AP-2α knockout mice exhibit optic cup patterning defects and failure of optic stalk morphogenesis

Human Molecular Genetics

Volumn 19, Issue 9, 2010, Pages 1791-1804

  Bassett, Erin A ^a   Williams, Trevor ^b   Zacharias, Amanda L ^c   Gage, Philip J ^c   Fuhrmann, Sabine ^d   West Mays, Judith A ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR AP 2ALPHA; TRANSCRIPTION FACTOR PAX2; UNCLASSIFIED DRUG; PRIMER DNA; SHH PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; COLOBOMA; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; EYE DEVELOPMENT; EYE MALFORMATION; FOREBRAIN; KNOCKOUT MOUSE; MOUSE; NEUROEPITHELIUM; NONHUMAN; OPTIC DISK CUP; OPTIC NERVE; PHENOTYPE; PIGMENT EPITHELIUM; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TISSUE INTERACTION; ANIMAL; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MORPHOGENESIS; MOUSE MUTANT; NICK END LABELING; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PRENATAL DEVELOPMENT; RETINA;

ERINACEIDAE; MUS;

ANIMALS; DISEASE MODELS, ANIMAL; DNA PRIMERS; EYE ABNORMALITIES; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; MICE; MICE, KNOCKOUT; MORPHOGENESIS; OPTIC NERVE; POLYMERASE CHAIN REACTION; PROSENCEPHALON; RETINA; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-2;

EID: 77952532606     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq060     Document Type: Article

References (88)

