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. 1996 Jul;16(7):3893–3900. doi: 10.1128/mcb.16.7.3893

Differences between MyoD DNA binding and activation site requirements revealed by functional random sequence selection.

J Huang 1, T K Blackwell 1, L Kedes 1, H Weintraub 1
PMCID: PMC231386  PMID: 8668207

Abstract

A method has been developed for selecting functional enhancer/promoter sites from random DNA sequences in higher eukaryotic cells. Of sequences that were thus selected for transcriptional activation by the muscle-specific basic helix-loop-helix protein MyoD, only a subset are similar to the preferred in vitro binding consensus, and in the same promoter context an optimal in vitro binding site was inactive. Other sequences with full transcriptional activity instead exhibit sequence preferences that, remarkably, are generally either identical or very similar to those found in naturally occurring muscle-specific promoters. This first systematic examination of the relation between DNA binding and transcriptional activation by basic helix-loop-helix proteins indicates that binding per se is necessary but not sufficient for transcriptional activation by MyoD and implies a requirement for other DNA sequence-dependent interactions or conformations at its binding site.

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Selected References

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  1. Aplan P. D., Nakahara K., Orkin S. H., Kirsch I. R. The SCL gene product: a positive regulator of erythroid differentiation. EMBO J. 1992 Nov;11(11):4073–4081. doi: 10.1002/j.1460-2075.1992.tb05500.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Auradé F., Pinset C., Chafey P., Gros F., Montarras D. Myf5, MyoD, myogenin and MRF4 myogenic derivatives of the embryonic mesenchymal cell line C3H10T1/2 exhibit the same adult muscle phenotype. Differentiation. 1994 Feb;55(3):185–192. doi: 10.1046/j.1432-0436.1994.5530185.x. [DOI] [PubMed] [Google Scholar]
  3. Bain G., Gruenwald S., Murre C. E2A and E2-2 are subunits of B-cell-specific E2-box DNA-binding proteins. Mol Cell Biol. 1993 Jun;13(6):3522–3529. doi: 10.1128/mcb.13.6.3522. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benezra R. An intermolecular disulfide bond stabilizes E2A homodimers and is required for DNA binding at physiological temperatures. Cell. 1994 Dec 16;79(6):1057–1067. doi: 10.1016/0092-8674(94)90036-1. [DOI] [PubMed] [Google Scholar]
  5. Black B. L., Martin J. F., Olson E. N. The mouse MRF4 promoter is trans-activated directly and indirectly by muscle-specific transcription factors. J Biol Chem. 1995 Feb 17;270(7):2889–2892. doi: 10.1074/jbc.270.7.2889. [DOI] [PubMed] [Google Scholar]
  6. Blackwell T. K., Huang J., Ma A., Kretzner L., Alt F. W., Eisenman R. N., Weintraub H. Binding of myc proteins to canonical and noncanonical DNA sequences. Mol Cell Biol. 1993 Sep;13(9):5216–5224. doi: 10.1128/mcb.13.9.5216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blackwell T. K. Selection of protein binding sites from random nucleic acid sequences. Methods Enzymol. 1995;254:604–618. doi: 10.1016/0076-6879(95)54043-1. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. Buckingham M. E. Muscle: the regulation of myogenesis. Curr Opin Genet Dev. 1994 Oct;4(5):745–751. doi: 10.1016/0959-437x(94)90142-p. [DOI] [PubMed] [Google Scholar]
  11. Chalfie M., Tu Y., Euskirchen G., Ward W. W., Prasher D. C. Green fluorescent protein as a marker for gene expression. Science. 1994 Feb 11;263(5148):802–805. doi: 10.1126/science.8303295. [DOI] [PubMed] [Google Scholar]
  12. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cheng T. C., Wallace M. C., Merlie J. P., Olson E. N. Separable regulatory elements governing myogenin transcription in mouse embryogenesis. Science. 1993 Jul 9;261(5118):215–218. doi: 10.1126/science.8392225. [DOI] [PubMed] [Google Scholar]
