Mouse Eya homologues of the Drosophila eyes absent gene require Pax6 for expression in lens and nasal placode

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JOURNAL ARTICLES

Mouse Eya homologues of the Drosophila eyes absent gene require Pax6 for expression in lens and nasal placode

PX Xu, I Woo, H Her, DR Beier and RL Maas
Howard Hughes Medical Institute, Brigham and Women's Hospital, Boston, MA 02115, USA.

We have identified and mapped three members of a new family of vertebrate genes, designated Eya1, Eya2 and Eya3, which share high sequence similarity with the Drosophila eyes absent (eya) gene. Comparison of all three murine Eya gene products and that encoded by the Drosophila eya gene defines a 271 amino acid carboxyl terminal Eya domain, which has been highly conserved during evolution. Eya1 and Eya2, which are closely related, are extensively expressed in cranial placodes, in the branchial arches and CNS and in complementary or overlapping patterns during organogenesis. Eya3 is also expressed in the branchial arches and CNS, but lacks cranial placode expression. All three Eya genes are expressed in the developing eye. Eyal is expressed in developing anterior chamber structures, including the lens placode, the iris and ciliary region and the prospective corneal ectoderm. Eyal is also expressed in retinal pigment epithelium and optic nerve. Eya2 is expressed in neural retina, sclera and optic nerve sheath. Moreover, Eya1 and Eya2 expressions in the lens and nasal placode overlap with and depend upon expression of Pax6. The high sequence similarity with Drosophila eya, the conserved developmental expression of Eya genes in the eye and the Pax6 dependence of Eya expression in the lens and nasal placode indicates that these genes likely represent functional homologues of the Drosophila eya gene. These results suggest that members of the Eya gene family play critical roles downstream of Pax genes in specifying placodal identity and support the idea that despite enormous morphological differences, the early development of insect and mammalian eyes is controlled by a conserved regulatory hierarchy.

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				E. Takaki, M. Fujimoto, K. Sugahara, T. Nakahari, S. Yonemura, Y. Tanaka, N. Hayashida, S. Inouye, T. Takemoto, H. Yamashita, et al. Maintenance of Olfactory Neurogenesis Requires HSF1, a Major Heat Shock Transcription Factor in Mice J. Biol. Chem., February 24, 2006; 281(8): 4931 - 4937. [Abstract] [Full Text] [PDF]

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				M. Mutsuddi, B. Chaffee, J. Cassidy, S. J. Silver, T. L. Tootle, and I. Rebay Using Drosophila to Decipher How Mutations Associated With Human Branchio-Oto-Renal Syndrome and Optical Defects Compromise the Protein Tyrosine Phosphatase and Transcriptional Functions of Eyes Absent Genetics, June 1, 2005; 170(2): 687 - 695. [Abstract] [Full Text] [PDF]

				Z. Lin, R. Cantos, M. Patente, and D. K. Wu Gbx2 is required for the morphogenesis of the mouse inner ear: a downstream candidate of hindbrain signaling Development, May 15, 2005; 132(10): 2309 - 2318. [Abstract] [Full Text] [PDF]

				H. Zou, N. K. Osborn, J. J. Harrington, K. K. Klatt, J. R. Molina, L. J. Burgart, and D. A. Ahlquist Frequent Methylation of Eyes Absent 4 Gene in Barrett's Esophagus and Esophageal Adenocarcinoma Cancer Epidemiol. Biomarkers Prev., April 1, 2005; 14(4): 830 - 834. [Abstract] [Full Text] [PDF]

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				R. Grifone, C. Laclef, F. Spitz, S. Lopez, J. Demignon, J.-E. Guidotti, K. Kawakami, P.-X. Xu, R. Kelly, B. J. Petrof, et al. Six1 and Eya1 Expression Can Reprogram Adult Muscle from the Slow-Twitch Phenotype into the Fast-Twitch Phenotype Mol. Cell. Biol., July 15, 2004; 24(14): 6253 - 6267. [Abstract] [Full Text] [PDF]

				C. L. Himeda, J. A. Ranish, J. C. Angello, P. Maire, R. Aebersold, and S. D. Hauschka Quantitative Proteomic Identification of Six4 as the Trex-Binding Factor in the Muscle Creatine Kinase Enhancer Mol. Cell. Biol., March 1, 2004; 24(5): 2132 - 2143. [Abstract] [Full Text] [PDF]

