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Comparative Genetics of Heart Development: Conserved Cardiogenic Factors in Drosophila and Vertebrates

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Cardiac Development

Part of the book series: Progress in Experimental Cardiology ((PREC,volume 4))

Summary

Despite differences in structure and complexity, the hearts of Drosophila and vertebrates share important developmental characteristics. Five different transcription factors that play vital roles in the formation of the fly heart have also been shown to be necessary for the early steps in vertebrate cardiogenesis. Despite the divergence between the two groups, there is a high degree of functional conservation of these factors, which has made information gained in Drosophila relevant to the investigation of heart cell specification and tube formation in vertebrates. Additionally, the mechanisms that generate the diversity of cell types in the Drosophila heart may also be conserved in the later steps of vertebrate heart development.

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References

  1. Rugendorff A, Younossi-Hartenstein A, Hartenstein V. 1994. Embryonic origin and differentiation of the Drosophila heart. Roux’s Arch Dev Biol 203:266–280.

    Google Scholar 

  2. Rizki TM. 1978. The circulatory system and associated cells and tissues. In: The Genetics and Biology of Drosophila. Ed. M Ashburner and TRF Wright, 397–452. London and New York: Academic Press.

    Google Scholar 

  3. Bate M. 1993. The mesoderm and its derivatives. In: The Development of Drosophila melanogaster. Ed. M Bate and AM Arias, 1013–1090. Plainview, NY: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  4. Fishman MC, Chien KR. 1997. Fashioning the vertebrate heart: earliest embryonic decisions. Development 124:2099–2117. Review.

    PubMed  CAS  Google Scholar 

  5. Haag TA, Haag NP, Lekven AC, Hartenstein V. 1999. The role of cell adhesion molecules in Drosophila heart morphogenesis: faint sausage, shotgun/DE-cadherin, and laminin A are required for discrete stages in heart development. Dev Biol 208:56–69.

    PubMed  CAS  Google Scholar 

  6. Grant DS, Tashiro K, Segui-Real B, Yamada Y, Martin GR, Kleinman HK. 1989. Two different laminin domains mediate the differentiation of human endothelial cells into capillary-like structures in vitro. Cell 58:933–943.

    PubMed  CAS  Google Scholar 

  7. Sugi Y, Markwald RR. 1996. Formation and early morphogenesis of endocardial endothelial precursor cells and the role of endoderm. Dev Biol 175:66–83.

    PubMed  CAS  Google Scholar 

  8. Kim Y, Nirenberg M. 1989. Drosophila NK-homeobox genes. Proc Natl Acad Sci USA 86:7716–7720.

    PubMed  CAS  Google Scholar 

  9. Harvey RP. 1996. NK-2 homeobox genes and heart development. Dev Biol 178:203–216.

    PubMed  CAS  Google Scholar 

  10. Azpiazu N, 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.

    PubMed  CAS  Google Scholar 

  11. Bodmer R. 1993. The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118:719–729.

    PubMed  CAS  Google Scholar 

  12. Yin Z, Frasch M. 1998. Regulation and function of tinman during dorsal mesoderm induction and heart specification in Drosophila. Dev Genet 22:187–200.

    PubMed  CAS  Google Scholar 

  13. Yin Z, Xu XL, Frasch M. 1997. Regulation of the twist target gene tinman by modular as-regulatory elements during early mesoderm development. Development 124:4871–4982.

    Google Scholar 

  14. Xu X, Yin Z, Hudson JB, Ferguson EL, Frasch M. 1998. Smad proteins act in combination with synergistic and antagonistic regulators to target Dpp responses to the Drosophila ectoderm. Genes Dev 12:2354–2370.

    PubMed  CAS  Google Scholar 

  15. Wu X, Golden K, Bodmer R. 1995. Heart development in Drosophila requires the segment polarity gene wingless. Dev Biol 169:619–628.

    PubMed  CAS  Google Scholar 

  16. Venkatesh T, Park M, Ocorr K, Nemaceck J, Golden K, Wemple M, Bodmer R. 2000. Cardiac enhancer activity of the homeobox gene tinman depends on CREB consensus binding sites in Drosophila. Genesis 26:55–66.

    PubMed  CAS  Google Scholar 

  17. Gajewski K, Kim Y, Lee YM, Olson EN, Schulz RA. 1997. D-mef2 is a target for Tinman activation during Drosophila heart development. EMBO J 16:515–522.

    PubMed  CAS  Google Scholar 

  18. Gajewski K, Fossett N, Molkentin JD, Schulz RA. 1999. The zinc finger proteins Pannier and GATA4 function as cardiogenic factors in Drosophila. Development 126:5679–5688.

    PubMed  CAS  Google Scholar 

  19. Kremser T, Gajewski K, Schulz RA, Renkawitz-Pohl R. 1999. Tinman regulates the transcription of the beta3 tubulin gene (betaTub60D) in the dorsal vessel of Drosophila. Dev Biol 216:327–339.

    PubMed  CAS  Google Scholar 

  20. Gajewski K, Kim Y, Choi CY, Schulz RA. 1998. Combinatorial control of Drosophila mefl gene expression in cardiac and somatic muscle cell lineages. Dev Genes Evol 208:382–392.

