Skip to main content

IGFs and Skeletal Muscle

  • Chapter
Book cover The IGF System

Part of the book series: Contemporary Endocrinology ((COE,volume 17))

Abstract

The insulin-like growth factors (IGFs) are unique in that they are the only known mitogens that, when free of other serum components, stimulate both the proliferation and differentiation of skeletal muscle cells. This dual effect of IGFs is of particular interest because these two processes are believed to be mutually exclusive in this tissue and in a wide variety of cell types (1). Thus, exploring this model of IGF action in skeletal muscle provides an opportunity to address a fundamental issue in cell biology: understanding the mechanisms that influence the decision of a particular cell type to proliferate or differentiate. The focus of this chapter is on the interface of IGF biology with that of skeletal muscle embryogenesis/differentiation and cell cycle regulation, with particular emphasis on exploring the mechanisms by which IGFs influence the decision of skeletal muscle cells to proliferate or differentiate.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Olson EN. Interplay between proliferation and differentiation within the myogenic lineage. Dev Biol 1992; 154: 261–272.

    Article  PubMed  CAS  Google Scholar 

  2. Buckingham M. Molecular biology of muscle development. Cell 1994; 78: 15–21.

    Article  PubMed  CAS  Google Scholar 

  3. Lassar A, Münsterberg AE. Wiring diagrams: regulatory circuits and the control of skeletal myogenesis. Curr Opin Cell Biol 1994; 6: 432–442.

    Article  PubMed  CAS  Google Scholar 

  4. Lassar A, Münsterberg AE. The role of positive and negative signals in somite patterning. Curr Opin Neurobiol 1996; 6: 57–63.

    Article  PubMed  CAS  Google Scholar 

  5. Molkentin JD, Olson EN. Defining the regulatory networks for muscle development. Curr Opin Genet Dev 1996; 6: 445–453.

    Article  PubMed  CAS  Google Scholar 

  6. Olson EN, Klein WH. bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev 1994; 8: 1–8.

    Article  PubMed  CAS  Google Scholar 

  7. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 1990; 61: 49–59.

    Article  PubMed  CAS  Google Scholar 

  8. Jen Y, Weintraub H, Benezra R. Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of Id with E2A proteins. Genes Dev 1992; 6: 1466–1479.

    Article  PubMed  CAS  Google Scholar 

  9. Rudnicki MA, Schneglesberg PNJ, Stead RH, Braun T, Arnold H-H, Jaenisch R. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 1993; 75: 1351–1359.

    Article  PubMed  CAS  Google Scholar 

  10. Hasty P, Bradley A, Morris JH, Edmondson DG, Venuti JM, Olson EN, Klein WH. Muscle deficiency and neonatal death in mice with a targeted mutation in myogenin gene. Nature 1993; 364: 501–506.

    Article  PubMed  CAS  Google Scholar 

  11. Nabeshima Y, Hanaoka K, Hayasaka M, Esumi E, Li S, Nonaka I, Nabeshima Y. Moygenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 1993; 364: 532–535.

    Article  PubMed  CAS  Google Scholar 

  12. Olson EN, Arnold H-H, Rigby PWJ, Wold BJ. Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell 1996; 85: 1–4.

    Article  PubMed  CAS  Google Scholar 

  13. Rhodes SJ, Konieczny SF. Identification of MRF4: A new member of the muscle regulatory factor gene family. Genes Dev 1989; 3: 2050–2061.

    Article  PubMed  CAS  Google Scholar 

  14. Tajbakhsh S, Rocancourt D, Cossu G, Buckingham M. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 1997; 89: 127–138.

    Article  PubMed  CAS  Google Scholar 

  15. Maroto M, Reshef R, Münsterberg AE, Koester S, Goulding M, Lassar AB. Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell 1997; 89: 139–148.

    Article  PubMed  CAS  Google Scholar 

  16. Rawls A, Olson EN. MyoD meets its maker. Cell 1997; 89: 5–8.

    Article  PubMed  CAS  Google Scholar 

  17. Molkentin JD, Black BL, Martin JF, Olson EN. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 1995; 83: 1125–1136.

    Article  PubMed  CAS  Google Scholar 

  18. Molkentin JD, Olson EN. Combinatorial control of muscle development by basic helix-loop-helix and MADS-box transcription factors. Proc Natl Acad Sci USA 1996; 93: 9366–9373.

    Article  PubMed  CAS  Google Scholar 

  19. Gu W, Schneider JW, Condorelli G, Kaushal S, Mandavi V, Nadal-Ginard B. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell 1993; 72: 309–324.

