Dual transcriptional activities of SIX proteins define their roles in normal and ectopic eye development

Development

Volumn 139, Issue 5, 2012, Pages 991-1000

  Anderson, Abigail M ^a   Weasner, Bonnie M ^a   Weasner, Brandon P ^a   Kumar, Justin P ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Drosophila; Optix; Retinal determination; Sine oculis

Indexed keywords

DNA BINDING PROTEIN; PROTEIN VP16; SIX PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHIMERA; CONTROLLED STUDY; DROSOPHILA; ECTOPIC EYE; EMBRYO; EYE DEVELOPMENT; EYE MALFORMATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RETINA; TRANSCRIPTION INITIATION;

ANIMALS; CELL LINE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MODELS, BIOLOGICAL; PHOTORECEPTOR CELLS, INVERTEBRATE; RECOMBINANT FUSION PROTEINS; REGULATORY SEQUENCES, NUCLEIC ACID; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

VERTEBRATA;

EID: 84856739365     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.077255     Document Type: Article

References (60)

1. Aldaz, S., Morata, G. and Azpiazu, N. (2003). The Pax-homeobox gene eyegone is involved in the subdivision of the thorax of Drosophila. Development 130, 4473-4482.
2. Altmann, C. R., Chow, R. L., Lang, R. A. and Hemmati-Brivanlou, A. (1997). Lens induction by Pax-6 in Xenopus laevis. Dev. Biol. 185, 119-123.
3. Berger, M. F., Badis, G., Gehrke, A. R., Talukder, S., Philippakis, A. A., Pena- Castillo, L., Alleyne, T. M., Mnaimneh, S., Botvinnik, O. B., Chan, E. T. et al. (2008). Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133, 1266-1276.
4. Bischof, J. and Basler, K. (2008). Recombinases and their use in gene activation, gene inactivation, and transgenesis. Methods Mol. Biol. 420, 175-195.
5. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. and Basler, K. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104, 3312-3317.
6. Blochlinger, K., Jan, L. Y. and Jan, Y. N. (1993). Postembryonic patterns of expression of cut, a locus regulating sensory organ identity in Drosophila. Development 117, 441-450.
7. Bodmer, R., Barbel, S., Sheperd, S., Jack, J. W., Jan, L. Y. and Jan, Y. N. (1987). Transformation of sensory organs by mutations of the cut locus of D. melanogaster. Cell 51, 293-307.
8. Bonini, N. M., Leiserson, W. M. and Benzer, S. (1993). The eyes absent gene: genetic control of cell survival and differentiation in the developing Drosophila eye. Cell 72, 379-395.
9. Brugmann, S. A., Pandur, P. D., Kenyon, K. L., Pignoni, F. and Moody, S. A. (2004). Six1 promotes a placodal fate within the lateral neurogenic ectoderm by functioning as both a transcriptional activator and repressor. Development 131, 5871-5881.
10. Cheyette, B. N., Green, P. J., Martin, K., Garren, H., Hartenstein, V. and Zipursky, S. L. (1994). The Drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system. Neuron 12, 977-996.
11. Cohen, S. M. (1993). Imaginal disc development. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez Arias), pp. 747-841. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
12. Czerny, T., Halder, G., Kloter, U., Souabni, A., Gehring, W. J. and Busslinger, M. (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.
13. Datta, R. R., Cruickshank, T. and Kumar, J. P. (2011). Differential selection within the Drosophila retinal determination network and evidence for functional divergence between paralog pairs. Evol. Dev. 13, 58-71.
14. Gallardo, M. E., Lopez-Rios, J., Fernaud-Espinosa, I., Granadino, B., Sanz, R., Ramos, C., Ayuso, C., Seller, M. J., Brunner, H. G., Bovolenta, P. et al. (1999). Genomic cloning and characterization of the human homeobox gene SIX6 reveals a cluster of SIX genes in chromosome 14 and associates SIX6 hemizygosity with bilateral anophthalmia and pituitary anomalies. Genomics 61, 82-91.
15. Giot, L., Bader, J. S., Brouwer, C., Chaudhuri, A., Kuang, B., Li, Y., Hao, Y. L., Ooi, C. E., Godwin, B., Vitols, E. et al. (2003). A protein interaction map of Drosophila melanogaster. Science 302, 1727-1736s.
16. Halder, G., Callaerts, P. and Gehring, W. J. (1995). Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267, 1788-1792.
17. Halder, G., Callaerts, P., Flister, S., Walldorf, U., Kloter, U. and Gegring, W. J. (1998). Eyeless initiates the expression of both sine oculis and eyes absent during drosophila compound eye development. Development 125, 2181-2191.
