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. 1992 Sep;12(9):3665–3677. doi: 10.1128/mcb.12.9.3665

Analysis of the myogenin promoter reveals an indirect pathway for positive autoregulation mediated by the muscle-specific enhancer factor MEF-2.

D G Edmondson 1, T C Cheng 1, P Cserjesi 1, T Chakraborty 1, E N Olson 1
PMCID: PMC360220  PMID: 1324403

Abstract

Transcriptional cascades that specify cell fate have been well described in invertebrates. In mammalian development, however, gene hierarchies involved in determination of cell lineage are not understood. With the recent cloning of the MyoD family of myogenic regulatory factors, a model system has become available with which to study the dynamics of muscle determination in mammalian development. Myogenin, along with other members of the MyoD gene family, possesses the apparent ability to redirect nonmuscle cells into the myogenic lineage. This ability appears to be due to the direct activation of an array of subordinate or downstream genes which are responsible for formation and function of the muscle contractile apparatus. Myogenin-directed transcription has been shown to occur through interaction with a DNA consensus sequence known as an E box (CANNTG) present in the control regions of numerous downstream genes. In addition to activating the transcription of subordinate genes, members of the MyoD family positively regulate their own expression and cross-activate one another's expression. These autoregulatory interactions have been suggested as a mechanism for induction and maintenance of the myogenic phenotype, but the molecular details of the autoregulatory circuits are undefined. Here we show that the myogenin promoter contains a binding site for the myocyte-specific enhancer-binding factor, MEF-2, which can function as an intermediary of myogenin autoactivation. Since MEF-2 can be induced by myogenin, these results suggest that myogenin and MEF-2 participate in a transcriptional cascade in which MEF-2, once induced by myogenin, acts to amplify and maintain the myogenic phenotype by acting as a positive regulator of myogenin expression.

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Selected References

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  1. Alonso M. C., Cabrera C. V. The achaete-scute gene complex of Drosophila melanogaster comprises four homologous genes. EMBO J. 1988 Aug;7(8):2585–2591. doi: 10.1002/j.1460-2075.1988.tb03108.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beckmann H., Su L. K., Kadesch T. TFE3: a helix-loop-helix protein that activates transcription through the immunoglobulin enhancer muE3 motif. Genes Dev. 1990 Feb;4(2):167–179. doi: 10.1101/gad.4.2.167. [DOI] [PubMed] [Google Scholar]
  3. Benezra R., Davis R. L., Lockshon D., Turner D. L., Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell. 1990 Apr 6;61(1):49–59. doi: 10.1016/0092-8674(90)90214-y. [DOI] [PubMed] [Google Scholar]
  4. Blackwell T. K., Weintraub H. Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science. 1990 Nov 23;250(4984):1104–1110. doi: 10.1126/science.2174572. [DOI] [PubMed] [Google Scholar]
  5. Bober E., Lyons G. E., Braun T., Cossu G., Buckingham M., Arnold H. H. The muscle regulatory gene, Myf-6, has a biphasic pattern of expression during early mouse development. J Cell Biol. 1991 Jun;113(6):1255–1265. doi: 10.1083/jcb.113.6.1255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Braun T., Bober E., Buschhausen-Denker G., Kohtz S., Grzeschik K. H., Arnold H. H., Kotz S. Differential expression of myogenic determination genes in muscle cells: possible autoactivation by the Myf gene products. EMBO J. 1989 Dec 1;8(12):3617–3625. doi: 10.1002/j.1460-2075.1989.tb08535.