    Article  PubMed  CAS  Google Scholar 

  20. Chen PL, Scully P, Shew JY, Wang JY, Lee WH. Phosphorylation of the retinoblastoma gene product is modulated during the cell cycle and cellular differentiation. Cell 1989; 58: 1193–1198.

    Article  PubMed  CAS  Google Scholar 

  21. Laiho M, DeCaprio JA, Ludlow JW, Livingston DM, Massague J. Growth inhibition by TGF-beta linked to suppression of retinoblastoma protein phosphorylation. Cell 1990; 62: 175–185.

    Article  PubMed  CAS  Google Scholar 

  22. Sherr CJ. Cl phase progression: cycling on cue. Cell 1994; 79: 551–555.

    Article  PubMed  CAS  Google Scholar 

  23. Matsushime H, Ewen ME, Strom DK, Kato J-Y, Hanks SK, Roussel MF, Sherr CJ. Identification and properties of an atypical catalytic subunit (p34PSK-J3/cdk4) for mammalian D type G1 cyclins. Cell 1992; 71: 323–334.

    Article  PubMed  CAS  Google Scholar 

  24. Kato J-Y, Matsushime H, Hiebert SW, Ewen ME, Sherr CJ. Direct binding of cyclin D to the retino-blastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4. Genes Dev 1993; 7: 331–342.

    Article  PubMed  CAS  Google Scholar 

  25. Matsushime H, Quelle DE, Shurtleff SA, Shibuya M, Shen CJ, Kato J-Y. D-type cyclin-dependent kinase activity in mammalian cells. Mol Cell Biol 1994; 14: 2066–2076.

    PubMed  CAS  Google Scholar 

  26. Fisher RP, Morgan DO. A novel cyclin associates with MO15/CDK7 to form the CDK-activating kinase. Cell 1994; 78: 713–724.

    Article  PubMed  CAS  Google Scholar 

  27. Matsuoka M, Kato J-Y, Fisher RP, Morgan DO, Sherr CJ. Activation of cyclin-dependent kinase 4 (cdk4) by mouse MO15-associated kinase. Mol Cell Biol 1994; 14: 7265–7275.

    PubMed  CAS  Google Scholar 

  28. Fisher RP, En P, Chamberlin HM, Morgan DO. Alternative mechanisms of CAK assembly require an assembly factor or an activating kinase. Cell 1995; 83: 47–57.

    Article  PubMed  CAS  Google Scholar 

  29. Quelle DE, Ashmun RA, Hannon GJ, Rehberger PA, Trono D, Richter KH, Walker C, Beach D, Sherr CJ, Serrano M. Cloning and characterization of murine p 16INK4A and p 1 5INK4B genes. Oncogene 1995; 11: 635–645.

    PubMed  CAS  Google Scholar 

  30. Hirai H, Roussel MF, Kato J-Y, Ashmun RA, Sherr CJ. Novel INK4 proteins, p19 and p18, are specific inhibitors of the cyclin D-dependent kinases CDK4 and CDK6. Mol Cell Biol 1995; 15: 2672–2681.

    PubMed  CAS  Google Scholar 

  31. Xiong Y, Hannon GJ, Zhang H, Casso D, Kobayashi R, Beach D. p21 is a universal inhibitor of cyclin kinases. Nature 1993; 366: 701–704.

    Article  PubMed  CAS  Google Scholar 

  32. Polyak K, Lee M-H, Erdjument-Bromage H, Koff A, Roberts JM, Tempst P, Massaque J. Cloning of P27K`P1 a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 1994; 78: 59–66.

    Article  PubMed  CAS  Google Scholar 

  33. Lee M-H, Reynisdottir I, Massague J. Cloning of p57MP2, a cyclin-dependent kinase inhibitor with unique domain structure and tissue distribution. Genes Dev 1995; 9: 639–649.

    Article  PubMed  CAS  Google Scholar 

  34. Sherr CJ, Roberts JM. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 1995; 9: 1149–1163.

    Article  PubMed  CAS  Google Scholar 

  35. Franklin DS, Xiong Y. Induction of pl8INK4c and its predominant association with CDK4 and CDK6 during myogenic differentiation. Mol Biol Cell 1996; 7: 1587–1599.

    PubMed  CAS  Google Scholar 

  36. Halevy O, Novitch BG, Spicer DB, Skapek SX, Rhee J, Hannon GJ, Beach D, Lassar AB. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science 1995; 267: 1018–1021.

