Recruitment of the tinman homolog Nkx-2.5 by serum response factor activates cardiac α-actin gene transcription

Molecular and Cellular Biology

Volumn 16, Issue 11, 1996, Pages 6372-6384

  Chen, Ching Yi ^a   Schwartz, Robert J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTIN;

ANIMAL CELL; ARTICLE; GENE ACTIVATION; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TRANSCRIPTION INITIATION;

ANIMALIA; GENETTA; MURINAE;

EID: 0000634381     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.11.6372     Document Type: Article

References (82)

1. Ananthan, J., R. Baler, D. Morissey, J. Zuo, Y. Lan, M. Weir, and R. Voellmy. 1993. Synergistic activation of transcription is mediated by the amino-terminal domain of Drosophila fushi tarazu homeodomain protein and can occur without DNA binding by the protein. Mol. Cell. Biol. 13:1599-1609.
2. Arceci, R. J., A. A. 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.
3. Azpiazu, N., and M. Frasch. 1993. Tinman and bagpipe: two homeobox genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev. 7:1325-1340.
4. Belaguli, S., and R. J. Schwartz. Unpublished data.
5. Bodmer, R. 1993. The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118:119-729.
6. Bodmer, R., L. Y. Jan, and Y. N. Jan. 1990. A new homeobox-containing gene, msh-2, is transiently expressed early during mesoderm formation of Drosophila. Development 110:661-669.
7. Bohinski, R. J., R. Di Lauro, and J. A. Whitsett. 1994. The lung-specific surfactant protein B gene is a target for thyroid transcription factor 1 and hepatocyte nuclear factor 3, indicating common factors for organ-specific gene expression along the foregut axis. Mol. Cell. Biol. 14:5671-5681.
8. Chang, K., K. Rothblum, and R. J. Schwartz. 1985. The complete sequence of the chicken α-cardiac actin gene: a highly conserved vertebrate gene. Nucleic Acids Res. 13:1223-1237.
9. Chen, C. Y., J. Croissant, M. Majeskv, S. Topouz, T. McQuinn, M. J. Frankovsky, and R. J. Schwartz. 1996. Transcriptional regulation of striated muscle specific actin genes: role of serum response factor and the murine Tinman homologue, Nkx-2.5. Dev. Genet. 19:119-130.
10. 1. J. Biol. Chem. 270:15628-15633.
11. Chen, C. Y., and R. J. Schwartz. Unpublished data.
12. Christy, B., and D. Nathans. 1989. Functional serum response elements upstream of growth factor-inducible gene zif268. Mol. Cell. Biol. 9:4884-4895.
13. Chow, K.-L., and R. J. Schwartz. 1990. A combination of closely associated positive and negative cis-acting promoter elements regulates transcription of the skeletal α-actin gene. Mol. Cell. Biol. 10:528-538.
14. Civitareale, D. R., R. Lonigro, A. J. Sinclair, and R. Di Lauro. 1989. A thyroid-specific nuclear protein essential for tissue-specific expression of the thyroglobulin promoter. EMBO J. 8:2537-2542.
15. Croissant, J., J. H. Kim, G. Eichele, J. Lough, R. Prywes, and R. J. Schwartz. Restricted serum response factor expression in avian embryonic muscle tissues is obligatory for α-actin gene transcription. Dev. Biol., in press.
16. Cserjesi, P., B. Lilly, L. Bryson, Y. Wang, D. A. Sasson, and E. N. Olson. 1992. MHox: a mesodermally restricted homeodomain protein that binds an essential site in the muscle creatine kinase enhancer. Development 115: 1087-1101.
17. Dalton, S., and R. Treisman. 1992. Characterization of SAP-1, a protein recruited by serum response factor to the c-fos serum response element. Cell 68:597-612.
18. Emerson, C. P. 1993. Skeletal myogenesis: genetics and embryology to the fore. Curr. Opin. Genet. Dev. 3:265-274.
