Stage-dependent modes of Pax6-Sox2 epistasis regulate lens development and eye morphogenesis

Development

Volumn 136, Issue 17, 2009, Pages 2977-2985

  Smith, April N ^a   Miller, Leigh Anne ^a   Radice, Glenn ^b   Ashery Padan, Ruth ^c   Lang, Richard A ^a,d  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

^d UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Development; Eye; Lens; Morphogenesis; Mouse; Pax6; Sox2

Indexed keywords

NERVE CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX2;

ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA BINDING; ECTODERM; EMBRYO; EPISTASIS; EYE DEVELOPMENT; GENE DELETION; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE INACTIVATION; GENETIC ASSOCIATION; HETEROZYGOSITY; IMMUNOREACTIVITY; LENS; MOUSE; NONHUMAN; OPTIC DISK CUP; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION;

ALLELES; ANIMALS; CADHERINS; EMBRYO, MAMMALIAN; EPISTASIS, GENETIC; EYE; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; LENS, CRYSTALLINE; MICE; MICE, KNOCKOUT; MORPHOGENESIS; PAIRED BOX TRANSCRIPTION FACTORS; PHENOTYPE; REPRESSOR PROTEINS; SOXB1 TRANSCRIPTION FACTORS;

EID: 69049119231     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.037341     Document Type: Article

References (51)