    PubMed  CAS  Google Scholar 

  21. Baylies MK, Bate M. 1996. twist: A myogenic switch in Drosophila. Science 272:1481–1484.

    PubMed  CAS  Google Scholar 

  22. Gajewski K, Zhang Q, Choi CY, Fossett N, Dang A, Kim YH, Kim Y, Schulz RA. 2001. Pannier is a transcriptional target and partner of Tinman during Drosophila cardiogenesis. Dev Biol 233:425–436.

    PubMed  CAS  Google Scholar 

  23. Lints TJ, Parsons LM, Hartley L, Li R, Andrews JE, Robb L, Harvey RP. 1995. Myogenic and morphogenic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx-2.5. Genes Dev 9:1654–1666.

    Google Scholar 

  24. Komuro I, Izumo S. 1993. Csx: a murine homeobox-containing gene specifically expressed in the developing heart. Proc Natl Acad Sci USA 90:8145–8149.

    PubMed  CAS  Google Scholar 

  25. Tonissen KF, Drysdale TA, Lints TJ, Harvey RP, Krieg PA. 1994. XNkx-2.5, a Xenopus gene related to Nkx-2.5 and tinman: evidence for a conserved role in cardiac development. Dev Biol 162:235–328.

    Google Scholar 

  26. Evans SM,Yan W, Murillo MP, Ponce J, Papalopulu N. 1995. tinman, a Drosophila homeobox gene required for heart and visceral mesoderm specification, may be represented by a family of genes in vertebrates: XNkx-2.3, a second vertebrate homologue of tinman. Development 121:3889–3899.

    PubMed  CAS  Google Scholar 

  27. Schultheiss TM, Xydas S, Lassar AB. 1995. Induction of avian cardiac myogenesis by anterior endoderm. Development 121:4204–4214.

    Google Scholar 

  28. Buchberger A, Pabst O, Brand T, Seidl K, Arnold HH. 1996. Chick NKx-2.3 represents a novel family member of vertebrate homologs to the Drosophila homeobox gene tinman: different expression of cNKx-2.3 and cNKx-2.5 during heart and gut development. Mech Dev 56:151–163.

    PubMed  CAS  Google Scholar 

  29. Chen JN, Fishman MC. 1996. Zebrafish tinman homolog demarcates the heart field and initiates myocardial differentiation. Development 122:3809–3816.

    PubMed  CAS  Google Scholar 

  30. Lee KH, Xu Q, Breitbart RE. 1996. A new tinman-related gene, nkx2.7, anticipates the expression of nkx2.5 and nkx2.3 in Zebrafish heart and pharyngeal endoderm. Dev Biol 180:722–731.

    PubMed  CAS  Google Scholar 

  31. Nikolova M, Chen X, Lufkin T. 1997. Nkx2.6 expression is transiently and specifically restricted to the branchial region of pharyngeal-stage mouse embryos. Mech Dev 69:215–218.

    PubMed  CAS  Google Scholar 

  32. Pabst O, Scheider A, Brand T, Arnold HH. 1997. The mouse Nkx2–3 homeobox gene is expressed in gut mesenchyme during pre- and postnatal mouse development. Dev Dynam 209:29–35.

    CAS  Google Scholar 

  33. Reecy JM, Yamada M, Cummings K, Sosic D, Chen CY, Eichele G, Olson EN, Schwartz RJ. 1997. Chicken Nkx-2.8: a novel homeobox gene expressed in early heart progenitor cells in pharyngeal pouch–3 and –3 endoderm. Dev Bio 188:295–311.

    CAS  Google Scholar 

  34. Biben C, Hatzistavrou T, Harvey RP. 1998. Expression of NK-2 class homeobox gene Nkx2–6 in foregut endoderm and heart. Mech Dev 73:125–127.

    PubMed  CAS  Google Scholar 

  35. Newman CS, Krieg PA. 1998. Tinman-related genes expressed during heart development in Xenopus. Dev Genet 22:230–238.

    PubMed  CAS  Google Scholar 

  36. Newman CS, Reecy J, Grow MW, Ni K, Boettger T, Kessel M, Schwartz RJ, Krieg PA. 2000. Transient cardiac expression of the tinman-family homeobox gene, XNkx2–10. Mech Dev 91:369–373.

    PubMed  CAS  Google Scholar 

  37. Schott JJ, Benson DW, Basson CT, Pease W, Silberbach GM, Moak JP, Maron BJ, Seidman CE, Seidman JG. 1998. Congenital heart disease caused by mutations in the transcription factor NKX2–5. Science 281:108–111.

    PubMed  CAS  Google Scholar 

  38. Ranganayakulu G, Elliot DA, Harvey RP, Olson EN. 1998. Divergent roles for NK-2 class homeobox genes in cardiogenesis in flies and mice. Development 125:3037–3048.

    PubMed  CAS  Google Scholar 

  39. Lyons I, Parsons LM, Hardey L, Li R, Andrews JE, Robb L, Harvey RP. 1995. Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2–5. Genes Dev 9:1654–1666.

    PubMed  CAS  Google Scholar 

  40. Biben C, Harvey RP. 1997. Homeodomain factor Nkx2–5 controls left-right asymmetric expression of bHLH eHand during murine heart development. Genes Dev 11:1357–1369.

    PubMed  CAS  Google Scholar 

  41. Zou Y, Evans S, Chen J, Kuo HC, Harvey RP, Chien KR. 1997. CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2–5 homeobox gene pathway. Development 124:793–804.

