Inhibition of Skeletal Muscle Development: Less Differentiation Gives More Muscle

  • Ernst-Martin Füchtbauer
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 38)

Abstract

Differentiation of cells during organogenesis or regeneration is regulated by the complex interaction of signals conducting the differential activity of transcription factors. Proliferation and differentiation of cells are in many cases mutually exclusive and often seen as two opposing modes. This is particularly obvious in the development of skeletal muscle, in which myoblasts have to leave the cell cycle before they fully differentiate and fuse to become myotubes (Olson 1992). The decision of a cell to either divide or differentiate is, therefore, often the result of a competition between growth promoting factors and tissue-specific differentiation factors. However, whether a factor promotes cell proliferation or differentiation depends on the type and status of the cell that receives the signal. Differentiation of cells, e.g. fusion of myoblasts into myotubes, is often viewed as a cell’s final goal, but reaching this goal has its price. To differentiate, i.e. to cease proliferation, is a dramatic step for a cell because no daughter cells will be available to participate in the future life of the organism. For the organism as a whole, namely for an embryo, it is therefore of great importance not only to control proliferation in order to avoid neo-plastic growth, but also to fine tune differentiation in order to avoid a lack of stem cells that are needed for further development, growth and regeneration. For several reasons, inhibition of premature or ectopic differentiation seems to be especially important during myogenesis: Firstly, in the vertebrate somite the first muscle differentiation starts before the limbs even develop, yet undifferentiated cells from the somites have to migrate into the limbs and to the body wall in order to form the major muscles of the body. Secondly, muscle development proceeds in waves, where embryonic muscle fibres are followed by foetal muscle fibres, which precede neonatal muscle. Each new wave of myogenesis needs undifferentiated stem cells, which must have escaped differentiation because the pool of myogenic cells is determined early on. Thirdly, muscle has a very high regeneration capacity, which is not only needed to heal injury, but also for repair of the daily wear and tear. To fulfil these different demands for undifferentiated cells, signals are required that protect them from premature differentiation. These signals are produced either in tissues that are adjacent to myogenic cells (as the lateral plate mesoderm is adjacent to the somites) or within the population of differentiating cells. In the latter case, signalling cells might themselves become insensitive to the inhibitory signal, but protect other cells of the pool from differentiating.

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References

  1. Anant S, Roy S, ViiayRaghavan K (1998) Twist and Notch negatively regulate adult muscle differentiation in Drosophila. Development 125: 1361–1369PubMedGoogle Scholar
  2. Baylies MK, Bate M (1996) Twist: a myogenic switch in Drosophila. Science 272:1481–1484 Bendall AJ, Ding J, Hu G, Shen MM, Abate-Shen C (1999) Msxl antagonizes the myogenic activ- ity of Pax3 in migrating limb muscle precursors. Development 126: 4965–4976Google Scholar
  3. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H (1990) The protein Id: a negative reg- ulator of helix-loop-helix DNA binding proteins. Cell 61: 49–59PubMedCrossRefGoogle Scholar