  14. Christensen T. H., Prentice H., Gahlmann R., Kedes L. Regulation of the human cardiac/slow-twitch troponin C gene by multiple, cooperative, cell-type-specific, and MyoD-responsive elements. Mol Cell Biol. 1993 Nov;13(11):6752–6765. doi: 10.1128/mcb.13.11.6752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Crescenzi M., Fleming T. P., Lassar A. B., Weintraub H., Aaronson S. A. MyoD induces growth arrest independent of differentiation in normal and transformed cells. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8442–8446. doi: 10.1073/pnas.87.21.8442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Davis R. L., Weintraub H. Acquisition of myogenic specificity by replacement of three amino acid residues from MyoD into E12. Science. 1992 May 15;256(5059):1027–1030. doi: 10.1126/science.1317057. [DOI] [PubMed] [Google Scholar]
  18. Desiderio S. Lymphopoiesis. Transcription factors controlling B-cell development. Curr Biol. 1995 Jun 1;5(6):605–608. doi: 10.1016/s0960-9822(95)00121-7. [DOI] [PubMed] [Google Scholar]
  19. Ellenberger T., Fass D., Arnaud M., Harrison S. C. Crystal structure of transcription factor E47: E-box recognition by a basic region helix-loop-helix dimer. Genes Dev. 1994 Apr 15;8(8):970–980. doi: 10.1101/gad.8.8.970. [DOI] [PubMed] [Google Scholar]
  20. Emerson C. P. Myogenesis and developmental control genes. Curr Opin Cell Biol. 1990 Dec;2(6):1065–1075. doi: 10.1016/0955-0674(90)90157-a. [DOI] [PubMed] [Google Scholar]
  21. Ferré-D'Amaré A. R., Prendergast G. C., Ziff E. B., Burley S. K. Recognition by Max of its cognate DNA through a dimeric b/HLH/Z domain. Nature. 1993 May 6;363(6424):38–45. doi: 10.1038/363038a0. [DOI] [PubMed] [Google Scholar]
  22. Fiering S. N., Roederer M., Nolan G. P., Micklem D. R., Parks D. R., Herzenberg L. A. Improved FACS-Gal: flow cytometric analysis and sorting of viable eukaryotic cells expressing reporter gene constructs. Cytometry. 1991;12(4):291–301. doi: 10.1002/cyto.990120402. [DOI] [PubMed] [Google Scholar]
  23. Fujisawa-Sehara A., Hanaoka K., Hayasaka M., Hiromasa-Yagami T., Nabeshima Y. Upstream region of the myogenin gene confers transcriptional activation in muscle cell lineages during mouse embryogenesis. Biochem Biophys Res Commun. 1993 Mar 15;191(2):351–356. doi: 10.1006/bbrc.1993.1224. [DOI] [PubMed] [Google Scholar]
  24. Funk W. D., Wright W. E. Cyclic amplification and selection of targets for multicomponent complexes: myogenin interacts with factors recognizing binding sites for basic helix-loop-helix, nuclear factor 1, myocyte-specific enhancer-binding factor 2, and COMP1 factor. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9484–9488. doi: 10.1073/pnas.89.20.9484. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Genetta T., Ruezinsky D., Kadesch T. Displacement of an E-box-binding repressor by basic helix-loop-helix proteins: implications for B-cell specificity of the immunoglobulin heavy-chain enhancer. Mol Cell Biol. 1994 Sep;14(9):6153–6163. doi: 10.1128/mcb.14.9.6153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gilmour B. P., Fanger G. R., Newton C., Evans S. M., Gardner P. D. Multiple binding sites for myogenic regulatory factors are required for expression of the acetylcholine receptor gamma-subunit gene. J Biol Chem. 1991 Oct 25;266(30):19871–19874. [PubMed] [Google Scholar]
  27. Gu W., Schneider J. W., Condorelli G., Kaushal S., Mahdavi V., Nadal-Ginard B. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell. 1993 Feb 12;72(3):309–324. doi: 10.1016/0092-8674(93)90110-c. [DOI] [PubMed] [Google Scholar]
  28. Halevy O., Novitch B. G., Spicer D. B., Skapek S. X., Rhee J., Hannon G. J., Beach D., Lassar A. B. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science. 1995 Feb 17;267(5200):1018–1021. doi: 10.1126/science.7863327. [DOI] [PubMed] [Google Scholar]
  29. Hanahan D., Jessee J., Bloom F. R. Plasmid transformation of Escherichia coli and other bacteria. Methods Enzymol. 1991;204:63–113. doi: 10.1016/0076-6879(91)04006-a. [DOI] [PubMed] [Google Scholar]
  30. Hasty P., Bradley A., Morris J. H., Edmondson D. G., Venuti J. M., Olson E. N., Klein W. H. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature. 1993 Aug 5;364(6437):501–506. doi: 10.1038/364501a0. [DOI] [PubMed] [Google Scholar]
  31. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. doi: 10.1016/0022-2836(67)90307-5. [DOI] [PubMed] [Google Scholar]