19. Fitzpatrick, V. D., A. Percival-Smith, C. J. Ingles, and H. M. Krause. 1992. Homeodomain-independent activity of the fushi tarazu polypeptide in Drosophila embryos. Nature (London) 356:610-612.
20. Florence, B., R. Handrow, and A. Laughon. 1991. DNA-binding specificity of the fushi tarazu homeodomain. Mol. Cell. Biol. 11:3613-3623.
21. French, B. A., K.-L. Chow, E. N. Olson, and R. J. Schwartz. 1991. Heterodimers of myogenic helix-loop-helix regulatory factors and E12 bind a complex element governing myogenic induction of the avian cardiac α-actin promoter. Mol. Cell. Biol. 11:2439-2450.
22. Gehring, W. J., Y. Q. Qian, M. Billeter, K. Furukubo-Tokunaga, A. F. Schier, D. Resendez-Perez, M. Affolter, G. Otting, and K. Wuthrich. 1994. Homeodomain-DNA recognition. Cell 78:211-223.
23. Gilman, M. Z., R. N. Wilson, and R. A. Weinberg. 1986. Multiple protein-binding sites in the 5′-flanking region regulate c-fos expression. Mol. Cell. Biol. 6:4305-4314.
24. Greenberg, M. E., Z. Siegried, and E. B. Ziff. 1987. Mutation of the c-fos gene dyad symmetry element inhibits serum inducibility of transcription in vivo and nuclear regulatory factor binding in vitro. Mol. Cell. Biol. 7:1217-1225.
25. Grepin, 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.
26. Grueneberg, D. A., S. Natesan, C. Alexandre, and M. Z. Gilman. 1992. Human and Drosophila homeodomain proteins that enhance the DNA-binding activity of serum response factor. Science 257:1089-1095.
27. Grueneberg, D. A., K. J. Simon, K. Brennan, and M. Gilman. 1995. Sequence-specific targeting of nuclear signal transduction pathways by homeodomain proteins. Mol. Cell. Biol. 15:3318-3326.
28. Gualberto, A., D. LePage, G. Pons, S. Mader, K. Park, M. Atchison, and K. Walsh. 1992. Functional antagonism between YY1 and the serum response factor. Mol. Cell. Biol. 12:4209-4214.
29. Guazzi, S., M. Price, M. DeFelice, G. Damante, M.-G. Mattei, and R. DiLauro. 1990. Thyroid nuclear factor 1 (TTF-1) contains a homeodomain and displays a novel DNA binding specificity. EMBO J. 9:3631-3639.
30. Hayashi, S., and M. Scott. 1990. What determines the specificity of action of Drosophila homeodomain proteins? Cell 63:883-894.
31. Hennighausen, L., and H. Lubon. 1987. Interaction of protein with DNA in vitro. Methods Enzymol. 152:721-735.
32. Herskowitz, I. 1989. A regulatory hierarchy for cell specialization in yeast. Nature (London) 342:749-757.
33. Johansen, F.-E., and R. Prywes. 1993. Identification of transcriptional activation and inhibitory domains in serum response factor (SRF) using GAL4-SRF constructs. Mol. Cell. Biol. 13:4640-4647.
34. Johnson, A. D., and I. Herskowitz. 1985. A repressor (MATα2 product) and its operator control expression of a set of cell type specific genes in yeast. Cell 42:237-247.
35. Kissinger, S. R., B. Liu, E. Martin-Blanco, T. B. Kornberg, and C. O. Pabo. 1990. Crystal structure of an Engrailed homeodomain-DNA complex at 2.8 Å resolution: a framework for understanding homeodomain-DNA interactions. Cell 63:579-590.
36. 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.
37. Kornberg, T. B. 1993. Understanding the homeodomain. J. Biol. Chem. 268:26813-26816.
38. Krause, M., A. Fire, S. White Harrison, J. Priess, and H. Weintraub. 1990. CeMyoD accumulation defines the body wall muscle cell fate during C. elegans embryogenesis. Cell 63:907-919.
39. Kristie, T. M., and P. A. Sharp. 1990. Interaction of the Oct-1 POU subdomains with specific DNA sequences and with the HSV α-trans-activator protein. Genes Dev. 4:2383-2396.
40. Lazzaro, D., M. Price, M. De Felice, and R. Di Lauro. 1991. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113:1093-1104.