1. Wilson, S.W. and Houart, C. (2004) Early steps in the development of the forebrain. Dev. Cell, 6, 167-181.
2. Rubenstein, J.L. and Beachy, P.A. (1998) Patterning of the embryonic forebrain. Curr. Opin. Neurobiol., 8, 18-26.
3. Gage, P.J., Rhoades, W., Prucka, S.K. and Hjalt, T. (2005) Fate maps of neural crest and mesoderm in the mammalian eye. Invest. Ophthalmol. Vis. Sci., 46, 4200-4208.
4. Chow, R.L. and Lang, R.A. (2001) Early eye development in vertebrates. Annu. Rev. Cell. Dev. Biol., 17, 255-296.
5. Yang, X.J. (2004) Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis. Semin. Cell Dev. Biol., 15, 91-103.
6. Huh, S., Hatini, V., Marcus, R.C., Li, S.C. and Lai, E. (1999) Dorsal-ventral patterning defects in the eye of BF-1-deficient mice associated with a restricted loss of shh expression. Dev. Biol., 211, 53-63.
7. Macdonald, R., Barth, K.A., Xu, Q., Holder, N., Mikkola, I. and Wilson, S.W. (1995) Midline signalling is required for Pax gene regulation and patterning of the eyes. Development, 121, 3267-3278.
8. Take-uchi, M., Clarke, J.D. and Wilson, S.W. (2003) Hedgehog signalling maintains the optic stalk-retinal interface through the regulation of Vax gene activity. Development, 130, 955-968.
9. Zhang, X.M. and Yang, X.J. (2001) Temporal and spatial effects of Sonic hedgehog signaling in chick eye morphogenesis. Dev. Biol., 233, 271-290.
10. 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.
11. Hyer, J., Mima, T. and Mikawa, T. (1998) FGF1 patterns the optic vesicle by directing the placement of the neural retina domain. Development, 125, 869-877.
12. 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.
13. Fuhrmann, S., Levine, E.M. and Reh, T.A. (2000) Extraocular mesenchyme patterns the optic vesicle during early eye development in the embryonic chick. Development, 127, 4599-4609.
14. Berry, F.B., Lines, M.A., Oas, J.M., Footz, T., Underhill, D.A., Gage, P.J. and Walter, M.A. (2006) Functional interactions between FOXC1 and PITX2 underlie the sensitivity to FOXC1 gene dose in Axenfeld-Rieger syndrome and anterior segment dysgenesis. Hum. Mol. Genet., 15, 905-919.
15. Evans, A.L. and Gage, P.J. (2005) Expression of the homeobox gene Pitx2 in neural crest is required for optic stalk and ocular anterior segment development. Hum. Mol. Genet., 14, 3347-3359.
16. Cvekl, A. and Tamm, E.R. (2004) Anterior eye development and ocular mesenchyme: new insights from mouse models and human diseases. Bioessays, 26, 374-386.
17. Gage, P.J. and Zacharias, A.L. (2009) Signaling 'cross-talk' is integrated by transcription factors in the development of the anterior segment in the eye. Dev. Dyn., 238, 2149-2162.
18. Adler, R. and Canto-Soler, M.V. (2007) Molecular mechanisms of optic vesicle development: complexities, ambiguities and controversies. Dev. Biol., 305, 1-13.
19. Bharti, K., Nguyen, M.T., Skuntz, S., Bertuzzi, S. and Arnheiter, H. (2006) The other pigment cell: specification and development of the pigmented epithelium of the vertebrate eye. Pigment Cell Res., 19, 380-394.
20. Fujimura, N., Taketo, M.M., Mori, M., Korinek, V. and Kozmik, Z. (2009) Spatial and temporal regulation of Wnt/beta-catenin signaling is essential for development of the retinal pigment epithelium. Dev. Biol., 334, 31-45.
21. Martinez-Morales, J.R., Rodrigo, I. and Bovolenta, P. (2004) Eye development: a view from the retina pigmented epithelium. Bioessays, 26, 766-777.
22. Westenskow, P., Piccolo, S. and Fuhrmann, S. (2009) {beta}-catenin controls differentiation of the retinal pigment epithelium in the mouse optic cup by regulating Mitf and Otx2 expression. Development, 136, 2505-2510.
23. Stoetzel, C., Riehm, S., Bennouna Greene, V., Pelletier, V., Vigneron, J., Leheup, B., Marion, V., Helle, S., Danse, J.M., Thibault, C. et al. (2009) Confirmation of TFAP2A gene involvement in branchio-oculo-facial syndrome (BOFS) and report of temporal bone anomalies. Am. J. Med. Genet. A, 149A, 2141-2146.
24. Tekin, M., Sirmaci, A., Yuksel-Konuk, B., Fitoz, S. and Sennaroglu, L. (2009) A complex TFAP2A allele is associated with branchio-oculo-facial syndrome and inner ear malformation in a deaf child. Am. J. Med. Genet. A, 149A, 427-430.
25. Milunsky, J.M., Maher, T.A., Zhao, G., Roberts, A.E., Stalker, H.J., Zori, R.T., Burch, M.N., Clemens, M., Mulliken, J.B., Smith, R. et al. (2008) TFAP2A mutations result in branchio-oculo-facial syndrome. Am. J. Hum. Genet., 82, 1171-1177.
