibroblast growth factor promotes recruitment of skeletal muscle satellite cells in young and old rats. J Histochem Cytochem 47, 23–42.PubMedCrossRefGoogle Scholar
  40. 40.
    Anderson, J.E. (2006) The satellite cell as a companion in skeletal muscle plasticity: currency, conveyance, clue, connector and colander. J Exp Biol 209, 2276–2292.PubMedCrossRefGoogle Scholar
  41. 41.
    Gopinath, S.D., and Rando, T.A. (2008) Stem cell review series: aging of the skeletal muscle stem cell niche. Aging Cell 7, 590–598.PubMedCrossRefGoogle Scholar
  42. 42.
    Conboy, I.M., Conboy, M.J., Wagers, A.J., Girma, E.R., Weissman, I.L., and Rando, T.A. (2005) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433, 760–764.PubMedCrossRefGoogle Scholar
  43. 43.
    Carlson, M.E., Conboy, M.J., Hsu, M., Barchas, L., Jeong, J., Agrawal, A., Mikels, A.J., Agrawal, S., Schaffer, D.V., and Conboy, I.M. (2009) Relative roles of TGF-beta1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell 8, 676–689.PubMedCrossRefGoogle Scholar
  44. 44.
    Shavlakadze, T., McGeachie, J., and Grounds, M.D. (2010) Delayed but excellent myogenic stem cell response of regenerating geriatric skeletal muscles in mice. Biogerontology 11, 363–366.PubMedCrossRefGoogle Scholar
  45. 45.
    Shefer, G., and Yablonka-Reuveni, Z. (2008) Ins and outs of satellite cell myogenesis: the role of the ruling growth factors., in Skeletal Muscle Repair and Regeneration (Schiaffino, S., and Partridge, T., Eds.) pp 107–144, Springer, Dordrecht, Netherlands.CrossRefGoogle Scholar
  46. 46.
    Day, K., Paterson, B., and Yablonka-Reuveni, Z. (2009) A distinct profile of myogenic regulatory factor detection within Pax7+ cells at S phase supports a unique role of Myf5 during posthatch chicken myogenesis. Dev Dyn 238, 1001–1009.PubMedCrossRefGoogle Scholar
  47. 47.
    Sacco, A., Doyonnas, R., Kraft, P., Vitorovic, S., and Blau, H.M. (2008) Self-renewal and expansion of single transplanted muscle stem cells. Nature 456, 502–506.PubMedCrossRefGoogle Scholar
  48. 48.
    Zammit, P.S., Heslop, L., Hudon, V., Rosenblatt, J.D., Tajbakhsh, S., Buckingham, M.E., Beauchamp, J.R., and Partridge, T.A. (2002) Kinetics of myoblast proliferation show that resident satellite cells are competent to fully regenerate skeletal muscle fibers. Exp Cell Res 281, 39–49.PubMedCrossRefGoogle Scholar
  49. 49.
    Collins, C.A., Zammit, P.S., Ruiz, A.P., Morgan, J.E., and Partridge, T.A. (2007) A population of myogenic stem cells that survives skeletal muscle aging. Stem Cells 25, 885–894.PubMedCrossRefGoogle Scholar
  50. 50.
    Thompson, L.V. (2009) Age-related muscle dysfunction. Exp Gerontol 44, 106–111.PubMedCrossRefGoogle Scholar
  51. 51.
    Grounds, M.D. (1998) Age-associated changes in the response of skeletal muscle cells to exercise and regeneration. Ann N Y Acad Sci 854, 78–91.PubMedCrossRefGoogle Scholar
  52. 52.
    Carlson, B.M., and Faulkner, J.A. (1989) Muscle transplantation between young and old rats: age of host determines recovery. Am J Physiol 256, C1262–1266.PubMedGoogle Scholar
  53. 53.
    Aguennouz, M., Vita, G.L., Messina, S., Cama, A., Lanzano, N., Ciranni, A., Rodolico, C., Di Giorgio, R.M., and Vita, G. Telomere shortening is associated to TRF1 and PARP1 overexpression in Duchenne muscular dystrophy. Neurobiol Aging. 2010 Feb 4. Google Scholar
  54. 54.