41. Lee, T. C., K.-L. Chow, P. Fang, and R. J. Schwartz. 1991. Activation of skeletal α-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. 11:5090-5100.
42. Lee, T. C., Y. Shi, and R. J. Schwartz. 1992. Displacement of BrdUrd-induced YY1 by serum response factor activates skeletal α-actin transcription in embryonic myoblasts. Proc. Natl. Acad. Sci. USA 89:9814-9818.
43. Lee, T.-C., Y. Zhang, and R. J. Schwartz. 1994. Bifunctional transcriptional properties of YY1 in regulating muscle actin and c-myc gene expression during myogenesis. Oncogene 9:1047-1052.
44. Lilly, B., S. Galewsky, A. B. Firulli, R. A. Schulz, and E. N. Olson. 1994. mef2: a MADS gene expressed in the differentiating mesoderm and the somatic muscle cell lineage during Drosophila embryogenesis. Proc. Natl. Acad. Sci. USA 91:5662-5666.
45. 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 119:419-431.
46. 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 homeobox gene Nkx-2.5. Genes Dev. 9:1654-1666.
47. 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.
48. McGinnis, W., and R. Krumlauf. 1992. Homeobox genes and axial patterning. Cell 68:283-302.
49. McMahon, S. B., and J. G. Monroe. 1995. A ternary complex factor-dependent mechanism mediates induction of egr-1 through selective serum response elements following antigen receptor cross-linking in B lymphocytes. Mol. Cell. Biol. 15:1086-1093.
50. Michelson, A. M., S. M. Abmayr, M. Bate, A. M. Arias, and T. Maniatis. 1990. Expression of a MyoD family member per figures muscle pattern in Drosophila embryos. Genes Dev. 4:2086-2097.
51. Miwa, T., and L. Kedes. 1987. Duplicated CArG box domains have positive and mutually dependent regulatory roles in expression of the human α-cardiac actin gene. Mol. Cell. Biol. 7:2803-2813.
52. Mohun, T. J., M. V. Taylor, N. Garrett, and J. B. Gurdon. 1989. The CArG promoter sequence is necessary for muscle-specific transcription of the cardiac actin gene in Xenopus embryos. EMBO J. 8:1153-1161.
53. 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.
54. Moss, J. B., T. C. McQuinn, and R. J. Schwartz. 1994. The avian cardiac α-actin promoter is regulated through a pair of complex elements composed of E boxes and serum response elements that binds both positive- and negative-acting factors. J. Biol. Chem. 269:12731-12740.
55. Okkema, P. G., and A. Fire. 1994. The Caenorhabditis elegans NK-2 class homeodomain CEH-22 is involved in combinatorial activation of gene expression in pharyngeal muscle. Development 120:2175-2186.
56. Opstelten, D.-J. E., R. Volgels, B. Robert, E. Kalkhoven, F. Zwartkruis, L. de Laaf, O. H. Destrée, J. Deschamps, K. A. Lawson, and F. Meijlink. 1991. The mouse homeobox gene, S8, is expressed during embryogenesis predominantly in mesenchyme. Mech. Dev. 34:29-42.
57. Otting, G., Y. Q. Qian, M. Billeter, M. Muller, M. Affolter, W. J. Gehring, and K. Wuthrick. 1990. Protein-DNA contacts in the structure of a homeodomain-DNA complex determined by nuclear magnetic resonance spectroscopy in solution. EMBO J. 9:3085-3092.
58. Pellegrini, L., S. Tan, and T. J. Richmond. 1995. Structure of serum response factor core bound to DNA. Nature (London) 376:490-498.
59. Pollock, R., and R. Treisman. 1990. A sensitive method for the determination of protein DNA binding specificities. Nucleic Acids Res. 18:6197-6204.
60. Price, M., D. Lazzaro, T. Pohl, M.-G. Mattei, U. Ruther, J.-C. Olivo, D. Duboule, and R. DiLauro. 1992. Regional expression of the homeobox gene Nkx-2.2 in the developing mammalian forebrain. Neuron 8:241-255.
61. Prywes, R. Personal communication.
62. Prywes, R., and R. G. Roeder. 1986. Inducible binding of a factor to the c-fos enhancer. Cell 47:777-784.
