A positive GATA element and a negative vitamin D receptor-like element control atrial chamber-specific expression of a slow myosin heavy-chain gene during cardiac morphogenesis

Molecular and Cellular Biology

Volumn 18, Issue 10, 1998, Pages 6023-6034

  Wang, Gang Feng ^a   Nikovits Jr , William ^a   Schleinitz, Mark ^a   Stockdale, Frank E ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN HEAVY CHAIN;

ANIMAL TISSUE; ARTICLE; EMBRYO; GENE EXPRESSION REGULATION; GENE STRUCTURE; HEART DEVELOPMENT; HEART MUSCLE CELL; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REPORTER GENE;

ANIMALIA; AVES; PHASIANIDAE; VERTEBRATA;

EID: 0031656077     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.10.6023     Document Type: Article

References (64)

1. Arceci, R. J., A. A. J. King, M. C. Simon, S. H. Orkin, and D. B. Wilson. 1993. Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol. Cell. Biol. 13:2235-2246.
2. Argentin, S., A. Ardati, S. Tremblay, I. Lihrmann, L. Robitaille, J. Drouin, and M. Nemer. 1994. Developmental stage-specific regulation of atrial natriuretic factor gene transcription in cardiac cells. Mol. Cell. Biol. 14:777-790.
3. Biben, C., and R. P. Harvey. 1997. Homeodomain factor Nkx2-5 controls left/right asymmetric expression of bHLH gene eHand during murine heart development. Genes Dev. 11:1357-1369.
4. Bodmer, R. 1993. The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118:719-729.
5. Chen, C. Y., and R. J. Schwartz. 1996. Recruitment of the tinman homolog Nkx-2.5 by serum response factor activates cardiac α-actin gene transcription. Mol. Cell. Biol. 16:6372-6384.
6. Crow, M. T., and F. E. Stockdale. 1986. The developmental program of fast myosin heavy chain expression in avian skeletal muscles. Dev. Biol. 118:333-342.
7. de Groot, I. J., W. H. Lamers, and A. F. Moorman. 1989. Isomyosin expression patterns during rat heart morphogenesis: an immunohistochemical study. Anat. Rec. 224:365-373.
8. DeHaan, R. L. 1965. Morphogenesis of the vertebrate heart, p. 377-419. In R. L. DeHaan and H. Ursprung (ed.), Organogenesis. Holt, Rinehart and Winston. New York. N.Y.
9. Drysdale, T. A., K. D. Patttrson, M. Saha, and P. A. Krieg. 1997. Retinoic acid can block differentiation of the myocardium after heart specification. Dev. Biol. 188:205-215.
10. Durocher, D., F. Charron, R. Warren, R. J. Schwartz, and M. Nemer. 1997. The cardiac transcription factors Nkx2-5 and GATA-4 are mutual cofactors. EMBO J. 16:5687-5696.
11. Durocher, D., C.-Y. Chen, A. Ardati, R. J. Schwartz, and M. Nemer. 1996. The atrial natriuretic factor promoter is a downstream target for Nkx-2.5 in the myocardium. Mol. Cell. Biol. 16:4648-4655.
12. Dyson, E., H. M. Sucov, S. W. Kubalak, G. W. Schmid-Schonbein, F. A. DeLano, R. M. Evans, J. Ross, Jr., and K. R. Chien. 1995. Atrial-like phenotype is associated with embryonic ventricular failure in retinoid X receptor alpha -/- mice. Proc. Natl. Acad. Sci. USA 92:7386-7390.
13. Edmondson, D. G., G. E. Lyons, J. F. Martin, and E. N. Olson. 1994. Mef2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis. Development 120:1251-1263.
14. Gorman, C. 1985. Pages 143-190. In D. M. Glover (ed.), DNA cloning. IRL Press, Oxford, United Kingdom.
15. Grëpin C., L. Dagnino, L. Robitaille, L. Haberstroh, T. Antakly, and M. Nemer. 1994. A hormone-encoding gene identifies a pathway for cardiac but not skeletal muscle gene transcription. Mol. Cell. Biol. 14:3115-3129.
16. Grépin, C., L. Robitaille, T. Antakly, and M. Nemer. 1995. Inhibition of transcription factor GATA-4 expression blocks in vitro cardiac muscle differentiation. Mol. Cell. Biol. 15:4095-1102.
17. Heikinheimo, M., J. M. Scandrett, and D. B. Wilson. 1994. Localization of transcription factor GATA-4 to regions of the mouse embryo involved in cardiac development. Dev. Biol. 164:361-373.
18. Ip, H. S, D. B. Wilson, M. Heikinheimo, Z. Tang, C.-N. Ting, M. C. Simon, J. M. Leiden, and M. S. Pharmacek. 1994. The GATA-4 transcription factor transactivates the cardiac muscle-specific troponin C promoter-enhancer in nonmuscle cells. Mol. Cell. Biol. 14:7517-7526.
