Retinal patterning by Pax6-dependent cell adhesion molecules

Developmental Neurobiology

Volumn 70, Issue 11, 2010, Pages 764-780

  Rungger Brändle, Elisabeth ^a   Ripperger, Jürgen A ^b   Steiner, Kurt ^c   Conti, Alain ^a   Stieger, Ariane ^d   Soltanieh, Sahar ^d   Rungger, Duri ^d  

^a HUG   (Switzerland)

^b UNIVERSITY OF FRIBOURG   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Cadherins; Duplication; NCAM; Rosette; RPE

Indexed keywords

BETA ACTIN; CELL ADHESION MOLECULE; MESSENGER RNA; MORPHOLINE DERIVATIVE; NERVE CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR PAX6;

ANIMAL TISSUE; ARTICLE; BINDING SITE; CENTRAL NERVOUS SYSTEM; CHROMATIN IMMUNOPRECIPITATION; COMPUTER ANALYSIS; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; GENE; GENE EXPRESSION; GENE TARGETING; NONHUMAN; NUCLEOTIDE SEQUENCE; PAX6 GENE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RETINA DEVELOPMENT; XENOPUS LAEVIS;

ANIMALS; BLOTTING, WESTERN; BODY PATTERNING; CELL ADHESION MOLECULES, NEURONAL; CHROMATIN IMMUNOPRECIPITATION; EMBRYO, NONMAMMALIAN; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; HOMEODOMAIN PROTEINS; MICROSCOPY, FLUORESCENCE; PAIRED BOX TRANSCRIPTION FACTORS; REPRESSOR PROTEINS; RETINA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; XENOPUS;

EID: 77956704785     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20816     Document Type: Article

References (78)

1. Altmann CR, Chow RL, Lang RA, Hemmati-Brivanlou A. 1997. Lens induction by Pax6 in Xenopus laevis. Dev Biol 185:119-123. (Pubitemid 27244222)
2. Andrews GL, Mastick GS. 2003. R-cadherin is a Pax6-regulated, growth-promoting cue for pioneer axons. J Neurosci 23:9873-9880.
3. Ashery-Padan R, Gruss P. 2001. Pax6 lights-up the way for eye development. Curr Opin Cell Biol 13:706-714. (Pubitemid 33042731)
4. Ashery-Padan R, Marquardt T, Zhou X, 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. (Pubitemid 32531197)
5. Babb SG, Kotradi SM, Shah B, Chiappini-Williamsson C, Bell LN, Schmeiser G, Chen E, et al. 2005. Zebrafish R-cadherin (Cdh4) controls visual system development and differentiation. Dev Dyn 233:930-945. (Pubitemid 40853469)
6. Bailey TA, Kanuga N, Romero IA, Greenwood J, Luthert PJ, Cheetham ME. 2004. Oxidative stress affects the junctional integrity of retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 45:675-684. (Pubitemid 38140530)
7. Barnstable CJ, Hofstein R, Akagawa K. 1985. A marker of early amacrine cell development in rat retina. Brain Res 352:286-290. (Pubitemid 15053561)
8. Bäumer N, Marquardt T, Stoykova A, Spieler D, Treichel D, Ashery-Padan R, Gruss P. 2003. Retinal pigmented epithelium requires the redundant activities of Pax2 and Pax6. Development 130:2903-2915. (Pubitemid 36857239)
9. Bumsted KM, Barnstable CJ. 2000. Dorsal retinal pigment epithelium differentiates as neural retina in the microphthalmia (mi/mi) mouse. Invest Ophthalmol Vis Sci 41:903-908.
10. Cartier L, Laforge T, Feki A, Arnaudeau S, Dubois-Dauphin M, Krause K-H. 2006. Pax6-induced alteration of cell fate: Shape changes, expression of neuronal alpha tubulin, postmitotic phenotype, and cell migration. J Neurobiol 66:421-436.
11. Chalepakis G, Wijnholds J, Giese P, Schachner M, Gruss P. 1994. Characterization of Pax-6 and Hoxa-1 binding to the promoter region of the neural cell adhesion molecule L1. DNA Cell Biol 13:891-900. (Pubitemid 24376821)
12. Chapouton P, Gärtner A, Götz M. 1999. The role of Pax6 in restricting cell migration between developing cortex and basal ganglia. Development 126:5569-5579. (Pubitemid 30035006)
13. Chauhan BK, Reed NA, Yang Y, Cermak L, Renekerm L, Duncan MK, Cvekl A. 2002. A comparative cDNA microarray analysis reveals a spectrum of genes regulated by Pax6 in mouse lens. Genes Cells 7:1267-1283. (Pubitemid 36024602)
14. Chow RL, Altmann CR, Lang RA, Hemmati-Brivanlou A. 1999. Pax6 induces ectopic eyes in a vertebrate. Development 126:4213-4222. (Pubitemid 29509337)
15. Collinson JM, Hill RE, West JD. 2000. Different roles of Pax6 in the optic vesicle and facial epithelium mediate early morphogenesis of the murine eye. Development 127:945-956.
16. Coulombre JL, Coulombre AJ. 1965. Regeneration of neural retina from the pigmented epithelium in the chick embryo. Dev Biol 12:79-92.
17. Cvekl A, Tamm ER. 2004. Anterior eye development and ocular mesenchyme: New insights from mouse models and human diseases. Bioessays 26:374-386. (Pubitemid 38461618)
18. Czerny T, Busslinger M. 1995. DNA-binding and transactivation properties of Pax-6: Three amino acids in the paired domain are responsible for the different sequence recognition of Pax-6 and BSAP (Pax-5). Mol Cell Biol 15:2858-2871.
19. Czerny T, Schaffner G, Busslinger M. 1993. DNA sequence recognition by Pax proteins: Bipartite structure of the paired domain and its binding site. Genes Dev 7:2048-2061. (Pubitemid 23312955)
20. Epstein J, Cai J, Glaser T, Jepeal L, Maas R. 1994. Identification of a Pax paired domain recognition sequence and evidence for DNA-dependent conformational changes. J Biol Chem 269:8355-8361. (Pubitemid 24200253)
21. Erdmann B, Kirsch F-P, Rathien FG, Moré MI. 2003. Ncadherin is essential for retinal lamination in the zebrafish. Dev Dyn 226:570-577. (Pubitemid 36278487)
22. Ginsberg D, DeSimone D, Geiger B. 1991. Expression of a novel cadherin (EP-cadherin) in unfertilized eggs and early Xenopus embryos. Development 111:315-325. (Pubitemid 21920417)
23. Giovannini N, Rungger D. 2002. Antisense inhibition of Xbrachyury impairs mesoderm formation in Xenopus embryos. Dev Growth Differ 44:147-159. (Pubitemid 34437836)
24. Grinchuk O, Kozmik Z, Wu X, Tomarev S. 2005. The optimedin gene is a downstream target of Pax6. J Biol Chem 280:35228-35237. (Pubitemid 41532710)
25. Hill RE, Favor J, Hogan BL, Ton CC, Saunders GF, Hanson IM, Prosser J, et al. 1991. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354:522-525.
26. Hirsch N, Grainger RM. 2000. Induction of the lens. Results Probl Cell Differ 31:51-68.
27. Hirsch N, Harris WA. 1997. Xenopus Pax6 retinal development. J Neurobiol 32:45-61.
28. Hojyo T, Tooi O, Tashiro K, Shiokawa K. 1998. Exogastrula formation in Xenopus laevis embryos depleted with maternal XmN-cadherin mRNA by antisense S-oligo DNA. Biochem Biophys Res Commun 242:170-175. (Pubitemid 28412397)
29. Hollemann T, Bellefroid E, Pieler T. 1998. The Xenopus homolog of the Drosophila gene tailless has a function in early eye development. Development 125:2425-2432. (Pubitemid 28362402)
30. Holst BD, Wang Y, Jones FS, Edelman GM. 1997. A binding site for Pax6 proteins regulates expression of the gene for the neural cell adhesion molecule in the embryonic spinal chord. Proc Natl Acad Sci USA 94:1465-1470. (Pubitemid 27087874)
31. Jaworski C, Sperbeck S, Graham C, Wistow G. 1997. Alternative splicing of Pax6 in bovine eye and evolutionary conservation of intron sequences. Biochem Biophys Res Commun 240:196-202. (Pubitemid 27503774)
32. Jean D, Ewan K, Gruss P. 1998. Molecular regulators involved in vertebrate eye development. Mech Dev 76:3-18. (Pubitemid 28467899)
33. Jimenez D, Lopez-Mascaraque L, de Carlos JA, Valverde F. 2002. Further studies on cortical tangential migration in wild type and Pax-6 mutant mice. J Neurocytol 31:719-728. (Pubitemid 37386660)
34. Job C, Tan S-S. 2003. Constructing the neopallium: The role of intrinsic factors. Dev Biol 257:221-232. (Pubitemid 36506841)
35. Jones L, Lopez-Bendito G, Gruss P, Stoykova A, Molnar Z. 2002. Pax6 is required for the normal development of the forebrain axonal connections. Development 129:5041-5052. (Pubitemid 35355921)
36. Kawano H, Fukuda T, Kubo K, Horie M, Uyemuram K, Takeuchi K, Osumi N, et al. 1999. Pax-6 is required for thalamocortical pathway formation in fetal rats. J Comp Neurol 408:147-160. (Pubitemid 29211194)
37. Kozmik Z. 2005. Pax genes in eye development evolution. Curr Opin Genet Dev 15:430-438. (Pubitemid 40982095)
38. Kudo M, Takayama E, Tadakuma T, Shiokawa K. 1998. Molecular cloning of ssd-form neural cell adhesion molecules (NCAMs) as the major form in Xenopus heart. Biochem Biophys Res Commun 245:127-132. (Pubitemid 28414257)
39. Lee HS, Tomarev SI. 2007. Optimedin induces expression of N-cadherin and stimulates aggregation of NGF-stimulated PC12 cells. Exp Cell Res 313:98-108.
40. Li H, Tierney C, Wen L, Wu JY, Rao Y. 1997. A single morphogenetic field gives rise to two retina primordia under the influence of the prechordal plate. Development 124:603-615. (Pubitemid 27092426)
41. Liu Q, Marrs JA, Chuang JC, Raymond PA. 2001. Cadherin-4 expression in the zebrafish central nervous system and regulation by ventral midline signaling. Brain Res Dev Brain Res 131:17-29. (Pubitemid 33079214)
42. Liu X, Mizoguchi A, Takeichi M, Honda Y, Ide C. 1997. Developmental changes in the subcellular localization of R-cadherin in chick retinal pigment epithelium. Histochem Cell Biol 108:35-43. (Pubitemid 27321671)
43. Malicki J, Jo H, Pujic Z. 2003. Zebrafish N-cadherin, encoded by the glass onion locus, plays an essential role in retinal patterning. Dev Biol 259:95-108. (Pubitemid 36703146)
44. Marmorstein AD, Finnemann SC, Bonilha VL, Rodriguez-Boulan E. 1998. Morphogenesis of the retinal pigment epithelium: Toward understanding retinal degenerative diseases. Ann N Y Acad Sci 857:1-12. (Pubitemid 28526251)
45. Marquardt T, Ashery-Padan R, Andrejewski N, Scardigli R, Guillemot F, Gruss P. 2001. Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105:43-55. (Pubitemid 32323915)
46. Martinez-Morales JR, Rodrigo I, Bovolenta P. 2004. Eye development: A view from the retina pigmented epithelium. Bioessays 26:766-777. (Pubitemid 38987610)
47. Masai I, Lele Z, Yamaguchi M, Komori A, Nakata A, Nishiwaki Y, Wada H, et al. 2003. N-cadherin mediates retinal lamination, maintenance of forebrain compartments and patterning of retinal neurites. Development 130:2479-2494.
48. Mathers PH, Grinberg A, Mahon KA, Jamrich M. 1997. The Rx1a homeobox gene is essential for vertebrate eye development. Nature 387:603-607. (Pubitemid 27248765)
49. Meech R, Kallunki P, Edelman GM, Jones FS. 1999. A binding site for homeodomain and Pax proteins is necessary for L1 cell adhesion molecule gene expression by Pax6 and bone morphogenetic proteins. Proc Natl Acad Sci USA 96:2420-2425. (Pubitemid 29117930)
50. Nakamura H, Watanabe Y. 2005. Isthmus organizer and regionalization of the mesencephalon and metencephalon. Int J Dev Biol 49:231-235. (Pubitemid 40917343)
51. Nichols A, Rungger-Brändle E, Muster L, Rungger D. 1995. Inhibition of Xhox1A gene expression in Xenopus embryos by antisense RNA produced from an expression vector read by RNA polymerase III. Mech Dev 52:37-49.
52. Peng HB. 1991. Xenopus laevis: Practical uses in cell and molecular biology. Solutions and protocols. Methods Cell Biol 36:657-662.
53. Planque N, Leconte L, Coquelle FM, Martin P, Saule S. 2001. Specific Pax6/ Microphthalmia transcription factor interactions involve their DNA-binding domains and inhibit transcriptional properties of both proteins. J Biol Chem 276:29330-29337. (Pubitemid 37452026)
54. Quinn JC, West JD, Hill RE. 1996. Multiple functions of Pax6 in mouse eye and nasal development. Genes Dev 10:435-446.
55. Ripperger JA, Schibler U. 2006. Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nature Gen 38:369-374. (Pubitemid 43315762)
56. Rungger-Brändle E, Englert U, Leuenberger PM. 1987. Exocytic clearing of degraded membrane material from pigment epithelial cells in frog retina. Invest Ophthalmol Vis Sci 28:2026-2037. (Pubitemid 18019961)
57. Sakata-Haga H, Sawada K, Hisano S, Fukui Y. 2001. Abnormalities of cerebellar foliation in rats prenatally exposed to ethanol. Acta Neuropathol (Berl) 102:36-40. (Pubitemid 32734263)
58. Schonhoff SE, Giel-Moloney M, Leiter A. 2004. Minireview: Development and differentiation of gut. Endocrinology 145:2639-2644.
59. Sharma RK, Bergström A, Ehinger B. 1997. Influence of technique and transplantation site on rosette formation in rabbit retinal transplants. Acta Ophthalmol Scand 75:3-10. (Pubitemid 27117175)
60. Simpson TI, Price DJ. 2002. Pax6: A pleiotropic player in development. Bio Essays 24:1041-1061.
61. Sjödin A, Dahl U, Semb H. 1995. Mouse R-cadherin: expression during the organogenesis of pancreas and intestinal tract. Exp Cell Res 221:413-425.
62. Sosinsky A, Bonin CP, Mann RS, Honig B. 2003. Target Explorer: An automated tool for the identification of new target genes for a specified set of transcription factors. Nucleic Acids Res 31:3589-3592. (Pubitemid 37448489)
63. Stoykova A, Götz M, Gruss P, Price J. 1997. Pax6-dependent regulation of adhesive patterning. R-cadherin expression and boundary formation in developing forebrain. Development 124:3765-3777.
64. Stoykova A, Hatano O, Gruss P, Götz M. 2003. Increase in reelin-positive cells in the marginal zone of Pax6 mutant mouse cortex. Cereb Cortex 13:560-571. (Pubitemid 36613162)
65. Stroeva OG, Mitashow VI. 1983. Retinal pigment epithelium: Proliferation and differentiation during development and regeneration. Int Rev Cytol 83:221-293. (Pubitemid 14237808)
66. Summerton J, Weller D. 1997. Morpholino antisense oligomers: Design preparation and properties. Antisense nucleic. Acid Drug Dev 7:187-195. (Pubitemid 27323077)
67. Tashiro K, Tooi O, Nakamura H, Koga C, Ito Y, Hikasa H, Shiokawa K. 1996. Cloning and expression studies of cDNA for a novel Xenopus cadherin (XmN-cadherin), expressed maternally and later neural-specifically in embryogenesis. Mech Dev 54:161-171. (Pubitemid 26062374)
68. Ton CC, Miwa H, Saunders GF. 1992. Small eye (Sey): Cloning and characterization of the murine homolog of the human aniridia gene. Genomics 13:251-256.
69. Tulvatana W, Adamian M, Berson EL, Dryia TP. 1999. Photoreceptor rosettes in autosomal dominant retinitis pigmentosa with reduced penetrance. Arch Ophthalmol 117:399-402. (Pubitemid 29133742)
70. Tuoc TC, Stoykowa A. 2008. Er81 is a downstream target of Pax6 in cortical progenitors. BMC Dev Biol 8:23.
71. Tyas DA, Pearson H, Rashbass P, Price DJ. 2003. Pax6 regulates cell adhesion during cortical development. Cereb Cortex 13:612-619. (Pubitemid 36613169)
72. van Raamsdonk CD, Tilghman SM. 2000. Dosage requirement and allelic expression of PAX6 during lens placode formation. Development 127:5439-5448.
73. Walther C, Gruss P. 1991. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113:1435-1449.
74. Willbold E, Rothermel A, Tomlinson S, Layer P. 2000. Müller cell glia cells reorganize reaggregating chicken retinal cells into correctly laminated in vitro retinae. Glia 29:45-57. (Pubitemid 30031133)
75. Wolf LV, Yang Y, Wang J, Xie Q, Braunger B, Tamm ER, Zavadil J, et al. 2009. Identification of Pax6-dependent gene regulatory networks in the mouse lens. PLOS one 4:e4190.
76. Zaniolo K, Leclerc S, Cvekl A, Vallières L, Bazin R, Larouche K, Guérin SL. 2004. Expression of the alpha4 integrin gene promoter is modulated by the transcription factor Pax-6 in corneal epithelial cells. Invest Ophtalmol Vis Sci 45:1692-1704. (Pubitemid 38868960)
77. Zuber ME, Gestri G, Viczian AS, Barsacchi G, Harris WA. 2003. Specification of the vertebrate eye by a network of eye field transcription factors. Development 130:5155-5167. (Pubitemid 37369675)
78. Zygar CA, Cook TL, Grainger RM Jr. 1998. Gene activation during early stages of lens induction in Xenopus. Development 125:3509-3519. (Pubitemid 28458349)