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Braun T., Bober E., Winter B., Rosenthal N., Arnold H. H. Myf-6, a new member of the human gene family of myogenic determination factors: evidence for a gene cluster on chromosome 12. EMBO J. 1990 Mar;9(3):821–831. doi: 10.1002/j.1460-2075.1990.tb08179.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Braun T., Buschhausen-Denker G., Bober E., Tannich E., Arnold H. H. A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO J. 1989 Mar;8(3):701–709. doi: 10.1002/j.1460-2075.1989.tb03429.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Braun T., Tannich E., Buschhausen-Denker G., Arnold H. H. Promoter upstream elements of the chicken cardiac myosin light-chain 2-A gene interact with trans-acting regulatory factors for muscle-specific transcription. Mol Cell Biol. 1989 Jun;9(6):2513–2525. doi: 10.1128/mcb.9.6.2513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brennan T. J., Chakraborty T., Olson E. N. Mutagenesis of the myogenin basic region identifies an ancient protein motif critical for activation of myogenesis. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5675–5679. doi: 10.1073/pnas.88.13.5675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brennan T. J., Edmondson D. G., Li L., Olson E. N. Transforming growth factor beta represses the actions of myogenin through a mechanism independent of DNA binding. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3822–3826. doi: 10.1073/pnas.88.9.3822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Brennan T. J., Edmondson D. G., Olson E. N. Aberrant regulation of MyoD1 contributes to the partially defective myogenic phenotype of BC3H1 cells. J Cell Biol. 1990 Apr;110(4):929–937. doi: 10.1083/jcb.110.4.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Brennan T. J., Olson E. N. Myogenin resides in the nucleus and acquires high affinity for a conserved enhancer element on heterodimerization. Genes Dev. 1990 Apr;4(4):582–595. doi: 10.1101/gad.4.4.582. [DOI] [PubMed] [Google Scholar]
  14. Buskin J. N., Hauschka S. D. Identification of a myocyte nuclear factor that binds to the muscle-specific enhancer of the mouse muscle creatine kinase gene. Mol Cell Biol. 1989 Jun;9(6):2627–2640. doi: 10.1128/mcb.9.6.2627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Caudy M., Vässin H., Brand M., Tuma R., Jan L. Y., Jan Y. N. daughterless, a Drosophila gene essential for both neurogenesis and sex determination, has sequence similarities to myc and the achaete-scute complex. Cell. 1988 Dec 23;55(6):1061–1067. doi: 10.1016/0092-8674(88)90250-4. [DOI] [PubMed] [Google Scholar]
  16. Chakraborty T., Brennan T. J., Li L., Edmondson D., Olson E. N. Inefficient homooligomerization contributes to the dependence of myogenin on E2A products for efficient DNA binding. Mol Cell Biol. 1991 Jul;11(7):3633–3641. doi: 10.1128/mcb.11.7.3633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Chakraborty T., Brennan T., Olson E. Differential trans-activation of a muscle-specific enhancer by myogenic helix-loop-helix proteins is separable from DNA binding. J Biol Chem. 1991 Feb 15;266(5):2878–2882. [PubMed] [Google Scholar]
  18. Cserjesi P., Olson E. N. Myogenin induces the myocyte-specific enhancer binding factor MEF-2 independently of other muscle-specific gene products. Mol Cell Biol. 1991 Oct;11(10):4854–4862. doi: 10.1128/mcb.11.10.4854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Davis R. L., Cheng P. F., Lassar A. B., Weintraub H. The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell. 1990 Mar 9;60(5):733–746. doi: 10.1016/0092-8674(90)90088-v. [DOI] [PubMed] [Google Scholar]
  20. Davis R. L., Weintraub H., Lassar A. B. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell. 1987 Dec 24;51(6):987–1000. doi: 10.1016/0092-8674(87)90585-x. [DOI] [PubMed] [Google Scholar]