1. Ashery-Padan, R., Marquardt, T., Zhou, X. and Gruss, P. (2000). Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes Dev. 14, 2701-2711.
2. Avilion, A. A., Nicolis, S. K., Pevny, L. H., Perez, L., Vivian, N. and Lovell-Badge, R. (2003). Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 17, 126-140.
3. Bakrania, P., Robinson, D. O., Bunyan, D. J., Salt, A., Martin, A., Crolla, J. A., Wyatt, A., Fielder, A., Ainsworth, J., Moore, A. et al. (2007). SOX2 anophthalmia syndrome: 12 new cases demonstrating broader phenotype and high frequency of large gene deletions. Br. J. Ophthalmol. 91, 1471-1476.
4. Burmeister, M., Novak, J., Liang, M. Y., Basu, S., Ploder, L., Hawes, N. L., Vidgen, D., Hoover, F., Goldman, D., Kalnins, V. I. et al. (1996). Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation. Nat. Genet. 12, 376-384.
5. Callaerts, P., Halder, G. and Gehring, W. J. (1997). PAX-6 in development and evolution. Annu. Rev. Neurosci. 20, 483-532.
6. Chow, R. L. and Lang, R. A. (2001). Early eye development in vertebrates. Annu. Rev. Cell Dev. Biol. 17, 255-296.
7. Chow, R. L., Altmann, C. R., Lang, R. A. and Hemmati-Brivanlou, A. (1999). Pax6 induces ectopic eyes in a vertebrate. Development 126, 4213-4222.
8. Collinson, J. M., Hill, R. E. and West, J. D. (2000). Different roles for Pax6 in the optic vesicle and facial epithelium mediate early morphogenesis of the murine eye. Development 127, 945-956.
9. Dimanlig, P. V., Faber, S. C., Auerbach, W., Makarenkova, H. P. and Lang, R. A. (2001). The upstream ectoderm enhancer in Pax6 has an important role in lens induction. Development 128, 4415-4424.
10. Donner, A. L., Episkopou, V. and Maas, R. L. (2007). Sox2 and Pou2f1 interact to control lens and olfactory placode development. Dev. Biol. 303, 784-799.
11. Fantes, J., Ragge, N. K., Lynch, S. A., McGill, N. I., Collin, J. R., Howard-Peebles, P. N., Hayward, C., Vivian, A. J., Williamson, K., van Heyningen, V. et al. (2003). Mutations in SOX2 cause anophthalmia. Nat. Genet. 33, 461-463.
12. Fujiwara, M., Uchida, T., Osumi-Yamashita, N. and Eto, K. (1994). Uchida rat (rSey): a new mutant rat with craniofacial abnormalities resembling those of the mouse Sey mutant. Differentiation 57, 31-38.
13. Furuta, Y. and Hogan, B. L. M. (1998). BMP4 is essential for lens induction in the mouse embryo. Genes Dev. 12, 3764-3775.
14. Grindley, J. C., Davidson, D. R. and Hill, R. E. (1995). The role of Pax-6 in eye and nasal development. Development 121, 1433-1442.
15. Grindley, J. C., Hargett, L. K., Hill, R. E., Ross, A. and Hogan, B. L. (1997). Disruption of PAX6 function in mice homozygous for the Pax6Sey-1Neu mutation produces abnormalities in the early development and regionalization of the diencephalon. Mech. Dev. 64, 111-126.
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. Hever, A. M., Williamson, K. A. and van Heyningen, V. (2006). Developmental malformations of the eye: the role of PAX6, SOX2 and OTX2. Clin. Genet. 69, 459-470.
18. Hill, R. E., Favor, J., Hogan, B. L., Ton, C. C., Saunders, G. F., Hanson, I. M., Prosser, J., Jordan, T., Hastie, N. D. and van Heyningen, V. (1991). Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354, 522-525.
19. Horsford, D. J., Nguyen, M. T., Sellar, G. C., Kothary, R., Arnheiter, H. and McInnes, R. R. (2005). Chx10 repression of Mitf is required for the maintenance of mammalian neuroretinal identity. Development 132, 177-187.
20. Inoue, M., Kamachi, Y., Matsunami, H., Imada, K., Uchikawa, M. and Kondoh, H. (2007). PAX6 and SOX2-dependent regulation of the Sox2 enhancer N-3 involved in embryonic visual system development. Genes Cells 12, 1049-1061.
21. Kamachi, Y., Uchikawa, M., Collignon, J., Lovell-Badge, R. and Kondoh, H. (1998). Involvement of Sox1, 2 and 3 in the early and subsequent molecular events of lens induction. Development 125, 2521-2532.
22. Kamachi, Y., Uchikawa, M. and Kondoh, H. (2000). Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet. 16, 182-187.
23. Kamachi, Y., Uchikawa, M., Tanouchi, A., Sekido, R. and Kondoh, H. (2001). Pax6 and SOX2 form a co-DNA-binding partner complex that regulates initiation of lens development. Genes Dev. 15, 1272-1286.
24. Kammandel, B., Chowdhury, K., Stoykova, A., Aparicio, S., Brenner, S. and Gruss, P. (1999). Distinct cis-essential modules direct the time-space pattern of the Pax6 gene activity. Dev. Biol. 205, 79-97.
25. Kondoh, H. (2008). Shedding light on developmental gene regulation through the lens. Dev. Growth Differ. 50 Suppl. 1, S57-S69.