    Article  PubMed  CAS  Google Scholar 

  37. Guo K, Wang J, Andres V, Smith RC, Walsh K. MyoD-induced expression of p21 inhibits cyclindependent kinase activity upon myocyte terminal differentiation. Mol Cell Biol 1995; 15: 3823–3829.

    PubMed  CAS  Google Scholar 

  38. Stylianopoulou F, Efstratiadis A, Herbert J, Pintar J. Pattern of the insulin-like growth factor II gene expression during rat embryogenesis. Dev Biol 1988; 103: 497–506.

    CAS  Google Scholar 

  39. Bondy CA, Werner H, Roberts CT Jr, LeRoith D. Cellular pattern of insulin-like growth factor-I (IGFI) and type I IGF receptor gene expression in early organogenesis: comparison with IGF-II gene expression. Mol Endocrinol 1990; 4: 1386–1398.

    Article  PubMed  CAS  Google Scholar 

  40. Hill DJ, Crace CJ, Nissley SP, Morrell D, Holder AT, Milner RDG. Fetal rat myoblasts release both rat somatomedin-C (SM-C)/insulin-like growth factor I (IGF I) and multiplication-stimulating activity in vitro: partial characterization and biological activity of myoblast-derived SM-C/IGF I. Endocrinology 1985; 117: 2061–2072.

    Article  PubMed  CAS  Google Scholar 

  41. Brown AL, Graham DE,. Nissley SP, Hill DJ, Strain AJ, Rechler MM. Developmental regulation of insulin-like growth factor II mRNA in different rat tissues. J Biol Chem 1986; 261: 13144–13150.

    PubMed  CAS  Google Scholar 

  42. Murphy LJ, Bell GI, Friesen HG. Tissue distribution of insulin-like growth factor I and II messenger ribonucleic acid in the adult rat. Endocrinology 1987; 120: 1279–1282.

    Article  PubMed  CAS  Google Scholar 

  43. Rosen KM, Wentworth BM, Rosenthal N, Villa-Komaroff L. Specific, temporally regulated expression of the insulin-like growth factor II gene during muscle cell differentiation. Endocrinology 1993; 133: 474–481.

    Article  PubMed  CAS  Google Scholar 

  44. Yaffe D, Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 1977; 270: 725–727.

    Article  PubMed  CAS  Google Scholar 

  45. Yaffe D. Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc Natl Acad Sci USA 1968; 61: 477–483.

    Article  PubMed  CAS  Google Scholar 

  46. Schubert D, Harris AJ, Devine CE, Heinemann S. Characterization of a unique muscle cell line. J Cell Biol 1974; 61: 398–413.

    Article  PubMed  CAS  Google Scholar 

  47. Mulle C, Benoit P, Pinset C, Roa M, Changeux JP. Calcitonin gene-related peptide enhances the rate of desensitization of the nicotinic acetylcholine receptor in cultured mouse muscle cells. Proc Natl Acad Sci USA 1988; 85: 5728–5732.

    Article  PubMed  CAS  Google Scholar 

  48. Tollefsen SE, Sadow JL, Rotwein P. Coordinate expression of insulin-like growth factor II and its receptor during muscle differentiation. Proc Natl Acad Sci USA 1989; 86: 1543–1547.

    Article  PubMed  CAS  Google Scholar 

  49. Rosenthal SM, Brunetti A, Brown EJ, Mamula PW, Goldfine ID. Regulation of insulin-like growth factor (IGF) I receptor expression during muscle cell differentiation. J Clin Invest 1991; 87: 1212–1219.

    Article  PubMed  CAS  Google Scholar 

  50. Florini JR, Magri KA, Ewton DZ, James PL, Grindstaff K, Rotwein PS. “Spontaneous” differentiation of skeletal myoblasts is dependent upon autocrine secretion of insulin-like growth factor-II. J Biol Chem 1991; 266: 15917–15923.

    PubMed  CAS  Google Scholar 

  51. Kou K, Rotwein P. Transcriptional activation of the insulin-like growth factor-II gene during myoblast differentiation. Mol Endocrinol 1993; 7: 291–302.

    Article  PubMed  CAS  Google Scholar 

  52. Magri KA, Benedict MR, Ewton DZ, Florini JR. Negative feedback regulation of insulin-like growth factor-II gene expression in differentiating myoblasts in vitro. Endocrinology 1994; 135: 53–62.