  32. Hollenberg S. M., Cheng P. F., Weintraub H. Use of a conditional MyoD transcription factor in studies of MyoD trans-activation and muscle determination. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8028–8032. doi: 10.1073/pnas.90.17.8028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hu J. C., O'Shea E. K., Kim P. S., Sauer R. T. Sequence requirements for coiled-coils: analysis with lambda repressor-GCN4 leucine zipper fusions. Science. 1990 Dec 7;250(4986):1400–1403. doi: 10.1126/science.2147779. [DOI] [PubMed] [Google Scholar]
  34. Jan Y. N., Jan L. Y. HLH proteins, fly neurogenesis, and vertebrate myogenesis. Cell. 1993 Dec 3;75(5):827–830. doi: 10.1016/0092-8674(93)90525-u. [DOI] [PubMed] [Google Scholar]
  35. Jaynes J. B., Johnson J. E., Buskin J. N., Gartside C. L., Hauschka S. D. The muscle creatine kinase gene is regulated by multiple upstream elements, including a muscle-specific enhancer. Mol Cell Biol. 1988 Jan;8(1):62–70. doi: 10.1128/mcb.8.1.62. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Jia H. T., Tsay H. J., Schmidt J. Analysis of binding and activating functions of the chick muscle acetylcholine receptor gamma-subunit upstream sequence. Cell Mol Neurobiol. 1992 Jun;12(3):241–258. doi: 10.1007/BF00712929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kadesch T. Helix-loop-helix proteins in the regulation of immunoglobulin gene transcription. Immunol Today. 1992 Jan;13(1):31–36. doi: 10.1016/0167-5699(92)90201-h. [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. Li H., Capetanaki Y. An E box in the desmin promoter cooperates with the E box and MEF-2 sites of a distal enhancer to direct muscle-specific transcription. EMBO J. 1994 Aug 1;13(15):3580–3589. doi: 10.1002/j.1460-2075.1994.tb06665.x. [DOI] [PMC free article] [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. Ma P. C., Rould M. A., Weintraub H., Pabo C. O. Crystal structure of MyoD bHLH domain-DNA complex: perspectives on DNA recognition and implications for transcriptional activation. Cell. 1994 May 6;77(3):451–459. doi: 10.1016/0092-8674(94)90159-7. [DOI] [PubMed] [Google Scholar]
  43. Maddon P. J., Littman D. R., Godfrey M., Maddon D. E., Chess L., Axel R. The isolation and nucleotide sequence of a cDNA encoding the T cell surface protein T4: a new member of the immunoglobulin gene family. Cell. 1985 Aug;42(1):93–104. doi: 10.1016/s0092-8674(85)80105-7. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. Molkentin J. D., Black B. L., Martin J. F., Olson E. N. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell. 1995 Dec 29;83(7):1125–1136. doi: 10.1016/0092-8674(95)90139-6. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. 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]
  48. Nabeshima Y., Hanaoka K., Hayasaka M., Esumi E., Li S., Nonaka I., Nabeshima Y. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature. 1993 Aug 5;364(6437):532–535. doi: 10.1038/364532a0. [DOI] [PubMed] [Google Scholar]
  49. Nelson C., Shen L. P., Meister A., Fodor E., Rutter W. J. Pan: a transcriptional regulator that binds chymotrypsin, insulin, and AP-4 enhancer motifs. Genes Dev. 1990 Jun;4(6):1035–1043. doi: 10.1101/gad.4.6.1035. [DOI] [PubMed] [Google Scholar]
  50. Neuhold L. A., Wold B. HLH forced dimers: tethering MyoD to E47 generates a dominant positive myogenic factor insulated from negative regulation by Id. Cell. 1993 Sep 24;74(6):1033–1042. doi: 10.1016/0092-8674(93)90725-6. [DOI] [PubMed] [Google Scholar]
  51. Nolan G. P., Fiering S., Nicolas J. F., Herzenberg L. A. Fluorescence-activated cell analysis and sorting of viable mammalian cells based on beta-D-galactosidase activity after transduction of Escherichia coli lacZ. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2603–2607. doi: 10.1073/pnas.85.8.2603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Oliphant A. R., Struhl K. Defining the consensus sequences of E.coli promoter elements by random selection. Nucleic Acids Res. 1988 Aug 11;16(15):7673–7683. doi: 10.1093/nar/16.15.7673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Olson E. N. Proto-oncogenes in the regulatory circuit for myogenesis. Semin Cell Biol. 1992 Apr;3(2):127–136. doi: 10.1016/s1043-4682(10)80022-4. [DOI] [PubMed] [Google Scholar]
