Avian serum response factor expression restricted primarily to muscle cell lineages is required for α-actin gene transcription

Developmental Biology

Volumn 177, Issue 1, 1996, Pages 250-264

  Croissant, Jeffrey D ^a   Kim, Jae Hong ^a   Eichele, Gregor ^a   Goering, Lisa ^a   Lough, John ^b   Prywes, Ron ^c   Schwartz, Robert J ^a,d  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d Department of Cell Biology ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTIN; DNA BINDING PROTEIN; MESSENGER RNA; MUTANT PROTEIN; SERUM RESPONSE FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; DIMERIZATION; DNA TRANSFECTION; EMBRYO; EMBRYO DEVELOPMENT; EXPRESSION VECTOR; GENE ACTIVATION; GENE EXPRESSION; HEART DEVELOPMENT; HEART MUSCLE; IMMUNOHISTOCHEMISTRY; MESODERM; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; REPORTER GENE; SKELETAL MUSCLE; SOMITE; TRANSCRIPTION REGULATION;

EID: 0030578427     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1996.0160     Document Type: Article

References (75)

1. Arrick, B. A., Lee, A. L., Grendell, R. L., and Derynck, R. (1991). Inhibition of translation of transforming growth factor-β3 mRNA by its 5′ untranslated region. Mol. Cell. Biol. 11, 4036-4313.
2. Azpiazu, N., and Frasch, M. (1993). tinman and bagpipe: Two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev. 7, 1325-1340.
3. Bains, W., Ponte, P., Blau, H., and Kedes, L. (1984). Cardiac actin is the major actin gene product in skeletal muscle cell differentiation in vitro. Mol. Cell. Biol. 4, 1449-1453.
4. Benezra, R., Davis, R. L., Lockshon, D., Turner, D. L., and Weintraub, H. (1990). The protein Id: A negative regulator of helix-loop-helix DNA binding protein. Cell 61, 49-59.
5. Bergsma, D. J., Grichnik, J. M., Gosset, L. M. A., and Schwartz, R. J. (1986). Delimitation and characterization of cis-acting DNA sequence required for the regulated expression and transcriptional control of the chicken skeletal α-actin gene. Mol. Cell. Biol. 6, 2462-2475.
6. Biben, C., Kirschbaum, B. J., Garner, I., and Buckingham, M. (1994). Novel muscle-specific enhancer sequences upstream of the cardiac actin gene. Mol. Cell. Biol. 14, 3504-3513.
7. Blau, H. M., Pavlath, G. K., Hardeman, E. C., Chiu, C. P., Silberstein, L., Webster, S. G., Miller, S. C., and Webster, C. (1985). Plasticity of the differentiated state. Science 230, 758-766.
8. Bodmer, R. (1993). The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118, 719-729.
9. Bour, B. A., O'Brien, M. A., Lockwood, W. L., Goldstein, E. S., Bodmer, R., Taghert, P. H., Abmayr, S. M., and Nguyen, H. T. (1995). Drosophila MEF2, a transcription factor that is essential for myogenesis. Genes Dev. 9, 730-741.
10. Brennan, K. J., and Hardeman, E. C. (1993). Quantitative analysis of the human α-skeletal actin gene in transgenic mice. J. Biol. Chem. 268, 719-725.
11. Chambers, A. E., Kotecha, S., Towers, N., and Mohun, T. J. (1992). Muscle-specific expression of SRF-related genes in the early embryo of Xenopus laevis. EMBO J. 11, 4981-4991.
12. Chen, C. Y., McQuinn, T. C., Frankovsky, M. J., and Schwartz, R. J. (1996). Cardiac α-actin gene, a downstream target for tinman homologue, Nkx-2.5 and serum response factor, submitted for publication.
13. Chomczynski, P., and Sacchi, N. (1987). Single step method of RNA isolation by acid guanidinium thiocynanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
14. Chow, K.-L., and Schwartz, R. J. (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.
15. Coleman, M. E., DeMayo, F., Yin, K. C., Lee, H. M., Geske, R., Montgomery, C., and Schwartz, R. J. (1995). Myogenic vector expression of insulin-like growth factor I stimulates muscle cell differentiation and myofiber hypertrophy in transgenic mice. J. Biol. Chem. 270, 12109-12116.