				H. Ozaki, K. Nakamura, J.-i. Funahashi, K. Ikeda, G. Yamada, H. Tokano, H.-o. Okamura, K. Kitamura, S. Muto, H. Kotaki, et al. Six1 controls patterning of the mouse otic vesicle Development, February 1, 2004; 131(3): 551 - 562. [Abstract] [Full Text] [PDF]

				G. Gu, J. M. Wells, D. Dombkowski, F. Preffer, B. Aronow, and D. A. Melton Global expression analysis of gene regulatory pathways during endocrine pancreatic development Development, January 1, 2004; 131(1): 165 - 179. [Abstract] [Full Text] [PDF]

				S. J. Silver, E. L. Davies, L. Doyon, and I. Rebay Functional Dissection of Eyes absent Reveals New Modes of Regulation within the Retinal Determination Gene Network Mol. Cell. Biol., September 1, 2003; 23(17): 5989 - 5999. [Abstract] [Full Text] [PDF]

				W. Zheng, L. Huang, Z.-B. Wei, D. Silvius, B. Tang, and P.-X. Xu The role of Six1 in mammalian auditory system development Development, September 1, 2003; 130(17): 3989 - 4000. [Abstract] [Full Text] [PDF]

				S. Assimacopoulos, E. A. Grove, and C. W. Ragsdale Identification of a Pax6-Dependent Epidermal Growth Factor Family Signaling Source at the Lateral Edge of the Embryonic Cerebral Cortex J. Neurosci., July 23, 2003; 23(16): 6399 - 6403. [Abstract] [Full Text] [PDF]

				P.-X. Xu, W. Zheng, L. Huang, P. Maire, C. Laclef, and D. Silvius Six1 is required for the early organogenesis of mammalian kidney Development, July 15, 2003; 130(14): 3085 - 3094. [Abstract] [Full Text] [PDF]

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				K. Ikeda, Y. Watanabe, H. Ohto, and K. Kawakami Molecular Interaction and Synergistic Activation of a Promoter by Six, Eya, and Dach Proteins Mediated through CREB Binding Protein Mol. Cell. Biol., October 1, 2002; 22(19): 6759 - 6766. [Abstract] [Full Text] [PDF]

				G. Goudreau, P. Petrou, L. W. Reneker, J. Graw, J. Loster, and P. Gruss Mutually regulated expression of Pax6 and Six3 and its implications for the Pax6 haploinsufficient lens phenotype PNAS, June 25, 2002; 99(13): 8719 - 8724. [Abstract] [Full Text] [PDF]

				B. K. Chauhan, W. Zhang, K. Cveklova, M. Kantorow, and A. Cvekl Identification of Differentially Expressed Genes in Mouse Pax6 Heterozygous Lenses Invest. Ophthalmol. Vis. Sci., June 1, 2002; 43(6): 1884 - 1890. [Abstract] [Full Text] [PDF]

				D. M. Wellik, P. J. Hawkes, and M. R. Capecchi Hox11 paralogous genes are essential for metanephric kidney induction Genes & Dev., June 1, 2002; 16(11): 1423 - 1432. [Abstract] [Full Text] [PDF]

				B. K. Chauhan, N. A. Reed, W. Zhang, M. K. Duncan, M. W. Kilimann, and A. Cvekl Identification of Genes Downstream of Pax6 in the Mouse Lens Using cDNA Microarrays J. Biol. Chem., March 22, 2002; 277(13): 11539 - 11548. [Abstract] [Full Text] [PDF]

				S. W. Clark, B. E. Fee, and J. L. Cleveland Misexpression of the Eyes Absent Family Triggers the Apoptotic Program J. Biol. Chem., January 25, 2002; 277(5): 3560 - 3567. [Abstract] [Full Text] [PDF]

				J. Bai and D. Montell Eyes Absent, a key repressor of polar cell fate during Drosophila oogenesis Development, January 12, 2002; 129(23): 5377 - 5388. [Abstract] [Full Text] [PDF]

				P.-X. Xu, W. Zheng, C. Laclef, P. Maire, R. L. Maas, H. Peters, and X. Xu Eya1 is required for the morphogenesis of mammalian thymus, parathyroid and thyroid Development, January 7, 2002; 129(13): 3033 - 3044. [Abstract] [Full Text] [PDF]