19. Jiang, Y., and T. Evans. 1996. The Xenopus GATA-4/5/6 genes are associated with cardiac specification and can regulate cardiac-specific transcription during embryogenesis. Dev. Biol. 174:258-270.
20. Komuro, I., and S. Izumo. 1993. Csx: a murine homeobox-containing gene specifically expressed in the developing heart. Proc. Natl. Acad. Sci. USA 90:8145-8149.
21. Kubalak, S. W., W. C. Miller-Hance, T. X. O'Brien, E. Dyson, and K. R. Chien. 1994. Chamber specification of atrial myosin light chain-2 expression precedes septation during murine cardiogenesis. J. Biol. Chem. 269:16961-16970.
22. Kuo, C. T., E. E. Morrisey, R. Anandappa, K. Sigrist, M. M. Lu, M. S. Pharmacek, C. Soudais, and J. M. Leiden. 1997. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev. 11:1048-1060.
23. Laverriere, A. C., C. MacNeill, C. Mueller, R. E. Poelmann, J. B. Burch, and T. Evans. 1994. GATA-4/5/6, a subfamily of three transcription factors transcribed in developing heart and gut. J. Biol. Chem. 269:23177-23184.
24. 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-cardiac myosin heavy-chain gene. Mol. Cell. Biol. 17:2745-2755.
25. Lefeuvre, B., F. Crossin, J. Fontaine-Perus, E. Bandman, and M. F. Gardahaut. 1996. Innervation regulates myosin heavy chain isoform expression in developing skeletal muscle fibers. Mech. Dev. 58:115-127.
26. 3. J. Biol. Chem. 269:4934-4939.
27. Lin, N. U., P. J. Malloy, N. Sakati, A. al-Ashwal, and D. Feldman. 1996. A novel mutation in the deoxyribonucleic acid-binding domain of the vitamin D receptor causes hereditary 1,25-dihydroxyvitamin D-resistant rickets. J. Clin. Endocrinol. Metab. 81:2564-2569.
28. Lin, Q., J. Schwarz, C. Bucana, and E. N. Olson. 1997. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276:1404-1407.
29. Lints, T. J., L. M. Parsons, L. Hartley, I. Lyons, and R. P. Harvey. 1993. Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119:969.
30. Lyons, G. E. 1994. In situ analysis of the cardiac muscle gene program during embryogenesis. TCM 4:70-77.
31. Lyons, G. E, S. Schiaffino, D. Savsoon, P. Barton, and M. Buckingham. 1990. Developmental regulation of myosin gene expression in mouse cardiac muscle. J. Cell Biol. 111:2427-2436.
32. Lyons, I., L. M. Parsons, L. Hartley, R. Li, J. E. Andrews, L. Robb, and R. P. Harvey. 1995. Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev. 9:1654-1666.
33. Mangelsdorf, D. J., U. Borgmeyer, R. A. Heyman, J. Y. Zhou, E. S. Ong, A. E. Oro, A. Kakizuka, and R. M. Evans. 1992. Characterization of three RXR genes that mediate the action of 9-cis retinoic acid. Genes Dev. 6:329-344.
34. Mangelsdorf, D. J., and R. M. Evans. 1995. The RXR heterodimers and orphan receptors. Cell 83:841-850.
35. Martin, J. F., J. J. Schwarz, and E. N. Olson. 1993. Myocyte enhancer factor (MEF) 2C; a tissue-restricted member of the MEF-2 family of transcription factors. Proc. Natl. Acad. Sci. USA 90:5282-5286.
36. McGrew, M. J., N. Bogdanova, K. Hasegawa, S. H. Hughes, R. N. Kitsis, and N. Rosenthal. 1996. Distinct gene expression patterns in skeletal and cardiac muscle are dependent on common regulatory sequences in the MLC1/3 locus. Mol. Cell. Biol. 16:4524-4534.
37. Molkentin. J. D., B. L. Black J. F. Martin, and E. N. Olson. 1995. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 83:1125-1136.
38. Molkentin, J. D., D. V. Kalvakolanu, 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.
39. Molkentin. J. D., Q. Lin, S. A. Duncan, and E. N. Olson. 1997. Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev. 11:1061-1972.
40. Molkentin, J. D., and B. E. Markham. 1993. Myocyte-specific enhancer-binding factor (MEF-2) regulates alpha-cardiac myosin heavy chain gene expression in vitro and in vivo. J. Biol. Chem. 268:19512-19520.
41. Morrisey, E. E., H. S. Ip, M. M. Lu, and M. S. Parmaeek. 1996. GATA-6: a zinc finger transcription factor that is expressed in multiple cell lineages derived from lateral mesoderm. Dev. Biol. 177:309-322.