  21. Edmondson D. G., Brennan T. J., Olson E. N. Mitogenic repression of myogenin autoregulation. J Biol Chem. 1991 Nov 15;266(32):21343–21346. [PubMed] [Google Scholar]
  22. Edmondson D. G., Olson E. N. 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. 1989 May;3(5):628–640. doi: 10.1101/gad.3.5.628. [DOI] [PubMed] [Google Scholar]
  23. French B. A., Chow K. L., Olson E. N., Schwartz R. J. Heterodimers of myogenic helix-loop-helix regulatory factors and E12 bind a complex element governing myogenic induction of the avian cardiac alpha-actin promoter. Mol Cell Biol. 1991 May;11(5):2439–2450. doi: 10.1128/mcb.11.5.2439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gossett L. A., Kelvin D. J., Sternberg E. A., Olson E. N. A new myocyte-specific enhancer-binding factor that recognizes a conserved element associated with multiple muscle-specific genes. Mol Cell Biol. 1989 Nov;9(11):5022–5033. doi: 10.1128/mcb.9.11.5022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gregor P. D., Sawadogo M., Roeder R. G. The adenovirus major late transcription factor USF is a member of the helix-loop-helix group of regulatory proteins and binds to DNA as a dimer. Genes Dev. 1990 Oct;4(10):1730–1740. doi: 10.1101/gad.4.10.1730. [DOI] [PubMed] [Google Scholar]
  26. Gronostajski R. M., Adhya S., Nagata K., Guggenheimer R. A., Hurwitz J. Site-specific DNA binding of nuclear factor I: analyses of cellular binding sites. Mol Cell Biol. 1985 May;5(5):964–971. doi: 10.1128/mcb.5.5.964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Harvey R. P. The Xenopus MyoD gene: an unlocalised maternal mRNA predates lineage-restricted expression in the early embryo. Development. 1990 Apr;108(4):669–680. doi: 10.1242/dev.108.4.669. [DOI] [PubMed] [Google Scholar]
  28. Henthorn P., Kiledjian M., Kadesch T. Two distinct transcription factors that bind the immunoglobulin enhancer microE5/kappa 2 motif. Science. 1990 Jan 26;247(4941):467–470. doi: 10.1126/science.2105528. [DOI] [PubMed] [Google Scholar]
  29. Hinterberger T. J., Sassoon D. A., Rhodes S. J., Konieczny S. F. Expression of the muscle regulatory factor MRF4 during somite and skeletal myofiber development. Dev Biol. 1991 Sep;147(1):144–156. doi: 10.1016/s0012-1606(05)80014-4. [DOI] [PubMed] [Google Scholar]
  30. Hiromi Y., Gehring W. J. Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell. 1987 Sep 11;50(6):963–974. doi: 10.1016/0092-8674(87)90523-x. [DOI] [PubMed] [Google Scholar]
  31. Hopwood N. D., Pluck A., Gurdon J. B. MyoD expression in the forming somites is an early response to mesoderm induction in Xenopus embryos. EMBO J. 1989 Nov;8(11):3409–3417. doi: 10.1002/j.1460-2075.1989.tb08505.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Horlick R. A., Hobson G. M., Patterson J. H., Mitchell M. T., Benfield P. A. Brain and muscle creatine kinase genes contain common TA-rich recognition protein-binding regulatory elements. Mol Cell Biol. 1990 Sep;10(9):4826–4836. doi: 10.1128/mcb.10.9.4826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hu J. S., Olson E. N., Kingston R. E. HEB, a helix-loop-helix protein related to E2A and ITF2 that can modulate the DNA-binding ability of myogenic regulatory factors. Mol Cell Biol. 1992 Mar;12(3):1031–1042. doi: 10.1128/mcb.12.3.1031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hu Y. F., Lüscher B., Admon A., Mermod N., Tjian R. Transcription factor AP-4 contains multiple dimerization domains that regulate dimer specificity. Genes Dev. 1990 Oct;4(10):1741–1752. doi: 10.1101/gad.4.10.1741. [DOI] [PubMed] [Google Scholar]