  4. Bettenhausen B, de Angelis MH, Simon D, Guénet J-L, Gossler A (1995) Transient and restricted expression during mouse embryogenesis of Dlll, a murine gene closely related to Drosophila Delta. Development 121: 2407–2418PubMedGoogle Scholar
  5. Black BL, Molkentin JD, Olson EN (1998) Multiple roles for the MyoD basic region in transmission of transcriptional activation signals and interaction with MEF2. Mol Cell Biol 18: 69–77PubMedGoogle Scholar
  6. Bouche M, Canipari R, Melchionna R, Willems D, Senni MI, Molinaro M (2000) TGF-beta autocrine loop regulates cell growth and myogenic differentiation in human rhabdomyosarcoma cells. FASEB J 14: 1147–1158PubMedGoogle Scholar
  7. Braun T, Buschhausen-Denker G, Bober E, Tannich E, Arnold HH (1989) A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO J 8: 701–709PubMedGoogle Scholar
  8. Braun T, Bober E, Winter E, Rosenthal N, Arnold HH (1990) Myf-6, a new member of the human gene family of myogenic determination factors: evidence for a gene cluster on chromosome 12. EMBO J 9: 821–831PubMedGoogle Scholar
  9. Brennan TJ, Edmondson DG, Li L, Olson EN (1991) Transforming growth factor 13 represses the actions of myogenin through a mechanism independent of DNA binding. Proc Natl Acad Sci USA 88: 3822–3826PubMedCrossRefGoogle Scholar
  10. Choi J, Costa ML, Mermelstein CS, Chagas C, Holtzer S, Holtzer H (1990) MyoD converts primary dermal fibroblasts, chondroblasts, smooth muscle, and retinal pigmented epithelial cells into striated mononucleated myoblasts and multinucleated myotubes. Proc Natl Acad Sci USA 87: 7988–7992PubMedCrossRefGoogle Scholar
  11. Christy BA, Sanders L, Lau LF, Copeland NG, Jenkins NA, Nathans D (1991) An Id-related helixloop-helix protein encoded by a growth factor-inducible gene. Proc Natl Acad Sci USA 88: 1815–1819PubMedCrossRefGoogle Scholar
  12. Clegg CH, Linkhart TA, Olwin BB, Hauschka SD (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: 949–956PubMedCrossRefGoogle Scholar
  13. Cossu G, Borello U (1999) Wnt signaling and the activation of myogenesis in mammals. EMBO J 18: 6867–6872PubMedCrossRefGoogle Scholar
  14. Cusella-De Angelis MG, Molinari S, Le Donne A, Coletta M, Vivarelli E, Bouche M, Molinaro M, Ferrari S, Cossu G (1994) Differential response of embryonic and fetal myoblasts toGoogle Scholar
  15. TGF-O: a possible regulatory mechanism of skeletal muscle histogenesis. Development 120: 925–933Google Scholar
  16. Davis RL, Weintraub H, Lassar AB (1987) Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51: 987–1000PubMedCrossRefGoogle Scholar
  17. De Angelis L, Borghi S, Melchionna R, Berghella L, Baccarani-Contri M, Parise F, Ferrari S, Cossu G (1998) Inhibition of myogenesis by transforming growth factor beta is density-dependent and related to the translocation of transcription factor MEF2 to the cytoplasm. Proc Natl Acad Sci USA 95: 12358–12363PubMedCrossRefGoogle Scholar
  18. Drucker BJ, Goldfarb M (1993) Murine FGF-4 gene expression is spatially restricted within embryonic skeletal muscle and other tissues. Mech Dev 40: 155–163PubMedCrossRefGoogle Scholar
  19. Edmondson DG (1989) A gene with homology to the myc similarity region of MyoDi is sufficient to activate the muscle differentiation program. Genes Dev 3: 628–640PubMedCrossRefGoogle Scholar
  20. Filvaroff EH, Ebner R, Derynck R (1994) Inhibition of myogenic differentiation in myoblasts expressing a truncated type II TGF-13 receptor. Development 120: 1085–1095PubMedGoogle Scholar
