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. 1994 Aug 1;13(15):3580–3589. doi: 10.1002/j.1460-2075.1994.tb06665.x

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.

H Li 1, Y Capetanaki 1
PMCID: PMC395263  PMID: 8062833

Abstract

The first 85 nt upstream of the transcription initiation site of the mouse desmin gene, which contain an E box (E1), the binding site of the helix-loop-helix myogenic regulators, are sufficient to confer low level muscle-specific expression. High levels of desmin expression are due to an enhancer, located between nucleotides -798 and -976, which contains an additional E box (E2) and a muscle-specific enhancer factor-2 (MEF-2) binding site. We have previously shown that both myoD and myogenin can bind to the proximal (E1) and distal (E2) boxes. Here we demonstrate that MEF-2C, a myocyte-restricted member of the MEF-2 family, can bind to the desmin MEF-2 site. Functional units for the enhancer activity required intact E2 and MEF-2 elements. The desmin enhancer can function relatively well with either the E2 box or the MEF-2 site and only mutation of both eliminates transcriptional enhancement; the presence of both of these elements is required for maximum enhancer activity. On the other hand, mutagenesis of just the proximal E1 box showed that this element is essential for desmin gene expression. Double mutations of E1 with E2 or MEF-2 sites suggested that, to achieve high levels of desmin gene expression, E1 serves most possibly as an intermediary for either E2 or MEF-2 enhancer elements to function. The location of the E1 site relative to the TATA box is crucial. Its activity is DNA turn- and distance-dependent. Furthermore, this box seems to be the main element for desmin transactivation by myoD and myogenin in 10T1/2 cells. Its inactivation diminishes the transactivation by these factors; MRF4 and Myf5, however, can still partially function, possibly by using the distal E2 box.