    Article  PubMed  CAS  Google Scholar 

  53. Rosenthal SM, Brown EJ, Brunetti A, Goldfine ID. Fibroblast growth factor inhibits insulin-like growth factor-II (IGF-II) gene expression and increases IGF-I receptor abundance in BC3H-1 muscle cells. Mol Endocrinol 1991; 5: 678–684.

    Article  PubMed  CAS  Google Scholar 

  54. Tollefsen SW, Lajara R, McCusker RH, Clemmons DR, Rotwein P. Insulin-like growth factors (IGF) in muscle development. Expression of IGF-I, the IGF-I receptor, and an IGF binding protein during myoblast differentiation. J Biol Chem 1989; 264: 13810–13817.

    PubMed  CAS  Google Scholar 

  55. Jennische E, Skottner A, Hansson H-A. Satellite cells express the trophic factor IGF-I in regenerating skeletal muscle. Acta Physiol Scand 1987; 129: 9–15.

    Article  PubMed  CAS  Google Scholar 

  56. Edwall D, Schalling M, Jennische E, Norstedt G. Induction of insulin-like growth factor I messenger ribonucleic acid during regeneration of rat skeletal muscle. Endocrinology 1989; 124: 820–825.

    Article  PubMed  CAS  Google Scholar 

  57. Marsh DR, Criswell DS, Hamilton MT, Booth FW. Association of insulin-like growth factor mRNA expressions with muscle regeneration in young, adult, and old rats. Am J Physiol 1997; 273 (Regul Integrat Comp Physiol 42): R353 - R358.

    PubMed  CAS  Google Scholar 

  58. Ishii DN. Relationship of insulin-like growth factor II gene expression in muscle to synaptogenesis. Proc Natl Acad Sci USA 1989; 86: 2898–2902.

    Article  PubMed  CAS  Google Scholar 

  59. Turner JD, Rotwein P, Novakofski J, Bechtel PJ. Induction of mRNA for IGF-I and -II during growth hormone-stimulated muscle hypertrophy. Am J Physio11988; 255 (Endocrinol Metab 18 ): E513 - E517.

    Google Scholar 

  60. Alexandrides T, Moses AC, Smith RJ. Developmental expression of receptors for insulin, insulin-like growth factor I (IGF-I), and IGF-II in rat skeletal muscle. Endocrinology 1989; 124: 1064–1076.

    Article  PubMed  CAS  Google Scholar 

  61. Shimizu M, Webster C, Morgan DO, Blau HM, Roth RA. Insulin and insulinlike growth factor receptors and responses in cultured human muscle cells. Am J Physiol 1986; 251 (Endocrinol Metab 14): E611 - E615.

    PubMed  CAS  Google Scholar 

  62. Beguinot F, Kahn CR, Moses AC, Smith RJ. Distinct biologically active receptors for insulin, insulin-like growth factor I, and insulin-like growth factor II in cultured skeletal muscle cells. J Biol Chem 1985; 260: 15892–15898.

    PubMed  CAS  Google Scholar 

  63. Alexandrides TK, Smith RJ. A novel fetal insulin-growth factor (IGF) I receptor. J Biol Chem 1989; 264: 12922–12930.

    PubMed  CAS  Google Scholar 

  64. Barenton B, Domeyne A, Garandel V, Garofalo RS. A developmentally regulated form of insulin-like growth factor receptor (3-subunit in C2 myoblasts exhibiting altered requirements for differentiation. Endocrinology 1993; 133: 651–660.

    Article  PubMed  CAS  Google Scholar 

  65. Domeyne A, Pinset C, Montarras D, Garandel V, Rosenfeld RG, Barenton B. Preferential binding of insulin-like growth factor-II (IGF-II) to a putative a2ß2 IGF-II receptor type in C2 myoblasts. Eur J Biochem 1992; 208: 273–279.

    Article  PubMed  CAS  Google Scholar 

  66. Yee D, Lebovic GS, Marcus RR, Rosen N. Identification of an alternate type-I insulin-like growth factor receptor (3 subunit mRNA transcript. J Biol Chem 1989; 264: 21439–21441.

    PubMed  CAS  Google Scholar 

  67. Abbott AM, Bueno R, Pedrini MT, Murray JM, Smith RJ. Insulin-like growth factor I receptor gene structure. J Biol Chem 1992; 267: 10759–10763.

    PubMed  CAS  Google Scholar 

  68. Bailyes EM, Navé BT, Soos MA, On SR, Hayward AC, Siddle K. Insulin receptor/IGF-I receptor hybrids are widely distributed in mammalian tissues: quantification of individual receptor species by selective immunoprecipitation and immunoblotting. Biochem J 1997; 327: 209–215.

