Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation

Genes and Development

Volumn 13, Issue 24, 1999, Pages 3231-3243

  Heanue, Tiffany A ^a   Reshef, Ram ^a,e   Davis, Richard J ^b   Mardon, Graeme ^b   Oliver, Guillermo ^c   Tomarev, Stanislav ^d   Lassar, Andrew B ^a   Tabin, Clifford J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d NATIONAL EYE INSTITUTE   (United States)

^e TEL AVIV UNIVERSITY   (Israel)

Author keywords

Dach2; Dachshund; Eya2; Myogenesis; Pax3; Six1; Somite development

Indexed keywords

COMPLEMENTARY DNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DROSOPHILA; EMBRYO; EYE DEVELOPMENT; GENE EXPRESSION REGULATION; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SOMITE; VERTEBRATE;

AMINO ACID SEQUENCE; ANIMALS; CHICK EMBRYO; CONSERVED SEQUENCE; CROSSES, GENETIC; DNA-BINDING PROTEINS; DROSOPHILA; EYE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; MYOD PROTEIN; NUCLEAR PROTEINS; PAIRED BOX TRANSCRIPTION FACTORS; PROTEIN-TYROSINE-PHOSPHATASE; RETINA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; VERTEBRATES;

EID: 0033573003     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.13.24.3231     Document Type: Article

References (71)