18. Heanue, T. A., Reshef, R., Davis, R. J., Mardon, G., Oliver, G., Tomarev, S., Lassar, A. B. and Tabin, C. J. (1999). Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation. Genes Dev. 13, 3231-3243.
19. Ikeda, K., Watanabe, Y., Ohto, H. and Kawakami, K. (2002). Molecular interaction and synergistic activation of a promoter by Six, Eya, and Dach proteins mediated through CREB binding protein. Mol. Cell. Biol. 22, 6759-6766.
20. Jang, C. C., Chao, J. L., Jones, N., Yao, L. C., Bessarab, D. A., Kuo, Y. M., Jun, S., Desplan, C., Beckendorf, S. K. and Sun, Y. H. (2003). Two Pax genes, eyegone and eyeless, act cooperatively in promoting Drosophila eye development. Development 130, 2939-2951.
21. Jean, D., Bernier, G. and Gruss, P. (1999). Six6 (Optx2) is a novel murine Six3- related homeobox gene that demarcates the presumptive pituitary/hypothalamic axis and the ventral optic stalk. Mech. Dev. 84, 31-40.
22. Jemc, J. and Rebay, I. (2007a). The eyes absent family of phosphotyrosine phosphatases: properties and roles in developmental regulation of transcription. Annu. Rev. Biochem. 76, 513-538.
23. Jemc, J. and Rebay, I. (2007b). Identification of transcriptional targets of the dualfunction transcription factor/phosphatase eyes absent. Dev. Biol. 310, 416-429.
24. Kenyon, K. L., Ranade, S. S., Curtiss, J., Mlodzik, M. and Pignoni, F. (2003). Coordinating proliferation and tissue specification to promote regional identity in the Drosophila head. Dev. Cell 5, 403-414.
25. Kenyon, K. L., Li, D. J., Clouser, C., Tran, S. and Pignoni, F. (2005a). Fly SIX-type homeodomain proteins Sine oculis and Optix partner with different cofactors during eye development. Dev. Dyn. 234, 497-504.
26. Kenyon, K. L., Yang-Zhou, D., Cai, C. Q., Tran, S., Clouser, C., Decene, G., Ranade, S. and Pignoni, F. (2005b). Partner specificity is essential for proper function of the SIX-type homeodomain proteins Sine oculis and Optix during fly eye development. Dev. Biol. 286, 158-168.
27. Kobayashi, M., Nishikawa, K., Suzuki, T. and Yamamoto, M. (2001). The homeobox protein Six3 interacts with the Groucho corepressor and acts as a transcriptional repressor in eye and forebrain formation. Dev. Biol. 232, 315-326.
28. Li, X., Perissi, V., Liu, F., Rose, D. W. and Rosenfeld, M. G. (2002). Tissuespecific regulation of retinal and pituitary precursor cell proliferation. Science 297, 1180-1183.
29. Li, X., Oghi, K. A., Zhang, J., Krones, A., Bush, K. T., Glass, C. K., Nigam, S. K., Aggarwal, A. K., Maas, R., Rose, D. W. and Rosenfeld, M. G. (2003). Eya protein phosphatase activity regulates Six1-Dach-Eya transcriptional effects in mammalian organogenesis. Nature 426, 247-254.
30. Liu, W., Lagutin, O. V., Mende, M., Streit, A. and Oliver, G. (2006). Six3 activation of Pax6 expression is essential for mammalian lens induction and specification. EMBO J. 25, 5383-5395.
31. Lopez-Rios, J., Tessmar, K., Loosli, F., Wittbrodt, J. and Bovolenta, P. (2003). Six3 and Six6 activity is modulated by members of the groucho family. Development 130, 185-195.
32. Michaut, L., Flister, S., Neeb, M., White, K. P., Certa, U. and Gehring, W. J. (2003). Analysis of the eye developmental pathway in Drosophila using DNA microarrays. Proc. Natl. Acad. Sci. USA 100, 4024-4029.
33. Milani, R. (1941). Two new eye-shape mutant alleles in Drosophila melanogaster. Dros. Inf. Serv. 14, 52.
34. Milani, R. (1951). Linkage data: the locus so of Drosophila melanogaster. Dros. Inf. Serv. 25, 79.
35. Niimi, T., Seimiya, M., Kloter, U., Flister, S. and Gehring, W. J. (1999). Direct regulatory interaction of the eyeless protein with an eye-specific enhancer in the sine oculis gene during eye induction in Drosophila. Development 126, 2253-2260.
36. Noyes, M. B., Christensen, R. G., Wakabayashi, A., Stormo, G. D., Brodsky, M. H. and Wolfe, S. A. (2008). Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 133, 1277-1289.
37. Ohto, H., Kamada, S., Tago, K., Tominaga, S. I., Ozaki, H., Sato, S. and Kawakami, K. (1999). Cooperation of six and eya in activation of their target genes through nuclear translocation of Eya. Mol. Cell. Biol. 19, 6815-6824.
38. Oliver, G., Mailhos, A., Wehr, R., Copeland, N. G., Jenkins, N. A. and Gruss, P. (1995). 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.