    PubMed  CAS  Google Scholar 

  69. Brunetti A, Maddux BA, Wong KY, Goldfine ID. Muscle cell differentiation is associated with increased insulin receptor biosynthesis and messenger RNA levels. J Clin Invest 1989; 83: 192–198.

    Article  PubMed  CAS  Google Scholar 

  70. Rosenthal SM, Brown EJ. Mechanisms of insulin-like growth factor (IGF)-II-induced IGF-I receptor down-regulation in BC3H-1 muscle cells. J Endocrinol 1994; 141: 69–74.

    Article  PubMed  CAS  Google Scholar 

  71. De Vroede MA, Romanus JA, Standaert ML, Pollet RJ, Nissley SP, Rechler MM. Interaction of insulin-like growth factors with a nonfusing mouse muscle cell line: binding, action, and receptor down-regulation. Endocrinology 1984; 114: 1917–1929.

    Article  PubMed  Google Scholar 

  72. Hernandez-Sanchez C, Werner H, Roberts CT Jr, Woo EJ, Hum DW, Rosenthal SM, LeRoith D. Differential regulation of insulin-like growth factor-I (IGF-I) receptor gene expression by IGF-I and basic fibroblastic growth factor. J Biol Chem 1997; 272: 4663–4670.

    Article  PubMed  CAS  Google Scholar 

  73. McCusker RH, Clemmons DR. Insulin-like growth factor binding protein secretion by muscle cells: effect of cellular differentiation and proliferation. J Cell Physiol 1988; 137: 505–512.

    Article  PubMed  CAS  Google Scholar 

  74. McCusker RH, Camacho-Huber C, Clemmons DR. Identification of the types of insulin-like growth factor-binding proteins that are secreted by muscle cell in vitro. J Biol Chem 1989; 264: 7795–7800.

    PubMed  CAS  Google Scholar 

  75. Ernst CW, McCusker RH, White ME. Gene expression and secretion of insulin-like growth factor-binding proteins during myoblast differentiation. Endocrinology 1992; 130: 607–615.

    Article  PubMed  CAS  Google Scholar 

  76. James PL, Jones SB, Busby WH Jr, Clemmons DR, Rotwein P. A highly conserved insulin-like growth factor-binding protein (IGFBP-5) is expressed during myoblast differentiation. J Biol Chem 1993; 268: 22305–22312.

    PubMed  CAS  Google Scholar 

  77. Delhanty PJD, Hill DJ, Shimasaki S, Han VKM. IGFBP-4, -5 and -6 mRNAs in the human fetus: localization to sits of growth and differentiation? Growth Regul 1993; 3: 8–11.

    PubMed  CAS  Google Scholar 

  78. McCusker RH, Clemmons DR. Effects of cytokines on insulin-like growth factor-binding protein secretion by muscle cells in vitro. Endocrinology 1994; 134: 2095–2102.

    Article  PubMed  CAS  Google Scholar 

  79. Rotwein P, James PL, Kou K. Rapid activation of insulin-like growth factor-binding protein-5 gene transcription during myoblast differentiation. Mol Endocrinol 1995; 9: 913–923.

    Article  PubMed  CAS  Google Scholar 

  80. Silverman LA, Cheng Z-Q, Hsiao D, Rosenthal SM. Skeletal muscle cell-derived insulin-like growth factor (IGF) binding proteins inhibit IGF-I induced myogenesis in rat L6E9 cells. Endocrinology 1995; 136: 720–726.

    Article  PubMed  CAS  Google Scholar 

  81. Ewton DZ, Florini JR. IGF binding proteins-4, -5 and -6 may play specialized roles during L6 myoblast proliferation and differentiation. J Endocrinol 1995; 144: 539–553.

    Article  PubMed  CAS  Google Scholar 

  82. Ernst CW, McFarland DC, White ME. Expression of insulin-like growth factor II (IGF-II), IGF binding protein-2 and myogenin during differentiation of myogenic satellite cells derived from the turkey. Differentiation 1996; 61: 25–33.

    Article  PubMed  CAS  Google Scholar 

  83. Damon SE, Haugk KL, Birnbaum RS, Quinn LS. Retrovirally mediated overexpression of insulin-like growth factor binding protein 4: evidence that insulin-like growth factor is required for skeletal muscle differentiation. J Cell Physiol. 1998; 175: 109–120.

    Article  PubMed  CAS  Google Scholar 

  84. Heino J, Massague J. Cell adhesion to collagen and decreased myogenic gene expression implicated in the control of myogenesis by transforming growth factor beta. J Biol Chem 1990; 265: 10181–10184.