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Selected References

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  1. Allen R. E., Rankin L. L., Greene E. A., Boxhorn L. K., Johnson S. E., Taylor R. G., Pierce P. R. Desmin is present in proliferating rat muscle satellite cells but not in bovine muscle satellite cells. J Cell Physiol. 1991 Dec;149(3):525–535. doi: 10.1002/jcp.1041490323. [DOI] [PubMed] [Google Scholar]
  2. Babai F., Musevi-Aghdam J., Schurch W., Royal A., Gabbiani G. Coexpression of alpha-sarcomeric actin, alpha-smooth muscle actin and desmin during myogenesis in rat and mouse embryos I. Skeletal muscle. Differentiation. 1990 Aug;44(2):132–142. doi: 10.1111/j.1432-0436.1990.tb00546.x. [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. Bennett G. S., Fellini S. A., Toyama Y., Holtzer H. Redistribution of intermediate filament subunits during skeletal myogenesis and maturation in vitro. J Cell Biol. 1979 Aug;82(2):577–584. doi: 10.1083/jcb.82.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bessereau J. L., Mendelzon D., LePoupon C., Fiszman M., Changeux J. P., Piette J. Muscle-specific expression of the acetylcholine receptor alpha-subunit gene requires both positive and negative interactions between myogenic factors, Sp1 and GBF factors. EMBO J. 1993 Feb;12(2):443–449. doi: 10.1002/j.1460-2075.1993.tb05676.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Block N. E., Miller J. B. Expression of MRF4, a myogenic helix-loop-helix protein, produces multiple changes in the myogenic program of BC3H-1 cells. Mol Cell Biol. 1992 Jun;12(6):2484–2492. doi: 10.1128/mcb.12.6.2484. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Borgmeyer U., Nowock J., Sippel A. E. The TGGCA-binding protein: a eukaryotic nuclear protein recognizing a symmetrical sequence on double-stranded linear DNA. Nucleic Acids Res. 1984 May 25;12(10):4295–4311. doi: 10.1093/nar/12.10.4295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. Breitbart R. E., Liang C. S., Smoot L. B., Laheru D. A., Mahdavi V., Nadal-Ginard B. A fourth human MEF2 transcription factor, hMEF2D, is an early marker of the myogenic lineage. Development. 1993 Aug;118(4):1095–1106. doi: 10.1242/dev.118.4.1095. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Capetanaki Y. G., Ngai J., Flytzanis C. N., Lazarides E. Tissue-specific expression of two mRNA species transcribed from a single vimentin gene. Cell. 1983 Dec;35(2 Pt 1):411–420. doi: 10.1016/0092-8674(83)90174-5. [DOI] [PubMed] [Google Scholar]
  13. Capetanaki Y. G., Ngai J., Lazarides E. Characterization and regulation in the expression of a gene coding for the intermediate filament protein desmin. Proc Natl Acad Sci U S A. 1984 Nov;81(22):6909–6913. doi: 10.1073/pnas.81.22.6909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Caravatti M., Minty A., Robert B., Montarras D., Weydert A., Cohen A., Daubas P., Buckingham M. Regulation of muscle gene expression. The accumulation of messenger RNAs coding for muscle-specific proteins during myogenesis in a mouse cell line. J Mol Biol. 1982 Sep;160(1):59–76. doi: 10.1016/0022-2836(82)90131-0. [DOI] [PubMed] [Google Scholar]
  15. Chakraborty T., Olson E. N. Domains outside of the DNA-binding domain impart target gene specificity to myogenin and MRF4. Mol Cell Biol. 1991 Dec;11(12):6103–6108. doi: 10.1128/mcb.11.12.6103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Chambers A. E., Kotecha S., Towers N., Mohun T. J. Muscle-specific expression of SRF-related genes in the early embryo of Xenopus laevis. EMBO J. 1992 Dec;11(13):4981–4991. doi: 10.1002/j.1460-2075.1992.tb05605.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Choi J., Costa M. L., Mermelstein C. S., Chagas C., Holtzer S., Holtzer H. MyoD converts primary dermal fibroblasts, chondroblasts, smooth muscle, and retinal pigmented epithelial cells into striated mononucleated myoblasts and multinucleated myotubes. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7988–7992. doi: 10.1073/pnas.87.20.7988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Chow K. L., Hogan M. E., Schwartz R. J. Phased cis-acting promoter elements interact at short distances to direct avian skeletal alpha-actin gene transcription. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1301–1305. doi: 10.1073/pnas.88.4.1301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Cullen K. E., Kladde M. P., Seyfred M. A. Interaction between transcription regulatory regions of prolactin chromatin. Science. 1993 Jul 9;261(5118):203–206. doi: 10.1126/science.8327891. [DOI] [PubMed] [Google Scholar]
  21. 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]