63. Prywes, R., and H. Zhu. 1992. In vitro squelching of activated transcription by serum response factor: evidence for a common coactivator used by multiple transcriptional activators. Nucleic Acids Res. 20:513-520.
64. Quitschke, W. W., L. DePonti-Zilli, Z.-Y. Lin, and B. Paterson. 1989. Identification of two nuclear factor-binding domains on the chicken cardiac actin promoter: implications for regulation of the gene. Mol. Cell. Biol. 9:3218-3230.
65. Rao, V. N., K. Huebner, M. Isobe, A. Ab Rushidi, C. M. Croce, and E. S. P. Reddy. 1989. Elk, tissue-specific Ets-related genes on chromosome X and 14 near translocation breakpoints. Science 244:66-70.
66. Schroter, H., C. G. F. Mueller, K. Meese, and A. Nordheim. 1990. Purification of intercalator released p67, a polypeptide that interacts specifically with the c-fos serum response element. EMBO J. 9:1123-1130.
67. Schwarz-Sommer, Z., P. Huijser, W. Nacken, H. Saedler, and H. Sommer. 1990. Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250:931-936.
68. Scott, M. P., J. W. Tamkun, and G. W. Hartzell III. 1989. The structure and function of the homeodomain. Biochim. Biophys. Acta 989:25-48.
69. TCF exhibits dual component specificity with contacts to DNA and an extended structure in the DNA-binding domain of p67SRF. EMBO J. 11:3011-3019.
70. Shore, P., and A. D. Sharrocks. 1994. The transcription factors Elk-1 and serum response factor interact by direct protein-protein contacts mediated by a short region of Elk-1. Mol. Cell. Biol. 14:3283-3291.
71. Stern, S., and W. Herr. 1991. The herpes simplex virus trans-activator VP16 recognizes the Oct-1 homeodomain: evidence for a homeodomain recognition subdomain. Genes Dev. 5:2555-2566.
72. Stern, S., M. Tanaka, and W. Herr. 1989. The Oct-1 homeodomain directs formation of a multiprotein-DNA complex with the HSV transactivator VP16. Nature (London) 341:624-630.
73. Taylor, A., H. P. Erba, G. E. O. Muscat, and L. Kedes. 1988. Nucleotide sequence and expression of the human skeletal α-actin gene: evolution of functional regulatory domains. Genomics 3:323-336.
74. Tonissen, K. F., T. A. Drysdale, T. J. Lints, R. P. Harvey, and P. A. Krieg. 1994. XNkx-2.5, a Xenopus gene related to Nkx-2.5 and tinman: evidence for a conserved role in cardiac development. Dev. Biol. 162:325-328.
75. Treisman, R. 1985. Transient accumulation of c-fos RNA following serum stimulation requires a conserved 5′ element and c-fos 3′ sequences. Cell 42:889-902.
76. Treisman, R. 1986. Identification of a protein-binding site that mediates transcription response of the c-fos gene to serum factors. Cell 46:567-574.
77. Treisman, R. 1990. The SRE: a growth factor responsive transcriptional regulator. Semin. Cancer Biol. 1:47-58.
78. Trouche, D., M. Grigoriev, J.-L. Lenormand, P. Robin, S. A. Leibovitch, P. Sassone-Corsi, and A. Harel-Bellan. 1993. Repression of c-fos promoter by MyoD on muscle cell differentiation. Nature (London) 363:79-82.
79. Wilson, D., G. Sheng, T. Lecuit, N. Dostatni, and C. Desplan. 1993. Cooperative dimerization of paired class homeo domains on DNA. Genes Dev. 7:2120-2134.
80. Wolberger, C., A. K. Vershon, B. Liu, A. D. Johnson, and C. O. Pabo. 1991. Crystal structure of a MATα2 homeo domain-operator complex suggests a general model for homeo domain-DNA interactions. Cell 67:517-528.
81. Zappavigna, V., D. Sartori, and F. Mavilio. 1994. Specificity of HOX protein function depends on DNA-protein and protein-protein interactions, both mediated by the homeo domain. Genes Dev. 8:732-744.
82. Zhu, H., V. Joliot, and R. Prywes. 1994. Role of transcription factor TFIIF in serum response factor-activated transcription. J. Biol. Chem. 269:3489-3497.