Myogenesis – The Early Years

  • Frank E. Stockdale
Part of the Advances in Muscle Research book series (ADMR, volume 3)


Satellite Cell Myosin Heavy Chain Muscle Regeneration Plasma Clot Myogenic Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Abbott J, Holtzer H (1966) The loss of phenotypic traits by differentiated cells. 3. The reversible behavior of chondrocytes in primary cultures. J Cell Biol 28:473–487PubMedCrossRefGoogle Scholar
  2. Bader D, Masaki T, Fischman DA (1982) Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J Cell Biol 95:763–770PubMedCrossRefGoogle Scholar
  3. Bandman E (1985a) Continued expression of neonatal myosin heavy chain in adult dystrophic skeletal muscle. Science 227: 780–782CrossRefGoogle Scholar
  4. Bandman E (1985b) Myosin isoenzyme transitions in muscle development, maturation, and disease. Int Rev Cytol 97:97–131Google Scholar
  5. Bandman E, Matsuda R, Micou-Eastwood J, Strohman R (1981) In vitro translation of RNA from embryonic and from adult chicken pectoralis muscle produces different myosin heavy chains. FEBS Lett 136:301–305PubMedCrossRefGoogle Scholar
  6. Bárány M (1967) ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol Suppl 50:197–218CrossRefGoogle Scholar
  7. Bischoff R (1975) Regeneration of single skeletal muscle fibers in vitro. Anat Rec 182:215–35PubMedCrossRefGoogle Scholar
  8. Blau HM, Hughes SM (1990) Cell lineage in vertebrate development. Curr Opin Cell Biol 2:981–985PubMedCrossRefGoogle Scholar
  9. Carrel A, Burrows M (1911) Cultivation of tissues in vitro and its technique. J Exp Med 13:387–396CrossRefPubMedGoogle Scholar
  10. Clark WE (1946) An experimental study of the regeneration of mammalian striped muscle. J Anat 80:24–36PubMedGoogle Scholar
  11. Coleman JR, Coleman AW (1968) Muscle differentiation and macromolecular synthesis. J Cell Physiol 72:19–34PubMedCrossRefGoogle Scholar
  12. Cooper G, Konigsberg I (1961) Dynamics of myogenesis in vitro. Anat Rec 140:195–205PubMedCrossRefGoogle Scholar
  13. Coons AH, Kaplan MH (1950) Localization of antigen in tissue cells; improvements in a method for the detection of antigen by means of fluorescent antibody. J Exp Med 91:1–13PubMedCrossRefGoogle Scholar
  14. Crow MT, Stockdale FE (1986a) Myosin expression and specialization among the earliest muscle fibers of the developing avian limb. Dev Biol 113:238–254CrossRefGoogle Scholar
  15. Crow MT, Stockdale FE (1986b) The developmental program of fast myosin heavy chain expression in avian skeletal muscles. Dev Biol 118:333–342CrossRefGoogle Scholar
  16. Devoto SH, Melançon E, Eisen JS, Westerfield M (1996) Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122:3371–3380PubMedGoogle Scholar
  17. DiMario JX, Stockdale FE (1997) Both myoblast lineage and innervation determine fiber type and are required for expression of the slow myosin heavy chain 2 gene. Dev Biol 188:167–80PubMedCrossRefGoogle Scholar
  18. Dulbecco R (1952) Production of plagues in monolayer tissue culture by single particles of an animal virus. Proc Nat Acad Sci 38:747–752PubMedCrossRefGoogle Scholar
  19. Düsterhoft S, Yablonka-Reuveni Z, Pette D (1990) Characterization of myosin isoforms in satellite cell cultures from adult rat diaphragm, soleus and tibialis anterior muscles. Differentiation 45:185–191PubMedCrossRefGoogle Scholar
  20. Duxson MJ, Usson Y, Harris AJ (1989) The origin of secondary myotubes in mammalian skeletal muscles: ultrastructural studies. Development 107:743–750PubMedGoogle Scholar