16. Edmondson, D. G., Lyons, G. E., Martin, J. F., and Olson, E. N. (1994). Mef-2 gene expression marks the cardiac and skeletal muscle lineages during mouse myogenesis. Development 120, 1251-1263.
17. French, B. A., Chow, K. L., Olson, E. N., and Schwartz, R. J. (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.
18. Gilman, M.Z., Wilson, R. N., and Weinberg, R. A. (1986). Multiple protein-binding sites in the 5′-flanking region regulate c-fos expression. Mol. Cell. Biol. 6, 4305-4316.
19. Grichnik, J. M., French, B. A., and Schwartz, R. J. (1988). The chicken skeletal α-actin gene promoter region exhibits partial dyad symmetry and a capacity to drive bidirectional transcription. Mol. Cell. Biol. 8, 4587-4597.
20. Grueneberg, D. A., Natesan, S., Alexandre, C., and Gilman, M.Z. (1992). Human and Drosophila homeodomain proteins that enhance the DNA-binding activity of serum response factor. Science 257, 1089-1095.
21. Grueneberg, D. A., Simon, K. J., Brennan, K., and Gilman, M. (1995). Sequence-specific targeting of nuclear signal transduction pathways by homeodomain proteins. Mol. Cell. Biol. 15, 3318-3326.
22. Gualberto, A., LePage, D., Pons, G., Mader, S. L., Park, K., Atchison, M. L., and Walsh, K. (1992). Functional antagonism between YY1 and the serum response factor. Mol. Cell. Biol. 12, 4209-4214.
23. Hamburger, V., and Hamilton, H. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
24. Hayward, L. J., and Schwartz, R. J. (1986). Sequential expression of chicken actin genes during myogenesis. J. Cell Biol. 102, 1485-1493.
25. Hayward, L. J., Zhu, Y. Y., and Schwartz, R. J. (1988). Cellular localization of muscle and nonmuscle actin mRNAs in chicken primary myoblast cultures: The induction of α-skeletal actin mRNA is regulated independently of α-cardiac gene expression. J. Cell Biol. 106, 2077-2086.
26. Johansen, F.-E., and Prywes, R. (1993). Identification of transcriptional activation and inhibitory domains in serum response factor (SRF) by using GAL4-SRF constructs. Mol. Cell. Biol. 13, 4640-4647.
27. Keleher, C. A., Passmore, S., and Johnson, A. D. (1989). Yeast repressor α2 binds to its operator cooperatively with yeast protein MCM1. Mol. Cell. Biol. 9, 5228-5230.
28. Kim, J. H., Johansen, F. E., Robertson, N., Catino, J. J., Prywes, R., and Kumar, C. C. (1994). Suppression of Ras transformation by serum response factor. J. Biol. Chem. 269, 13740-13743.
29. Komuro, I., and Izumo, A. (1993). Csx: A murine homeobox-containing gene specifically expressed in the developing heart. Proc. Natl. Acad. Sci. USA 90, 8145-8149.
30. Lee, T.-C., Chow, K. L., Fang, P., and Schwartz, R. J. (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.
31. Lee, T.-C., Shi, Y., and Schwartz, R. J. (1992). Displacement of BrdU-induced YY1 by SRF activates skeletal α-actin gene transcription in embryonic myoblasts. Proc. Natl. Acad. Sci. USA 89, 9814-9818.
32. Li, H. S., Yang, J. M., Jacobson, R. D., Pasko, D., and Sundin, O. (1994). Pax-6 is first expressed in a region of ectoderm anterior to the early neural plate: Implications for stepwise determination of the lens. Dev. Biol. 162, 181-194.
33. Lilly, B., Zhao, B., Ranganayakulu, G., Paterson, B. M., Schulz, R. A., and Olson, E. N. (1995). Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 267, 688-693.
34. Lints, T. J., Parsons, L. M., Hartley, L., Lyons, I., and Harvey, R. P. (1993). Nkx-2.5: A novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119, 419-431.