    PubMed  CAS  Google Scholar 

  42. Fu YC, Izumo S. 1995. Cardiac myogenesis-overexpression of xcsx2 or xmef2a in whole Xenopus embryos induces the precocious expression of xmhc-α gene. Roux Arch Dev Biol 205:198–202.

    CAS  Google Scholar 

  43. Cleaver OB, Patterson KD, Krieg PA. 1996. Overexpression of the tinman-related genes XNkx-2.5 and XNkx-2.3 in Xenopus embryos results in myocardial hyperplasia. Development 122:3549–3556.

    PubMed  CAS  Google Scholar 

  44. Fu Y,Yan W, Mihun TJ, Evans SM. 1998. Vertebrate tinman homologues XNKx2–3 and XNKx2–5 are required for heart formation in a functionally redundant manner. Development 125:4439–4449.

    Google Scholar 

  45. Grow MW, Krieg PA. 1998. Tinman function is essential for vertebrate heart development: Elimination of cardiac differentiation by dominant inhibitory mutants of the tinman-related genes, XNkx2–3 and XNkx2–5. Dev Biol 204:187–196.

    PubMed  CAS  Google Scholar 

  46. Searcy RD, Vincent EB, Liberatore CM, Yutzey KE. 1998. A GATA-dependent nkx-2.5 regulatory element activates early cardiac gene expression in transgenic mice. Development 125:4461–4470.

    PubMed  CAS  Google Scholar 

  47. Durocher D, Chen CY, Ardati A, Schwartz RJ, Nemer M. 1996. The atrial natriuretic factor promoter is a downstream target for Nkx-2.5 in the myocardium. Mol Cell Biol 16:4648–4655.

    PubMed  CAS  Google Scholar 

  48. Durocher D, Charron F, Warren R, Schwartz RJ, Nemer M. 1997. The cardiac transcription factors Nkx2–5 and GATA-4 are mutual cofactors. EMBO J 16:5687–5696.

    PubMed  CAS  Google Scholar 

  49. Lee Y, Shioi T, Kasahara H, Jobe SM, Wiese RJ, Markham BE, Izumo S. 1998. The cardiac tissue-restricted homeobox protein Csx/Nkx2.5 physically associates with the zinc finger protein GATA4 and cooperatively activates atrial natriuretic factor gene expression. Mol Cell Biol 18:3120–3129.

    PubMed  CAS  Google Scholar 

  50. Sepulveda JL, Belaguli N, Nigam V, Chen CY, Nemer M, Schwartz RJ. 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.

    PubMed  CAS  Google Scholar 

  51. Molkentin JD, Antos C, Mercer B, Taigen T, Miano JM, Olson EN. 2000. Direct activation of a GATA6 cardiac enhancer by Nkx2.5: evidence for a reinforcing regulatory network of Nkx2.5 and GATA transcription factors in the developing heart. Dev Biol 217:301–309.

    PubMed  CAS  Google Scholar 

  52. Bruneau BG, Bao ZZ, Tanaka M, Schott JJ, Izumo S, Cepko CL, Seidman JG, Seidman CE. 2000. Cardiac expression of the ventricle-specific homeobox gene Irx4 is modulated by Nkx2–5 and dHand. Dev Biol 217:266–277.

    PubMed  CAS  Google Scholar 

  53. Merika M, Orkin SH. 1993. DNA-binding specificity of GATA family transcription factors. Mol Cell Biol 13:3999–4010.

    PubMed  CAS  Google Scholar 

  54. Jürgens G,Wiechaus E, Nüsslein-Volhard C, Kluding H. 1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the third chromosome. Roux’s Arch Dev Biol 193:283–295.

    Google Scholar 

  55. Ramain P, Heitzler P, Haenlin M, Simpson P. 1993. pannier, a negative regulator of achaete and scute in Drosophila, encodes a zinc finger protein with homology to the vertebrate transcription factor GATA-1. Development 199:1277–1291.

    Google Scholar 

  56. Winick J, Abel T, Leonard MW, Michelson AM, Chardon-Loriaux I, Holmgren RA, Maniatis T, Engel JD. 1993. A GATA family transcription factor is expressed along the embryonic dorsoventral axis in Drosophila melanogaster. Development 119:1055–1065.

    PubMed  CAS  Google Scholar 

  57. Heitzler P, Haenlin M, Ramain P, Calleja M, Simpson P. 1996. A genetic analysis of pannier, a gene necessary for viability of dorsal tissues and brisde positioning in Drosophila. Genetics 143:1271–1286.

    PubMed  CAS  Google Scholar 

  58. Rehorn KP,Thelen H, Michelson AM, Reuter R. 1996. A molecular aspect of hematopoiesis and endoderm development common to vertebrates and Drosophila. Development 122:4023–4031.

    PubMed  CAS  Google Scholar 

  59. Lin WH, Huang LH, Yeh JY, Hoheisel J, Lehrach H, Sun YH,Tsai SF. 1995. Expression of a Drosophila GATA transcription factor in multiple tissues in the developing embryos: identification of homozygous lethal mutants with P-element insertion at the promoter region. J Biol Chem 270: 25150–25158.

