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Transcription Factors Controlling Muscle-Specific Gene Expression

  • John J. Schwarz
  • James F. Martin
  • Eric N. Olson
Part of the Progress in Gene Expression book series (PRGE)

Abstract

Understanding the mechanisms responsible for activation of cell-type-specific gene expression during development is a fundamental problem in molecular biology. Skeletal muscle has provided an important system for investigating this problem because differentiation of skeletal myoblasts is accompanied by the coordinate induction of a battery of genetically unlinked muscle-specific genes whose products are required for the specialized functions of the mature muscle fiber. Analysis of the events associated with muscle differentiation has also been facilitated by the availability of established muscle cell lines that differentiate rapidly and synchronously and whose differentiation can be negatively regulated by individual peptide growth factors or activated oncogenes encoding proteins which transduce growth factor signals from the cell membrane to the nucleus.

Keywords

Serum Response Factor Muscle Cell Line Myogenic Factor MyoD Family bHLH Region 
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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References

  1. Bergsma D, Grichnik J, Gossett L, Schwartz R (1986): Delimitation and characterization of cis-acting DNA sequences required for the regulated expression and transcriptional control of the chicken skeletal α-actin gene. Mol Cell Biol 6:2462–2475.Google Scholar
  2. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H (1990): The protein Id: A negative regulatory of helix-loop-helix DNA binding proteins. Cell 61:49–59.CrossRefGoogle Scholar
  3. Blackwell TK, Weintraub H (1990): Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science 250:1104–1110.CrossRefGoogle Scholar
  4. Bober E, Lyons GE, Braun T, Cossu G, Buckingham M, Arnold H (1991): The muscle regulatory gene, myf-6, has a biphasic pattern of expression during early mouse development. J Cell Biol 113:1255–1265.CrossRefGoogle Scholar
  5. Boxer LM, Prywes R, Roeder RG, Kedes L (1989): The sarcomeric actin CArG-binding factor is indistinguishable from the c-fos serum response factor. Mol Cell Biol 9:515–522.Google Scholar
  6. Braun T, Tannich E, Buschhausen-Denker G, Arnold HH (1989a): Promoter upstream elements of the chicken cardiac myosin light-chain 2A gene interact with taws-acting regulatory factors for muscle-specific transcription. Mol Cell Biol 9:2513–2525.Google Scholar
  7. Braun T, Buschhausen-Denker G, Bober E, Tannich E, Arnold HH (1989b): A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO J 8:701–709.Google Scholar
  8. Braun T, Bober E, Buschhausen-Denker G, Kotz S, Grzeschik K, Arnold HH (1989c): Differential expression of myogenic determination genes in muscle cells: Possible autoactivation by the myf gene products. EMBO J 8:3617–3625.Google Scholar
  9. Braun T, Winter B, Bober E, Arnold HH (1990a): Transcriptional activation domain of the muscle-specific gene-regulatory protein myf-5. Nature (Lond) 346:663–665.CrossRefGoogle Scholar
  10. Braun T, Bober B, Winter B, Rosenthal N, Arnold HH (1990b): Myf-6, a new member of the human gene family of myogenic determination factors: Evidence for a gene cluster on chromosome 12. EMBO J 9:821–831.Google Scholar
  11. Brennan TJ, Chakraborty T, Olson EN (1991a): Mutagenesis of the myogenin basic region identifies an ancient protein motif critical for activation of myo-genesis. Proc Natl Acad Sci USA 88:5675–5679.CrossRefGoogle Scholar
  12. Brennan TJ, Edmondson DG, Li L, Olson EN (1991b): Transforming growth factor β represses the actions of myogenin through a mechanism independent of DNA binding. 88:3822–3826.Google Scholar