35. Lyons, I., Parsons, L., Hartley, L., Li, R., Andrews, J., Robb, L., and Harvey, R. (1995). Myogenic and morphogenic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev. 9, 1654-1666.
36. MacLellan, W. R., Lee, T.-C., Schwartz, R. J., and Schneider, M. D. (1994). TGF-β response elements of the skeletal α-actin gene. J. Biol. Chem. 269, 16754-16760.
37. Manak, J. R., and Prywes, R. (1993). Phosphorylation of serum response factor by casein kinase II: Evidence against a role in growth factor regulation of fos expression. Oncogene 8, 703-711.
38. Minty, A., and Kedes, L. (1986). Upstream region of the human cardiac actin gene that modulates its transcription in muscle cells: Presence of evolutionarily conserved repeat motif. Mol. Cell. Biol. 9, 2125-2136.
39. Miwa, T., and Kedes, L. (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.
40. Mohun, T. J., Taylor, M. V., Garrett, N., and Gurdon, J. B. (1989). The CArG promoter sequence is necessary for muscle-specific transcription of the cardiac actin gene in Xenopus embryos. EMBO J. 8, 1153-1161.
41. Mohun, T. J., Chambers, A. E., Towers, N., and Taylor, M. V. (1991). Expression of genes encoding the transcription factor SRF during early development of Xenopus laevis: Identification of a CArG box-binding activity as SRF. EMBO J. 10, 933-940.
42. Molkentin, J. D., Black, B. L., Martin, J. F., and Olson, E. N. (1995). Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 83, 1125-1136.
43. Moss, J. B., McQuinn, T. C., and Schwartz, R. J. (1994). The avian cardiac α-actin promoter is regulated through a pair of complex elements composed of Eboxes and serum response elements that bind both positive-and negative-acting factors. J. Biol. Chem. 269, 12731-12740.
44. Mueller, C. G., and Nordheim, A. (1991). A protein domain conserved between yeast MCM1 and human SRF directs ternary complex formation. EMBO J. 10, 4219-4229.
45. Muscat, G. E., and Kedes, L. (1987). Multiple 5′-flanking regions of the human α-skeletal actin gene synergistically modulate muscle-specific expression. Mol. Cell. Biol. 7, 4089-4099.
46. Norman, C., Runswick, M., Pollock, R., and Treisman, R. (1988). Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell 55, 989-1003.
47. Olson, E. N. (1992). Activation of muscle-specific transcription by myogenic helix-loop-helix proteins. Symp. Soc. Exp. Biol. 46, 331-341.
48. Olson, E. N., Perry, M., and Schulz, R. A. (1995). Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. Dev. Biol. 172, 2-14.
49. Parkin, N. A., Darveau, Nicholson, R., and Sonenberg, N. (1988). cis-acting translational effects of the 5′ noncoding region of c-myc mRNA. Mol. Cell. Biol. 8, 2875-2883.
50. Parlow, M. H., Bolender, D. L., Kokan-Moore, N. T., and Lough, J. (1991). Localization of bFGF-like proteins as punctate inclusions in the preseptation myocardium of the chicken embryo. Dev. Biol. 146, 139-147.
51. Pellegrini, L., Tan, S., and Richmond, T. J. (1995). Structure of serum response factor core bound to DNA. Nature 376, 490-498.
52. Petropoulos, C. J., Rosenberg, M. P., Jenkins, N. A., Copeland, N. G., and Hughes, S. H. (1989). The chicken skeletal muscle α-actin promoter is tissue specific in transgenic mice. Mol. Cell. Biol. 9, 3785-3792.
53. Pollock, R., and Treisman, R. (1991). Human SRF-related proteins: DNA-binding properties and potential regulatory targets. Genes Dev. 5, 2327-2341.
54. Quitschke, W. W., DePonti-Zilli, L., Lin, Z. Y., and Paterson, B. M. (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.
55. Ruzicka, D. L., and Schwartz, R. J. (1988). Sequential activation of α-actin genes during avian cardiogenesis: Vascular smooth muscle α-actin transcripts mark the onset of cardiomyocyte differentiation. J. Cell Biol. 107, 2575-2586.
56. Sanger, F., Nicklen, S., and Coulson, A. R. (1977). DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA 7, 5463-5467.