    Blau, H.M., Webster, C., and Pavlath, G.K. (1983) Defective myoblasts identified in Duchenne muscular dystrophy. Proc Natl Acad Sci USA 80, 4856–4860.PubMedCrossRefGoogle Scholar
  55. 55.
    Webster, C., and Blau, H.M. (1990) Accelerated age-related decline in replicative life-span of Duchenne muscular dystrophy myoblasts: implications for cell and gene therapy. Somat Cell Mol Genet 16, 557–565.PubMedCrossRefGoogle Scholar
  56. 56.
    Charge, S.B., and Rudnicki, M.A. (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84, 209–238.PubMedCrossRefGoogle Scholar
  57. 57.
    Yablonka-Reuveni, Z., Day, K., Vine, A., and Shefer, G. (2008) Defining the transcriptional signature of skeletal muscle stem cells. J Anim Sci 86, E207–216.PubMedCrossRefGoogle Scholar
  58. 58.
    Olguin, H.C., Yang, Z., Tapscott, S.J., and Olwin, B.B. (2007) Reciprocal inhibition between Pax7 and muscle regulatory factors modulates myogenic cell fate determination. J Cell Biol 177, 769–779.PubMedCrossRefGoogle Scholar
  59. 59.
    Collins, C.A., Gnocchi, V.F., White, R.B., Boldrin, L., Perez-Ruiz, A., Relaix, F., Morgan, J.E., and Zammit, P.S. (2009) Integrated functions of Pax3 and Pax7 in the regulation of proliferation, cell size and myogenic differentiation. PLoS One 4, e4475.PubMedCrossRefGoogle Scholar
  60. 60.
    Lepper, C., Conway, S.J., and Fan, C.M. (2009) Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460, 627–631.PubMedCrossRefGoogle Scholar
  61. 61.
    Andres, V., and Walsh, K. (1996) Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J Cell Biol 132, 657–666.PubMedCrossRefGoogle Scholar
  62. 62.
    Kastner, S., Elias, M.C., Rivera, A.J., and Yablonka-Reuveni, Z. (2000) Gene expression patterns of the fibroblast growth factors and their receptors during myogenesis of rat satellite cells. J Histochem Cytochem 48, 1079–1096.PubMedCrossRefGoogle Scholar
  63. 63.
    Yablonka-Reuveni, Z., Rudnicki, M.A., Rivera, A.J., Primig, M., Anderson, J.E., and Natanson, P. (1999) The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD. Dev Biol 210, 440–455.PubMedCrossRefGoogle Scholar
  64. 64.
    Clegg, C.H., Linkhart, T.A., Olwin, B.B., and Hauschka, S.D. (1987) Growth factor control of skeletal muscle differentiation: commitment to terminal differentiation occurs in G1 phase and is repressed by fibroblast growth factor. J Cell Biol 105, 949–956.PubMedCrossRefGoogle Scholar
  65. 65.
    Yablonka-Reuveni, Z., Balestreri, T.M., and Bowen-Pope, D.F. (1990) Regulation of proliferation and differentiation of myoblasts derived from adult mouse skeletal muscle by specific isoforms of PDGF. J Cell Biol 111, 1623–1629.PubMedCrossRefGoogle Scholar
  66. 66.
    Yablonka-Reuveni, Z., and Rivera, A.J. (1997) Influence of PDGF-BB on proliferation and transition through the MyoD-myogenin-MEF2A expression program during myogenesis in mouse C2 myoblasts. Growth Factors 15, 1–27.PubMedCrossRefGoogle Scholar
  67. 67.
    Graves, D.C., and Yablonka-Reuveni, Z. (2000) Vascular smooth muscle cells spontaneously adopt a skeletal muscle phenotype: a unique Myf5(-)/MyoD(+) myogenic program. J Histochem Cytochem 48, 1173–1193.PubMedCrossRefGoogle Scholar
  68. 68.
    Kwiatkowski, B.A., Kirillova, I., Richard, R.E., Israeli, D., and Yablonka-Reuveni, Z. (2008) FGFR4 and its novel splice form in myogenic cells: Interplay of glycosylation and tyrosine phosphorylation. J Cell Physiol 215, 803–817.PubMedCrossRefGoogle Scholar
  69. 69.