  21. Flanagan-Steet H, Hannon K, McAvoy MJ, Hullinger R, Olwin BB (2000) Loss of FGF receptor 1 signaling reduces skeletal muscle mass and disrupts myofiber organization in the developing limb. Dev Biol 218: 21–37PubMedCrossRefGoogle Scholar
  22. Floss T, Arnold HH, Braun T (1997) A role for FGF-6 in skeletal muscle regeneration. Genes Dev 11: 2040–2051PubMedCrossRefGoogle Scholar
  23. Füchtbauer E-M (1995) Expression of M-twist during postimplantation development of the mouse. Dev Dyn 204: 316–322PubMedCrossRefGoogle Scholar
  24. Fuentealba L, Carey DJ, Brandan E (1999) Antisense inhibition of syndecan-3 expression during skeletal muscle differentiation accelerates myogenesis through a basic fibroblast growth factor-dependent mechanism. J Biol Chem 274: 37876–37884PubMedCrossRefGoogle Scholar
  25. Grass S, Arnold H-H, Braun T (1996) Alterations in somite patterning of Myf-5-deficient mice: a possible role for FGF-4 and FGF-6. Development 122: 141–150PubMedGoogle Scholar
  26. Grobet L, Martin LJ, Poncelet D, Pirottin D, Brouwers B, Riquet J, Schoeberlein A, Dunner S, Menissier F, Massabanda J, Fries R, Hanset R, Georges M (1997) A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat Genet 17: 71–74PubMedCrossRefGoogle Scholar
  27. Guillemot F (1995) Analysis of the role of basic-helix-loop-helix transcription factors in the development of neural lineages in the mouse. Biol Cell 84: 3–6PubMedCrossRefGoogle Scholar
  28. Halevy O, Monsonego E, Marcelle C, Hodik V, Mett A, Pines M (1994) A new avian fibroblast growth factor receptor in myogenic and chondrogenic cell differentiation. Exp Cell Res 221: 278–284CrossRefGoogle Scholar
  29. Hamamori Y, Wu HY, Sartorelli V, Kedes L (1997) The basic domain of myogenic basic helix-loop-helix (bHLH) proteins is the novel target for direct inhibition by another bHLH protein, Twist. Mol Cell Biol 17: 6563–6573Google Scholar
  30. Hamamori Y, Sartorelli V, Ogryzko V, Puri PL, Wu H-Y, Wang JYJ, Nakatani Y, Kedes L (1999) Regulation of histon acetyltransferases p300 and PCFA by the bHLH protein Twist and adenoviral oncoprotein E1A. Cell 96: 405–413PubMedCrossRefGoogle Scholar
  31. Han J-K, Martin GR (1993) Embryonic expression of FGF-6 is restricted to the skeletal muscle lineage. Dev Biol 158: 549–554PubMedCrossRefGoogle Scholar
  32. Hardy S, Kong Y, Konieczny SF (1993) Fibroblast growth factor inhibits MRF4 activity independently of the phosphorylation status of a conserved threonine residue within the DNA-binding domain. Mol Cell Biol 13: 5943–5956PubMedGoogle Scholar
  33. Hebrok M, Wertz K, Füchtbauer E-M (1994) M-twist is an inhibitor of muscle differentiation. Dev Biol 165: 537–544PubMedCrossRefGoogle Scholar
  34. Hebrok M, Füchtbauer A, Füchtbauer E-M (1997) Repression of muscle-specific gene activation by the murine twist protein. Exp Cell Res 232: 295–303PubMedCrossRefGoogle Scholar
  35. Heino J, Massagué J (1990) Cell adhesion to collagen and decreased myogenic gene expression implicated in the control of myogenesis by transforming growth factor P. J Biol Chem 265: 10181–10184PubMedGoogle Scholar
  36. Hill RE, Jones PF, Rees AR, Sime CM, Justice MJ, Copeland NG, Jenkins NA, Graham E, Davidson DR (1989) A new family of mouse homeo box-containing genes: molecular structure, chromosomal localisation, and developmental expression of Hox-7.1. Genes Dev 3: 26–37PubMedCrossRefGoogle Scholar
  37. Hirsinger E, Malapert P, Dubrulle J, Delfini MC, Duprez D, Henrique D, Ish-Horowicz D, PourquieGoogle Scholar
  38. (2001).