1. Bao, Z.Z. and C.L. Cepko. 1997. The expression and function of Notch pathway genes in the developing rat eye. J. Neurosci. 17: 1425-1434.
2. Berk, M., S.Y. Desai, H.C. Heyman, and C. Colmenares. 1997. Mice lacking the ski proto-oncogene have defects in neurulation, craniofacial, patterning, and skeletal muscle development. Genes & Dev. 11: 2029-2039.
3. Blackman, R.K., M. Sanicola, L.A. Raftery, T. Gillevet, and W.M. Gelbart. 1991. An extensive 3′ cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-beta family in Drosophila. Development 111: 657-666.
4. Bonini, N.M., W.M. Leiserson, and S. Benzer. 1993. The eyes absent gene: Genetic control of cell survival and differentiation in the developing Drosophila eye. Cell 72: 379-395.
5. Bonini, N.M., Q.T. Bui, G.L. Gray-Board, and J.M. Warrick. 1997. The Drosophila eyes absent gene directs ectopic eye formation in a pathway conserved between flies and vertebrates. Development 124: 4819-4826.
6. Borsani, G., A. DeGrandi, A. Ballabio, A. Bulfone, L. Bernard, S. Banfi, C. Gattuso, M. Mariani, M. Dixon, D. Donnai, K. Metcalfe, R. Winter, M. Robertson, R. Axton, A. Brown, V. van Heyningen, and I. Hanson. 1999. EYA4, a novel vertebrate gene related to Drosophila eyes absent. Hum. Mol. Genet. 8: 11-23.
7. Borycki, A.G., J. Li, F. Jin, C.P. Emerson, and J.A. Epstein. 1999. Pax3 functions in cell survival and in pax7 regulation. Development 126: 1665-1674.
8. Boyer, P.L., C. Colmenares, E. Stavnezer, and S.H. Hughes. 1993. Sequence and biological activity of chicken snoN cDNA clones. Oncogene 8: 457-466.
9. Brand, A.H. and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
10. Caubit, X., R. Thangarajah, T. Theil, J. Wirth, H.G. Nothwang, U. Ruther, and S. Krauss. 1999. Mouse Dac, a novel nuclear factor with homology to Drosophila dachshund shows a dynamic expression in the neural crest, the eye, the neocortex, and the limb bud. Dev. Dyn. 214: 66-80.
11. Chen, R., M. Amoui, Z. Zhang, and G. Mardon. 1997. Dachshund and eyes absent proteins form a complex and function synergistically to induce ectopic eye development in Drosophila [see comments]. Cell 91: 893-903.
12. Cheyette, B.N., P.J. Green, K. Martin, H. Garren, V. Hartenstein, and S.L. Zipursky. 1994. The Drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system. Neuron 12: 977-996.
13. Christ, B. and C.P. Ordahl. 1995. Early stages of chick somite development. Anat. Embryol. (Berl.) 191: 381-396.
14. Cossu, G., S. Tajbakhsh, and M. Buckingham. 1996. How is myogenesis initiated in the embryo? Trends Genet. 12: 218-223.
15. Czerny, T., G. Halder, U. Kloter, A. Souabni, W.J. Gehring, and M. Busslinger. 1999. twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. Mol Cell 3: 297-307.
16. Davis, R.J., W. Shen, T.A. Heanue, and G. Mardon. 1999. Mouse Dach, a homolog of Drosophila dachshund, is expressed in the developing retina, brain, and limbs. Dev. Genes Evol. (in press)
17. Denetclaw, W.F., Jr., B. Christ, and C.P. Ordahl. 1997. Location and growth of epaxial myotome precursor cells. Development 124: 1601-1610.
18. Dietrich, S., F.R. Schubert, and A. Lumsden. 1997. Control of dorsoventral pattern in the chick paraxial mesoderm. Development 124: 3895-3908.
19. Dressier, G.R., U. Deutsch, K. Chowdhury, H.O. Nornes, and P. Gruss. 1990. Pax2, a new murine paired-box-containing gene and its expression in the developing excretory system. Development 109: 787-795.
20. Ebensperger, C., J. Wilting, B. Brand-Saberi, Y. Mizutani, B. Christ, R. Balling, and H. Koseki. 1995. Pax-1, a regulator of sclerotome development is induced by notochord and floor plate signals in avian embryos. Anat. Embryol. (Berl.) 191: 297-310.
21. Epstein, D.J., M. Vekemans, and P. Gros. 1991. Splotch (Sp2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax-3. Cell 67: 767-774.
22. Esteve, P. and P. Bovolenta. 1999. cSix4, a member of the six gene family of transcription factors, is expressed during placode and somite development. Mech. Dev. 85: 161-165.
23. Fan, C.M. and M. Tessier-Lavigne. 1994. Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog. Cell 79: 1175-1186.