42. Morrisey, E. E., H. S. Ip, Z. Tang, M. M. Lu, and M. S. Parmacek. 1997. GATA-5: a transcriptional activator expressed in a novel temporally and spatially-restricted pattern during embryonic development. Dev. Biol. 183:21-36.
43. Nikovits, W., Jr., 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.
44. O'Brien, T. X., K. J. Lee, and K. R. Chien. 1993. Positional specification of ventricular myosin tight chain 2 expression in the primitive murine heart tube. Proc. Natl. Acad. Sci. USA 90:5157-5161.
45. Ross, R. S., S. Navankasattusas, R. P. Harvey, and K. R. Chien. 1996. An HF-1a/HF-1b/MEF-2 combinatorial element confers cardiac ventricular specificity and established an anterior-posterior gradient of expression. Development 122:1799-1809.
46. Sepulveda, J. L., N. Belaguli, V. Nigam, C.-Y. Chen, M. Nemer, and R. J. Schwartz. 1998. GATA-4 and Nkx-2.5 coactivate Nkx-2 DNA binding targets: role for regulating early cardiac gene expression. Mol. Cell. Biol. 18:3405-3415.
47. Srivastava, D., P. Cserjesi, and E. N. Olson. 1995. A subclass of bHLH proteins required for cardiac morphogenesis. Science 270:1995-1999.
48. Srivastava, D., T. Thomas, Q. Lin, M. L. Kirby, D. Brown, and E. N. Olson. 1997. Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND. Nat. Genet. 16:154-160.
49. Stainier, D. Y., and M. C. Fishman. 1992. Patterning the zebrafish heart tube: acquisition of anteroposterior polarity. Dev. Biol. 153:91-101.
50. Tabin, C. J. 1991. Retinoids, homeoboxes, and growth factors: toward molecular models for limb development. Cell 66:199-217.
51. Thomas, T., H. Yamagishi, P. O. Overbeek, E. N. Olson, and D. Srivastava. 1998. The bHLH factors, dHAND and eHAND, specify pulmonary and systemic cardiac ventricles independent of left-right sideness. Dev. Biol. 196:228-236.
52. Thuerauf, D. J., D. S. Hanford, and C. C. Glembotski. 1994. Regulation of rat brain natriuretic peptide transcription. A potential role for GATA-related transcription factors in myocardial cell gene expression. J. Biol. Chem. 269:17772-17775.
53. Titcomb, M. W., M. M. Gottardis, J. W. Pike, and E. A. Allegretto. 1994. Sensitive and specific detection of retinoid receptor subtype proteins in cultured cell and tumor extracts. Mol. Endocrinol. 8:870-877.
54. 3 receptors. Cell 65:1255-1266.
55. Wang, G. F., and F. E. Stockdale. Chamber-specific gene expression and regulation during heart development. In R. Harvey and N. Rosenthal (ed.). Heart development, in press. Academic Press. New York, N.Y.
56. Wang, G. F., W. Nikovits, M. Schleinitz, and F. E. Stockdale. 1996. Atrial chamber-specific expression of the slow myosin heavy chain 3 gene in the embryonic heart. J. Biol. Chem. 271:19836-19845.
57. 3, and retinoic acid antagonize endothelin-stimulated hypertrophy of neonatal rat cardiac myocytes. J. Clin. Invest. 97:1577-1588.
58. Yoshizawa, T., Y. Handa, Y. Uematsu, S. Takeda, K. Sekine, Y. Yoshihara, T. Kawakami, K. Arioka, H. Sato, Y. Uchiyama, et al. 1997. Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning. Nat. Genet. 16:391-396.
59. Yutzey, K., M. Gannon, and D. Bader. 1995. Diversification of cardiomyogenic cell lineages in vitro. Dev. Biol. 170:531-541.
60. Yutzey, K. E, J. T. Rnee, and D. Bader. 1994. Expression of the atrial-specific myosin heavy chain AMHC1 and the establishment of anteroposterior polarity in the developing chicken heart. Development 120:871-883.
61. Zeller, R., K. D. Bloch, B. S. Williams, R. J. Arceci, and C. E. Seidman. 1987 Localized expression of the atrial natriuretic factor gene during cardiac embryogenesis. Genes Dev. 1:693-698.
62. Zhou, M. D., H. M. Sucov, R. M. Evans, and K. R. Chien. 1995. Retinoid-dependent pathways suppress myocardial cell hypertrophy. Proc. Natl. Acad, Sci. USA 92:7391-7395.
63. A/YB-1 is a component of cardiac HF-1A binding activity and positively regulates transcription of the myosin lightchain 2v gene. Mol. Cell. Biol. 15:2972-2982.
64. Zou, Y., S. Evans, J. Chen, H. C. Kuo, R. P. Harvey, and K. R. Chien. 1997. CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2-5 homeobox gene pathway. Development 124:793-804.