    Notch signalling acts in postmitotic avian myogenic cells to control MyoD activation. Development 128:107–116Google Scholar
  39. Houzelstein D, Auda-Boucher G, Cheraud Y, Rouaud T, Blanc I, Tajbakhsh S, Buckingham ME, Fontaine-Perus J, Robert B (1999) The homeobox gene Msxl is expressed in a subset of somites, and in muscle progenitor cells migrating into the forelimb. Development 126: 2689–2701PubMedGoogle Scholar
  40. Hu J-S, Olson EN (1990) Functional receptors for transforming growth factor-β are retained by biochemically differentiated C2 myocytes in growth factor deficient medium containing EGTA but down-regulated during terminal differentiation. J Biol Chem 265: 7914–7919PubMedGoogle Scholar
  41. Jen Y, Weintraub H, Benezra R (1992) Overexpression of Id protein inhibits the muscle differen- tiation program: in vivo association of ID with E2A proteins. Genes Dev 6: 1466–1479PubMedCrossRefGoogle Scholar
  42. Jensen J, Heller RS, Funder-Nielsen T, Pedersen EE, Lindsell C, Weinmaster G, Madsen OD, Serup P (2000) Independent development of pancreatic alpha-and beta-cells from neurogenin3expressing precursors: a role for the notch pathway in repression of premature differentiation. Diabetes 49: 163–176PubMedCrossRefGoogle Scholar
  43. Kaatinen V, Voncken JW, Shuler C, Warburton D, Bu D, Heisterkamp N, Groffen J (1995) Abnormal lung development and cleft palate in mice lacking TGF-[33 indicates defects of epithelial-mesenchymal interaction. Nat Genet 11: 415–421CrossRefGoogle Scholar
  44. Kageyama R, Ohtsuka T, Tomita K (2000) The bHLH gene Hesl regulates differentiation of multiple cell types. Mol Cells 10: 1–7PubMedCrossRefGoogle Scholar
  45. Kambadur R, Sharma M, Smith TP, Bass JJ (1997) Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res 7: 910–916.PubMedGoogle Scholar
  46. Katagiri T, Yamaguchi A, Komaki M, Abe E, Takahashi N, Ikeda T, Rosen V, Wozney JM, FujisawaSehara A, Suda T (1994) Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage [published erratum appears in J Cell Biol 1995 Feb;128(4):following 7131. J Cell Biol 127: 1755–1766Google Scholar
  47. Kaul A, Koster M, Neuhaus H, Braun T (2000) Myf-5 revisited: loss of early myotome formation does not lead to a rib phenotype in homozygous Myf-5 mutant mice. Cell 102:17–19 Klagsbrun M, Baird A (1991) A dual receptor system is required for basic fibroblast growth factor activity. Cell 67: 229–231Google Scholar
  48. Kopan R, Nye JS, Weintraub H (1994) The intracellular domain of mouse Notch: a constitutively activated repressor of myogenesis directed at the basic helix-loop-helix region of MyoD. Development 120: 2385–2396PubMedGoogle Scholar
  49. Lafyatis R, Lechleider R, Roberts AB, Sporn MB (1991) Secretion and transcriptional regulation of transforming growth factor-beta 3 during myogenesis. Mol Cell Biol 11: 3795–3803PubMedGoogle Scholar
  50. Larrain J, Cizmeci-Smith G, Troncoso V, Stahl RC, Carey DJ, Brandan E (1997) Syndecan-1 expression is down-regulated during myoblast terminal differentiation. Modulation by growth factors and retinoic acid. J Biol Chem 272: 18418–18424Google Scholar
  51. Larrain J, Carey DJ, Brandan E (1998) Syndecan-1 expression inhibits myoblast differentiation through a basic fibroblast growth factor-dependent mechanism. J Biol Chem 273: 32288–32296PubMedCrossRefGoogle Scholar
  52. Li L, Hu J-S, Olson EN (1990) Different members of the jun proto-oncogene family exhibit distinct patterns of expression in response to type [3 transforming growth factor. J Biol Chem 265: 1556–1562PubMedGoogle Scholar