24. Fan, C.M., C.S. Lee, and M. Tessier-Lavigne. 1997. A role for WNT proteins in induction of dermomyotome. Dev. Biol. 191: 160-165.
25. Goulding, M., A. Lumsden, and A.J. Paquette. 1994. Regulation of Pax-3 expression in the dermamyotome and its role in muscle development. Development 120: 957-971.
26. Halder, G., P. Callaerts, and W.J. Gehring. 1995. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila [see comments]. Science 267: 1788-1792.
27. Halder, G., P. Callaerts, S. Flister, U. Walldorf, U. Kloter, and W.J. Gehring. 1998. Eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development. Development 125: 2181-2191.
28. Hamburger, V. and H.L. Hamilton. 1951. A series of normal stages in the development of the chick embryo. J. Morphol. 88: 49-92.
29. Hammond, K.L., I.M. Hanson, A.C. Brown, L.A. Lettice, and R.E. Hill. 1998. Mammalian and Drosophila dachshund genes are related to the Ski proto-oncogene and are expressed in eye and limb. Mech. Dev. 74: 121-131.
30. Kimmel, B.E., U. Heberlein, and G.M. Rubin. 1990. The homeo domain protein rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype. Genes & Dev. 4: 712-727.
31. Kozak, M. 1996. Interpreting cDNA sequences: Some insights from studies on translation. Mamm. Genome 7: 563-574.
32. Lecuit, T. and S.M. Cohen. 1997. Proximal-distal axis formation in the Drosophila leg. Nature 388: 139-145.
33. Lennon, G., C. Auffray, M. Polymeropoulos, and M.B. Soares. 1996. The I.M.A.G.E. Consortium: An integrated molecular analysis of genomes and their expression. Genomics 33: 151-152.
34. Logan, M. and C. Tabin. 1998. Targeted gene misexpression in chick limb buds using avian replication-competent retroviruses. Methods 14: 407-420.
35. Mardon, G., N.M. Solomon, and G.M. Rubin. 1994. dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120: 3473-3486.
36. Maroto, M., R. Reshef, A.E. Munsterberg, S. Koester, M. Goulding, and A.B. Lassar. 1997. Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell 89: 139-148.
37. Mishima, N. and S. Tomarev. 1998. Chicken Eyes absent 2 gene: Isolation and expression pattern during development. Int. J. Dev. Biol. 42: 1109-1115.
38. Molkentin, J.D. and E.N. Olson. 1996. Defining the regulatory networks for muscle development. Curr. Opin. Genet. Dev. 6: 445-453.
39. Munsterberg, A.E., J. Kitajewski, D.A. Bumcrot, A.P. McMahon, and A.B. Lassar. 1995. Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes & Dev. 9: 2911-2922.
40. Nagase, T., N. Nomura, and S. Ishii. 1993. Complex formation between proteins encoded by the ski gene family. J. Biol. Chem. 268: 13710-13716.
41. Nomura, T., M.M. Khan, S.C. Kaul, H.D. Dong, R. Wadhwa, C. Colmenares, I. Kohno, and S. Ishii. 1999. Ski is a component of the histone deacetylase complex required for transcriptional repression by Mad and thyroid hormone receptor. Genes & Dev. 13: 412-423.
42. Ohto, H., S. Kamada, K. Tago, S.I. Tominaga, H. Ozaki, S. Sato, and K. Kawakami. 1999. Cooperation of Six and Eya in activation of their target genes through nuclear translocation of Eya. Mol Cell Biol. 19: 6815-6824.
43. Oliver, G., R. Wehr, N.A. Jenkins, N.G. Copeland, B.N. Cheyette, V. Hartenstein, S.L. Zipursky, and P. Gruss. 1995a. Homeohox genes and connective tissue patterning. Development 121: 693-705.
44. Oliver, G., A. Mailhos, R. Wehr, N.G. Copeland, N.A. Jenkins, and P. Gruss. 1995b. Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 121: 4045-4055.
45. Ordahl, C.P. and N.M. Le Douarin. 1992. Two myogenic lineages within the developing somite. Development 114: 339-353.
46. Ott, M.O., E. Boher, G. Lyons, H. Arnold, and M. Buckingham. 1991. Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111: 1097-1107.
47. Parr, B.A., M.J. Shea, G, Vassileva, and A.P. McMahon. 1993. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119: 247-261.
48. Pearse II, R.V., L.S. Collier, M.P. Scott, and C.J. Tahin. 1999. Vertebrate homologs of Drosophila suppressor of fused interact with the Gli family of transcriptional regulators. Dev. Biol 212: 323-336.
49. Pignoni, F., B. Hu, K.H. Zavitz, J. Xiao, P.A. Garrity, and S.L. Zipursky. 1997. The eye-specification proteins So and Eya form a complex and regulate multiple steps in Drosophila eye development [published erratum appears in Cell 1998 Feb 20, 92: (4) following 585]. Cell 91: 881-891.