    PubMed  CAS  Google Scholar 

  60. Haenlin M, Cubadda Y, Blondeau F, Heitzler P, Lutz Y, Simpson P, Ramain P. 1997. Transcriptional activity of pannier is regulated by heterodimerization of the GATA DNA-binding domain with a cofactor encoded by the u-shaped gene of Drosophila. Genes Dev 11:3096–3108.

    PubMed  CAS  Google Scholar 

  61. Fossett N, Zhang Q, Gajewski K, Choi CY, Kim Y, Schulz RA. 2000. The multitype zinc-finger protein U-shaped functions in heart cell specification in the Drosophila embryo. Proc Natl Acad Sci USA 97:7348–7353.

    PubMed  CAS  Google Scholar 

  62. Orkin SH. 1995. Hematopoiesis: how does it happen? Curr Opin Cell Biol 7:870–877. Review.

    PubMed  CAS  Google Scholar 

  63. Pevny L, Simon MC, Robertson E, Klein WH, Tsai SF, D’Agati V, Orkin SH, Costantini F. 1991. Erythroid differentiation in chimeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature 349:257–260.

    PubMed  CAS  Google Scholar 

  64. Tsai FY, Keller G, Kuo FC, Weiss M, Chen J, Rosenblatt M, Alt FW, Orkin SH. 1994. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 371:221–226.

    PubMed  CAS  Google Scholar 

  65. Pandolfi PP, Roth ME, Karis A, Leonard MW, Dzierzak E, Grosveld FG, Engel JD, Lindenbaum MH. 1995. Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat Genet 11:40–44.

    PubMed  CAS  Google Scholar 

  66. Simon MC. 1995. Gotta have GATA. Nat Genet 11:9–11.

    PubMed  CAS  Google Scholar 

  67. Zheng W, Flavell RA. 1997. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 cells. Cell 89:587–596.

    PubMed  CAS  Google Scholar 

  68. Heikinheimo M, Scandrett JM, Wilson DB. 1994. Localization of transcription factor to regions of the mouse embryo involved in cardiac development. Dev Biol 164:361–373.

    PubMed  CAS  Google Scholar 

  69. Laverriere AC, MacNeill C, Mueller C, Poelmann RE, Burch JBE, Evans T. 1994. GATA 4/5/6, a subfamily of three transcription factors transcribed in developing heart and gut. J Biol Chem 269:23177–23184.

    PubMed  CAS  Google Scholar 

  70. Jiang Y, Evans T. 1996. The Xenopus GATA-4/5/6 genes are associated with cardiac specification and can regulate cardiac-specific transcription during embryogenesis. Dev Biol 174:257–270.

    Google Scholar 

  71. Kelley C, Blumberg H, Zon LI, Evans T. 1993. GATA-4 is a novel transcription factor expressed in the endocardium of the developing heart. Development 118:817–827.

    PubMed  CAS  Google Scholar 

  72. Morrisey EE, Ip HS, Lu MM, Parmacek MS. 1996. GATA-6: a zinc finger transcription factor that is expressed in multiple cell lineages derived from lateral mesoderm. Dev Biol 177:309–322.

    PubMed  CAS  Google Scholar 

  73. Gove C, Walmsley M, Nijjar S, Bertwistle D, Guille M, Partington G, Bomford A, Patient R. 1997. Over-expression of GATA-6 in Xenopus embryos blocks differentiation of heart precursors. EMBO J 16:355–368.

    PubMed  CAS  Google Scholar 

  74. Jiang Y, Tarzami S, Burch JBE, Evans T 1998. Common role for each of the GATA-4/5/6 genes in the regulation of cardiac morphogenesis. Dev Genet 22:263–277.

    PubMed  CAS  Google Scholar 

  75. Kuo CT, Morrisey EE, Anandappa R, Sigrist K, Lu MM, Parmacek MS, Soudais C, Leiden JM. 1997. GATA-4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev 11:1048–1060.

    PubMed  CAS  Google Scholar 

  76. Molkentin JD, Lin Q, Duncan SA, Olson EN. 1997. Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev 11:1061–1072.

    PubMed  CAS  Google Scholar 

  77. Narita N, Bielinska M, Wilson DB. 1996. Cardiomyocyte differentiation by GATA-4-deficient embryonic stem cells. Development 122:3755–3764.

    Google Scholar 

  78. Morrisey EE, Tang Z, Sigrist K, Lu MM, Jiang F, Ip HS, Parmacek MS. 1998. GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev 12:3579–3590.

    PubMed  CAS  Google Scholar 

  79. Koutsourakis M, Langeveld A, Patient R, Beddington R, Grosveld F. 1999. The transcription factor GATA6 is essential for early extraembryonic development. Development 126:723–732.

    CAS  Google Scholar 

  80. Reiter JF, Alexander J, Rodaway A, Yelon D, Patient R, Holder N, Stainier DYR. 1999. Gata5 is required for the development of the heart and endoderm in zebrafish. Genes Dev 13:2983–2995.

    PubMed  CAS  Google Scholar 

  81. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN. 1998. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93:215–228.

    PubMed  CAS  Google Scholar 

  82. Jiang Y, Drysdale TA, Evans T. 1999. A role for GATA-4/5/6 in the regulation of Nkx2.5 expression with implications for patterning of the precardiac field. Dev Biol 16:57–71.

