Tissue-restricted expression of the cardiac α-myosin heavy chain gene is controlled by a downstream repressor element containing a palindrome of two Ets-binding sites

Molecular and Cellular Biology

Volumn 18, Issue 12, 1998, Pages 7243-7258

  Gupta, Madhu ^a,b   Zak, Radovan ^c   Libermann, Towia A ^d   Gupta, Mahesh P ^c  

^a ADVOCATE CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d HARVARD INSTITUTES OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN HEAVY CHAIN; PALINDROMIC DNA; TRANSCRIPTION FACTOR;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; DNA FOOTPRINTING; FETUS; GENE DELETION; GENE EXPRESSION REGULATION; GENE FUNCTION; HEART; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; RAT; REPRESSOR GENE; TISSUE SPECIFICITY;

ANIMALIA; TRIXIS;

EID: 0031785073     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.18.12.7243     Document Type: Article

References (75)

1. Ausoni, S., M. Campione, A. Picard, P. Moretti, M. Vitadello, C. D. Nardi, and S. Schiaffino. 1994. Structure and regulation of the mouse cardiac troponin I gene. J. Biol. Chem. 269:339-346.
2. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1994. Current protocols in molecular biology, vol. 1. Green Publishing Associates, Inc., and J. Wiley & Sons, Inc., New York, N.Y.
3. Bishopric, N. E., and L. Kedes. 1991. Adrenergic regulation of the skeletal α-actin gene promoter during myocardial cell hypertrophy. Proc. Natl. Acad. Sci. USA 88:2132-2136.
4. Bradford, A. P., C. Wasylyk, B. Wasylyk, and A. Gutierrez-Hartmann. 1997. Interaction of Ets-1 and the POU-homeodomain protein GHF-I/Pit-1 reconstitutes pituitary-specific gene expression. Mol. Cell. Biol. 17:1065-1074.
5. Buttrick, P. M., M. L. Kaplan, R. N. Kitsis, and L. A. Leinwand. 1993. Distinct behavior of cardiac myosin heavy chain gene constructs in vivo: discordance with in vitro results. Circ. Res. 72:1211-1217.
6. Chassagne, C., C. Wisnewsky, and K. Shwartz. 1993. Antithetical accumulation of myosin heavy chain but not α-actin mRNA isoforms during early stages of pressure overload-induced rat cardiac hypertrophy. Circ. Res. 72: 857-864.
7. Conard, K. E., J. M. Oberwetter, R. Vaillancourt, G. L. Johnson, and A. Gutierrez-Hartmann. 1994. Identification of the functional components of the Ras signaling pathway regulating pituitary cell-specific gene expression. Mol. Cell. Biol. 14:1553-1565.
8. Cowell, I. G. 1994. Repression versus activation in the control of gene transcription. Trends Biochem. Sci. 19:38-92.
9. Cribbs, L. L., N. Shimizu, C. E. Yockey, S. Jakovcic, and P. K. Umeda. 1988. Differential regulation of cardiac myosin heavy chain gene promoters, p. 280-283. In W. A. Clark, R. S. Decker, and T. K. Borg (ed.), Biology of isolated adult cardiac myocytes. Elsevier Science Publishing, Inc., New York, N.Y.
10. Cribbs, L. L., and P. K. Umeda. Unpublished data.
11. Dhar, M., E. M. Mascareno, and M. A. Q. Siddiqui. 1997. Two distinct factor-binding DNA elements in cardiac myosin light chain-2 gene are essential for repression of its expression in skeletal muscle. J. Biol. Chem. 272:18490-18497.
12. Eldridge, J., Z. Zehner, and B. M. Paterson. 1985. Nucleotide sequence of the chicken cardiac α-actin gene: absence of strong homologies in the promoter and 3′ untranslated regions with the skeletal α-actin sequence. Gene (Amsterdam) 36:55-63.
13. Garzon, R. J., and Z. H. Zehner. 1994. Multiple silencer elements are involved in regulating the chicken vimentin gene. Mol. Cell. Biol. 14:934-943.
14. Gulick, J., A. Subramaniam, J. Neumann, and J. Robbins. 1991. Isolation and characterization of the mouse cardiac myosin heavy chain genes. J. Biol. Chem. 266:9180-9185.
15. Gupta, M. P., C. S. Amin, M. Gupta, N. Hay, and R. Zak. 1997. Transcription enhancer factor-1 interacts with a basic helix-loop-helix protein, Max, for positive regulation of cardiac α-myosin heavy chain gene expression. Mol. Cell. Biol. 17:3924-3936.