    PubMed  CAS  Google Scholar 

  85. Rosen GD, Sanes JR, LaChance R, Cunningham JM, Roman J, Dean DC. Roles for the integrin VLA-4 and its counter receptor VCAM-1 in myogenesis. Cell 1990; 69: 1107–1119.

    Article  Google Scholar 

  86. Florini JR, Ewton DZ, Magri KA. Hormones, growth factors, and myogenic differentiation. Annu Rev Physiol 1991; 53: 201–216.

    Article  PubMed  CAS  Google Scholar 

  87. Ewton DZ, Roof SL, Magri KA, McWade FJ, Florini JR. IGF-II is more active than IGF-I in stimulating L6A1 myogenesis: greater mitogenic actions of IGF-I delay differentiation. J Cell Physiol 1994; 16: 277–284.

    Article  Google Scholar 

  88. Rosenthal SM, Cheng Z-Q. Opposing early and late effects of insulin-like growth factor I on differentiation and the cell cycle regulatory retinoblastoma protein in skeletal myoblasts. Proc Natl Acad Sci USA 1995; 92: 10307–10311.

    Article  PubMed  CAS  Google Scholar 

  89. Engert JC, Berglund EB, Rosenthal N. Proliferation precedes differentiation in IGF-I-stimulated myogenesis. J Cell Biol 1996; 135: 431–440.

    Article  PubMed  CAS  Google Scholar 

  90. Stewart CEH, Rotwein P. Insulin-like growth factor-II is autocrine survival factor for differentiating myoblasts. J Biol Chem 1996; 271: 11330–11338.

    Article  PubMed  CAS  Google Scholar 

  91. Florini JR, Nicholson ML, Dulak NC. Effects of peptide anabolic hormones on growth of myoblasts in culture. Endocrinology 1977; 101: 32–41.

    Article  PubMed  CAS  Google Scholar 

  92. Ewton DZ, Florini JR. Relative effects of the somatomedins, multiplication-stimulating activity, and growth hormone on myoblasts and myotubes in culture. Endocrinology 1980; 106: 577–583.

    Article  PubMed  CAS  Google Scholar 

  93. Ewton DZ, Florini JR. Effects of the somatomedins and insulin on myoblast differentiation in vitro. Dev Biol 1981; 86: 31–39.

    Article  PubMed  CAS  Google Scholar 

  94. Turo KA, Florini JR. Hormonal stimulation of myoblast differentiation in the absence of DNA synthesis. Am J Physiol 1982; 243 (Cell Physiol 12): C278 - C284.

    PubMed  CAS  Google Scholar 

  95. Schmid C, Steiner T, Froesch ER. Preferential enhancement of myoblast differentiation by insulin-like growth factors (IGF I and IGF II) in primary cultures of chicken embryonic cells. FEBS Lett 1983; 161: 117–121.

    Article  PubMed  CAS  Google Scholar 

  96. Dodson MV, Allen RE, Hossner KL. Ovine somatomedin, multiplication-stimulating activity, and insulin promote skeletal muscle satellite cell proliferation in vitro. Endocrinology 1985; 117: 2357–2363.

    Article  PubMed  CAS  Google Scholar 

  97. Allen RE, Boxhorn LK. Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. J Cell Physiol 1989; 138: 311–315.

    Article  PubMed  CAS  Google Scholar 

  98. Florini JR, Ewton DZ, Roof SL. Insulin-like growth factor-I stimulates terminal myogenic differentiation by induction of myogenin gene expression. Mol Endocrinol 1991; 5: 718–724.

    Article  PubMed  CAS  Google Scholar 

  99. Brown EJ, Hsiao D, Rosenthal SM. Induction and peak gene expression of insulin-like growth factor II follow that of myogenin during differentiation of BC3H-1 muscle cells. Biochem Biophys Res Commun 1992; 183: 1084–1089.

    Article  PubMed  CAS  Google Scholar 

  100. Milasincic DJ, Dhawan J, Fanner SR. Anchorage-dependent control of muscle-specific gene expression in C2C12 mouse myoblasts. In Vitro Cell Dev Biol Anim 1996; 32: 90–99.

    Article  PubMed  CAS  Google Scholar 

  101. Adi S, Wu NY, Rosenthal SM. Insulin-like growth factor (IGF)-I stimulates cyclin-dependent kinase (CDK)4 inhibitor p19 gene expression: a potential mechanism which limits the early mitogenic effect of IGFs and promotes subsequent differentiation in skeletal myoblasts. In: Fourth International Symposium on Insulin-Like Growth Factors, Tokyo, Oct, 1997.