  35. Jones P. A., Wolkowicz M. J., Rideout W. M., 3rd, Gonzales F. A., Marziasz C. M., Coetzee G. A., Tapscott S. J. De novo methylation of the MyoD1 CpG island during the establishment of immortal cell lines. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6117–6121. doi: 10.1073/pnas.87.16.6117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Krause M., Fire A., Harrison S. W., Priess J., Weintraub H. CeMyoD accumulation defines the body wall muscle cell fate during C. elegans embryogenesis. Cell. 1990 Nov 30;63(5):907–919. doi: 10.1016/0092-8674(90)90494-y. [DOI] [PubMed] [Google Scholar]
  37. Kuziora M. A., McGinnis W. Autoregulation of a Drosophila homeotic selector gene. Cell. 1988 Nov 4;55(3):477–485. doi: 10.1016/0092-8674(88)90034-7. [DOI] [PubMed] [Google Scholar]
  38. Lassar A. B., Buskin J. N., Lockshon D., Davis R. L., Apone S., Hauschka S. D., Weintraub H. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell. 1989 Sep 8;58(5):823–831. doi: 10.1016/0092-8674(89)90935-5. [DOI] [PubMed] [Google Scholar]
  39. Lassar A. B., Davis R. L., Wright W. E., Kadesch T., Murre C., Voronova A., Baltimore D., Weintraub H. Functional activity of myogenic HLH proteins requires hetero-oligomerization with E12/E47-like proteins in vivo. Cell. 1991 Jul 26;66(2):305–315. doi: 10.1016/0092-8674(91)90620-e. [DOI] [PubMed] [Google Scholar]
  40. Lassar A. B., Thayer M. J., Overell R. W., Weintraub H. Transformation by activated ras or fos prevents myogenesis by inhibiting expression of MyoD1. Cell. 1989 Aug 25;58(4):659–667. doi: 10.1016/0092-8674(89)90101-3. [DOI] [PubMed] [Google Scholar]
  41. Lin H., Yutzey K. E., Konieczny S. F. Muscle-specific expression of the troponin I gene requires interactions between helix-loop-helix muscle regulatory factors and ubiquitous transcription factors. Mol Cell Biol. 1991 Jan;11(1):267–280. doi: 10.1128/mcb.11.1.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Lin Z. Y., Dechesne C. A., Eldridge J., Paterson B. M. An avian muscle factor related to MyoD1 activates muscle-specific promoters in nonmuscle cells of different germ-layer origin and in BrdU-treated myoblasts. Genes Dev. 1989 Jul;3(7):986–996. doi: 10.1101/gad.3.7.986. [DOI] [PubMed] [Google Scholar]
  43. Mar J. H., Ordahl C. P. M-CAT binding factor, a novel trans-acting factor governing muscle-specific transcription. Mol Cell Biol. 1990 Aug;10(8):4271–4283. doi: 10.1128/mcb.10.8.4271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Michelson A. M., Abmayr S. M., Bate M., Arias A. M., Maniatis T. Expression of a MyoD family member prefigures muscle pattern in Drosophila embryos. Genes Dev. 1990 Dec;4(12A):2086–2097. doi: 10.1101/gad.4.12a.2086. [DOI] [PubMed] [Google Scholar]
  45. Miner J. H., Wold B. Herculin, a fourth member of the MyoD family of myogenic regulatory genes. Proc Natl Acad Sci U S A. 1990 Feb;87(3):1089–1093. doi: 10.1073/pnas.87.3.1089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Minty A., Kedes L. 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. 1986 Jun;6(6):2125–2136. doi: 10.1128/mcb.6.6.2125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Montarras D., Pinset C., Chelly J., Kahn A., Gros F. Expression of MyoD1 coincides with terminal differentiation in determined but inducible muscle cells. EMBO J. 1989 Aug;8(8):2203–2207. doi: 10.1002/j.1460-2075.1989.tb08343.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Murre C., McCaw P. S., Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell. 1989 Mar 10;56(5):777–783. doi: 10.1016/0092-8674(89)90682-x. [DOI] [PubMed] [Google Scholar]
  49. Murre C., McCaw P. S., Vaessin H., Caudy M., Jan L. Y., Jan Y. N., Cabrera C. V., Buskin J. N., Hauschka S. D., Lassar A. B. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell. 1989 Aug 11;58(3):537–544. doi: 10.1016/0092-8674(89)90434-0. [DOI] [PubMed] [Google Scholar]