  21. Earle WR, Sanford KK, Evans VJ, Waltz HK, Shannon JE Jr (1951) The influence of inoculum size on proliferation in tissue cultures. J Natl Cancer Inst 12:133–53PubMedGoogle Scholar
  22. Emerson CP Jr, Beckner SK (1975) Activation of myosin synthesis in fusing and mononucleated myoblasts. J Mol Biol 93: 431–447PubMedCrossRefGoogle Scholar
  23. Evans V, Earle W, Sanford KK, Shannon JE, Waltz HK (1951) The preparation and handling of replicate tissue cultures for quantitative studies. J Natl Cancer Inst 11:907–927PubMedGoogle Scholar
  24. Feldman JL, DiMario JX, Stockdale FE (1992) Developmental appearance of adult myoblasts (satellite cells): studies of adult myoblasts in culture and adult myoblast transfer into embryonic avian limbs. In: Limb Development & Regeneration, Part B. (Ed. J.A. Fallon, P.F. Goetinck, R.O. Kelly and D.L. Stocum). John Wiley & Sons, Inc., New York, NY 563–574Google Scholar
  25. Feldman JL, Stockdale FE (1988) Commitment to formation of distinct myotube types in chicken satellite cells. J Cell Bioch 12C:325Google Scholar
  26. Feldman JL, Stockdale FE (1990) Skeletal muscle satellite cell diversity: satellite cells form fibers of different types in cell culture. Dev Biol 143:320–334CrossRefGoogle Scholar
  27. Fell H (1972) Tissue culture and its contribution to biology and medicine. J Exp Biol 57:1–13PubMedGoogle Scholar
  28. Finck H, Holtzer H, Marshall JM, Jr. (1956) An immunochemical study of the distribution of myosin in glycerol extracted muscle. J Biophys Biochem Cytol 2(Suppl 4):175–178PubMedGoogle Scholar
  29. Gey GO (1954) Some aspects of the constitution and behavior of normal and malignant cells maintained in continuous culture. Harvey Lect 50:154–229PubMedGoogle Scholar
  30. Ghosh S, Dhoot GK (1998a) Both avian and mammalian embryonic myoblasts are intrinsically heterogeneous. J Muscle Res Cell Motil 19:787–795CrossRefGoogle Scholar
  31. Ghosh S, Dhoot GK (1998b) Evidence for distinct fast and slow myogenic cell lineages in human foetal skeletal muscle. J Muscle Res Cell Motil 19:431–441CrossRefGoogle Scholar
  32. Gilbert RK, Hazard JB (1965) Regeneration in human skeletal muscle. J Pathol Bacteriol 89:503–512PubMedCrossRefGoogle Scholar
  33. Glick D and Fisher EE (1945) Scientific apparatus and laboratory methods the histochemical localization of adenosinetriphosphatase in plant and animal tissues. Science 102:429–430PubMedCrossRefGoogle Scholar
  34. Gorza L, Sartore S, Triban C, Schiaffino S (1983) Embryonic-like myosin heavy chains in regenerating chicken muscle. Exp Cell Res 143:395–403PubMedCrossRefGoogle Scholar
  35. Grobstein C (1953) Morphogenetic interaction between embryonic mouse tissues separated by a membrane filter. Nature 172:869–870PubMedCrossRefGoogle Scholar
  36. Ham RG (1965) Clonal growth of mammalian cells in a chemically defined, synthetic medium. Proc Natl Acad Sci U S A 53:288–293PubMedCrossRefGoogle Scholar
  37. Harrison R (1907) Observations on the living developing nerve fibre. Proc Soc Exp Biol (N.Y.) 4:140–143Google Scholar
  38. Hauschka SD (1974) Clonal analysis of vertebrate myogenesis: III. Developmental changes in muscle-colony forming cells of the human fetal limb. Dev Biol 37:345–368PubMedCrossRefGoogle Scholar
  39. Hoh JF, Hughes S (1988) Myogenic and neurogenic regulation of myosin gene expression in cat jaw-closing muscles regenerating in fast and slow limb muscle beds. J Muscle Res Cell Motil 9:59–72PubMedCrossRefGoogle Scholar