  13. Brennan TJ, Olson EN (1990): Myogenin resides in the nucleus and acquires high affinity for a conserved enhancer element on heterodimerization. Genes & Dev 4:582–595.CrossRefGoogle Scholar
  14. Brunetti A, Goldfine ID (1990): Role of myogenin in myoblast differentiation and its regulation by fibroblast growth factor. J Biol Chem 265:5960–5963.Google Scholar
  15. Buskin JN, Hauschka SD (1989): Identification of a myocyte nuclear factor which binds to the muscle-specific enhancer of the mouse muscle creatine kinase gene. Mol Cell Biol 9:2627–2640.Google Scholar
  16. Chakraborty T, Brennan TJ, Li L, Edmondson D, Olson EN (1991a): Inefficient homodimerization contributes to the dependence of myogenin on EZA products for efficient DNA binding. Mol Cell Biol 11:3633–3641.Google Scholar
  17. Chakraborty T, Brennan TJ, Olson EN (1991b): Differential taws-activation of muscle-specific enhancer by myogenic helix-loop-helix proteins is separable from DNA binding. J Biol Chem 266:2878–2882.Google Scholar
  18. Chakraborty T, Olson EN (1991): Domains outside of the DNA-binding domain impart target gene specificity to myogenin and MRF4. Mol Cell Biol 11:6103–6108.Google Scholar
  19. 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 87:7988–7992.CrossRefGoogle Scholar
  20. Cooper T, Ordahl C (1984): A single troponin T gene regulated by different programs in cardiac and skeletal muscle development. Science 226:979–982.CrossRefGoogle Scholar
  21. Cooper T, Ordahl C (1985): A single troponin-T gene generates embryonic and adult isoforms via developmentally regulated alternate splicing. J Biol Chem 260:11140–11148.Google Scholar
  22. Crescenzi M, Fleming TP, Lassar AB, Weintraub H, Aaronson SA (1990): MyoD induces growth arrest independent of differentiation in normal and transformed cells. Proc Natl Acad Sci USA 87:8442–8446.CrossRefGoogle Scholar
  23. Cserjesi P, Olson EN (1991): Myogenin induces the myocyte-specific enhancer binding factor MEF-2 independently of other muscle-specific gene products. Mol Cell Biol 11:4854–4862.Google Scholar
  24. Davis RL, Weintraub H, Lassar AB (1987): Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51:987–1000.CrossRefGoogle Scholar
  25. Davis RL, Cheng P, Lassar AB, Weintraub H (1990): The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell 60:733–746.CrossRefGoogle Scholar
  26. Edmondson DG, Olson EN (1989): A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program. Genes & Dev 3:628–640.CrossRefGoogle Scholar
  27. Edmondson DG, Cheng TC, Cserjesi P, Chakraborty T, Olson EN (1992): Analysis of the myogenin promoter reveals an indirect pathway for positive au-toregulation mediated by the muscle-specific enhancer factor MEF-2. Mol Cell Biol 12:3665–3677.Google Scholar
  28. Enkemann SA, Konieczny SF, Taparowsky EJ (1990): Adenovirus 5 E1A represses muscle-specific enhancers and inhibits expression of the myogenic regulatory factor genes, MyoD1 and myogenin. Cell Growth & Differ 1:375 – 382.Google Scholar
  29. Ernst H, Walsh K, Harrison CA, Rosenthal N (1991): The myosin light chain enhancer and the skeletal actin promoter share a binding site for factors involved in muscle-specific gene expression. Mol Cell Biol 11:3735–3744.Google Scholar
  30. Florini JR, Ewton DZ (1990): Highly specific inhibition of IGF-I-stimulated differentiation by an antisense oligodeoxyribonucleotide to myogenin mRNA. J Biol Chem 265:13435–13437.Google Scholar
  31. Florini JR, Ewton DZ, Magri KA (1991): Hormones, growth factors, and myogenic differentiation. Annu Rev Physiol 53:201–216.CrossRefGoogle Scholar
  32. Florini JR, Magri KA (1989): Effects of growth factors on myogenic differentiation. Am J Physiol 256:c701–711.Google Scholar