    Google Scholar 

  83. Nüsslein-Volhard C, Wiechaus E, Kluding H. 1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. Roux Arch Dev Biol 193:297–282.

    Google Scholar 

  84. Cubadda Y, Heitzler P, Ray RP, Bourouis M, Remain P, Gelbart W, Simpson P, Haenlin M. 1997. u-shaped encodes a zinc finger protein that regulates the proneural genes acheate and scute during the formation of brisdes in Drosophila. Genes Dev 11:3083–3095.

    PubMed  CAS  Google Scholar 

  85. Lu JR, McKinsey TA, Xu H, Wang DZ, Richardson JA, Olson EN. 1999. FOG-2, a heart- and brain-enriched cofactor for GATA transcription factors. Mol Cell Biol 19:4495–4502.

    PubMed  CAS  Google Scholar 

  86. Fossett N, Tevosian SG, Gajewski R, Zhang Q, Orkin SH, Schulz RA. 2001. The friend of GATA proteins U-shaped, FOG-1, and FOG-2 function as negative regulators of blood, heart, and eye development in Drosophila. Proc Natl Acad Sci USA 98:7342–7347.

    PubMed  CAS  Google Scholar 

  87. Frasch M. 1995. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 374:464–467.

    PubMed  CAS  Google Scholar 

  88. Beiman M, Shilo B, Volk T. 1996. Heartless, a Drosophila FGF receptor homolog, is essential for cell migration and establishment of several mesodermal lineages. Genes Dev 10:2993–3002.

    PubMed  CAS  Google Scholar 

  89. Gisselbrecht S, Skeath J, Doe C, Michelson A. 1996. Heartless encodes a fibroblast growth factor receptor (DFR1/DFGF-R2) involved in the directional migration of early mesodermal cells in the Drosophila embryo. Genes Dev 10:3003–3017.

    PubMed  CAS  Google Scholar 

  90. Tsang AP,Visvader JE, Turner CA, Fujiwara Y, Yu C, Weiss MJ, Crossley M, Orkin SH. 1997. FOG, a multitype zinc finger protein, acts as a cofactor for transcription factor GATA-1 in erythroid and megakaryocytic differentiation. Cell 90:109–119.

    PubMed  CAS  Google Scholar 

  91. Svensson EC, Tufts RL, Polk CE, Leiden JM. 1999. Molecular cloning of FOG-2: a modulator of transcription factor GATA-4 in cardiomyocytes. Proc Natl Acad Sci USA 96:956–961.

    PubMed  CAS  Google Scholar 

  92. Tevosian SG, Deconinck AE, Cantor AB, Rieff HI, Fujiwara Y, Corfas G, Orkin SH. 1999. FOG-2: a novel GATA-family cofactor related to multitype zinc-finger proteins Friend of GATA-1 and U-shaped. Proc Natl Acad Sci USA 96:950–955.

    PubMed  CAS  Google Scholar 

  93. Fox AH, Kowalski K, King GF, Mackay JP, Crossley M. 1998. Key residues characteristic of GATA N-fingers are recognized by FOG. J Biol Chem 273:33595–33603.

    PubMed  CAS  Google Scholar 

  94. Tevosian SG, Deconinck AE, Tanaka M, Schinke M, Litovsky SH, Izumo S, Fujiwara Y, Orkin SH. 2000. FOG-2, a cofactor for GATA transcription factors, is essential for heart morphogenesis and development of coronary vessels from epicardium. Cell 101:729–739.

    PubMed  CAS  Google Scholar 

  95. Svensson EC, Huggins GS, Lin H, Clendenin C, Jiang F, Tufts R, Dardik FB, Leiden JM. 2000. A syndrome of tricuspid atresia in mice with a targeted mutation of the gene encoding Fog-2. Nat Genet 25:353–356.

    PubMed  CAS  Google Scholar 

  96. Gossett LA, Kelven DJ, Sternberg EA, Olson EN. 1989. A new myocyte-specific enhancer-binding factor that recognizes a conserved element associated with multiple muscle-specific genes. Mol Cell Biol 15:1870–1878.

    Google Scholar 

  97. Lilly B, Galewsky S, Firulli AB, Schulz RA, Olson EN. 1994. D-MEF2: a MADS box transcription factor expressed in differentiating mesoderm and muscle cell lineages during Drosophila embryogenesis. Proc Natl Acad Sci USA 91:5662–5666.

    PubMed  CAS  Google Scholar 

  98. Nguyen HT, Bodmer R, Abmayr SM, McDermott JC, Spoerel NA. 1994. D-mef2: a Drosophila mesoderm-specific MADS box-containing gene with a biphasic expression profile during embryo-genesis. Proc Natl Acad Sci USA 91:7520–7524.

    PubMed  CAS  Google Scholar 

  99. Bour BA, O’Brien MA, Lockwood WL, Goldstein ES, Bodmer R,Taghert PH, Abmayr SM, Nguyen HT. 1995. Drosophila MEF2, a transcription factor that is essential for myogenesis. Genes Dev 9:730–741.

    PubMed  CAS  Google Scholar 

  100. Lilly B, Zhao B, Ranganayakulu G, Paterson B, Schulz RA, Olson EN. 1995. Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 267:688–693.