26. Gestri, G., Osborne, R.J., Wyatt, A.W., Gerrelli, D., Gribble, S., Stewart, H., Fryer, A., Bunyan, D.J., Prescott, K., Collin, J.R. et al. (2009) Reduced TFAP2A function causes variable optic fissure closure and retinal defects and sensitizes eye development to mutations in other morphogenetic regulators. Hum. Genet., 126, 719-803.
27. Lin, A.E., Losken, H.W., Jaffe, R. and Biglan, A.W. (1991) The branchio-oculo-facial syndrome. Cleft Palate Craniofac. J., 28, 96-102.
28. Lin, A.E., Gorlin, R.J., Lurie, I.W., Brunner, H.G., van der Burgt, I., Naumchik, I.V., Rumyantseva, N.V., Stengel-Rutkowski, S., Rosenbaum, K., Meinecke, P. et al. (1995) Further delineation of the branchio-oculo-facial syndrome. Am. J. Med. Genet., 56, 42-59.
29. West-Mays, J.A., Zhang, J., Nottoli, T., Hagopian-Donaldson, S., Libby, D., Strissel, K.J. and Williams, T. (1999) AP-2alpha transcription factor is required for early morphogenesis of the lens vesicle. Dev. Biol., 206, 46-62.
30. West-Mays, J.A., Coyle, B.M., Piatigorsky, J., Papagiotas, S. and Libby, D. (2002) Ectopic expression of AP-2alpha transcription factor in the lens disrupts fiber cell differentiation. Dev. Biol., 245, 13-27.
31. West-Mays, J.A., Sivak, J.M., Papagiotas, S.S., Kim, J., Nottoli, T., Williams, T. and Fini, M.E. (2003) Positive influence of AP-2alpha transcription factor on cadherin gene expression and differentiation of the ocular surface. Differentiation, 71, 206-216.
32. Pontoriero, G.F., Deschamps, P., Ashery-Padan, R., Wong, R., Yang, Y., Zavadil, J., Cvekl, A., Sullivan, S., Williams, T. and West-Mays, J.A. (2008) Cell autonomous roles for AP-2alpha in lens vesicle separation and maintenance of the lens epithelial cell phenotype. Dev. Dyn., 237, 602-617.
33. Dwivedi, D.J., Pontoriero, G.F., Ashery-Padan, R., Sullivan, S., Williams, T. and West-Mays, J.A. (2005) Targeted deletion of AP-2alpha leads to disruption in corneal epithelial cell integrity and defects in the corneal stroma. Invest. Ophthalmol. Vis. Sci., 46, 3623-3630.
34. Bassett, E.A., Pontoriero, G.F., Feng, W., Marquardt, T., Fini, M.E., Williams, T. and West-Mays, J.A. (2007) Conditional deletion of activating protein 2alpha (AP-2alpha) in the developing retina demonstrates non-cell-autonomous roles for AP-2alpha in optic cup development. Mol. Cell. Biol., 27, 7497-7510.
35. Mitchell, P.J., Timmons, P.M., Hebert, J.M., Rigby, P.W. and Tjian, R. (1991) Transcription factor AP-2 is expressed in neural crest cell lineages during mouse embryogenesis. Genes Dev., 5, 105-119.
36. Moser, M., Ruschoff, J. and Buettner, R. (1997) Comparative analysis of AP-2 alpha and AP-2 beta gene expression during murine embryogenesis. Dev. Dyn., 208, 115-124.
37. Schorle, H., Meier, P., Buchert, M., Jaenisch, R. and Mitchell, P.J. (1996) Transcription factor AP-2 essential for cranial closure and craniofacial development. Nature, 381, 235-238.
38. Zhang, J., Hagopian-Donaldson, S., Serbedzija, G., Elsemore, J., Plehn-Dujowich, D., McMahon, A.P., Flavell, R.A. and Williams, T. (1996) Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature, 381, 238-241.
39. Bora, N., Conway, S.J., Liang, H. and Smith, S.B. (1998) Transient overexpression of the Microphthalmia gene in the eyes of Microphthalmia vitiligo mutant mice. Dev. Dyn., 213, 283-292.
40. 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.
41. Liu, I.S., Chen, J.D., Ploder, L., Vidgen, D., van der Kooy, D., Kalnins, V.I. and McInnes, R.R. (1994) Developmental expression of a novel murine homeobox gene (Chx10): evidence for roles in determination of the neuroretina and inner nuclear layer. Neuron, 13, 377-393.
42. Martinez-Morales, J.R., Signore, M., Acampora, D., Simeone, A. and Bovolenta, P. (2001) Otx genes are required for tissue specification in the developing eye. Development, 128, 2019-2030.
43. Galli-Resta, L., Resta, G., Tan, S.S. and Reese, B.E. (1997) Mosaics of islet-1-expressing amacrine cells assembled by short-range cellular interactions. J. Neurosci., 17, 7831-7838.
44. Pak, W., Hindges, R., Lim, Y.S., Pfaff, S.L. and O'Leary, D.D. (2004) Magnitude of binocular vision controlled by islet-2 repression of a genetic program that specifies laterality of retinal axon pathfinding. Cell, 119, 567-578.
45. Koike, C., Nishida, A., Ueno, S., Saito, H., Sanuki, R., Sato, S., Furukawa, A., Aizawa, S., Matsuo, I., Suzuki, N. et al. (2007) Functional roles of Otx2 transcription factor in postnatal mouse retinal development. Mol. Cell. Biol., 27, 8318-8329.