50. Pownall, M.E. and C.P. Emerson, Jr. 1992. Sequential activation of three myogenic regulatory genes during somite morphoØ genesis in quail embryos. Dev. Biol. 151: 67-79.
51. Quiring, R., U. Walldorf, U. Kloter, and W.J. Gehring. 1994. Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans [see comments]. Science 265: 785-789.
52. Reshef, R., M. Maroto, and A.B. Lassar. 1998. Regulation of dorsal somitic cell fates: BMPs and Noggin control the timing and pattern of myogenic regulator expression. Genes & Dev. 12: 290-303.
53. Riddle, R.D., R.L. Johnson, E. Laufer, and C. Tabin. 1993. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75: 1401-1416.
54. Robinow, S. and K. White. 1991. Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol. 22: 443-461.
55. Rubin, G.M. and A.C. Spradling. 1983. Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res. 11: 6341-6351.
56. Shen, W. and G. Mardon. 1997. Ectopic eye development in Drosophila induced by directed dachshund expression. Development 124: 45-52.
57. Spitz, F., J. Demignon, A. Porteu, A. Kahn, J.P. Concordet, D. Daegelen, and P. Maire. 1998. Expression of myogenin during embryogenesis is controlled by Six/sine oculis homeo-proteins through a conserved MEF3 binding site. Proc. Natl. Acad. Sci. 95: 14220-14225.
58. Spradling, A.C. and G.M. Rubin. 1982. Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218: 341-347.
59. Staehling-Hampton, K. and F.M. Hoffmann. 1994. Ectopic decapentaplegic in the Drosophila midgut alters the expression of five homeotic genes, dpp, and wingless, causing specific morphological defects. Dev. Biol. 164: 502-512.
60. Tajbakhsh, S., D. Rocancourt, G. Cossu, and M. Buckingham. 1997. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax- 3 and Myf-5 act upstream of MyoD. Cell 89: 127-138.
61. Tajbakhsh, S., U. Borello, E. Vivarelli, R. Kelly, J. Papkoff, D. Duprez, M. Buckingham, and G. Cossu. 1998. Differential activation of Myf5 and MyoD by different Wnts in explants of mouse paraxial mesoderm and the later activation of myogenesis in the absence of Myf5. Development 125: 4155-4162.
62. Toy, J., J.M. Yang, G.S. Leppert, and O.H. Sundin. 1998. The optx2 homeobox gene is expressed in early precursors of the eye and activates retina-specific genes. Proc. Natl. Acad. Sci. 95: 10643-10648.
63. Vortkamp, A., K. Lee, B. Lanske, G.V. Segre, H.M. Kronenberg, and C.J. Tabin. 1996. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein [see comments]. Science 273: 613-622.
64. Walther, C. and P. Gruss. 1991. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113: 1435-1449.
65. Weintraub, H., R. Davis, S. Tapscott, M. Thayer, M. Krause, R. Benezra, T.K. Blackwell, D. Turner, R. Rupp, S. Hollenberg et al. 1991. The myoD gene family: Nodal point during specification of the muscle cell lineage. Science 251: 761-766.
66. Williams, B.A. and C.P. Ordahl. 1994. Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification. Development 120: 785-796.
67. Wolff, T. and D.F. Ready. 1991. The beginning of pattern formation in the Drosophila compound eye: The morphogenetic furrow and the second mitotic wave. Development 113: 841-850.
68. Xu, P.X., J. Cheng, J.A. Epstein, and R.L. Maas. 1997. Mouse Eya genes are expressed during limb tendon development and encode a transcriptional activation function. Proc. Natl. Acad. Sci. 94: 11974-11979.
69. Yamamoto, M., Y. Gotoh, K. Tamura, M. Tanaka, A. Kawakami, H. Ide, and A. Kuroiwa. 1998. Coordinated expression of Hoxa-11 and Hoxa-13 during limb muscle patterning. Development 125: 1325-1335.
70. Zheng, G., J. Teumer, C. Colmenares, C. Richmond, and E. Stavnezer. 1997b. Identification of a core functional and structural domain of the v-Ski oncoprotein responsible for both transformation and myogenesis. Oncogene 15: 459-471.
71. Zheng, G., K.M. Blumenthal, Y. Ji, D.L. Shardy, S.B. Cohen, and E. Stavnezer. 1997a. High affinity dimerization by Ski involves parallel pairing of a novel bipartite alpha-helical domain. J. Biol. Chem. 272: 31855-31864.