    PubMed  CAS  Google Scholar 

  101. Taylor MV, Beatty KE, Hunter HK, Baylies MK. 1995. Drosophila MEF2 is regulated by twist and is expressed in both the primordia and differentiated cells of the embryonic somatic, visceral, and heart musculature. Mech Dev 50:26–41.

    Google Scholar 

  102. Cripps RM, Black BL, Zhao B, Lien CL, Schulz RA, Olson EN. 1998. The myogenic regulatory gene Mef2 is a direct target for transcriptional activation by Twist during Drosophila myogenesis. Genes Dev 12:422–434.

    PubMed  CAS  Google Scholar 

  103. Schulz RA, Chromey C, Lu MF, Zhao B, Olson EN. 1996. Expression of the D-MEF2 transcription factor in the Drosophila brain suggests a role in neuronal cell differentiation. Oncogene 12: 1827–1831.

    PubMed  CAS  Google Scholar 

  104. Ranganayakulu G, Zhoa B, Dokidis A, Molentin JD, Olson EN, Schulz RA. 1995. A series of mutations in the D-MEF2 transcription factor reveal multiple functions in larval and adult myogenesis in Drosophila. Dev Biol 171:169–181.

    PubMed  CAS  Google Scholar 

  105. Nguyen HT, Xu X. 1998. Drosophila mef2 expression during mesoderm development is controlled by a complex array of cis-acting regulatory modules. Dev Biol 204:550–566.

    PubMed  CAS  Google Scholar 

  106. Gajewski K, Choi CY, Kim Y, Schulz RA. 2000. Genetically distinct cardial cells within the Drosophila heart. Genesis, in press.

    Google Scholar 

  107. Martin JF, Miano JM, Hustad CM, Copeland NG, Jenkins NA, Olson EN. 1994. A Mef2 gene that generates a muscle-specific isoform via alternative mRNA splicing. Mol Cell Biol 14:1647–1656.

    PubMed  CAS  Google Scholar 

  108. Edmondson DG, Lyons GE, Martin JF, Olson EN. 1994. MEF2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis. Development 120:1251–1263.

    PubMed  CAS  Google Scholar 

  109. Molkentin JD, Firulli AB, Black BL, Martin JF, Hustad CM, Copeland N, Jenkins N, Lyons G, Olson EN. 1996. MEF2B is a potent transactivator expressed in early myogenic lineages. Mol Cell Biol 16:3814–3824.

    PubMed  CAS  Google Scholar 

  110. Yu YT, Breitbart RE, Smoot LB, Lee Y, Mahdavi V, 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.

    PubMed  CAS  Google Scholar 

  111. Leifer D, Golden J, Kowall NW. 1994. Myocyte-specific enhancer binding factor 2C expression in human brain development. Neuroscience 63:1067–1079.

    PubMed  CAS  Google Scholar 

  112. Leifer D, Krainc D, Yu YT, McDermott J, Breitbart RE, Heng J, Neve RL, Kosofsky B, Nadal-Ginard B, Lipton SA. 1993. MEF2C, a MADS/MEF2-family transcription factor expressed in a laminar distribution in cerebral cortex. Proc Natl Acad Sci USA 90:1546–1550.

    PubMed  CAS  Google Scholar 

  113. Lin Q, Schwarz J, Bucana C, Olson EN. 1997. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276:1404–1407.

    PubMed  CAS  Google Scholar 

  114. Lin Q, Lu J, Yangisawa H, Webb R, Lyons GE, Richardson JA, Olson EN. 1998. Requirement of the MADS-box transcription factor MEF2C for vascular development. Development 125: 4565–4574.

    PubMed  CAS  Google Scholar 

  115. Bi W, Drake CJ, Schwarz JJ. 1999. The transcription factor MEF2C-null mouse exhibits complex vascular malformations and reduced cardiac expression of angiopoietin I and VEGF. Dev Biol 211:255–267.

    PubMed  CAS  Google Scholar 

  116. Iannello RC, Mar JH, Ordahl CP. 1991. Characterization of a promoter element required for transcription in myocardial cells. J Biol Chem 266:3309–3316.

    PubMed  CAS  Google Scholar 

  117. Zhu H, Garcia AV, Ross RS, Evans SM, Chien KR. 1991. A conserved 28-base-pair element (HF-1) in the rat cardiac myosin light-chain-2 gene confers cardiac-specific and (X-adrenergic-inducible expression in cultured neonatal rat myocardial cells. Mol Cell Biol 11:2273–2281.

    PubMed  CAS  Google Scholar 

  118. Yu YT, Breitbart RE, Smoot LB, Lee Y, Mahdavi V, 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.

    PubMed  CAS  Google Scholar 

  119. Molkentin JD, Markham BE. 1993. Myocyte-specific enhancer-binding factor (MEF-2) regulates OC-cardiac myosin heavy chain gene expression in vitro and in vivo. J Biol Chem 268:19512–19520.

    PubMed  CAS  Google Scholar 

  120. Kuisk IR, Li H,Tran D, Capetanaki Y. 1996. A single MEF2 site governs desmin transcription in both heart and skeletal muscle during mouse embryogenesis. Dev Biol 174:1–13.

    PubMed  CAS  Google Scholar 

  121. Di Lisi R, Millino C, Calabria E, Altruda F, Schiaffino S, Ausoni S. 1998. Combinatorial as-acting elements control tissue-specific activation of the cardiac troponin I gene in vitro and in vivo. J Biol Chem 273:25371–25380.