  53. Li L, Zhou J, James G, Heller-Harrison R, Czech MP, Olson EN (1992) FGF inactivates myogenic helix-loop-helix proteins through phosphorylation of a conserved protein kinase C site in their DNA binding domains. Cell 71: 1181–1194PubMedCrossRefGoogle Scholar
  54. Lilly B, Galewsky S, Firulli AB, Schulz RA, Olson EN (1994) D-MEF2: a MADS box transcription factor expressed in differentiating mesoderm and muscle cell lineages during Drosophila embryogenesis. Proc Natl Acad Sci USA 91: 5662–5666PubMedCrossRefGoogle Scholar
  55. Lindsell CE, Shawber CJ, Boulter J, Weinmaster G (1995) Jagged: a mammalian ligand that activates Notchl. Cell 80: 909–917PubMedCrossRefGoogle Scholar
  56. Marcelle C, Stark MR, Bronner-Fraser M (1997) Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 124: 3955–3963Google Scholar
  57. Martin JF, Li L, Olson EN (1992) Repression of myogenic function by TGF-(31 is targeted at the basic helix-loop-helix motif and is independent of E2A products. J Biol Chem 267: 10956–10960PubMedGoogle Scholar
  58. McPherron AC, Lee SJ (1997) Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci USA 94: 12457–12461PubMedCrossRefGoogle Scholar
  59. McPherron AC, Lawler AM, Lee SJ (1997) Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387: 83–90PubMedCrossRefGoogle Scholar
  60. Miner JH, Wold BJ (1990) Herculin, a fourth member of the MyoD family of myogenic regulatory genes. Proc Natl Acad Sci USA 87: 1089–1093PubMedCrossRefGoogle Scholar
  61. Molkentin JD, Black BL, Martin JF, Olson EN (1995) Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 83: 1125–1136PubMedCrossRefGoogle Scholar
  62. Naya FS, Olson E (1999) MEF2: a transcriptional target for signaling pathways controlling skeletal muscle growth and differentiation. Curr Opin Cell Biol 11: 683–688PubMedCrossRefGoogle Scholar
  63. Nguyen HT, Bodmer R, Abmayr SM, McDermott JC, Spoerel NA (1994) D-mef2: a Drosophila mesoderm-specific MADS box-containing gene with a biphasic expression profile during embryogenesis. Proc Natl Acad Sci USA 91: 7520–7524PubMedCrossRefGoogle Scholar
  64. Niswander L, Martin GR (1992) Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114: 755–768PubMedGoogle Scholar
  65. Nye JS, Kopan R, Axel R (1994) An activated Notch suppresses neurogenesis and myogenesis but not gliogenesis in mammalian cells. Development 120:2421–2430Google Scholar
  66. Odelberg SJ, Kollhoff A, Keating MT (2000) Dedifferentiation of mammalian myotubes induced by msxl. Cell 103: 1099–1109PubMedCrossRefGoogle Scholar
  67. Olson EN (1992) Interplay between proliferation and differentiation within the myogenic lineage. Dev Biol 154: 261–272PubMedCrossRefGoogle Scholar
  68. Pelton RW, Saxena B, Jones M, Moses HL, Gold LI (1991) Immunohistochemical localization of TGF-131, TGF-ß2, and TGF-133 in the mouse embryo: expression pattern suggest multiple roles during embryonic development. J Cell Biol 115: 1091–1105PubMedCrossRefGoogle Scholar
  69. Pena TL, Chen SH, Konieczny SF, Rane SG (2000) Ras/MEK/ERK up-regulation of the fibroblast KCa channel FIK is a common mechanism for basic fibroblast growth factor and transforming growth factor-beta suppression of myogenesis. J Biol Chem 275: 13677–13682PubMedCrossRefGoogle Scholar
  70. Pertovaara L, Sistonen L, Bos TJ, Vogt PK, Keski-Oja J, Alitalo K (1989) Enhanced jun gene expression is an early genomic response to transforming growth factor 13 stimulation. Mol Cell Biol 9: 1255–1262PubMedGoogle Scholar