  40. Hoh JFY, Hughes S (1991) Expression of superfast myosin in aneural regenerates of cat jaw muscle. Muscle Nerve 14:316–325PubMedCrossRefGoogle Scholar
  41. Hoh JFY, McGrath PA, White RI (1976) Electrophoretic analysis of multiple forms of myosin in fast-twitch and slow-twitch muscles of the chick. Biochem J 157:87–95PubMedGoogle Scholar
  42. Holtfreter J (1943) Properties and functions of the surface coat in amphibian embryos. J Exp Zool 93:251–323CrossRefGoogle Scholar
  43. Holtzer H, Abbott J, Lash J, Holtzer S (1960) The loss of phenotypic traits by differentiated cells in Vitro, I. Dedifferentiation of Cartilage Cells. Proc Natl Acad Sci U S A 46:1533–1542PubMedCrossRefGoogle Scholar
  44. Holtzer H, Marshall JM, Finck H (1957) An analysis of myogenesis by the use of fluorescent antimyosin. J Biophysic Biochem Cytol 3:705–729CrossRefGoogle Scholar
  45. Kalhovde JM, Jerkovic R, Sefland I, Cordonnier C, Calabria E, Schiaffino S, Lomo T (2005) “Fast” and “slow” muscle fibres in hindlimb muscles of adult rats regenerate from intrinsically different satellite cells. J Physiol 562:847–57PubMedCrossRefGoogle Scholar
  46. Kirby E (1892) Experimentelle Untersuchungen uber die Regeneration des quergestreiftem Muskelgewebes. Beit zur Pathol Anat und Allegem Pathol 11:302–119Google Scholar
  47. Konigsberg IR (1963) Clonal analysis of myogenesis. Science 140:1273–1284PubMedCrossRefGoogle Scholar
  48. Konigsberg IR, McElvain N, Tootle M, Herrmann H (1960) The dissociability of deoxyribonucleic acid synthesis from the development of multinuclearity of muscle cells in culture. J Biophys Biochem Cytolo 8:333–343Google Scholar
  49. Konigsberg U, Lipton H, Konigsberg IR (1975) The regenerative response of single mature muscle fibers isolated in vitro. Dev Biol 45:260–275PubMedCrossRefGoogle Scholar
  50. Lash J, Holtzer H, Swift H (1957) Regeneration of mature skeletal muscle. Anat Rec 128:679–697PubMedCrossRefGoogle Scholar
  51. Lewis W, Lewis M. (1917) Behavior of cross striated muscle in tissue cultures. Amer J Anat 22:169–194CrossRefGoogle Scholar
  52. Locke FS (1895) Towards the ideal artificial circulating fluid for the isolated frog’s heart: preliminary communication. J Physiol 5: 332–333Google Scholar
  53. Marshall JM (1951) Localization of adrenocorticotropic hormone by histochemical and immunochemical methods. J Exp Med 94:21–30PubMedCrossRefGoogle Scholar
  54. Matsuda R, Spector DH, Strohman RC (1983) Regenerating adult chicken skeletal muscle and satellite cell cultures express embryonic patterns of myosin and tropomysin isoforms. Dev Biol 100:478–488PubMedCrossRefGoogle Scholar
  55. Mauro A (1961) Satellite cell of skeletal muscle. J Biophys Biochem Cytolo 9:493–495Google Scholar
  56. Miller JB, Crow MT, Stockdale FE (1985) Slow and fast myosin heavy chain content defines three types of myotubes in early muscle cell cultures. J Cell Biol 101:1643–1650PubMedCrossRefGoogle Scholar
  57. Miller JB, Stockdale FE. (1986a) Developmental origins of skeletal muscle fibers: clonal analysis of myogenic cell lineages based on expression of fast and slow myosin heavy chains. Proc Natl Acad Sci U S A 83:3860–3864CrossRefGoogle Scholar
  58. Miller JB, Stockdale FE (1986b) Developmental regulation of the multiple myogenic cell lineages of the avian embryo. J Cell Biol 103:2197–2208CrossRefGoogle Scholar