  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. Edmondson D. G., Olson E. N. Helix-loop-helix proteins as regulators of muscle-specific transcription. J Biol Chem. 1993 Jan 15;268(2):755–758. [PubMed] [Google Scholar]
  24. Farrance I. K., Mar J. H., Ordahl C. P. M-CAT binding factor is related to the SV40 enhancer binding factor, TEF-1. J Biol Chem. 1992 Aug 25;267(24):17234–17240. [PubMed] [Google Scholar]
  25. Fujisawa-Sehara A., Nabeshima Y., Komiya T., Uetsuki T., Asakura A., Nabeshima Y. Differential trans-activation of muscle-specific regulatory elements including the mysosin light chain box by chicken MyoD, myogenin, and MRF4. J Biol Chem. 1992 May 15;267(14):10031–10038. [PubMed] [Google Scholar]
  26. 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]
  27. Fürst D. O., Osborn M., Weber K. Myogenesis in the mouse embryo: differential onset of expression of myogenic proteins and the involvement of titin in myofibril assembly. J Cell Biol. 1989 Aug;109(2):517–527. doi: 10.1083/jcb.109.2.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gard D. L., Lazarides E. The synthesis and distribution of desmin and vimentin during myogenesis in vitro. Cell. 1980 Jan;19(1):263–275. doi: 10.1016/0092-8674(80)90408-0. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. Gunning P., Hardeman E., Wade R., Ponte P., Bains W., Blau H. M., Kedes L. Differential patterns of transcript accumulation during human myogenesis. Mol Cell Biol. 1987 Nov;7(11):4100–4114. doi: 10.1128/mcb.7.11.4100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hayward L. J., Schwartz R. J. Sequential expression of chicken actin genes during myogenesis. J Cell Biol. 1986 Apr;102(4):1485–1493. doi: 10.1083/jcb.102.4.1485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hill C. S., Duran S., Lin Z. X., Weber K., Holtzer H. Titin and myosin, but not desmin, are linked during myofibrillogenesis in postmitotic mononucleated myoblasts. J Cell Biol. 1986 Dec;103(6 Pt 1):2185–2196. doi: 10.1083/jcb.103.6.2185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hochschild A., Ptashne M. Cooperative binding of lambda repressors to sites separated by integral turns of the DNA helix. Cell. 1986 Mar 14;44(5):681–687. doi: 10.1016/0092-8674(86)90833-0. [DOI] [PubMed] [Google Scholar]
  35. Kaufman S. J., Foster R. F. Replicating myoblasts express a muscle-specific phenotype. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9606–9610. doi: 10.1073/pnas.85.24.9606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Lee T. C., Chow K. L., Fang P., Schwartz R. J. Activation of skeletal alpha-actin gene transcription: the cooperative formation of serum response factor-binding complexes over positive cis-acting promoter serum response elements displaces a negative-acting nuclear factor enriched in replicating myoblasts and nonmyogenic cells. Mol Cell Biol. 1991 Oct;11(10):5090–5100. doi: 10.1128/mcb.11.10.5090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Leifer D., Krainc D., Yu Y. T., McDermott J., Breitbart R. E., Heng J., Neve R. L., Kosofsky B., Nadal-Ginard B., Lipton S. A. MEF2C, a MADS/MEF2-family transcription factor expressed in a laminar distribution in cerebral cortex. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1546–1550. doi: 10.1073/pnas.90.4.1546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Li H., Capetanaki Y. Regulation of the mouse desmin gene: transactivated by MyoD, myogenin, MRF4 and Myf5. Nucleic Acids Res. 1993 Jan 25;21(2):335–343. doi: 10.1093/nar/21.2.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Li H., Choudhary S. K., Milner D. J., Munir M. I., Kuisk I. R., Capetanaki Y. Inhibition of desmin expression blocks myoblast fusion and interferes with the myogenic regulators MyoD and myogenin. J Cell Biol. 1994 Mar;124(5):827–841. doi: 10.1083/jcb.124.5.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Li Z. L., Paulin D. High level desmin expression depends on a muscle-specific enhancer. J Biol Chem. 1991 Apr 5;266(10):6562–6570. [PubMed] [Google Scholar]
  43. Li Z., Paulin D. Different factors interact with myoblast-specific and myotube-specific enhancer regions of the human desmin gene. J Biol Chem. 1993 May 15;268(14):10403–10415. [PubMed] [Google Scholar]
  44. 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]
  45. Lyons G. E., Mühlebach S., Moser A., Masood R., Paterson B. M., Buckingham M. E., Perriard J. C. Developmental regulation of creatine kinase gene expression by myogenic factors in embryonic mouse and chick skeletal muscle. Development. 1991 Nov;113(3):1017–1029. doi: 10.1242/dev.113.3.1017. [DOI] [PubMed] [Google Scholar]