    PubMed  Google Scholar 

  122. Morin S, Charron F, Robitaille L, Nemer M. 2000. GATA-dependent recruitment of MEF2 protein to target promoters. EMBO J 19:2046–2055.

    PubMed  CAS  Google Scholar 

  123. Black BL, Molkentin JD, Olson EN. 1998. Multiple roles for the MyoD basic region in transmission of transcriptional activation signals and interaction with MEF2. Mol Cell Biol 18:69–77.

    PubMed  CAS  Google Scholar 

  124. Mlodzik M, Hiromi Y, Weber U, Goodman CS, Rubin GM. 1990. The Drosophila seven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates. Cell 60:211–224.

    PubMed  CAS  Google Scholar 

  125. Hiromi Y, Mlodzik M, West SR, Rubin GM, Goodman CS. 1993. Ectopic expression of seven-up causes cell fate changes during ommatidial assembly. Development 118:1123–1135.

    PubMed  CAS  Google Scholar 

  126. Hoshizaki DK, Blackburn T, Price C, Ghosh M, Miles K, Ragucci M, Sweis R. 1994. Embryonic fat-cell lineage in Drosophila melanogaster. Development 120:2489–2499.

    PubMed  CAS  Google Scholar 

  127. Kerber B, Fellert S, Hoch M. 1998. Seven-up, the Drosophila homolog of the COUP-TF orphan receptors, controls cell proliferation in the insect kidney. Genes Dev 12:1781–1786.

    PubMed  CAS  Google Scholar 

  128. Ward EJ, Skeath JB. 2000. Characterization of a novel subset of cardial cells and their progenitors in the Drosophila embryo. Development 127:4959–4969.

    PubMed  CAS  Google Scholar 

  129. Bodmer R, Frasch M. 1999. Genetic determination of Drosophila heart development. In: Heart development. Ed. N Rosethal and R Harvey, 65–90. San Diego: Academic Press.

    Google Scholar 

  130. Frémion F, Astier M, Zaffran S, Guillen A, Homburger V, Sémériva M. 1999. The heterotrimeric protein G0 is required for the formation of heart epithelium in Drosophila. J Cell Biol 145: 1063–1076.

    PubMed  Google Scholar 

  131. Pastoric M, Wang H, Elbrecht A, Tsai SY, Tsai MJ, O’Malley BW. 1986. Control of transcription initiation in vitro requires binding of a transcription factor to the distal promoter of the ovalbumin gene. Mol Cell Biol 6:2784–2791.

    Google Scholar 

  132. Sagami I, Tsai SY, Wang H, Tsai MJ, O’Malley BW. 1986. Identification of two factors required for transcription of the ovalbumin gene. Mol Cell Biol 6:4259–4267.

    PubMed  CAS  Google Scholar 

  133. Wang LH, Tsai SY, Cook RG, Beattie WG, Tsai MJ, O’Malley BW. 1989. COUP transcription factor is a member of the steroid receptor superfamily. Nature 340:163–166.

    PubMed  CAS  Google Scholar 

  134. Tsai SY, Sagami I, Wang H, Tsai MJ, O’Malley BW. 1987. Interactions between a DNA-binding transcription factor (COUP) and a non-DNA binding factor (S300-II). Cell 50:701–709.

    PubMed  CAS  Google Scholar 

  135. Renaud JP, Rochel N, Ruff M, Vivat V, Chambon P, Gronemyer H, Moras D. 1995. Crystal structure of the RAR-gamma ligand-binding domain bound to all-trans retinoic acid. Nature 378:681–689.

    PubMed  CAS  Google Scholar 

  136. Cooney AJ, Tsai SY, O’Malley BW, Tsai MJ. 1992. Chicken ovalbumin upstream promoter transcription factor (COUP-TF) dimers bind to different GGTCA response elements, allowing COUP-TF to repress hormonal induction of the vitamin D3, thyroid hormone, and retinoic acid receptors. Mol Cell Biol 12:4153–4163.

    PubMed  CAS  Google Scholar 

  137. Kliewer SA, Umesono K, Heyman RA, Mangelsdorf DJ, Dyck JA, Evans RM. 1992. Retinoid X receptor-COUP-TF interactions modulate retinoic acid signaling. Proc Natl Acad Sci USA 89:1448–1452.

    PubMed  CAS  Google Scholar 

  138. Tran P, Zhang XK, Salbert G, Hermann T, Lehmann JM, Pfahl M. 1992. COUP orphan receptors are negative regulators of retinoic acid response pathways. Mol Cell Biol 12:4666–4676.

    PubMed  CAS  Google Scholar 

  139. Cooney AJ, Leng X, Tsai SY, O’Malley BW, Tsai MJ. 1993. Multiple mechanisms of chicken ovalbumin upstream promoter transcription factor-dependent repression of transactivation by the vitamin D, thyroid hormone, and retinoic acid receptors. J Biol Chem 268:4152–4160.

    PubMed  CAS  Google Scholar 

  140. Zelhof A, Yao TP, Chen JD, Evans R, McKeown M. 1995. Seven-up inhibits Ultraspiracle-based signaling pathways in vitro and in vivo. Molec Cell Biol 15:6736–6745.