  33. French BA, Chow K, Olson EN, Schwartz RJ (1991): Heterodimers of myogenic helix-loop-helix regulatory factors and E12 bind a complex element governing myogenic induction of the avian cardiac α-actin promoter. Mol Cell Biol 11:2439–2450.Google Scholar
  34. Gossett LA, Kelvin DJ, Sternberg EA, Olson EN (1989): A new myocyte-specific enhancer-binding factor that recognizes a conserved element associated with multiple muscle-specific genes. Mol Cell Biol 9:5022–5033.Google Scholar
  35. Heino J, Massague J (1990): Cell adhesion to collagen and decreased myogenic gene expression implicated in the control of myogenesis by transforming growth factor-β. J Biol Chem 265:10181–10184.Google Scholar
  36. Horlick RA, Benfield PA (1989): The upstream muscle-specific enhancer of the rat muscle creatine kinase gene is composed of multiple elements. Mol Cell Biol 9:2396–2413.Google Scholar
  37. Horlick RA, Hobson GM, Patterson JH, Mitchell MT, Benfield PA (1990): Brain and muscle creatine kinase genes contain common TA-rich recognition protein-binding regulatory elements. Mol Cell Biol 10:4826–4836.Google Scholar
  38. Ianello RC, Mar JH, Ordahl CP (1991): Characterization of a promoter element required for transcription in myocardial cells. J Biol Chem 266:3309–3316.Google Scholar
  39. Lassar AB, Thayer MJ, Overell RW, Weintraub H (1989a): Transformation by activated ras or fos prevents myogenesis by inhibiting expression of MyoD1. Cell 58:659–667.CrossRefGoogle Scholar
  40. Lassar AB, Buskin JN, Lockshon D, Davis RL, Apone S, Hauschka SD, Weintraub H (1989b): MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell 58:823–831.CrossRefGoogle Scholar
  41. Lassar AB, Davis RL, Wright WE, Kadesch T, Murre C, Voronova A, Baltimore D, Weintraub H (1991): Functional activity of myogenic HLH proteins requires heterooligomerization with E12/E47-like proteins in vivo. Cell 66:305–315.CrossRefGoogle Scholar
  42. Li L, Chambard J-C, Karin M, Olson EN (1992): Fos and Jun repress transcriptional activation by myogenin and MyoD: The amino terminus of Jun mediates repression. Genes & Dev 6:676–689.CrossRefGoogle Scholar
  43. Lin H, Yutzey K, Koniecny SF (1991): Muscle-specific expression of the troponin I gene requires interactions between helix-loop-helix muscle regulatory factors and uniquitous transcription factors. Mol Cell Biol 11:267–280.Google Scholar
  44. Long C, Ordahl C (1988): Transcriptional repression of an embryo-specific muscle gene. Dev Biol 127:228–234.CrossRefGoogle Scholar
  45. Mar J, Ordahl C (1988): A conserved CATTCCT motif is required for skeletal muscle-specific expression of the cardiac troponin T gene promoter. Proc Natl Acad Sci USA 85:6404–6408.CrossRefGoogle Scholar
  46. Mar J, Ordahl CP (1990): M-CAT binding factor, a novel trans-acting factor governing muscle-specific transcription. Mol Cell Biol 10:4271–4283.Google Scholar
  47. Martin J, Li L, Olson EN (1992): Repression of myogenin function by TGF-ß is targeted at the basic-helix-loop-helix motif and is independent of E2A products J Biol Chem 267:10956–10960.Google Scholar
  48. Miller JB (1990): Myogenic programs of mouse muscle cell lines: Expression of myosin heavy chain isoforms, MyoDl, and myogenin. J Cell Biol 111:1149–1159.CrossRefGoogle Scholar
  49. Miner JH, Wold B (1990): Herculin, a fourth member of the MyoD family of myogenic regulatory genes. Proc Nail Acad Sci USA 87:1089–1093.CrossRefGoogle Scholar
  50. Miner JH, Wold B (1991): c-myc inhibition of MyoD and myogenin-initiated myogenic differentiation. Mol Cell Biol 11:2842–2851.Google Scholar
  51. Minty A, Kedes L (1986): Upstream regions of the human cardiac actin gene that modulate its transcription in muscle cells: Presence of an evolutionarily conserved repeated motif. Mol Cell Biol 6:2125–2136.Google Scholar