  71. Peters KG, Werner S, Chen G, Williams LT (1992) Two FGF receptor genes are differentially expressed in epithelial and mesenchymal tissues during limb formation and organogenesis in the mouse. Development 114: 233–243PubMedGoogle Scholar
  72. Pourquié O, Fan C-M, Coltey M, Hirsinger E, Watanabe Y, Bréant C, Francis-West P, Brickell P, Tessier-Lavigne M, Le Douarin NM (1996) Lateral and axial signals involved in avian somite patterning: a role for BMP4. Cell 84: 461–471PubMedCrossRefGoogle Scholar
  73. Proetzel G, Pawlowski SA, Wiles MV, Yin M, Boivin GP, Howles PN, Ding J, Ferguson MWJ, Doetschman T (1995) Transforming growth factor-(33 is required for secondary palate fusion. Nat Genet 11: 409–414PubMedCrossRefGoogle Scholar
  74. Reshef R, Maroto M, Lassar AB (1998) Regulation of dorsal somitic cell fates: BMPs and Noggin control the timing and pattern of myogenic regulator expression. Genes Dev 12: 290–303Google Scholar
  75. Rhodes SJ, Konieczny SF (1989) Identification of MRF4: a new member of the muscle regulatory factor gene family. Genes Dev 3: 2050–2061PubMedCrossRefGoogle Scholar
  76. Riechmann V, van Crüchten I, Sablitzky F (1994) The expression pattern of Id4, a novel dominant negative helix-loop-helix protein, is distinct from Idl, Id2 and Id3. Nucleic Acids Res 22: 749–755PubMedCrossRefGoogle Scholar
  77. Rios R, Carneiro I, Arce VM, Devesa J (2001) Myostatin regulates cell survival during C2C12 myogenesis. Biochem Biophys Res Commun 280: 561–566PubMedCrossRefGoogle Scholar
  78. Riquelme C, Larrain J, Schonherr E, Henriquez JP, Kresse H, Brandan E (2000) Antisense inhibition of decorin expression in myoblasts decreases cell responsiveness to transforming growth factor beta and accelerates skeletal muscle differentiation [published correction appears in J Biol Chem 276:9580–9581]. J Biol Chem 276: 3589–3596Google Scholar
  79. Robert B, Sassoon D, Jacq B, Gehring W, Buckingham M (1989) Expression of a novel Hox gene, Hox-7, during mouse embryogenesis, is associated with morphogenetic phenomena. EMBO J 8: 91–100PubMedGoogle Scholar
  80. Rohwedel J, Horâk V, Hebrok M, Füchtbauer E-M, Wobus AM (1995) M-twist expression inhibits mouse embryonic stem cell-derived myogenic differentiation in vitro. Exp Cell Res 220: 92–100PubMedCrossRefGoogle Scholar
  81. Saitoh O, Periasamy M, Kan M, Matsuda R (1992) Cis-4-hydoxy-L-proline and ethyl-3,4dihydroxybenzoate prevent myogenesis of C2C12 muscle cells and block MyoD1 and myogenin expression. Exp Cell Res 200: 70–76PubMedCrossRefGoogle Scholar
  82. Sakuma K, Watanabe K, Sano M, Uramoto I, Totsuka T (2000) Differential adaptation of growth and differentiation factor 8/myostatin, fibroblast growth factor 6 and leukemia inhibitory factor in overloaded, regenerating and denervated rat muscles. Biochim Biophys Acta 1497: 77–88PubMedCrossRefGoogle Scholar
  83. Scaal M, Füchtbauer EM, Brand-Saberi B (2001) cDermo-1 expression indicates a role in avian skin development. Anat Embryol (Berl) 203: 1–7Google Scholar
  84. Schäfer BW, Blakely BT, Darlington GJ, Blau HM (1990) Effect of cell history on response to helix-loop-helix family of myogenic regulators. Nature 344: 454–458PubMedCrossRefGoogle Scholar
  85. Schubert D, Harris AJ, Devine CE, Heinemann S (1974) Characterization of a unique muscle cell line. J Cell Biol 61: 398–413PubMedCrossRefGoogle Scholar
  86. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D et al. (1992) Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359: 693–699PubMedCrossRefGoogle Scholar
  87. Song K, Wang Y, Sassoon D (1992) Expression of Hox-7.1 in myoblast inhibits terminal differentiation and induces cell transformation. Nature 360: 477–481PubMedCrossRefGoogle Scholar