    Google Scholar 

  102. Montarras D, Pinset C, Perez MC, Ilan J, Gros F. Muscle differentiation: insulin-like growth factors as positive modulators of myogenic regulatory genes? CR Acad Sci Paris Ser III Sci Vie 1993; 316: 1029–1031.

    Google Scholar 

  103. Stewart CEH, James PL, Fant ME, Rotwein P. Overexpression of insulin-like growth factor-II induces accelerated myoblast differentiation. J Cell Physiol 1996; 169: 23–32.

    Article  PubMed  CAS  Google Scholar 

  104. Coleman ME, DeMayo F, Yin KC, Lee HM, Geske R, Montgomery C, Schwartz RJ. Myogenic vector expression of insulin-like growth factor I stimulates muscle cell differentiation and myofiber hypertrophy in transgenic mice. J Biol Chem 1995; 270: 12109–12116.

    Article  PubMed  CAS  Google Scholar 

  105. Powell-Braxton L, Hollingshead P, Warburton C, Dowd M, Pitts-Meek S, Dalton D, Gillett N, Stewart TA. IGF-I is required for normal embryonic growth in mice. Genes Dev 1993; 7: 2609–2617.

    Article  PubMed  CAS  Google Scholar 

  106. Liu J-P, Baker J, Perkins AS, Robertson EJ, Efstratiadis A. Mice carrying null mutations of the genes encoding insulin-like growth factor I (IGF-1) and type 1 IGF receptor (IGF1r). Cell 1993; 75: 59–72.

    PubMed  CAS  Google Scholar 

  107. Florini JR, Ewton DZ. Highly specific inhibition of IGF-I-stimulated differentiation by an antisense oligodeoxyribonucleotide to myogenin mRNA. J Biol Chem 1990; 265: 13435–13437.

    PubMed  CAS  Google Scholar 

  108. Adi S, Zhang P, Wu NY, Mellon SH, Rosenthal SM. Insulin-like growth factor (IGF)-I inhibits myogenin promoter activity through element(s) contained within the sequence-94 to of the myogenin gene. In: Fifth Joint Meeting, European Society for Pediatric Endocrinology and Lawson Wilkins Pediatric Endocrinology Society, Stockholm, June, 1997.

    Google Scholar 

  109. Coolican SA, Samuel DS, Ewton DZ, McWade FJ, Florini JR. The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J Biol Chem 1997; 272: 6653–6662.

    Article  PubMed  CAS  Google Scholar 

  110. Ewton DZ, Falen SL, Florini JR. The type II insulin-like growth factor (IGF) receptor has low affinity for IGF-I analogs: pleiotypic actions of IGFs on myoblasts are apparently mediated by the type I receptor. Endocrinology 1987; 120: 115–123.

    Article  PubMed  CAS  Google Scholar 

  111. Bach LA, Salemi R, Leeding KS. Roles of insulin-like growth factor (IGF) receptors and IGF-binding proteins in IGF-II-induced proliferation and differentiation of L6A1 rat myoblasts. Endocrinology 1995; 136: 5061–5069.

    Article  PubMed  CAS  Google Scholar 

  112. Rosenthal SM, Hsiao D, Silverman LA. An insulin-like growth factor-II (IGF-II) analog with highly selective affinity for IGF-II receptors stimulates differentiation, but not IGF-I receptor down-regulation in muscle cells. Endocrinology 1994; 135: 38–44.

    Article  PubMed  CAS  Google Scholar 

  113. Kiess W, Haskell JF, Lee L, Greenstein LA, Miller BE, Aarons AL, Rechler MM, Nissley SP. An antibody that blocks insulin-like growth factor (IGF) binding to the type II IGF receptor is neither an agonist nor an inhibitor of IGF-stimulated biologic responses in L6 myoblasts. J Biol Chem 1987; 262: 12745–12751.

    PubMed  CAS  Google Scholar 

  114. Rosenthal SM, Cheng Z-Q, Hsiao D, Woo EJ, Filvaroff EH, Gustafson TA. Functional inactivation of the insulin-like growth factor-I receptor delays differentiation of skeletal muscle cells. Manuscript submitted, 1999.

    Google Scholar 

  115. Quinn LS, Steinmetz B, Maas A, Ong L, Kaleko M. Type-1 insulin-like growth factor receptor overexpression produces dual effects on myoblast proliferation and differentiation. J Cell Physiol 1994; 159: 387–398.