  52. Montarras D, Chelly J, Bober E, Arnold H, Ott M, Gros F, Pinset C (1991): Developmental patterns in the expression of Myf5, MyoD, myogenin, and MRF4 during myogenesis. New Biol 3:592–600.Google Scholar
  53. Murre C, McCaw PS, Baltimore D (1989a): A new DNA binding and dimer-ization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56:777–783.CrossRefGoogle Scholar
  54. Murre C, McCaw PS, Vaessin H, Caudy M, Jan LY, Jan YN, Cabrera CV, Buskin JN, Hauschka SD, Lassar AB, Weintraub H, Baltimore D (1989b): Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58:537–544.CrossRefGoogle Scholar
  55. Ott M-O, Bober E, Lyons G, Arnold H, Buckingham M (1991): Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111:1097–1107.Google Scholar
  56. Piette J, Bessereau J, Huchet M, Changeux J (1990): Two adjacent MyoD1-binding sites regulate expression of the acetylcholine receptor α-subunit gene. Nature (Lond) 345:353–355.CrossRefGoogle Scholar
  57. Pollock R, Treisman R (1991): Human SRF-related proteins: DNA-binding properties and potential regulatory targets. Genes & Dev 5:2327–2341.CrossRefGoogle Scholar
  58. Rhodes SJ, Konieczny SF (1989): Identification of MRF4: A new member of the muscle regulatory factor gene family. Genes & Dev 3:2050–2061.CrossRefGoogle Scholar
  59. Rosenthal N, Berglund EB, Wentworth BM, Donoghue M, Winter B, Bober E, Braun T, Arnold HH (1990): A highly conserved enhancer downstream of the human MLCY3 locus is a target for multiple myogenic determination factors. Nuc Acid Res 18:6239–6246.CrossRefGoogle Scholar
  60. Sartorelli V, Webster KA, Kedes L (1990): Muscle-specific expression of the cardiac α-actin gene requires MyoDl, CArG-box binding factor, and Spl. Genes & Dev 4:1811–1822.CrossRefGoogle Scholar
  61. Sassoon D, Lyons G, Wright WE, Lin V, Lassar A, Weintraub H, Buckingham M (1989): Expression of two myogenic regulatory factors myogenin and MyoDl during mouse embryogenesis. Nature (Lond) 341:303–307.CrossRefGoogle Scholar
  62. Schafer BW, Blakely BT, Darlington GJ, Blau HM (1990): Effect of cell history on response to helix-loop-helix family of myogenic regulators. Nature (Lond) 344:454–458.CrossRefGoogle Scholar
  63. Schneider MD, Perryman MB, Payne PA, Spizz G, Roberts R, Olson EN (1987): Autonomous expression of c-myc in BC3HI cells partially inhibits but does not prevent myogenic differentiation. Mol Cell Biol 7:1973–1977.Google Scholar
  64. Schroter H, Mueller CG, Meese K, Nordheim A (1990): Synergism in ternary complex formation between the dimeric glycoprotein p67SRF, polypeptide p62TCF and the c-fos serum response element. EMBO J 9:1123–1130.Google Scholar
  65. Schwarz JJ, Chakraborty T, Martin J, Zhou J, Olson EN (1992): The basic region of myogenin cooperates with two transcription activation domains to induce muscle-specific transcription. Mol Cell Biol 12:266–275.Google Scholar
  66. Sorrentino V, Pepperkok R, Davis RL, Ansorge W, Philipson L (1990): Cell proliferation inhibited by MyoDl independently of myogenic differentiation. Nature (Lond) 345:813–815.CrossRefGoogle Scholar
  67. Stern S, Tanaka M, Herr W (1989): The Oct-1 homoeodomain directs formation of a multiprotein-DNA complex with the HSV transactivator VP16. Nature (Lond) 341:624–630.CrossRefGoogle Scholar
  68. Sternberg EA, Spizz G, Perry WM, Vizard D, Weil T, Olson EN (1988): Identification of upstream and intragenic regulatory elements that confer cell-type-restricted and differentiation-specific expression on the muscle creatine kinase gene. Mol Cell Biol 8:2896–2909.Google Scholar
  69. Sun X-H, Baltimore D (1991): An inhibitory domain of E12 transcription factor prevents DNA binding in E12 homodimers but not in E12 heterodimers. Cell 64:459–470.CrossRefGoogle Scholar
  70. Tan S, Richmond TJ (1990): DNA binding-induced conformational change of the yeast transcriptional activator PRTF. Cell 62:367–377.CrossRefGoogle Scholar