57. Sassoon, D., Lyons, G., Wright, W. E., Lin, V., Lassar, A., Weintraub, H., and Buckingham, M. (1989). Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis. Nature 341, 303-307.
58. Sartorelli, V., Webster, K. A., and Kedes, L. (1990). Muscle-specific expression of the cardiac alpha-actin gene requires MyoD1, CArG-box binding factor, and Sp1. Genes Dev. 4, 1811-1822.
59. Sawtell, N., and Lessard, J. (1989). Cellular distribution of smooth muscle actins during mammalian embryogenesis: expression of the α-vascular but not the γ-enteric isoform in differentiating striated myocytes. J. Cell Biol. 109, 2929-2937.
60. Schultheiss, T. M., Xydas, S., and Lassar, A. B. (1995). Induction of avian cardiac myogenesis by anterior mesoderm. Development 121, 4203-4214.
61. Schwartz, R. J., and Rothblum, K. (1981). Gene switching in myogenesis: Differential expression of the chicken actin multigene family. Biochemistry 20, 4122-4129.
62. Skinner, S. M., Niu, E. M., Bundman, D. S., Lo, C., and Dunbar, B. S. (1987). Use of immunoaffinity purified antibodies to zona pellucida to compare alloimmunization of male and female rabbits. J. Reprod. Immunol. 12, 81-92.
63. Stern, C. D., Yu, R. T., Kakizuka, A., Kintner, C. R., Mathews, L. S., Vale, W. W., Evans, R. M., and Umesono, K. (1995). Activin and its receptors during gastrulation and the later phases of mesoderm development in the chick embryo. Dev. Biol. 172, 192-205.
64. Sundin, O. H., Busse, H. G., Rogers, M. B., Gudas, L. J., and Eichele, G. (1990). Region specific expression in the early chick and mouse embryos of Ghox-1ab and Hox 1.6, vertebrate homeobox containing genes related to Drosophila labial. Development 108, 47-58.
65. Sundin, O. H., and Eichele, G. (1990). A homeodomain protein reveals the metameric nature of the developing hindbrain. Genes Dev. 4, 1267-1276.
66. Suzuki, E., Guo, K., Kolman, M., Yu, Y.-T., and Walsh, K. (1995). Serum induction of MEF2/RSRF expression in vascular myocytes is mediated at the level of translation. Mol. Cell. Biol. 15, 3415-3423.
67. Treisman, R. (1985). Transient accumulation of c-fos RNA following serum stimulation requires a conserved 5′ element and c-fos 3′ sequences. Cell 42, 899-902.
68. Treisman, R. (1986). Identification of a protein-binding site that mediates transcription factor response of the c-fos gene to serum factors. Cell 46, 567-574.
69. Treisman, R. (1987). Identification and purification of a polypeptide that binds the c-fos serum response element. EMBO J. 6, 2711-2717.
70. Treisman, R., and Ammerer, G. (1992). The SRF and MCM1 transcription factors. Curr. Opin. Genet. Dev. 2, 221-226.
71. Vandromme, M., Gauthier-Rouviere, C., Carnac, G., Lamb, N., and Fernandez, A. (1992). Serum response factor p67SRF is expressed and required during myogenic differentiation of both mouse C2 and rat L6 muscle cell lines. J. Cell Biol. 118, 1489-1500.
72. Vershon, A. K., and Johnson, A. D. (1993). A short, disordered protein region mediates interactions between the homeodomain of the yeast alpha 2 protein and the MCM1 protein. Cell 72, 105-112.
73. Walsh, K. (1989). Cross-binding of factors to functionally different promoter elements in the c-fos and skeletal actin genes. Mol. Cell. Biol. 9, 2191-2201.
74. Wharton, R. P., and Struhl, G. (1991). RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos. Cell 67, 955-967.
75. Yu, Y.-T., Breitbart, R. E., Smoot, L. B., Lee, Y., Mahdavi, V., and Nadal-Ginard, B. (1992). Human myocyte-specific enhancer factor 2 comprises a group of tissue-restricted MADS box transcription factors. Genes Dev. 6, 1783-1798.