    Article  PubMed  CAS  Google Scholar 

  116. Quinn LS, Haugk KL. Overexpression of the type-1 insulin-like growth factor receptor increases ligand-dependent proliferation and differentiation in bovine skeletal myogenic cultures. J Cell Physiol 1996; 168: 34–41.

    Article  PubMed  CAS  Google Scholar 

  117. Florini JR, Ewton DZ, Falen SL, Van Wyk JJ. Biphasic concentration dependency of stimulation of myoblast differentiation by somatomedins. Am J Physiol 1986; 250 (Cell Physiol 19):C77l-C778.

    Google Scholar 

  118. Lau MMH, Stewart CEH, Liu Z, Bhatt H, Rotwein P, Stewart CL. Loss of the imprinted IGF2/cationindependent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev 1994; 8: 2953–2963.

    Article  PubMed  CAS  Google Scholar 

  119. Ludwig T, Eggenschwiler J, Fisher P, D’Ercole AJ, Davenport ML, Efstratiadis A. Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1 r null backgrounds. Dev Biol 1996; 177: 517–535.

    Article  PubMed  CAS  Google Scholar 

  120. Ong J, Yamashita S, Melmed S. Insulin-like growth factor I induced c-fos messenger ribonucleic acid in L6 rat skeletal muscle cells. Endocrinology 1987; 120: 353–357.

    Article  PubMed  CAS  Google Scholar 

  121. Giorgino F, Smith RJ. Dexamethasone enhances insulin-like growth factor-I effects on skeletal muscle cell proliferation. J Clin Invest 1995; 96: 1473–1483.

    Article  PubMed  CAS  Google Scholar 

  122. Milasincic DJ, Calera MR, Farmer SR, Pilch PF. Stimulation of C2C12 myoblast growth by basic fibroblast growth factor and insulin-like growth factor 1 can occur via mitogen-activated protein kinase-dependent and -independent pathways. Mol Cell Biol 1996; 16: 5964–5973.

    PubMed  CAS  Google Scholar 

  123. Olson EN, Spizz G, Tainsky MA. The oncogenic forms of N-ras or H-ras prevent skeletal myoblast differentiation. Mol Cell Biol 1987; 7: 2104–2111.

    PubMed  CAS  Google Scholar 

  124. Gossett LA, Zhang W, Olson EN. Dexamethasone-dependent inhibition of differentiation of C2 myoblasts bearing steroid-inducible N-ras oncogenes. J Cell Biol 1988; 106: 2127–2137.

    Article  PubMed  CAS  Google Scholar 

  125. Wu NY, Adi S, Rosenthal SM. Evidence that insulin-like growth factor(IGF)-I-induced inhibition of myogenin gene expression is not mediated by the ras,mitogen-activated protein (MAP) kinase signaling pathway. In: 79th Annual Meeting, Endocrine Society, June 1997.

    Google Scholar 

  126. Sarbassov DD, Jones LG, Peterson CA. Extracellular signal-regulated kinase-1 and -2 respond differently to mitogenic and differentiative signaling pathways in myoblasts. Mol Endocrinol 1997; 11: 2038–2047.

    Article  PubMed  CAS  Google Scholar 

  127. Kaliman P, Vinals F, Testar X, Palacin M, Zorzano A. Phosphatidylinositol 3-kinase inhibitors block differentiation of skeletal muscle cells. J Biol Chem 1996; 271: 19146–19151.

    Article  PubMed  CAS  Google Scholar 

  128. James PL, Stewart CEH, Rotwein P. Insulin-like growth factor binding protein-5 modulates muscle differentiation through an insulin-like growth factor-dependent mechanism J Cell Biol 1996; 133: 683–693.

    CAS  Google Scholar 

  129. Bach LA, Hsieh SP, Brown AL, Rechler MM. Recombinant human insulin-like growth factor (IGF)binding protein-6 inhibits IGF-II-induced differentiation of L6A1 myoblasts. Endocrinology 1994; 135: 2168–2176.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1999 Springer Science+Business Media New York

About this chapter

Cite this chapter

Rosenthal, S.M. (1999). IGFs and Skeletal Muscle. In: Rosenfeld, R.G., Roberts, C.T. (eds) The IGF System. Contemporary Endocrinology, vol 17. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-59259-712-3_21

Download citation

  • DOI: https://doi.org/10.1007/978-1-59259-712-3_21

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-61737-138-7

  • Online ISBN: 978-1-59259-712-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics