Transcription factors involved in lens development from the preplacodal ectoderm

Developmental Biology

Volumn 363, Issue 2, 2012, Pages 333-347

  Ogino, Hajime ^a,b   Ochi, Haruki ^a,b   Reza, Hasan Mahmud ^c   Yasuda, Kunio ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c NORTH SOUTH UNIVERSITY   (Bangladesh)

Author keywords

Cranial sensory tissues; Lens; Placode; Preplacodal ectoderm; Regulatory network; Transcription factor

Indexed keywords

TRANSCRIPTION FACTOR;

C MAF GENE; CELL CYCLE; CELL DIFFERENTIATION; CELL ELONGATION; CELL VACUOLE; CRYSTALLIN GENE; DEVELOPMENTAL STAGE; DLX3 GENE; DLX5 GENE; DLX6 GENE; ECTODERM; EYA1 GENE; EYA2 GENE; EYE DEVELOPMENT; FOXE3 GENE; FRAMESHIFT MUTATION; GENE; GENE ACTIVATION; GENE ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; GENE TARGETING; GENOMICS; HUB GENE; HUMAN; L MAF GENE; LENS DEVELOPMENT; MAB21L1 GENE; MAFB GENE; MORPHOGENESIS; NERVOUS TISSUE; NEURAL STEM CELL; NONHUMAN; OPTIC NERVE; OTX2 GENE; PAX6 GENE; PIGMENT EPITHELIUM; PITX3 GENE; PREPLACODAL ECTODERM; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SEQUENCE HOMOLOGY; SIX1 GENE; SIX4 GENE; TISSUE DIFFERENTIATION; TRANSCRIPTION FACTOR GENE; TRANSCRIPTION INITIATION;

EID: 84857115472     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.01.006     Document Type: Review

References (183)

1. Ahrens K., Schlosser G. Tissues and signals involved in the induction of placodal Six1 expression in Xenopus laevis. Dev. Biol. 2005, 288:40-59.
2. Akimenko M.A., et al. Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J. Neurosci. 1994, 14:3475-3486.
3. Andreazzoli M., et al. Xrx1 controls proliferation and neurogenesis in Xenopus anterior neural plate. Development 2003, 130:5143-5154.
4. Aota S., et al. Pax6 autoregulation mediated by direct interaction of Pax6 protein with the head surface ectoderm-specific enhancer of the mouse Pax6 gene. Dev. Biol. 2003, 257:1-13.
5. Ashery-Padan R., et al. Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes Dev. 2000, 14:2701-2711.
6. Bailey A.P., et al. Lens specification is the ground state of all sensory placodes, from which FGF promotes olfactory identity. Dev. Cell 2006, 11:505-517.
7. Baker C.V., Bronner-Fraser M. Vertebrate cranial placodes I. Embryonic induction. Dev. Biol. 2001, 232:1-61.
8. Benkhelifa S., et al. mafA, a novel member of the maf proto-oncogene family, displays developmental regulation and mitogenic capacity in avian neuroretina cells. Oncogene 1998, 17:247-254.
9. Bessarab D.A., et al. Expression of zebrafish six1 during sensory organ development and myogenesis. Dev. Dyn. 2004, 230:781-786.
10. Bhattacharyya S., et al. Segregation of lens and olfactory precursors from a common territory: cell sorting and reciprocity of Dlx5 and Pax6 expression. Dev. Biol. 2004, 271:403-414.
11. Blixt A., et al. A forkhead gene, FoxE3, is essential for lens epithelial proliferation and closure of the lens vesicle. Genes Dev. 2000, 14:245-254.
12. Boucher C.A., et al. Structure, mapping and expression of the human gene encoding the homeodomain protein, SIX2. Gene 2000, 247:145-151.
13. Bovolenta P., et al. Implication of OTX2 in pigment epithelium determination and neural retina differentiation. J. Neurosci. 1997, 17:4243-4252.
14. Bovolenta P., et al. Expression pattern of cSix3, a member of the Six/sine oculis family of transcription factors. Mech. Dev. 1998, 70:201-203.
15. Brownell I., et al. Forkhead Foxe3 maps to the dysgenetic lens locus and is critical in lens development and differentiation. Genesis 2000, 27:81-93.
16. Brugmann S.A., Moody S.A. Induction and specification of the vertebrate ectodermal placodes: precursors of the cranial sensory organs. Biol. Cell 2005, 97:303-319.
17. Brugmann S.A., et al. Six1 promotes a placodal fate within the lateral neurogenic ectoderm by functioning as both a transcriptional activator and repressor. Development 2004, 131:5871-5881.
18. Chow K.L., Emmons S.W. HOM-C/Hox genes and four interacting loci determine the morphogenetic properties of single cells in the nematode male tail. Development 1994, 120:2579-2592.
19. Christophorou N.A., et al. Activation of Six1 target genes is required for sensory placode formation. Dev. Biol. 2009, 336:327-336.
20. Cohen S.M., et al. Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature 1989, 338:432-434.
21. Curtiss J., et al. Selector and signalling molecules cooperate in organ patterning. Nat. Cell Biol. 2002, 4:E48-E51.
22. Cvekl A., Duncan M.K. Genetic and epigenetic mechanisms of gene regulation during lens development. Prog. Retin. Eye Res. 2007, 26:555-597.
23. Cvekl A., et al. Transcriptional regulation of the mouse αA-crystallin gene: activation dependent on a cyclic AMP-responsive element (DE1/CRE) and a Pax-6-binding site. Mol. Cell. Biol. 1995, 15:653-660.
24. Czerny T., et al. Twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. Mol. Cell 1999, 3:297-307.
25. David R., et al. Xenopus Eya1 demarcates all neurogenic placodes as well as migrating hypaxial muscle precursors. Mech. Dev. 2001, 103:189-192.
26. Davidson E.H., et al. A genomic regulatory network for development. Science 2002, 295:1669-1678.
27. Davis R.L., Turner D.L. Vertebrate hairy and enhancer of split related proteins: transcriptional repressors regulating cellular differentiation and embryonic patterning. Oncogene 2001, 20:8342-8357.
28. Davis R.L., et al. Molecular targets of vertebrate segmentation: two mechanisms control segmental expression of Xenopus hairy2 during somite formation. Dev. Cell 2001, 1:553-565.
29. Denny P., et al. A conserved family of genes related to the testis determining gene, SRY. Nucleic Acids Res. 1992, 20:2887.
30. Depew M.J., et al. Dlx5 regulates regional development of the branchial arches and sensory capsules. Development 1999, 126:3831-3846.
31. Desplan C. Eye development: governed by a dictator or a junta?. Cell 1997, 91:861-864.
32. Dimanlig P.V., et al. The upstream ectoderm enhancer in Pax6 has an important role in lens induction. Development 2001, 128:4415-4424.
33. Dominguez M., et al. Growth and specification of the eye are controlled independently by Eyegone and Eyeless in Drosophila melanogaster. Nat. Genet. 2004, 36:31-39.
34. Donner A.L., et al. Sox2 and Pou2f1 interact to control lens and olfactory placode development. Dev. Biol. 2007, 303:784-799.
35. Duncan M.K., et al. Dual roles for Pax-6: a transcriptional repressor of lens fiber cell-specific β-crystallin genes. Mol. Cell. Biol. 1998, 18:5579-5586.
36. Duncan M.K., et al. Prox1 is differentially localized during lens development. Mech. Dev. 2002, 112:195-198.
37. Dutta S., et al. pitx3 defines an equivalence domain for lens and anterior pituitary placode. Development 2005, 132:1579-1590.
38. Eagleson G.W., Harris W.A. Mapping of the presumptive brain regions in the neural plate of Xenopus laevis. J. Neurobiol. 1990, 21:427-440.
39. Eagleson G., et al. Fate of the anterior neural ridge and the morphogenesis of the Xenopus forebrain. J. Neurobiol. 1995, 28:146-158.
40. Easter S.S., Nicola G.N. The development of vision in the zebrafish (Danio rerio). Dev. Biol. 1996, 180:646-663.
41. Esteve P., Bovolenta P. cSix4, a member of the six gene family of transcription factors, is expressed during placode and somite development. Mech. Dev. 1999, 85:161-165.
42. Faber S.C., et al. Fgf receptor signaling plays a role in lens induction. Development 2001, 128:4425-4438.
43. Feledy J.A., et al. Inhibitory patterning of the anterior neural plate in Xenopus by homeodomain factors Dlx3 and Msx1. Dev. Biol. 1999, 212:455-464.
44. Furuta Y., Hogan B.L. BMP4 is essential for lens induction in the mouse embryo. Genes Dev. 1998, 12:3764-3775.
45. Ghanbari H., et al. Molecular cloning and embryonic expression of Xenopus Six homeobox genes. Mech. Dev. 2001, 101:271-277.
46. Glasgow E., Tomarev S.I. Restricted expression of the homeobox gene prox 1 in developing zebrafish. Mech. Dev. 1998, 76:175-178.
47. Goudreau G., et al. Mutually regulated expression of Pax6 and Six3 and its implications for the Pax6 haploinsufficient lens phenotype. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:8719-8724.
48. Grainger R.M. Embryonic lens induction: shedding light on vertebrate tissue determination. Trends Genet. 1992, 8:349-355.
49. Grainger R.M., et al. Reinvestigation of the role of the optic vesicle in embryonic lens induction. Development 1988, 102:517-526.
50. Grifone R., et al. Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo. Development 2005, 132:2235-2249.
51. Grifone R., et al. Eya1 and Eya2 proteins are required for hypaxial somitic myogenesis in the mouse embryo. Dev. Biol. 2007, 302:602-616.
52. Grimm C., et al. Aphakia (ak), a mouse mutation affecting early eye development: fine mapping, consideration of candidate genes and altered Pax6 and Six3 gene expression pattern. Dev. Genet. 1998, 23:299-316.
53. Grindley J.C., et al. The role of Pax-6 in eye and nasal development. Development 1995, 121:1433-1442.
54. Grocott T., et al. Neural crest cells organize the eye via TGF-β and canonical Wnt signalling. Nat. Commun. 2011, 2:265.
55. Halder G., et al. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 1995, 267:1788-1792.
56. Hanson I., Van Heyningen V. Pax6: more than meets the eye. Trends Genet. 1995, 11:268-272.
57. Heanue T.A., et al. Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation. Genes Dev. 1999, 13:3231-3243.
58. Henry J.J., Grainger R.M. Inductive interactions in the spatial and temporal restriction of lens-forming potential in embryonic ectoderm of Xenopus laevis. Dev. Biol. 1987, 124:200-214.
59. Hill R.E., et al. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 1991, 354:522-525.
60. Hirata J., et al. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature 1995, 377:627-630.
61. Hisa T., et al. Hematopoietic, angiogenic and eye defects in Meis1 mutant animals. EMBO J. 2004, 23:450-459.
62. Ho H.Y., et al. Homeodomain protein Pitx3 maintains the mitotic activity of lens epithelial cells. Mech. Dev. 2009, 126:18-29.
63. Hogan B.L., et al. Small eyes (Sey): a homozygous lethal mutation on chromosome 2 which affects the differentiation of both lens and nasal placodes in the mouse. J. Embryol. Exp. Morphol. 1986, 97:95-110.
64. Inoue M., et al. PAX6 and SOX2-dependent regulation of the Sox2 enhancer N-3 involved in embryonic visual system development. Genes Cells 2007, 12:1049-1061.
65. Ishibashi S., Yasuda K. Distinct roles of maf genes during Xenopus lens development. Mech. Dev. 2001, 101:155-166.
66. Ishihara T., et al. Differential expression of Eya1 and Eya2 during chick early embryonic development. Gene Expr. Patterns 2008, 8:357-367.
67. Jacobson A.G. Inductive processes in embryonic development. Science 1966, 152:25-34.
68. Jamieson R.V., et al. Domain disruption and mutation of the bZIP transcription factor, MAF, associated with cataract, ocular anterior segment dysgenesis and coloboma. Hum. Mol. Genet. 2002, 11:33-42.
69. Jang C.C., et al. Two Pax genes, eye gone and eyeless, act cooperatively in promoting Drosophila eye development. Development 2003, 130:2939-2951.
70. Kajihara M., et al. Isolation, characterization, and expression analysis of zebrafish large Mafs. J. Biochem. 2001, 129:139-146.
71. Kamachi Y., et al. Involvement of SOX proteins in lens-specific activation of crystallin genes. EMBO J. 1995, 14:3510-3519.
72. Kamachi Y., et al. Involvement of Sox1, 2 and 3 in the early and subsequent molecular events of lens induction. Development 1998, 125:2521-2532.
73. Kamachi Y., et al. Pax6 and SOX2 form a co-DNA-binding partner complex that regulates initiation of lens development. Genes Dev. 2001, 15:1272-1286.
74. Kammandel B., et al. Distinct cis-essential modules direct the time-space pattern of the Pax6 gene activity. Dev. Biol. 1999, 205:79-97.
75. Kawakami K., et al. Structure, function and expression of a murine homeobox protein AREC3, a homologue of Drosophila sine oculis gene product, and implication in development. Nucleic Acids Res. 1996, 24:303-310.
76. Kawauchi S., et al. Regulation of lens fiber cell differentiation by transcription factor c-Maf. J. Biol. Chem. 1999, 274:19254-19260.
77. Kenyon K.L., et al. A novel fork head gene mediates early steps during Xenopus lens formation. Development 1999, 126:5107-5116.
78. Kleinjan D.A., et al. Aniridia-associated translocations, DNase hypersensitivity, sequence comparison and transgenic analysis redefine the functional domain of PAX6. Hum. Mol. Genet. 2001, 10:2049-2059.
79. Kleinjan D.A., et al. Long-range downstream enhancers are essential for Pax6 expression. Dev. Biol. 2006, 299:563-581.
80. Kobayashi M., et al. Overexpression of the forebrain-specific homeobox gene six3 induces rostral forebrain enlargement in zebrafish. Development 1998, 125:2973-2982.
81. Kobayashi M., et al. Expression of three zebrafish Six4 genes in the cranial sensory placodes and the developing somites. Mech. Dev. 2000, 98:151-155.
82. Konishi Y., et al. Six1 and Six4 promote survival of sensory neurons during early trigeminal gangliogenesis. Brain Res. 2006, 1116:93-102.
83. Laclef C., et al. Thymus, kidney and craniofacial abnormalities in Six 1 deficient mice. Mech. Dev. 2003, 120:669-679.
84. Lagutin O.V., et al. Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev. 2003, 17:368-379.
85. Lang R.A. Pathways regulating lens induction in the mouse. Int. J. Dev. Biol. 2004, 48:783-791.
86. Lee H.Y., et al. Multiple requirements for Hes1 during early eye formation. Dev. Biol. 2005, 284:464-478.
87. Lewis W. Experimental studies on the development of the eye in Amphibia. I. On the region of the lens, Rana Palustris. Am. J. Anat. 1904, 3:505-536.
88. Li H.S., et al. Pax-6 is first expressed in a region of ectoderm anterior to the early neural plate: implications for stepwise determination of the lens. Dev. Biol. 1994, 162:181-194.
89. Litsiou A., et al. A balance of FGF, BMP and WNT signalling positions the future placode territory in the head. Development 2005, 132:4051-4062.
90. Liu W., et al. Six3 activation of Pax6 expression is essential for mammalian lens induction and specification. EMBO J. 2006, 25:5383-5395.
91. Longabaugh W.J., et al. Computational representation of developmental genetic regulatory networks. Dev. Biol. 2005, 283:1-16.
92. Lovicu F.J., McAvoy J.W. Growth factor regulation of lens development. Dev. Biol. 2005, 280:1-14.
93. Luo T., et al. Differential regulation of Dlx gene expression by a BMP morphogenetic gradient. Int. J. Dev. Biol. 2001, 45:681-684.
94. Lyon M.F., et al. A dominant mutation within the DNA-binding domain of the bZIP transcription factor Maf causes murine cataract and results in selective alteration in DNA binding. Hum. Mol. Genet. 2003, 12:585-594.
95. Machon O., et al. Lens morphogenesis is dependent on Pax6-mediated inhibition of the canonical Wnt/β-catenin signaling in the lens surface ectoderm. Genesis 2010, 48:86-95.
96. Mariani M., et al. Mab21, the mouse homolog of a C. elegans cell-fate specification gene, participates in cerebellar, midbrain and eye development. Mech. Dev. 1998, 79:131-135.
97. Mariani M., et al. Two murine and human homologs of mab-21, a cell fate determination gene involved in Caenorhabditis elegans neural development. Hum. Mol. Genet. 1999, 8:2397-2406.
98. Martinez-Morales J.R., et al. Otx genes are required for tissue specification in the developing eye. Development 2001, 128:2019-2030.
99. Matsuo I., et al. Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 1995, 9:2646-2658.
100. McAvoy J.W. Induction of the eye lens. Differentiation 1980, 17:137-149.
101. McLarren K.W., et al. DLX5 positions the neural crest and preplacode region at the border of the neural plate. Dev. Biol. 2003, 259:34-47.
102. Medina-Martinez O., et al. Pitx3 controls multiple aspects of lens development. Dev. Dyn. 2009, 238:2193-2201.
103. Mercier P., et al. Expression pattern of two otx genes suggests a role in specifying anterior body structures in zebrafish. Int. J. Dev. Biol. 1995, 39:559-573.
104. Murato Y., Hashimoto C. Xhairy2 functions in Xenopus lens development by regulating p27(xic1) expression. Dev. Dyn. 2009, 238:2179-2192.
105. Muta M., et al. Distinct roles of SOX2, Pax6 and Maf transcription factors in the regulation of lens-specific δ1-crystallin enhancer. Genes Cells 2002, 7:791-805.
106. Nishiguchi S., et al. Sox1 directly regulates the γ-crystallin genes and is essential for lens development in mice. Genes Dev. 1998, 12:776-781.
107. Nornes S., et al. Zebrafish contains two pax6 genes involved in eye development. Mech. Dev. 1998, 77:185-196.
108. Ochi H., et al. The stability of the lens-specific Maf protein is regulated by fibroblast growth factor (FGF)/ERK signaling in lens fiber differentiation. J. Biol. Chem. 2003, 278:537-544.
109. Ogino H., Yasuda K. Induction of lens differentiation by activation of a bZIP transcription factor, L-Maf. Science 1998, 280:115-118.
110. Ogino H., Yasuda K. Sequential activation of transcription factors in lens induction. Dev. Growth Differ. 2000, 42:437-448.
111. Ogino H., et al. Convergence of a head-field selector Otx2 and Notch signaling: a mechanism for lens specification. Development 2008, 135:249-258.
112. Ohto H., et al. Cooperation of six and eya in activation of their target genes through nuclear translocation of Eya. Mol. Cell. Biol. 1999, 19:6815-6824.
113. Oliver G., et al. Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech. Dev. 1993, 44:3-16.
114. Oliver G., et al. 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 1995, 121:4045-4055.
115. Oliver G., et al. Homeobox genes and connective tissue patterning. Development 1995, 121:693-705.
116. Oliver G., et al. Ectopic lens induction in fish in response to the murine homeobox gene Six3. Mech. Dev. 1996, 60:233-239.
117. Ormestad M., et al. Foxe3 haploinsufficiency in mice: a model for Peters' anomaly. Invest. Ophthalmol. Vis. Sci. 2002, 43:1350-1357.
118. Ozaki H., et al. Six4, a putative myogenin gene regulator, is not essential for mouse embryonal development. Mol. Cell. Biol. 2001, 21:3343-3350.
119. Ozaki H., et al. Six1 controls patterning of the mouse otic vesicle. Development 2004, 131:551-562.
120. Pandur P.D., Moody S.A. Xenopus Six1 gene is expressed in neurogenic cranial placodes and maintained in the differentiating lateral lines. Mech. Dev. 2000, 96:253-257.
121. Panganiban G., Rubenstein J.L. Developmental functions of the Distal-less/Dlx homeobox genes. Development 2002, 129:4371-4386.
122. Penzel R., et al. Characterization and early embryonic expression of a neural specific transcription factor xSOX3 in Xenopus laevis. Int. J. Dev. Biol. 1997, 41:667-677.
123. Perveen R., et al. A heterozygous c-Maf transactivation domain mutation causes congenital cataract and enhances target gene activation. Hum. Mol. Genet. 2007, 16:1030-1038.
124. Piatigorsky J. Lens differentiation in vertebrates. A review of cellular and molecular features. Differentiation 1981, 19:134-153.
125. Pignoni F., et al. The eye-specification proteins So and Eya form a complex and regulate multiple steps in Drosophila eye development. Cell 1997, 91:881-891.
126. Plouhinec J.L., et al. Comparative analysis of gnathostome Otx gene expression patterns in the developing eye: implications for the functional evolution of the multigene family. Dev. Biol. 2005, 278:560-575.
127. Pommereit D., et al. Xpitx3: a member of the Rieg/Pitx gene family expressed during pituitary and lens formation in Xenopus laevis. Mech. Dev. 2001, 102:255-257.
128. Purcell P., et al. Pax6-dependence of Six3, Eya1 and Dach1 expression during lens and nasal placode induction. Gene Expr. Patterns 2005, 6:110-118.
129. Quint E., et al. Differential expression of orthologous Dlx genes in zebrafish and mice: implications for the evolution of the Dlx homeobox gene family. J. Exp. Zool. 2000, 288:235-241.
130. Quiring R., et al. Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science 1994, 265:785-789.
131. Rajagopal R., et al. The type I BMP receptors, Bmpr1a and Acvr1, activate multiple signaling pathways to regulate lens formation. Dev. Biol. 2009, 335:305-316.
132. Reza H.M., Yasuda K. Lens differentiation and crystallin regulation: a chick model. Int. J. Dev. Biol. 2004, 48:805-817.
133. Reza H.M., Yasuda K. Roles of Maf family proteins in lens development. Dev. Dyn. 2004, 229:440-448.
134. Reza H.M., et al. L-Maf, a downstream target of Pax6, is essential for chick lens development. Mech. Dev. 2002, 116:61-73.
135. Reza H.M., et al. L-Maf regulates p27kip1 expression during chick lens fiber differentiation. Differentiation 2007, 75:737-744.
136. Reza H.M., et al. Sequential and combinatorial roles of maf family genes define proper lens development. Mol. Vis. 2007, 13:18-30.
137. Rieger D.K., et al. A double-deletion mutation in the Pitx3 gene causes arrested lens development in aphakia mice. Genomics 2001, 72:61-72.
138. Ring B.Z., et al. Regulation of mouse lens fiber cell development and differentiation by the Maf gene. Development 2000, 127:307-317.
139. Robledo R.F., et al. The Dlx5 and Dlx6 homeobox genes are essential for craniofacial, axial, and appendicular skeletal development. Genes Dev. 2002, 16:1089-1101.
140. Rowan S., et al. Notch signaling regulates growth and differentiation in the mammalian lens. Dev. Biol. 2008, 321:111-122.
141. Rowan S., et al. Precise temporal control of the eye regulatory gene Pax6 via enhancer-binding site affinity. Genes Dev. 2010, 24:980-985.
142. Sahly I., et al. The zebrafish eya1 gene and its expression pattern during embryogenesis. Dev. Genes Evol. 1999, 209:399-410.
143. Sato S., et al. Conserved expression of mouse Six1 in the pre-placodal region (PPR) and identification of an enhancer for the rostral PPR. Dev. Biol. 2010, 344:158-171.
144. Schlosser G. Induction and specification of cranial placodes. Dev. Biol. 2006, 294:303-351.
145. Seimiya M., Gehring W.J. The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless-independent mechanism. Development 2000, 127:1879-1886.
146. Semina E.V., et al. Isolation of a new homeobox gene belonging to the Pitx/Rieg family: expression during lens development and mapping to the aphakia region on mouse chromosome 19. Hum. Mol. Genet. 1997, 6:2109-2116.
147. Semina E.V., et al. A novel homeobox gene PITX3 is mutated in families with autosomal-dominant cataracts and ASMD. Nat. Genet. 1998, 19:167-170.
148. Semina E.V., et al. Deletion in the promoter region and altered expression of Pitx3 homeobox gene in aphakia mice. Hum. Mol. Genet. 2000, 9:1575-1585.
149. Semina E.V., et al. Mutations in the human forkhead transcription factor FOXE3 associated with anterior segment ocular dysgenesis and cataracts. Hum. Mol. Genet. 2001, 10:231-236.
150. Seo H.C., et al. Six class homeobox genes in Drosophila belong to three distinct families and are involved in head development. Mech. Dev. 1999, 83:127-139.
151. Shi X., et al. Zebrafish foxe3: roles in ocular lens morphogenesis through interaction with pitx3. Mech. Dev. 2006, 123:761-782.
152. Shimada N., et al. Cooperative action between L-Maf and Sox2 on δ-crystallin gene expression during chick lens development. Mech. Dev. 2003, 120:455-465.
153. Simeone A., et al. A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J. 1993, 12:2735-2747.
154. Sjodal M., et al. Time of exposure to BMP signals plays a key role in the specification of the olfactory and lens placodes ex vivo. Dev. Cell 2007, 13:141-149.
155. Smith A.N., et al. The duality of β-catenin function: a requirement in lens morphogenesis and signaling suppression of lens fate in periocular ectoderm. Dev. Biol. 2005, 285:477-489.
156. Smith A.N., et al. Stage-dependent modes of Pax6-Sox2 epistasis regulate lens development and eye morphogenesis. Development 2009, 136:2977-2985.
157. Spemann H. Über Correlationen in der Entwicklung des Auges. Verh. Anat. Ges. 1901, 15:61-79.
158. Streit A. The preplacodal region: an ectodermal domain with multipotential progenitors that contribute to sense organs and cranial sensory ganglia. Int. J. Dev. Biol. 2007, 51:447-461.
159. Stump R.J., et al. A role for Wnt/β-catenin signaling in lens epithelial differentiation. Dev. Biol. 2003, 259:48-61.
160. Swindell E.C., et al. Eye formation in the absence of retina. Dev. Biol. 2008, 322:56-64.
161. Takeuchi T., et al. Neither MafA/L-Maf nor MafB is essential for lens development in mice. Genes Cells 2009, 14:941-947.
162. Tomarev S.I., et al. Chicken homeobox gene Prox1 related to Drosophila prospero is expressed in the developing lens and retina. Dev. Dyn. 1996, 206:354-367.
163. van Heyningen V., Williamson K.A. PAX6 in sensory development. Hum. Mol. Genet. 2002, 11:1161-1167.
164. Vogel-Hopker A., et al. Multiple functions of fibroblast growth factor-8 (FGF-8) in chick eye development. Mech. Dev. 2000, 94:25-36.
165. Walther C., Gruss P. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 1991, 113:1435-1449.
166. Wawersik S., Maas R.L. Vertebrate eye development as modeled in Drosophila. Hum. Mol. Genet. 2000, 9:917-925.
167. Wawersik S., et al. BMP7 acts in murine lens placode development. Dev. Biol. 1999, 207:176-188.
168. Wigle J.T., et al. Prox1 function is crucial for mouse lens-fibre elongation. Nat. Genet. 1999, 21:318-322.
169. Williams S.C., et al. A highly conserved lens transcriptional control element from the Pax-6 gene. Mech. Dev. 1998, 73:225-229.
170. Woda J.M., et al. Dlx proteins position the neural plate border and determine adjacent cell fates. Development 2003, 130:331-342.
171. Xu P.X., et al. Mouse Eya homologues of the Drosophila eyes absent gene require Pax6 for expression in lens and nasal placode. Development 1997, 124:219-231.
172. Xu P.X., et al. Eya1-deficient mice lack ears and kidneys and show abnormal apoptosis of organ primordia. Nat. Genet. 1999, 23:113-117.
173. Xu P.X., et al. Regulation of Pax6 expression is conserved between mice and flies. Development 1999, 126:383-395.
174. Yamada R., et al. Cell-autonomous involvement of Mab21l1 is essential for lens placode development. Development 2003, 130:1759-1770.
175. Yang L., et al. An early phase of embryonic Dlx5 expression defines the rostral boundary of the neural plate. J. Neurosci. 1998, 18:8322-8330.
176. Yang Y., et al. Regulation of αA-crystallin via Pax6, c-Maf, CREB and a broad domain of lens-specific chromatin. EMBO J. 2006, 25:2107-2118.
177. Yoshimoto A., et al. Regulation of ocular lens development by Smad-interacting protein 1 involving Foxe3 activation. Development 2005, 132:4437-4448.
178. Zhang X., et al. Meis homeoproteins directly regulate Pax6 during vertebrate lens morphogenesis. Genes Dev. 2002, 16:2097-2107.
179. Zhao H., et al. Fibroblast growth factor receptor signaling is essential for lens fiber cell differentiation. Dev. Biol. 2008, 318:276-288.
180. Zhou X., et al. Cloning and expression of xSix3, the Xenopus homologue of murine Six3. Mech. Dev. 2000, 91:327-330.
181. Zhu C.C., et al. Six3-mediated auto repression and eye development requires its interaction with members of the Groucho-related family of co-repressors. Development 2002, 129:2835-2849.
182. Zilinski C.A., et al. Modulation of zebrafish pitx3 expression in the primordia of the pituitary, lens, olfactory epithelium and cranial ganglia by hedgehog and nodal signaling. Genesis 2005, 41:33-40.
183. Zygar C.A., et al. Gene activation during early stages of lens induction in Xenopus. Development 1998, 125:3509-3519.