  59. Mintz B, Baker WW (1967) Normal mammalian muscle differentiation and gene control of isocitrate dehydrogenase synthesis. Proc Natl Acad Sci U S A 58:592–598PubMedCrossRefGoogle Scholar
  60. Moscona A (1951) Tissues from dissociated cells. Exp Cell Res 3:535–539CrossRefGoogle Scholar
  61. Nadal-Ginard B (1979) Most myosin heavy chain mRNA in L6E9 rat myotubes has a short poly (A) tail. Proc Natl Acad Sci U S A 76:1853–1857PubMedCrossRefGoogle Scholar
  62. Partridge TA, Grounds M, Sloper JC (1978) Evidence of fusion between host and donor myoblasts in skeletal muscle grafts. Nature 273:306–308PubMedCrossRefGoogle Scholar
  63. Paterson B, Strohman RC (1970) Myosin structure as revealed by simultaneous electrophoresis of heavy and light subunits. Biochemistry 9:4094–4105PubMedCrossRefGoogle Scholar
  64. Paterson B, Strohman RC (1972) Myosin synthesis in cultures of differentiating chicken embryo skeletal muscle. Dev Biol 29:113–138PubMedCrossRefGoogle Scholar
  65. Perry SV, Chappell JB (1957) The action of 2:4-dinitrophenol on myosin and mitochondrial adenosine triphosphatase systems. Biochem J 65:469–476PubMedGoogle Scholar
  66. Pin CL, Hrycyshyn AW, Rogers KA, Rushlow WJ, Merrifield PA (2002) Embryonic and fetal rat myoblasts form different muscle fiber types in an ectopic in vivo environment. Dev Dyn 224:253–266PubMedCrossRefGoogle Scholar
  67. Pin CL, Merrifield PA (1993) Embryonic and fetal rat myoblasts express different phenotypes following differentiation in vitro. Dev Genet 14:356–368PubMedCrossRefGoogle Scholar
  68. Puck T, Marcus P (1955) A rapid method for viable cell titration and clone production with HELA cells in tissue culture: The use of X-irradiated cells to supply conditioning factors. Proc Natl Acad Sci U S A 41:432–437PubMedCrossRefGoogle Scholar
  69. Puck TT, Marcus PI, Cieciura SJ (1956) Clonal growth of mammalian cells in vitro; growth characteristics of colonies from single HeLa cells with and without a feeder layer. J Exp Med 103:273–283PubMedCrossRefGoogle Scholar
  70. Ringer S (1882) Regarding the action of hydrate of soda, hydrate of ammonia, and hydrate of potash on the ventricle of the Frog’s Heart. J Physiol 3:195–202PubMedGoogle Scholar
  71. Rosenblatt J, Parry D, Partridge T (1996) Phenotype of adult mouse muscle myoblasts reflects their fiber type of origin. Differentiation 60:39–45PubMedCrossRefGoogle Scholar
  72. Rous P, Jones FS (1916) A method for obtaining suspensions of living cells from the fixed tissues, and for the plating out of individual cells. J Exp Med 23: 549–555CrossRefPubMedGoogle Scholar
  73. Rubinstein NA, Kelley AM (1978) Myogenic and neurogenic contributions to the development of fast and slow twitch muscles in rat. Dev Biol 62:473–485PubMedCrossRefGoogle Scholar
  74. Rushbrook JI, Stracher A (1979) Comparison of adult, embryonic, and dystrophic myosin heavy chains form chicken muscle by sodium dodecyl sulfate/polyacrylamide gel electrophoresis and peptide mapping. Proc Natl Acad Sci U S A 76:4331–4334PubMedCrossRefGoogle Scholar
  75. Sacks L, Cann G, Nikovits W, Conlon S, Espinoza N, Stockdale F (2003) Regulation of myosin expression during myotome formation. Development 130:3391–3402PubMedCrossRefGoogle Scholar
  76. Sanford K, Earle W, Likely G (1948) The growth in vitro of single Tissue cells. J Natl Cancer Inst 9:229–246PubMedGoogle Scholar
  77. Sartore S, Gorza L, Schiaffino S (1982) Fetal myosin heavy chains in regenerating muscle. Nature 298:294–296PubMedCrossRefGoogle Scholar