    PubMed  CAS  Google Scholar 

  141. Berrodin TJ, Marks MS, Ozato K, Linney E, Lazar MA. 1992. Heterodimerization among thyroid hormone receptor, retinoic acid receptor, retinoid X receptor, chicken ovalbumin upstream promoter transcription factor, and an endogenous liver protein. Mol Endocrinol 6:1468–1478.

    PubMed  CAS  Google Scholar 

  142. Widom RL, Rhee M, Karathanasis SK. 1992. Repression by ARP-1 sensitizes apolipoprotein AI gene responsiveness to RXR alpha and retinoic acid. Mol Cell Biol 12:3380–3389.

    PubMed  CAS  Google Scholar 

  143. Casanova J, Helmer E, Selmi-Ruby S, Qi JS, Au-Fliegner M, Desai-Yajnik V, Koudinova N, Yarm F, Raaka BM, Samuels HH. 1994. Functional evidence for ligand-dependent dissociation of thyroid hormone and retinoic acid receptors from an inhibitory cellular factor. Mol Cell Biol 14:5756–5765.

    PubMed  CAS  Google Scholar 

  144. Chen JD, Evans RM. 1995. A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature 377:454–457.

    PubMed  CAS  Google Scholar 

  145. Horlein AJ, Naar AM, Heinzel T, Torchia J, Gloss B, Kurokawa R, Ryan A, Kamei Y, Soderstrom M, Glass CK, Rosenfeld MG. 1995. Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 377:397–404.

    PubMed  CAS  Google Scholar 

  146. Leng X, Cooney AJ, Tsai SY, Tsai MJ. 1996. Molecular mechanisms of COUP-TF-mediated transcriptional repression: evidence for transrepression and active repression. Mol Cell Biol 16:2332–2340.

    PubMed  CAS  Google Scholar 

  147. Tsai SY, Tsai MJ. 1997. Chick ovalbumin upstream promoter-transcription factors (COUP TFs): coming of age. Endocr Rev 18:229–240.

    PubMed  Google Scholar 

  148. Fjose A, Weber U, Mlodzik M. 1995. A novel vertebrate svp-related nuclear receptor is expressed as a step gradient in developing rhombomeres and is affected by retinoic acid. Mech Dev 52: 233–246.

    PubMed  CAS  Google Scholar 

  149. Krishnan V, Elberg G, Tsai MJ, Tsai SY. 1997. Identification of a novel sonic hedgehog response element in the chicken ovalbumin upstream promoter-transcription factor II promoter. Mol Endocrinol 11:1458–1466.

    PubMed  CAS  Google Scholar 

  150. Krishnan V, Pereira FA, Qiu Y, Chen CH, Beachy PA,Tsai SY,Tsai MJ. 1997. Mediation of sonic hedgehog-induced expression of COUP-TFII by a protein phosphatase. Science 278:1947–1950.

    PubMed  CAS  Google Scholar 

  151. Pereira FA, Qiu Y, Tsai MJ, Tsai SY. 1995. Chicken ovalbumin upstream promoter transcription factor (COUP-TF): expression during embryogenesis. J Steroid Biochem Mol Biol 53:503–508. Review.

    PubMed  CAS  Google Scholar 

  152. Pereira FA, Qiu Y, Zhou G, Tsai MJ, Tsai SY. 1999. The orphan nuclear receptor COUP-TFII is required for angiogenesis and heart development. Genes Dev 13:1037–1049.

    PubMed  CAS  Google Scholar 

  153. Sato TN,Tozawa Y, Deutsch U, Wolburg-Buchholz K, Fujiwara Y, Gendron-Maguire M, Gridley T, Wolburg H, Risau W, Qin Y. 1995. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 376:70–74.

    PubMed  CAS  Google Scholar 

  154. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD. 1996. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87:1171–1180.

    PubMed  CAS  Google Scholar 

  155. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McClain J, Aldrich TH, Papadopoulos N, Daly TJ, Davis S, Sato TN, Yancopoulos GD. 1997. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277:55–60.

    PubMed  CAS  Google Scholar 

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  1. Department of Biochemistry and Molecular Biology, Graduate Program in Genes & Development, The University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Boulevard, Houston, TX, 77030, USA

    Kathleen Gajewski & Robert A. Schulz

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  1. Kathleen Gajewski
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Correspondence to Kathleen Gajewski .

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Editors and Affiliations

  1. Institute of Physiology, Academy of Sciences of the Czech Republic, Prague, Czech Republic

    Bohuslav Ostadal M.D., D.Sc. (Professor) (Professor)

  2. Jikei University School of Medicine, Tokyo, Japan

    Makoto Nagano M.D., Ph.D. (Professor Emeritus) (Professor Emeritus)

  3. Institute of Cardiovascular Sciences, St. Boniface General Hospital Research Centre, Faculty of Medicine, University of Manitoba, Winnipeg, Canada

    Naranjan S. Dhalla Ph.D., M.D. (Hon.), D.Sc. (Hon.) (Distinguished Professor and Director) (Distinguished Professor and Director)

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Gajewski, K., Schulz, R.A. (2002). Comparative Genetics of Heart Development: Conserved Cardiogenic Factors in Drosophila and Vertebrates. In: Ostadal, B., Nagano, M., Dhalla, N.S. (eds) Cardiac Development. Progress in Experimental Cardiology, vol 4. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0967-7_1

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