16. Gupta, M. P., M. Gupta, and R. Zak. 1994. An E-box/M-CAT hybrid motif and cognate binding protein regulate the basal muscle-specific and cAMP-inducible expression of the rat cardiac α-myosin heavy chain gene. J. Biol. Chem. 269:29677-29687.
17. Gupta, M. P., M. Gupta, R. Zak, and V. P. Sukhatme. 1991. Egr-1, a serum-inducible zinc finger protein, regulates transcription of the rat cardiac α-myosin heavy chain gene. J. Biol. Chem. 266:12813-12816.
18. Hagemeier, C., A. J. Bannister, A. Cook, and T. Kouzarides. 1993. The activation domain of transcription factor PU.1 binds the retinoblastoma (RB) protein and the transcription factor TFIID in vitro: RB shows sequence similarity to TFIID and TFIIB. Proc. Natl. Acad. Sci. USA 90:1580-1584.
19. Henderson, S. A., M. Spencer, A. Sen, C. Kumar, M. A. Q. Siddiqui, and K. R. Chien. 1989. Structure, organization and expression of the rat cardiac myosin light chain-2 gene. J. Biol. Chem. 264:18142-18148.
20. Hidaka, K., I. Yamamoto, Y. Arai, and T. Mukai. 1993. The MEF-3 motif is required for MEF-2-mediated skeletal muscle-specific induction of the rat aldolase A gene. Mol. Cell. Biol. 13:6469-6478.
21. Hodge, D. R., L. Robinson, D. Watson, J. Lautenberger, X. K. Zhanag, M. Vananzoni, and A. Seth. 1996. Interaction of Ets-1 and ERGB/FLI-1 protein with DNA is modulated by spacing between multiple binding sites as well as phosphorylation. Oncogene 12:11-18.
22. Hu, M. C., S. B. Sharp, and N. Davidson. 1986. The complete sequence of the mouse skeletal α-actin gene reveals several conserved and inverted repeat sequence outside of the protein-coding region. Mol. Cell. Biol. 6:15-25.
23. Iannello, R. C., J. H. Mar, and C. P. Ordahl. 1991. Characterization of a promoter element required for transcription in myocardial cells. J. Biol. Chem. 266:3309-3316.
24. Izumo, S., B. Nadal-Ginard, and V. Mahdavi. 1986. All members of the myosin heavy chain multigene family respond to thyroid hormone in a highly tissue-specific manner. Science 231:597-600.
25. Janknecht, R., D. Monte, J. L. Baert, and Y. de Launoit. 1996. The Ets-related transcription factor ERM is a nuclear target of signalling cascades involving MAPK and PK-A. Oncogene 13:1745-1754.
26. Lee, Y., B. Nadal-Ginard, V. Mahdavi, and S. Izumo. 1997. Myocyte-specific enhancer factor-2 and thyroid hormone receptor associate and synergistically activate the α-myosin heavy chain gene. Mol. Cell. Biol. 17:2745-2755.
27. Liew, C. C., M. J. Sole, K. Y. Takihara, B. Kellan, D. H. Anderson, L. Lin, and J. C. Liew. 1990. Complete sequence and organization of the human cardiac β-myosin heavy chain gene. Nucleic Acids Res. 18:3647-3651.
28. Lopez, M., P. Oettgen, Y. Akbarali, U. Dendorfer, and T. A. Libermann. 1994. EPR, a new member of the Ets transcription factor/oncoprotein family: cloning, characterization, and differential expression during B-lymphocyte development. Mol. Cell. Biol. 14:3292-3309.
29. Lyons, G. E., S. Schiaffino, D. Sassoon, P. Barton, and M. Buckingham. 1990. Developmental regulation of myosin heavy chain gene expression in mouse cardiac muscle. J. Cell Biol. 111:2427-2436.
30. Kawana, M., S. I. Kimata, A. Taira, K. Hirosawa, H. Koyanagi, H. Hidetsugu, and Y. Vazaki. 1986. Isozymic changes in myosin of human ventricular myocardium induced by pressure overload. Circulation 74(Suppl. II):II-82. (Abstract 326.)
31. Mahdavi, V., A. P. Chambers, and B. Nadal-Ginard. 1984. Cardiac α-and β-myosin heavy chain genes are organized in tandem. Proc. Natl. Acad. Sci. USA 81:2628-2630.
32. Maira, S. M., J. M. Wurtz, and B. Wasylyk. 1996. Net (ERP/SAP-2) one of the Ras-inducible TCFs, has a novel inhibitory domain with resemblance to the helix-loop-helix motif. EMBO J. 15:5849-5865.
33. Maroulakou, I. G., T. S. Papas, and J. E. Green. 1994. Differential expression of ets-1 and ets-2 proto-oncogenes during murine embryogenesis. Oncogene 9:1551-1565.
34. McCully, J. D., R. X. Wang, B. Kellam, M. J. Sole, and C. C. Liew. 1991. Isolation and characterization of a previously unrecognized myosin heavy chain gene present in the Syrian hamster. J. Mol. Biol. 218:657-665.