26. Kondoh, H., Uchikawa, M. and Kamachi, Y. (2004). Interplay of Pax6 and SOX2 in lens development as a paradigm of genetic switch mechanisms for cell differentiation. Int. J. Dev. Biol. 48, 819-827.
27. Kostetskii, I., Li, J., Xiong, Y., Zhou, R., Ferrari, V. A., Patel, V. V., Molkentin, J. D. and Radice, G. L. (2005). Induced deletion of the N-cadherin gene in the heart leads to dissolution of the intercalated disc structure. Circ. Res. 96, 346-354.
28. Lang, R. A. (2004). Pathways regulating lens induction in the mouse. Int. J. Dev. Biol. 48, 783-791.
29. Li, B., Carey, M. and Workman, J. L. (2007). The role of chromatin during transcription. Cell 128, 707-719.
30. Li, J., Patel, V. V., Kostetskii, I., Xiong, Y., Chu, A. F., Jacobson, J. T., Yu, C., Morley, G. E., Molkentin, J. D. and Radice, G. L. (2005). Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis. Circ. Res. 97, 474-481.
31. 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.
32. Luo, Y., Ferreira-Cornwell, M., Baldwin, H., Kostetskii, I., Lenox, J., Lieberman, M. and Radice, G. (2001). Rescuing the N-cadherin knockout by cardiac-specific expression of N- or E-cadherin. Development 128, 459-469.
33. Macatee, T. L., Hammond, B. P., Arenkiel, B. R., Francis, L., Frank, D. U. and Moon, A. M. (2003). Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 130, 6361-6374.
34. Matsumata, M., Uchikawa, M., Kamachi, Y. and Kondoh, H. (2005). Multiple N-cadherin enhancers identified by systematic functional screening indicate its Group B1 SOX-dependent regulation in neural and placodal development. Dev. Biol. 286, 601-617.
35. Medina-Martinez, O. and Jamrich, M. (2007). Foxe view of lens development and disease. Development 134, 1455-1463.
36. Miyagi, S., Masui, S., Niwa, H., Saito, T., Shimazaki, T., Okano, H., Nishimoto, M., Muramatsu, M., Iwama, A. and Okuda, A. (2008). Consequence of the loss of Sox2 in the developing brain of the mouse. FEBS Lett. 582, 2811-2815.
37. Nguyen, M. and Arnheiter, H. (2000). Signaling and transcriptional regulation in early mammalian eye development: a link between FGF and MITF. Development 127, 3581-3591.
38. Pontoriero, G. F., Smith, A. N., Miller, L. A., Radice, G. L., West-Mays, J. A. and Lang, R. A. (2009). Co-operative roles for E-cadherin and N-cadherin during lens vesicle separation and lens epithelial cell survival. Dev. Biol. 326, 403-417.
39. 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.
40. Radice, G. L., Rayburn, H., Matsunami, H., Knudsen, K. A., Takeichi, M. and Hynes, R. O. (1997). Developmental defects in mouse embryos lacking N-cadherin. Dev. Biol. 181, 64-78.
41. Rodriguez, C. I., Buchholz, F., Galloway, J., Sequerra, R., Kasper, J., Ayala, R., Stewart, A. F. and Dymecki, S. M. (2000). High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 25, 139-140.
42. Smith, A. N., Miller, L. A., Song, N., Taketo, M. M. and Lang, R. A. (2005). The duality of beta-catenin function: a requirement in lens morphogenesis and signaling suppression of lens fate in periocular ectoderm. Dev. Biol. 285, 477-489.
43. Song, N., Schwab, K. R., Patterson, L. T., Yamaguchi, T., Lin, X., Potter, S. S. and Lang, R. A. (2007). pygopus 2 has a crucial, Wnt pathway-independent function in lens induction. Development 134, 1873-1885.
44. St-Onge, L., Sosa-Pineda, B., Chowdhury, K., Mansouri, A. and Gruss, P. (1997). Pax6 is required for differentiation of glucagon-producing alpha-cells in mouse pancreas. Nature 387, 406-409.
45. Taranova, O. V., Magness, S. T., Fagan, B. M., Wu, Y., Surzenko, N., Hutton, S. R. and Pevny, L. H. (2006). SOX2 is a dose-dependent regulator of retinal neural progenitor competence. Genes Dev. 20, 1187-1202.
46. Treisman, J. E. (2004). How to make an eye. Development 131, 3823-3827.
47. Uchikawa, M., Ishida, Y., Takemoto, T., Kamachi, Y. and Kondoh, H. (2003). Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammals. Dev. Cell 4, 509-519.
48. Uwanogho, D., Rex, M., Cartwright, E. J., Pearl, G., Healy, C., Scotting, P. J. and Sharpe, P. T. (1995). Embryonic expression of the chicken Sox2, Sox3 and Sox11 genes suggests an interactive role in neuronal development. Mech. Dev. 49, 23-36.
49. van Raamsdonk, C. D. and Tilghman, S. M. (2000). Dosage requirement and allelic expression of PAX6 during lens placode formation. Development 127, 5439-5448.
50. Williams, S. C., Altmann, C. R., Chow, R. L., Hemmati-Brivanlou, A. and Lang, R. A. (1998). A highly conserved lens transcriptional control element from the Pax-6 gene. Mech. Dev. 73, 225-229.
51. Xu, P. X., Zhang, X., Heaney, S., Yoon, A., Michelson, A. M. and Maas, R. L. (1999). Regulation of Pax6 expression is conserved between mice and flies. Development 126, 383-395.