39. Ostrin, E. J., Li, Y., Hoffman, K., Liu, J., Wang, K., Zhang, L., Mardon, G. and Chen, R. (2006). Genome-wide identification of direct targets of the Drosophila retinal determination protein Eyeless. Genome Res. 16, 466-476.
40. Pappu, K. S., Ostrin, E. J., Middlebrooks, B. W., Sili, B. T., Chen, R., Atkins, M. R., Gibbs, R. and Mardon, G. (2005). Dual regulation and redundant function of two eye-specific enhancers of the Drosophila retinal determination gene dachshund. Development 132, 2895-2905.
41. Pauli, T., Seimiya, M., Blanco, J. and Gehring, W. J. (2005). Identification of functional sine oculis motifs in the autoregulatory element of its own gene, in the eyeless enhancer and in the signalling gene hedgehog. Development 132, 2771-2782.
42. Pignoni, F., Hu, B., Zavitz, K. H., Xiao, J., Garrity, P. A. and Zipursky, S. L. (1997). The eye-specification proteins So and Eya form a complex and regulate multiple steps in Drosophila eye development. Cell 91, 881-891.
43. Punzo, C., Seimiya, M., Flister, S., Gehring, W. J. and Plaza, S. (2002). Differential interactions of eyeless and twin of eyeless with the sine oculis enhancer. Development 129, 625-634.
44. Quiring, R., Walldorf, U., Kloter, U. and Gehring, W. J. (1994). Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science 265, 785-789.
45. Rayapureddi, J. P., Kattamuri, C., Steinmetz, B. D., Frankfort, B. J., Ostrin, E. J., Mardon, G. and Hegde, R. S. (2003). Eyes absent represents a class of protein tyrosine phosphatases. Nature 426, 295-298.
46. Salzer, C. L. and Kumar, J. P. (2009). Position dependent responses to discontinuities in the retinal determination network. Dev. Biol. 326, 121-130.
47. Salzer, C. L. and Kumar, J. P. (2010). Identification of retinal transformation hot spots in developing Drosophila epithelia. PLoS ONE 5, e8510.
48. Seimiya, M. and Gehring, W. J. (2000). The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless-independent mechanism. Development 127, 1879-1886.
49. Seo, H. C., Curtiss, J., Mlodzik, M. and Fjose, A. (1999). Six class homeobox genes in drosophila belong to three distinct families and are involved in head development. Mech. Dev. 83, 127-139.
50. Serikaku, M. A. and O'Tousa, J. E. (1994). sine oculis is a homeobox gene required for Drosophila visual system development. Genetics 138, 1137-1150.
51. Silver, S. J., Davies, E. L., Doyon, L. and Rebay, I. (2003). Functional dissection of eyes absent reveals new modes of regulation within the retinal determination gene network. Mol. Cell. Biol. 23, 5989-5999.
52. Tanaka-Matakatsu, M. and Du, W. (2008). Direct control of the proneural gene atonal by retinal determination factors during Drosophila eye development. Dev. Biol. 313, 787-801.
53. Tootle, T. L., Silver, S. J., Davies, E. L., Newman, V., Latek, R. R., Mills, I. A., Selengut, J. D., Parlikar, B. E. W. and Rebay, I. (2003). The transcription factor eyes absent is a protein tyrosine phosphatase. Nature 426, 299-302.
54. Toy, J., Yang, J. M., Leppert, G. S. and Sundin, O. H. (1998). The optx2 homeobox gene is expressed in early precursors of the eye and activates retinaspecific genes. Proc. Natl. Acad. Sci. USA 95, 10643-10648.
55. Venken, K. J., He, Y., Hoskins, R. A. and Bellen, H. J. (2006). P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314, 1747-1751.
56. Weasner, B., Salzer, C. and Kumar, J. P. (2007). Sine oculis, a member of the SIX family of transcription factors, directs eye formation. Dev. Biol. 303, 756-771.
57. Weasner, B. M., Weasner, B. P., DeYoung, S. M., Michaels, S. D. and Kumar, J. P. (2009). Transcriptional activities of the Pax6 gene eyeless regulate tissue specificity of ectopic eye formation in Drosophila. Dev. Biol. 334, 492-502.
58. Weasner, B. P. and Kumar, J. P. (2009). The non-conserved C-terminal segments of Sine Oculis Homeobox (SIX) proteins confer functional specificity. Genesis 47, 514-523.
59. Zhang, T., Ranade, S., Cai, C. Q., Clouser, C. and Pignoni, F. (2006). Direct control of neurogenesis by selector factors in the fly eye: regulation of atonal by Ey and So. Development 133, 4881-4889.
60. Zhu, C. C., Dyer, M. A., Uchikawa, M., Kondoh, H., Lagutin, O. V. and Oliver, G. (2002). Six3-mediated auto repression and eye development requires its interaction with members of the Groucho-related family of co-repressors. Development 129, 2835-2849.