35. Minty, A., and L. Kedes. 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.
36. Molkentin, J. D., D. V. Klavakolann, and B. E. Markham. 1994. Transcription factor GATA-4 regulates cardiac muscle specific expression of the α-myosin heavy chain gene. Mol. Cell. Biol. 14:4947-4957.
37. Molkentin, J. D., J. Lu, C. Antos, B. E. Markham, J. Richardson, J. Robbins, S. Grant, and E. Olson. 1998. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93:215-228.
38. Molkentin, J. D., and B. E. Markham. 1994. An M-CAT binding factor and an RSRF-related A-rich binding factor positively regulate expression of the α-cardiac myosin heavy chain gene in vivo. Mol. Cell. Biol. 14:5056-5065.
39. Molkentin, J. D., S. M. Jobe, and B. E. Markham. 1996. α-Myosin heavy chain gene regulation: delineation and characterization of the cardiac muscle specific enhancer and muscle-specific promoter. J. Mol. Cell. Cardiol. 28: 1211-1225.
40. + channel genes binds a factor present in non-neuronal cells but not in neuronal cells. Neuron 4:45-54.
41. Nakao, K., W. Minobe, R. Roden, R. M. Bristow, and L. A. Leinwand. 1997. Myosin heavy chain gene expression in the human heart failure. J. Clin. Investig. 100:2362-2370.
42. Nikovits, W. J., G. F. Wang, J. L. Feldman, J. B. Miller, R. Wade, L. Nelson, and F. E. Stockdale. 1996. Isolation and characterization of an avian slow myosin heavy chain gene expressed during embryonic skeletal muscle fiber formation. J. Biol. Chem. 271:17047-17056.
43. O'Hagan, R. C., R. G. Toze, M. Symons, F. McCormick, and J. A. Hassell. 1996. The activity of the Ets transcription factor PEA3 is regulated by two distinct MAPK cascades. Oncogene 13:1323-1333.
44. Ojamaa, K., A. M. Samarel, and I. Klein. 1996. Identification of a contractile response element in the cardiac α-myosin heavy chain gene. J. Biol. Chem. 270:31276-31281.
45. Parmacek, M. S., and J. M. Leiden. 1989. Structure and expression of the murine slow/cardiac troponin C gene. J. Biol. Chem. 264:13217-13225.
46. Patterson, D. 1987. The causes of Down's syndrome: the genes thought to be responsible for many of the pathologies associated with the disorder are being identified and mapped to sites on chromosome 21. Sci. Am. 257:52-60.
47. Pierce, J. W., A. M. Gifford, and D. Baltimore. 1991. Silencing of the expression of the immunoglobulin kappa gene in non-β cells. Mol. Cell. Biol. 11:1431-1437.
48. Price, M. A., A. E. Rogers, and R. Treisman. 1995. Comparative analysis of the ternary complex factors Elk-1, SAP-1a, and SAP-2 (ERP/NET). EMBO J. 14:2589-2601.
49. Rindt, H., J. Gulick, S. Knott, J. Neumann, and J. Robbins. 1993. In vivo analysis of the murine β-myosin heavy chain gene promoter. J. Biol. Chem. 268:5332-5338.
50. Robbins, J. 1996. Regulation of cardiac gene expression during development. Cardiovasc. Res. 31:E2-E16.
51. Rosen, G. D., J. L. Barks, M. F. Iademarco, R. J. Fisher, and D. C. Dean. 1994. An intricate arrangement of binding sites for the Ets family of transcription factors regulates activity of the α-4 integrin gene promoter. J. Biol Chem. 269:15652-15660.
52. Sadoshima, J., and S. Izumo. 1997. The cellular and molecular response of cardiac myocytes to mechanical stress. Annu. Rev. Physiol. 59:551-571.
53. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
54. Savagner, P., T. Miyashita, and Y. Yamada. 1990. Two silencers regulate the tissue-specific expression of collagen-II gene. J. Biol. Chem. 265:6669-6674.
55. Schneikert, J., H. Peterziel, P. A. Defossez, H. Klocker, Y. de Launoit, and A. C. B. Cato. 1996. Androgen receptor-Ets protein interaction is a novel mechanism for steroid hormone-mediated down-modulation of matrix metalloproteinase expression. J. Biol. Chem. 271:23907-23913.
56. Seidman, C. E., D. W. Wong, J. A. Jarcho, K. D. Bloch, and J. G. Seidman. 1988. cis-Acting sequences that modulate atrial natriuretic factor gene expression. Proc. Natl. Acad. Sci. USA 85:4104-4108.