  54. Pu W. T., Struhl K. Dimerization of leucine zippers analyzed by random selection. Nucleic Acids Res. 1993 Sep 11;21(18):4348–4355. doi: 10.1093/nar/21.18.4348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Rosenthal N., Berglund E. B., Wentworth B. M., Donoghue M., Winter B., Bober E., Braun T., Arnold H. H. A highly conserved enhancer downstream of the human MLC1/3 locus is a target for multiple myogenic determination factors. Nucleic Acids Res. 1990 Nov 11;18(21):6239–6246. doi: 10.1093/nar/18.21.6239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Rudnicki M. A., Schnegelsberg P. N., Stead R. H., Braun T., Arnold H. H., Jaenisch R. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell. 1993 Dec 31;75(7):1351–1359. doi: 10.1016/0092-8674(93)90621-v. [DOI] [PubMed] [Google Scholar]
  57. Sanes J. R., Rubenstein J. L., Nicolas J. F. Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J. 1986 Dec 1;5(12):3133–3142. doi: 10.1002/j.1460-2075.1986.tb04620.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. 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]
  60. Simon A. M., Burden S. J. An E box mediates activation and repression of the acetylcholine receptor delta-subunit gene during myogenesis. Mol Cell Biol. 1993 Sep;13(9):5133–5140. doi: 10.1128/mcb.13.9.5133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Singer V. L., Wobbe C. R., Struhl K. A wide variety of DNA sequences can functionally replace a yeast TATA element for transcriptional activation. Genes Dev. 1990 Apr;4(4):636–645. doi: 10.1101/gad.4.4.636. [DOI] [PubMed] [Google Scholar]
  62. Skerjanc I. S., McBurney M. W. The E box is essential for activity of the cardiac actin promoter in skeletal but not in cardiac muscle. Dev Biol. 1994 May;163(1):125–132. doi: 10.1006/dbio.1994.1128. [DOI] [PubMed] [Google Scholar]
  63. Sorrentino V., Pepperkok R., Davis R. L., Ansorge W., Philipson L. Cell proliferation inhibited by MyoD1 independently of myogenic differentiation. Nature. 1990 Jun 28;345(6278):813–815. doi: 10.1038/345813a0. [DOI] [PubMed] [Google Scholar]
  64. Sun X. H., Baltimore D. An inhibitory domain of E12 transcription factor prevents DNA binding in E12 homodimers but not in E12 heterodimers. Cell. 1991 Jan 25;64(2):459–470. doi: 10.1016/0092-8674(91)90653-g. [DOI] [PubMed] [Google Scholar]
  65. Szostak J. W. In vitro genetics. Trends Biochem Sci. 1992 Mar;17(3):89–93. doi: 10.1016/0968-0004(92)90242-2. [DOI] [PubMed] [Google Scholar]
  66. Tapscott S. J., Lassar A. B., Weintraub H. A novel myoblast enhancer element mediates MyoD transcription. Mol Cell Biol. 1992 Nov;12(11):4994–5003. doi: 10.1128/mcb.12.11.4994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. 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]
  68. Vara J., Malpartida F., Hopwood D. A., Jiménez A. Cloning and expression of a puromycin N-acetyl transferase gene from Streptomyces alboniger in Streptomyces lividans and Escherichia coli. Gene. 1985;33(2):197–206. doi: 10.1016/0378-1119(85)90094-0. [DOI] [PubMed] [Google Scholar]
  69. 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]
  70. 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]
  71. Weintraub H., Davis R., Tapscott S., Thayer M., Krause M., Benezra R., Blackwell T. K., Turner D., Rupp R., Hollenberg S. The myoD gene family: nodal point during specification of the muscle cell lineage. Science. 1991 Feb 15;251(4995):761–766. doi: 10.1126/science.1846704. [DOI] [PubMed] [Google Scholar]
  72. Weintraub H., Dwarki V. J., Verma I., Davis R., Hollenberg S., Snider L., Lassar A., Tapscott S. J. Muscle-specific transcriptional activation by MyoD. Genes Dev. 1991 Aug;5(8):1377–1386. doi: 10.1101/gad.5.8.1377. [DOI] [PubMed] [Google Scholar]
  73. Weintraub H., Genetta T., Kadesch T. Tissue-specific gene activation by MyoD: determination of specificity by cis-acting repression elements. Genes Dev. 1994 Sep 15;8(18):2203–2211. doi: 10.1101/gad.8.18.2203. [DOI] [PubMed] [Google Scholar]
  74. Weintraub H. The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell. 1993 Dec 31;75(7):1241–1244. doi: 10.1016/0092-8674(93)90610-3. [DOI] [PubMed] [Google Scholar]
  75. 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]
  76. 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]
  77. Zingg J. M., Pedraza-Alva G., Jost J. P. MyoD1 promoter autoregulation is mediated by two proximal E-boxes. Nucleic Acids Res. 1994 Jun 25;22(12):2234–2241. doi: 10.1093/nar/22.12.2234. [DOI] [PMC free article] [PubMed] [Google Scholar]

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