  78. Saunders JH, Sissons HA (1953) The effect of denervation on the regeneration of skeletal muscle after injury. J Bone Joint Surg Br 35-B:113–24Google Scholar
  79. Schiff J (2002) Old Yale – An Unsung Hero of Medical Research. Yale Alumni Magazine Vol. 64, FebruaryGoogle Scholar
  80. Schwann T (1839) Mikroskopische Untersuchungen über die Übereinstimmung in der Struktur und dem Wachsthum der Thiere und Pflanzen. Berlin: Verlag der Sander’schen Buchhandlung Google Scholar
  81. Shainberg A, Yagil G, Yaffe D (1971) Alterations of enzymatic activities during muscle differentiation in vitro. Dev Biol 25:1–29PubMedCrossRefGoogle Scholar
  82. Snow MH (1978) An autoradiographic study of satellite cell differentiation into regenerating myotubes following transplantation of muscles in young rats. Cell Tissue Res 186:535–540PubMedCrossRefGoogle Scholar
  83. Stockdale FE, Holtzer H (1961) DNA synthesis and myogenesis. Exp Cell Res 24:508–520PubMedCrossRefGoogle Scholar
  84. Stockdale FE, Miller JB (1987) The cellular basis of myosin heavy chain isoform expression during development of avian skeletal muscles. Dev Biol 123:1–9PubMedCrossRefGoogle Scholar
  85. Stockdale FE, O’Neill MC (1972) DNA synthesis, mitosis, and skeletal muscle differentiation. In Vitro 8:212–227PubMedCrossRefGoogle Scholar
  86. Strangeways T, Fell H (1926) Experimental studies on the differentiation of embryonic tissues growing in vivo and in vitro. Proc Royal Soc, London 99:340–366Google Scholar
  87. Taylor JH (1953) Intracellular localization of labeled nucleic acid determined with autoradiography. Science 118:555–557PubMedCrossRefGoogle Scholar
  88. Taylor J, Woods P, Hughes W (1957) The organization and duplication of chromosomes as revealed by autoradiographic studies using tritium-labeled thymidine. Proc Natl Acad Sci U S A 43:122–128PubMedCrossRefGoogle Scholar
  89. Waldeyer W (1865) Über die Veränderungen der quergestreiften Muskeln bei der Entzündung und dem Typhus – Prozess, sowie über die Regeneration derselben nach Substanzdefecten. Vircheress Arch path Anat Physiol 34:473–514CrossRefGoogle Scholar
  90. Whalen RG, Schwartz K, Bouveret P, Sell SM, Gros F (1979) Contractile protein synthesis in muscle development: Identification of an embryonic form of myosin heavy chain. Proc Natl Acad Sci U S A 76:5197–5201PubMedCrossRefGoogle Scholar
  91. Whalen RG, Sell SM, Butler-Browne GS, Schwartz K, Bouveret P, Pinset-Harstrom I (1981) Three myosin heavy-chain isozymes appear sequentially in rat muscle development. Nature 292:805–809PubMedCrossRefGoogle Scholar
  92. White NK, Bonner PH, Nelson DR, Hauschka SD (1975) Clonal analysis of vertebrate myogenesis. IV. Medium-dependent classification of colony-forming cells. Dev Biol 44:346–361PubMedCrossRefGoogle Scholar
  93. White NK, Hauschka SD (1971) Muscle development in vitro: A new conditioned medium effect on colony differentiation. Exp Cell Res 67:479–482PubMedCrossRefGoogle Scholar
  94. Yaffe D (1968) Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc Natl Acad Sci U S A 61:477–483PubMedCrossRefGoogle Scholar
  95. Yaffe D (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270:725–727PubMedCrossRefGoogle Scholar
  96. Zwilling E (1954) Dissociation of chick embryo cells by means of a chelating compound. Science 120:219Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Frank E. Stockdale
    • 1
  1. 1.Maureen Lyles D’Ambrogio Professor of MedicineEmeritus

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