  50. Murre C., Voronova A., Baltimore D. B-cell- and myocyte-specific E2-box-binding factors contain E12/E47-like subunits. Mol Cell Biol. 1991 Feb;11(2):1156–1160. doi: 10.1128/mcb.11.2.1156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Navankasattusas S., Zhu H., Garcia A. V., Evans S. M., Chien K. R. A ubiquitous factor (HF-1a) and a distinct muscle factor (HF-1b/MEF-2) form an E-box-independent pathway for cardiac muscle gene expression. Mol Cell Biol. 1992 Apr;12(4):1469–1479. doi: 10.1128/mcb.12.4.1469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Nordheim A., Rich A. The sequence (dC-dA)n X (dG-dT)n forms left-handed Z-DNA in negatively supercoiled plasmids. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1821–1825. doi: 10.1073/pnas.80.7.1821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Olson E. N. MyoD family: a paradigm for development? Genes Dev. 1990 Sep;4(9):1454–1461. doi: 10.1101/gad.4.9.1454. [DOI] [PubMed] [Google Scholar]
  54. Ott M. O., Bober E., Lyons G., Arnold H., Buckingham M. Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development. 1991 Apr;111(4):1097–1107. doi: 10.1242/dev.111.4.1097. [DOI] [PubMed] [Google Scholar]
  55. Paterson B. M., Walldorf U., Eldridge J., Dübendorfer A., Frasch M., Gehring W. J. The Drosophila homologue of vertebrate myogenic-determination genes encodes a transiently expressed nuclear protein marking primary myogenic cells. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3782–3786. doi: 10.1073/pnas.88.9.3782. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Piette J., Bessereau J. L., Huchet M., Changeux J. P. Two adjacent MyoD1-binding sites regulate expression of the acetylcholine receptor alpha-subunit gene. Nature. 1990 May 24;345(6273):353–355. doi: 10.1038/345353a0. [DOI] [PubMed] [Google Scholar]
  57. Pinney D. F., Pearson-White S. H., Konieczny S. F., Latham K. E., Emerson C. P., Jr Myogenic lineage determination and differentiation: evidence for a regulatory gene pathway. Cell. 1988 Jun 3;53(5):781–793. doi: 10.1016/0092-8674(88)90095-5. [DOI] [PubMed] [Google Scholar]
  58. Pollock R., Treisman R. Human SRF-related proteins: DNA-binding properties and potential regulatory targets. Genes Dev. 1991 Dec;5(12A):2327–2341. doi: 10.1101/gad.5.12a.2327. [DOI] [PubMed] [Google Scholar]
  59. Rhodes S. J., Konieczny S. F. Identification of MRF4: a new member of the muscle regulatory factor gene family. Genes Dev. 1989 Dec;3(12B):2050–2061. doi: 10.1101/gad.3.12b.2050. [DOI] [PubMed] [Google Scholar]
  60. Salminen A., Braun T., Buchberger A., Jürs S., Winter B., Arnold H. H. Transcription of the muscle regulatory gene Myf4 is regulated by serum components, peptide growth factors and signaling pathways involving G proteins. J Cell Biol. 1991 Nov;115(4):905–917. doi: 10.1083/jcb.115.4.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sartorelli V., Webster K. A., Kedes L. Muscle-specific expression of the cardiac alpha-actin gene requires MyoD1, CArG-box binding factor, and Sp1. Genes Dev. 1990 Oct;4(10):1811–1822. doi: 10.1101/gad.4.10.1811. [DOI] [PubMed] [Google Scholar]
  62. Sassoon D., Lyons G., Wright W. E., Lin V., Lassar A., Weintraub H., Buckingham M. Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis. Nature. 1989 Sep 28;341(6240):303–307. doi: 10.1038/341303a0. [DOI] [PubMed] [Google Scholar]