    Yablonka-Reuveni, Z., and Anderson, J.E. (2006) Satellite cells from dystrophic (mdx) mice display accelerated differentiation in primary cultures and in isolated myofibers. Dev Dyn 235, 203–212.PubMedCrossRefGoogle Scholar
  70. 70.
    Shefer, G., and Yablonka-Reuveni, Z. (2005) Isolation and culture of skeletal muscle myofibers as a means to analyze satellite cells. Methods Mol Biol 290, 281–304.PubMedGoogle Scholar
  71. 71.
    Keire, P., Shearer, A., Shefer, G., and Yablonka-Reuveni, Z. (2012) Isolation and culture of skeletal muscle myofibers as a means to analyze satellite cells. Methods Mol Biol (‘Basic Cell Culture Protocols’, 4th edition). In press.Google Scholar
  72. 72.
    Yablonka-Reuveni, Z. (2004) Isolation and culture of myogenic stem cells., in Handbook of Stem Cells - Vol 2: Adult and Fetal Stem Cells (Lanza, R., Blau, D., Melton, D., Moore, M., Thomas, E.D., Verfaillie, C., Weissman, I., and West, M., Eds.) pp 571–580, Elsevier: Academic Press, San Diego.Google Scholar
  73. 73.
    Richler, C., and Yaffe, D. (1970) The in vitro cultivation and differentiation capacities of myogenic cell lines. Dev Biol 23, 1–22.PubMedCrossRefGoogle Scholar
  74. 74.
    Rando, T.A., and Blau, H.M. (1994) Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J Cell Biol 125, 1275–1287.PubMedCrossRefGoogle Scholar
  75. 75.
    Qu-Petersen, Z., Deasy, B., Jankowski, R., Ikezawa, M., Cummins, J., Pruchnic, R., Mytinger, J., Cao, B., Gates, C., Wernig, A., and Huard, J. (2002) Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol 157, 851–864.PubMedCrossRefGoogle Scholar
  76. 76.
    Yablonka-Reuveni, Z., Quinn, L.S., and Nameroff, M. (1987) Isolation and clonal analysis of satellite cells from chicken pectoralis muscle. Dev Biol 119, 252–259.PubMedCrossRefGoogle Scholar
  77. 77.
    Yablonka-Reuveni, Z., and Nameroff, M. (1987) Skeletal muscle cell populations. Separation and partial characterization of fibroblast-like cells from embryonic tissue using density centrifugation. Histochemistry 87, 27–38.PubMedCrossRefGoogle Scholar
  78. 78.
    Morgan, J.E. (1988) Myogenicity in vitro and in vivo of mouse muscle cells separated on discontinuous Percoll gradients. J Neurol Sci 85, 197–207.PubMedCrossRefGoogle Scholar
  79. 79.
    Yablonka-Reuveni, Z. (1988) Discrimination of myogenic and nonmyogenic cells from embryonic skeletal muscle by 90 degrees light scattering. Cytometry 9, 121–125.PubMedCrossRefGoogle Scholar
  80. 80.
    Yablonka-Reuveni, Z. (1989) Application of density centrifugation and flow cytometry for the isolation and characterization of myogenic and fibroblast-like cells from skeletal muscle, in Cellular and Molecular Biology of Muscle Development (Kedes, L.H., Ed.) pp 869–879, John Wiley & Sons Inc, New York.Google Scholar
  81. 81.
    Ieronimakis, N., Balasundaram, G., Rainey, S., Srirangam, K., Yablonka-Reuveni, Z., and Reyes, M. (2010) Absence of CD34 on murine skeletal muscle satellite cells marks a reversible state of activation during acute injury. PLoS One 5, e10920.PubMedCrossRefGoogle Scholar
  82. 82.
    Cerletti, M., Jurga, S., Witczak, C.A., Hirshman, M.F., Shadrach, J.L., Goodyear, L.J., and Wagers, A.J. (2008) Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 134, 37–47.PubMedCrossRefGoogle Scholar
  83. 83.