  71. Tapscott SJ, Davis RL, Thayer MJ, Cheng P, Weintraub H, Lassar AB (1988): MyoDl: A nuclear phosphoprotein requiring a myc homology region to convert fibroblasts to myoblasts. Science 242:405–411.CrossRefGoogle Scholar
  72. Taylor M, Treisman R, Garrett N, Mohun T (1989): Muscle-specific (CArG) and serum-responsive (SRE) promoter elements are functionally interchangeable in Xenopus embryos and mouse fibroblasts. Development 106:67–78.Google Scholar
  73. Thayer MJ, Tapscott SJ, Davis RL, Wright WE, Lassar AB, Weintraub H (1989): Positive autoregulation of the myogenic determination gene MyoDl. Cell 58:241–248.CrossRefGoogle Scholar
  74. Treisman R (1990): The SRF: A growth factor responsive transcriptional regulator. Semin Cancer Biol 1:47–58.Google Scholar
  75. Tuil D, Clergue N, Montarras D, Pinset C, Kahn A, Phan-Dinh-Tuy F (1990): CC Ar GG boxes, cis-acting elements with a dual specificity. Muscle-specific transcriptional activation and serum responsiveness. J Mol Biol 213:677–686.CrossRefGoogle Scholar
  76. Vaidya TB, Rhodes SJ, Taparowsky EJ, Konieczny SF (1989): Fibroblast growth factor and transforming growth factor ß repress transcription of the myogenic regulatory gene MyoDl. Mol Cell Biol 9:3576–3579.Google Scholar
  77. Walsh K (1989): Cross-binding of factors of functionally different promoter elements in c-fos and skeletal actin genes. Mol Cell Biol 9:2191–2201.Google Scholar
  78. Walsh K, Schimmel P (1987): Two nuclear factors compete for the skeletal muscle actin promoter. J Biol Chem 262:9429–9432.Google Scholar
  79. Walsh K, Schimmel P (1988): DNA-binding site for two skeletal actin promoter factors is important for expression in muscle cells. Mol Cell Biol 8:1800–1802.Google Scholar
  80. Webster KA, Muscat GEO, Kedes L (1988): Adenovirus E1A products suppress myogenic differentiation and inhibit transcription from muscle-specific promoters. Nature (Lond) 332:553–557.CrossRefGoogle Scholar
  81. Weintraub H, Davis R, Lockshon D, Lassar A (1990): MyoD binds cooperatively to two sites in a target enhancer sequence: Occupancy of two sites is required for activation. Proc Natl Acad Sci USA 87:5623–5627.CrossRefGoogle Scholar
  82. Weintraub H, Dwarki VJ, Verma I, Davis R, Hollenberg S, Snider L, Lassar A, Tapscott SJ (1991): Muscle-specific transcriptional activation by MyoD. Genes & Dev 5:1377–1386.CrossRefGoogle Scholar
  83. Weintraub H, Tapscott SJ, Davis RL, Thayer MJ, Adam MA, Lassar AB, Miller AD (1989): Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc Natl Acad Sci USA 86:5434–5438.CrossRefGoogle Scholar
  84. Wentworth BM, Donoghue M, Engert JC, Berglund EB, Rosenthal N (1991): Paired MyoD binding sites regulate myosin light chain gene expression. Proc Natl Acad Sci USA 88:1242–1246.CrossRefGoogle Scholar
  85. Wright WE, Binder M, Funk W (1991): Cyclic amplification and selection of targets (CASTing) for the myogenin consensus binding site. Mol Cell Biol 11:4104–4110.Google Scholar
  86. Wright WE, Sassoon DA, Lin VK (1989): Myogenin, a factor regulating myo-genesis, has a domain homologous to MyoDl. Cell 56:607–617.CrossRefGoogle Scholar
  87. Xiao JH, Davidson I, Mathes H, Garnier JM, Chambon P (1991): Cloning, expression and transcriptional properties of the human enhancer factor TEF-1. Cell 65:551–568.CrossRefGoogle Scholar
  88. Yutzey KE, Rhodes SJ, Konieczny SF (1990): Differential trans activation associated with the muscle regulatory factors MyoDl, myogenin and MRF4. Mol Cell Biol 10:3934–3944.Google Scholar

Copyright information

© Birkhäuser Boston 1993

Authors and Affiliations

  • John J. Schwarz
  • James F. Martin
  • Eric N. Olson

There are no affiliations available

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