  63. Scales J. B., Olson E. N., Perry M. Two distinct Xenopus genes with homology to MyoD1 are expressed before somite formation in early embryogenesis. Mol Cell Biol. 1990 Apr;10(4):1516–1524. doi: 10.1128/mcb.10.4.1516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Schwarz J. J., Chakraborty T., Martin J., Zhou J. M., Olson E. N. The basic region of myogenin cooperates with two transcription activation domains to induce muscle-specific transcription. Mol Cell Biol. 1992 Jan;12(1):266–275. doi: 10.1128/mcb.12.1.266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Sternberg E. A., Spizz G., Perry W. M., Vizard D., Weil T., Olson E. N. 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. 1988 Jul;8(7):2896–2909. doi: 10.1128/mcb.8.7.2896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Tapscott S. J., Lassar A. B., Davis R. L., Weintraub H. 5-bromo-2'-deoxyuridine blocks myogenesis by extinguishing expression of MyoD1. Science. 1989 Aug 4;245(4917):532–536. doi: 10.1126/science.2547249. [DOI] [PubMed] [Google Scholar]
  67. Tapscott S. J., Weintraub H. MyoD and the regulation of myogenesis by helix-loop-helix proteins. J Clin Invest. 1991 Apr;87(4):1133–1138. doi: 10.1172/JCI115109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Thayer M. J., Tapscott S. J., Davis R. L., Wright W. E., Lassar A. B., Weintraub H. Positive autoregulation of the myogenic determination gene MyoD1. Cell. 1989 Jul 28;58(2):241–248. doi: 10.1016/0092-8674(89)90838-6. [DOI] [PubMed] [Google Scholar]
  69. Thompson W. R., Nadal-Ginard B., Mahdavi V. A MyoD1-independent muscle-specific enhancer controls the expression of the beta-myosin heavy chain gene in skeletal and cardiac muscle cells. J Biol Chem. 1991 Nov 25;266(33):22678–22688. [PubMed] [Google Scholar]
  70. Venuti J. M., Goldberg L., Chakraborty T., Olson E. N., Klein W. H. A myogenic factor from sea urchin embryos capable of programming muscle differentiation in mammalian cells. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6219–6223. doi: 10.1073/pnas.88.14.6219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Voronova A., Baltimore D. Mutations that disrupt DNA binding and dimer formation in the E47 helix-loop-helix protein map to distinct domains. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4722–4726. doi: 10.1073/pnas.87.12.4722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Weintraub H., Davis R., Lockshon D., Lassar A. MyoD binds cooperatively to two sites in a target enhancer sequence: occupancy of two sites is required for activation. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5623–5627. doi: 10.1073/pnas.87.15.5623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Wentworth B. M., Donoghue M., Engert J. C., Berglund E. B., Rosenthal N. Paired MyoD-binding sites regulate myosin light chain gene expression. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1242–1246. doi: 10.1073/pnas.88.4.1242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Wright W. E., Binder M., Funk W. Cyclic amplification and selection of targets (CASTing) for the myogenin consensus binding site. Mol Cell Biol. 1991 Aug;11(8):4104–4110. doi: 10.1128/mcb.11.8.4104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Wright W. E., Sassoon D. A., Lin V. K. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell. 1989 Feb 24;56(4):607–617. doi: 10.1016/0092-8674(89)90583-7. [DOI] [PubMed] [Google Scholar]
  76. Yaffe D., Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 1977 Dec 22;270(5639):725–727. doi: 10.1038/270725a0. [DOI] [PubMed] [Google Scholar]
  77. de Vries E., van Driel W., van den Heuvel S. J., van der Vliet P. C. Contactpoint analysis of the HeLa nuclear factor I recognition site reveals symmetrical binding at one side of the DNA helix. EMBO J. 1987 Jan;6(1):161–168. doi: 10.1002/j.1460-2075.1987.tb04734.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. de la Brousse F. C., Emerson C. P., Jr Localized expression of a myogenic regulatory gene, qmf1, in the somite dermatome of avian embryos. Genes Dev. 1990 Apr;4(4):567–581. doi: 10.1101/gad.4.4.567. [DOI] [PubMed] [Google Scholar]

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