    Tanaka, K.K., Hall, J.K., Troy, A.A., Cornelison, D.D., Majka, S.M., and Olwin, B.B. (2009) Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration. Cell Stem Cell 4, 217–225.PubMedCrossRefGoogle Scholar
  84. 84.
    Uezumi, A., Fukada, S., Yamamoto, N., Takeda, S., and Tsuchida, K. (2010) Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol 12, 143–152.PubMedCrossRefGoogle Scholar
  85. 85.
    Bosnakovski, D., Xu, Z., Li, W., Thet, S., Cleaver, O., Perlingeiro, R.C., and Kyba, M. (2008) Prospective isolation of skeletal muscle stem cells with a Pax7 reporter. Stem Cells 26, 3194–3204.PubMedCrossRefGoogle Scholar
  86. 86.
    Biressi, S., Tagliafico, E., Lamorte, G., Monteverde, S., Tenedini, E., Roncaglia, E., Ferrari, S., Ferrari, S., Cusella-De Angelis, M.G., Tajbakhsh, S., and Cossu, G. (2007) Intrinsic phenotypic diversity of embryonic and fetal myoblasts is revealed by genome-wide gene expression analysis on purified cells. Dev Biol 304, 633–651.PubMedCrossRefGoogle Scholar
  87. 87.
    Christov, C., Chretien, F., Abou-Khalil, R., Bassez, G., Vallet, G., Authier, F.J., Bassaglia, Y., Shinin, V., Tajbakhsh, S., Chazaud, B., and Gherardi, R.K. (2007) Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol Biol Cell 18, 1397–1409.PubMedCrossRefGoogle Scholar
  88. 88.
    Gayraud-Morel, B., Chretien, F., Flamant, P., Gomes, D., Zammit, P.S., and Tajbakhsh, S. (2007) A role for the myogenic determination gene Myf5 in adult regenerative myogenesis. Dev Biol 312, 13–28.PubMedCrossRefGoogle Scholar
  89. 89.
    Joe, A.W., Yi, L., Natarajan, A., Le Grand, F., So, L., Wang, J., Rudnicki, M.A., and Rossi, F.M. (2010) Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol 12, 153–163.PubMedCrossRefGoogle Scholar
  90. 90.
    Kanisicak, O., Mendez, J.J., Yamamoto, S., Yamamoto, M., and Goldhamer, D.J. (2009) Progenitors of skeletal muscle satellite cells express the muscle determination gene, MyoD. Dev Biol 332, 131–141.PubMedCrossRefGoogle Scholar
  91. 91.
    Kuang, S., Kuroda, K., Le Grand, F., and Rudnicki, M.A. (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129, 999–1010.PubMedCrossRefGoogle Scholar
  92. 92.
    Schienda, J., Engleka, K.A., Jun, S., Hansen, M.S., Epstein, J.A., Tabin, C.J., Kunkel, L.M., and Kardon, G. (2006) Somitic origin of limb muscle satellite and side population cells. Proc Natl Acad Sci USA 103, 945–950.PubMedCrossRefGoogle Scholar
  93. 93.
    Jinno, H., Morozova, O., Jones, K.L., Biernaskie, J.A., Paris, M., Hosokawa, R., Rudnicki, M.A., Chai, Y., Rossi, F., Marra, M.A., and Miller, F.D. Convergent genesis of an adult neural crest-like dermal stem cell from distinct developmental origins. Stem Cells 28, 2027–2040.Google Scholar
  94. 94.
    Seale, P., Bjork, B., Yang, W., Kajimura, S., Chin, S., Kuang, S., Scime, A., Devarakonda, S., Conroe, H.M., Erdjument-Bromage, H., Tempst, P., Rudnicki, M.A., Beier, D.R., and Spiegelman, B.M. (2008) PRDM16 controls a brown fat/skeletal muscle switch. Nature 454, 961–967.PubMedCrossRefGoogle Scholar
  95. 95.
    Gensch, N., Borchardt, T., Schneider, A., Riethmacher, D., and Braun, T. (2008) Different autonomous myogenic cell populations revealed by ablation of Myf5-expressing cells during mouse embryogenesis. Development 135, 1597–1604.PubMedCrossRefGoogle Scholar
  96. 96.