  88. Spicer DB, Rhee J, Cheung WL, Lassar AB (1996) Inhibition of myogenic bHLH and MEF2 transcription factors by the bHLH protein twist. Science 272: 1476–1480PubMedCrossRefGoogle Scholar
  89. Stark KL, McMahon JA, McMahon AP (1991) FGFR-4, a new member of the fibroblast growth factor receptor family, expressed in the definitive endoderm and skeletal muscle lineages of the mouse. Development 113: 641–651PubMedGoogle Scholar
  90. Struhl G, Greenwald I (2001) Presenilin-mediated transmembrane cleavage is required for Notch signal transduction in Drosophila. Proc Natl Acad Sci USA 98: 229–234PubMedCrossRefGoogle Scholar
  91. Sun X-H, Copeland NG, Jenkins NA, Baltimore D (1991) Id proteins Idl and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol Cell Biol 11: 5603–5611PubMedGoogle Scholar
  92. Taylor MV, Beatty KE, Hunter HK, Baylies MK (1995) Drosophila MEF2 is regulated by twist and is expressed in both the primordia and differentiated cells of the embryonic somatic, visceral and heart musculature [published erratum appears in Mech Dev 1995 May; 51(1):139–41]. Mech Dev 50:29–41Google Scholar
  93. Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R (2000) Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem 275: 40235–40243PubMedCrossRefGoogle Scholar
  94. Tsuda T, Kaibuchi K, Kawahara Y, Fukuzaki H, Taika Y (1985) Induction of proteinkinase C activation and Ca’ mobilization by fibroblast growth factor in Swiss 3T3 cells. FEBS Lett 191: 205–210PubMedCrossRefGoogle Scholar
  95. Vaidya TB, Rhodes SJ, Taparowsky EJ, Konieczny SF (1989) Fibroblast growth factor and transforming growth factor ß repress transcription of the myogenic regulatory gene MyoD1. Mol Cell Biol 9: 3576–3579PubMedGoogle Scholar
  96. Villavicencio EH, Yoon JW, Frank D, Füchtbauer E-M, Walterhouse DO, Iannaccone PM (2002) Twist is an upstream regulator of human Glil. Genesis 32:in pressGoogle Scholar
  97. Wang Y, Sassoon D (1995) Ectoderm-mesenchyme and mesenchyme-mesenchyme interactions regulate Msx-1 expression and cellular differentiation in murine limb bud. Dev Biol 168: 374–383PubMedCrossRefGoogle Scholar
  98. Wang Y, Benezra R, Sassoon DA (1992) Id expression during mouse development: a role in morphogenesis. Dev Dyn 194: 222–230PubMedCrossRefGoogle Scholar
  99. Wilson-Rawls J, Molkentin JD, Black BL, Olson EN (1999) Activated Notch inhibits myogenic activity of the MADS-Box transcription factor myocyte enhancer factor 2C. Mol Cell Biol 19: 2853–2862PubMedGoogle Scholar
  100. Wright WE, Sassoon DA, Lin VK (1989) Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56: 607–617PubMedCrossRefGoogle Scholar
  101. Yaffe D, Saxel O (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscles. Nature 270: 725–727PubMedCrossRefGoogle Scholar
  102. Yayon A, Klagsbrun M, Esko JD, Leder P, Ornitz DM (1991) Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64: 841–848PubMedCrossRefGoogle Scholar
  103. Yin Z, Xu XL, Frasch M (1997) Regulation of the twist target gene tinman by modular cis- regulatory elements during early mesoderm development. Development 124: 4971–4982PubMedGoogle Scholar
  104. Zentella A, Massagué J (1992) Transforming growth factor ß induces myoblast differentiation in the presence of mitogens. Proc Natl Acad Sci USA 89: 5176–5180PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • Ernst-Martin Füchtbauer
    • 1
  1. 1.Institute of Molecular and Structural BiologyAarhus UniversityÅrhus CDenmark

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