57. Seth, A., L. Robinson, D. M. Thompson, D. K. Watson, and T. S. Papas. 1993. Transactivation of GATA-1 promoter with Ets-1, Ets-2 and ERGB/ Hu-FLI-1 proteins: stabilization of the Ets-1 protein binding on GATA-1 promoter sequences by monoclonal antibody. Oncogene 8:1783-1790.
58. Shen, R., S. K. Goswami, E. Mascareno, A. Kumar, and M. A. Q. Siddiqui. 1991. Tissue-specific transcription of the cardiac myosin light chain-2 gene is regulated by an upstream repressor element. Mol. Cell. Biol. 11:1676-1683.
59. Shimizu, N., G. Prior, P. K. Umeda, and R. Zak. 1992. Cis-acting elements responsible for muscle-specific expression of the myosin heavy chain β gene. Nucleic Acids Res. 20:1793-1799.
60. Sternberg, E. A., G. Spizz, W. M. Perry, D. Vizard, T. Weil, and E. N. Olson. 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.
61. Subramaniam, A., W. K. Jones, J. Gulick, S. Wert, J. Neumann, and J. Robbins. 1991. Tissue-specific regulation of the α-myosin heavy chain gene promoter in transgenic mice. J. Biol. Chem. 266:24613-24620.
62. Sumarsono, S., T. Wilson, M. Tymms, D. Venter, C. E. Kola, M. Lahoud, J. Papas, A. Seth, and I. Kola. 1996. Down's syndrome-like skeletal abnormalities in ETS-2 transgenic mice. Nature 379:534-537.
63. Takihara, K. Y., M. J. Sole, J. Liew, D. Ing, and C. C. Liew. 1989. Characterization of human cardiac myosin heavy chain genes. Proc. Natl. Acad. Sci. USA 86:3416-3417.
64. Taylor, J. M., E. E. Dupont-Versteegden, J. D. Davis, J. A. Hassell, J. D. Houle, C. M. Gurley, and C. A. Peterson. 1997. A role for the Ets domain transcription factor PEA3 in myogenic differentiation. Mol. Cell. Biol. 17: 5550-5558.
65. Thompson, C. B., C. Y. Wang, I. C. Ho, P. R. Bohjanen, B. Petryniak, C. H. June, S. Miesfeldt, L, Zhang, G. J. Nabel, B. Karpinski, and J. M. Leiden. 1992. cis-acting sequences required for inducible interleukin-2 enhancer function bind a novel Ets-related protein, Elf-1. Mol. Cell. Biol. 12:1043-1053.
66. Thompson, W. R., B. Nadal-Ginard, and V. Mahdavi. 1991. A MyoD-1-independent muscle-specific enhancer controls the expression of the β-myosin heavy chain gene in skeletal and cardiac muscle cells. J. Biol. Chem. 266:22678-22688.
67. Tsika, R. W., J. J. Gahl, L. A. Leinwand, and E. Morkin. 1990. Thyroid hormone regulates expression of a transfected human α-myosin heavy chain fusion gene in fetal rat heart cells. Proc. Natl. Acad. Sci. USA 87:379-383.
68. Umezawa, A., H. Yamamoto, K. Rhodes, M. J. Klemsz, R. A. Maki, and R. G. Oshima. 1997. Methylation of an EtS site in the intron enhancer of the keratin 18 gene participates in tissue-specific repression. Mol. Cell. Biol. 17:4885-4897.
69. Wang, C. Y., B. Petryniak, C. B. Thompson, W. G. Kaelin, and J. M. Leiden. 1993. Regulation of the Ets-related transcription factor Elf-1 by binding to the retinoblastoma protein. Science 260:1330-1335.
70. Wang, R., M. J. Sole, E. Cukerman, and C. C. Liew. 1994. Characterization and nucleotide sequence of the cardiac α-myosin heavy chain gene from Syrian hamster. J. Mol. Cell. Cardiol. 26:1155-1165.
71. Wasylyk, B., C. Wasylyk, P. Flores, A. Begue, D. Leprince, and D. Stehelin. 1990. The c-Ets proto-oncogene encodes transcription factors that co-operate with c-fos and c-Jun for transcriptional activation. Nature 346:191-193.
72. Wasylyk, B., S. L. Hahn, and A. Giovane. 1993. The Ets family of transcription factors. Eur. J. Biochem. 211:7-18.
73. Wasylyk, C., A. Gutman, R. Nicolson, and B. Wasylyk. 1991. The c-ets oncoprotein activates the stromelysin promoter through the same element as several non-nuclear oncoproteins. EMBO J. 10:1127-1137.
74. Whitmarsh, A. J., P. Shore, A. D. Sharrocks, and R. J. Davis. 1995. Integration of MAP-kinase signal transduction pathways at the serum response element. Science 269:403-407.
75. Winoto, A., and D. Baltimore. 1989. α,β lineage-specific expression of the α T cell receptor gene by nearby silencers. Cell 59:649-655.