    Harel, I., Nathan, E., Tirosh-Finkel, L., Zigdon, H., Guimaraes-Camboa, N., Evans, S.M., and Tzahor, E. (2009) Distinct origins and genetic programs of head muscle satellite cells. Dev Cell 16, 822–832.PubMedCrossRefGoogle Scholar
  97. 97.
    Yablonka-Reuveni, Z., and Paterson, B.M. (2001) MyoD and myogenin expression patterns in cultures of fetal and adult chicken myoblasts. J Histochem Cytochem 49, 455–462.PubMedCrossRefGoogle Scholar
  98. 98.
    Kawakami, A., Kimura-Kawakami, M., Nomura, T., and Fujisawa, H. (1997) Distributions of PAX6 and PAX7 proteins suggest their involvement in both early and late phases of chick brain development. Mech Dev 66, 119–130.PubMedCrossRefGoogle Scholar
  99. 99.
    Dias, P., Parham, D.M., Shapiro, D.N., Tapscott, S.J., and Houghton, P.J. (1992) Monoclonal antibodies to the myogenic regulatory protein MyoD1: epitope mapping and diagnostic utility. Cancer Res 52, 6431–6439.PubMedGoogle Scholar
  100. 100.
    Wright, W.E., Binder, M., and Funk, W. (1991) Cyclic amplification and selection of targets (CASTing) for the myogenin consensus binding site. Mol Cell Biol 11, 4104–4110.PubMedGoogle Scholar
  101. 101.
    Wright, W.E., Dac-Korytko, I., and Farmer, K. (1996) Monoclonal antimyogenin antibodies define epitopes outside the bHLH domain where binding interferes with protein-protein and protein-DNA interactions. Dev Genet 19, 131–138.PubMedCrossRefGoogle Scholar
  102. 102.
    Bader, D., Masaki, T., and Fischman, D.A. (1982) Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J Cell Biol 95, 763–770.PubMedCrossRefGoogle Scholar
  103. 103.
    Narahashi, Y., and Yanagita, M. (1967) Studies on proteolytic enzymes (pronase) of Streptomyces griseus K-1. I. Nature and properties of the proteolytic enzyme system. J Biochem 62, 633–641.PubMedGoogle Scholar
  104. 104.
    Narahashi, Y. (1970) Pronase. Methods Enzymol 19, 651–664.CrossRefGoogle Scholar
  105. 105.
    Hartley, R.S., and Yablonka-Reuveni, Z. (1990) Long-term maintenance of primary myogenic cultures on a reconstituted basement membrane. In Vitro Cell Dev Biol 26, 955–961.PubMedCrossRefGoogle Scholar
  106. 106.
    Gilbert, P.M., Havenstrite, K.L., Magnusson, K.E., Sacco, A., Leonardi, N.A., Kraft, P., Nguyen, N.K., Thrun, S., Lutolf, M.P., and Blau, H.M. (2010) Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329, 1078–1081.PubMedCrossRefGoogle Scholar
  107. 107.
    Kleinman, H.K., McGarvey, M.L., Liotta, L.A., Robey, P.G., Tryggvason, K., and Martin, G.R. (1982) Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 21, 6188–6193.PubMedCrossRefGoogle Scholar
  108. 108.
    Greene, E.C. (1963) Anatomy of the rat., Hafner Publishing Company, New York, NY.Google Scholar
  109. 109.
    Hebel, R., and Stromberg, M.W. (1976) Anatomy of the laboratory rat, Williams & Wilkins, Baltimore.Google Scholar
  110. 110.
    Yablonka-Reuveni, Z. (1995) Myogenesis in the chicken: the onset of differentiation of adult myoblasts is influenced by tissue factors. Basic Appl. Myology (BAM) 5, 33–42.Google Scholar
  111. 111.
    O’Neill, M.C., and Stockdale, F.E. (1972) A kinetic analysis of myogenesis in vitro. J Cell Biol 52, 52–65.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Department of Biological Structure, School of MedicineUniversity of WashingtonSeattleUSA

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