  46. Mar J. H., Ordahl C. P. A conserved CATTCCT motif is required for skeletal muscle-specific activity of the cardiac troponin T gene promoter. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6404–6408. doi: 10.1073/pnas.85.17.6404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Martin J. F., Miano J. M., Hustad C. M., Copeland N. G., Jenkins N. A., Olson E. N. A Mef2 gene that generates a muscle-specific isoform via alternative mRNA splicing. Mol Cell Biol. 1994 Mar;14(3):1647–1656. doi: 10.1128/mcb.14.3.1647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Martin J. F., Schwarz J. J., Olson E. N. Myocyte enhancer factor (MEF) 2C: a tissue-restricted member of the MEF-2 family of transcription factors. Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5282–5286. doi: 10.1073/pnas.90.11.5282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Mayo M. L., Bringas P., Jr, Santos V., Shum L., Slavkin H. C. Desmin expression during early mouse tongue morphogenesis. Int J Dev Biol. 1992 Jun;36(2):255–263. [PubMed] [Google Scholar]
  50. McDermott J. C., Cardoso M. C., Yu Y. T., Andres V., Leifer D., Krainc D., Lipton S. A., Nadal-Ginard B. hMEF2C gene encodes skeletal muscle- and brain-specific transcription factors. Mol Cell Biol. 1993 Apr;13(4):2564–2577. doi: 10.1128/mcb.13.4.2564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. 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]
  52. 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]
  53. 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]
  54. 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]
  55. Olson E. N., Capetanaki Y. G. Developmental regulation of intermediate filament and actin mRNAs during myogenesis is disrupted by oncogenic ras genes. Oncogene. 1989 Jul;4(7):907–913. [PubMed] [Google Scholar]
  56. 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]
  57. Olson E. N. Regulation of muscle transcription by the MyoD family. The heart of the matter. Circ Res. 1993 Jan;72(1):1–6. doi: 10.1161/01.res.72.1.1. [DOI] [PubMed] [Google Scholar]
  58. Paterson B. M., Eldridge J. D. alpha-Cardiac actin is the major sarcomeric isoform expressed in embryonic avian skeletal muscle. Science. 1984 Jun 29;224(4656):1436–1438. doi: 10.1126/science.6729461. [DOI] [PubMed] [Google Scholar]
  59. Pieper F. R., Slobbe R. L., Ramaekers F. C., Cuypers H. T., Bloemendal H. Upstream regions of the hamster desmin and vimentin genes regulate expression during in vitro myogenesis. EMBO J. 1987 Dec 1;6(12):3611–3618. doi: 10.1002/j.1460-2075.1987.tb02692.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. 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]
  61. 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]
  62. Roy A. L., Carruthers C., Gutjahr T., Roeder R. G. Direct role for Myc in transcription initiation mediated by interactions with TFII-I. Nature. 1993 Sep 23;365(6444):359–361. doi: 10.1038/365359a0. [DOI] [PubMed] [Google Scholar]
  63. Roy A. L., Meisterernst M., Pognonec P., Roeder R. G. Cooperative interaction of an initiator-binding transcription initiation factor and the helix-loop-helix activator USF. Nature. 1991 Nov 21;354(6350):245–248. doi: 10.1038/354245a0. [DOI] [PubMed] [Google Scholar]
  64. Sadowski I., Ma J., Triezenberg S., Ptashne M. GAL4-VP16 is an unusually potent transcriptional activator. Nature. 1988 Oct 6;335(6190):563–564. doi: 10.1038/335563a0. [DOI] [PubMed] [Google Scholar]
  65. 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]
  66. Schaart G., Viebahn C., Langmann W., Ramaekers F. Desmin and titin expression in early postimplantation mouse embryos. Development. 1989 Nov;107(3):585–596. doi: 10.1242/dev.107.3.585. [DOI] [PubMed] [Google Scholar]
  67. Schwartz R. J., Rothblum K. N. Gene switching in myogenesis: differential expression of the chicken actin multigene family. Biochemistry. 1981 Jul 7;20(14):4122–4129. doi: 10.1021/bi00517a027. [DOI] [PubMed] [Google Scholar]
  68. Schwarz-Sommer Z., Hue I., Huijser P., Flor P. J., Hansen R., Tetens F., Lönnig W. E., Saedler H., Sommer H. Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development. EMBO J. 1992 Jan;11(1):251–263. doi: 10.1002/j.1460-2075.1992.tb05048.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Takahashi K., Vigneron M., Matthes H., Wildeman A., Zenke M., Chambon P. Requirement of stereospecific alignments for initiation from the simian virus 40 early promoter. Nature. 1986 Jan 9;319(6049):121–126. doi: 10.1038/319121a0. [DOI] [PubMed] [Google Scholar]
  70. 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]
  71. 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]
  72. Yu Y. T., Breitbart R. E., Smoot L. B., Lee Y., Mahdavi V., Nadal-Ginard B. Human myocyte-specific enhancer factor 2 comprises a group of tissue-restricted MADS box transcription factors. Genes Dev. 1992 Sep;6(9):1783–1798. doi: 10.1101/gad.6.9.1783. [DOI] [PubMed] [Google Scholar]

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