46. Baas, D., Bumsted, K.M., Martinez, J.A., Vaccarino, F.M., Wikler, K.C. and Barnstable, C.J. (2000) The subcellular localization of Otx2 is cell-type specific and developmentally regulated in the mouse retina. Brain Res. Mol. Brain Res., 78, 26-37.
47. Nishida, A., Furukawa, A., Koike, C., Tano, Y., Aizawa, S., Matsuo, I. and Furukawa, T. (2003) Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat. Neurosci., 6, 1255-1263.
48. Schwarz, M., Cecconi, F., Bernier, G., Andrejewski, N., Kammandel, B., Wagner, M. and Gruss, P. (2000) Spatial specification of mammalian eye territories by reciprocal transcriptional repression of Pax2 and Pax6. Development, 127, 4325-4334.
49. Nornes, H.O., Dressler, G.R., Knapik, E.W., Deutsch, U. and Gruss, P. (1990) Spatially and temporally restricted expression of Pax2 during murine neurogenesis. Development, 109, 797-809.
50. Torres, M., Gomez-Pardo, E. and Gruss, P. (1996) Pax2 contributes to inner ear patterning and optic nerve trajectory. Development, 122, 3381-3391.
51. Otteson, D.C., Shelden, E., Jones, J.M., Kameoka, J. and Hitchcock, P.F. (1998) Pax2 expression and retinal morphogenesis in the normal and Krd mouse. Dev. Biol., 193, 209-224.
52. Hero, I. (1990) Optic fissure closure in the normal cinnamon mouse. An ultrastructural study. Invest. Ophthalmol. Vis. Sci., 31, 197-216.
53. Bai, C.B., Auerbach, W., Lee, J.S., Stephen, D. and Joyner, A.L. (2002) Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development, 129, 4753-4761.
54. Sigulinsky, C.L., Green, E.S., Clark, A.M. and Levine, E.M. (2008) Vsx2/Chx10 ensures the correct timing and magnitude of Hedgehog signaling in the mouse retina. Dev. Biol., 317, 560-575.
55. Furimsky, M. and Wallace, V.A. (2006) Complementary Gli activity mediates early patterning of the mouse visual system. Dev. Dyn., 235, 594-605.
56. Hui, C.C., Slusarski, D., Platt, K.A., Holmgren, R. and Joyner, A.L. (1994) Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2 and Gli-3, in ectoderm-and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev. Biol., 162, 402-413.
57. Ericson, J., Muhr, J., Placzek, M., Lints, T., Jessell, T.M. and Edlund, T. (1995) Sonic hedgehog induces the differentiation of ventral forebrain neurons: a common signal for ventral patterning within the neural tube. Cell, 81, 747-756.
58. Patterson, V.L., Damrau, C., Paudyal, A., Reeve, B., Grimes, D.T., Stewart, M.E., Williams, D.J., Siggers, P., Greenfield, A. and Murdoch, J.N. (2009) Mouse hitchhiker mutants have spina bifida, dorso-ventral patterning defects and polydactyly: identification of Tulp3 as a novel negative regulator of the Sonic hedgehog pathway. Hum. Mol. Genet., 18, 1719-1739.
59. Eggenschwiler, J.T. and Anderson, K.V. (2000) Dorsal and lateral fates in the mouse neural tube require the cell-autonomous activity of the open brain gene. Dev. Biol., 227, 648-660.
60. Ericson, J., Muhr, J., Jessell, T.M. and Edlund, T. (1995) Sonic hedgehog: a common signal for ventral patterning along the rostrocaudal axis of the neural tube. Int. J. Dev. Biol., 39, 809-816.
61. Gage, P.J., Suh, H. and Camper, S.A. (1999) Dosage requirement of Pitx2 for development of multiple organs. Development, 126, 4643-4651.
62. Sowden, J.C. (2007) Molecular and developmental mechanisms of anterior segment dysgenesis. Eye, 21, 1310-1318.
63. Silver, J. and Hughes, A.F. (1973) The role of cell death during morphogenesis of the mammalian eye. J. Morphol., 140, 159-170.
64. Laemle, L.K., Puszkarczuk, M. and Feinberg, R.N. (1999) Apoptosis in early ocular morphogenesis in the mouse. Brain Res. Dev. Brain Res., 112, 129-133.
65. Lang, R.A. (1997) Apoptosis in mammalian eye development: lens morphogenesis, vascular regression and immune privilege. Cell Death Differ., 4, 12-20.
66. Silver, J. and Robb, R.M. (1979) Studies on the development of the eye cup and optic nerve in normal mice and in mutants with congenital optic nerve aplasia. Dev. Biol., 68, 175-190.
67. Serbedzija, G.N., Bronner-Fraser, M. and Fraser, S.E. (1992) Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development, 116, 297-307.
68. Brewer, S., Feng, W., Huang, J., Sullivan, S. and Williams, T. (2004) Wnt1-Cre-mediated deletion of AP-2alpha causes multiple neural crest-related defects. Dev. Biol., 267, 135-152.
69. Brewer, S., Jiang, X., Donaldson, S., Williams, T. and Sucov, H.M. (2002) Requirement for AP-2alpha in cardiac outflow tract morphogenesis. Mech. Dev., 110, 139-149.
70. Detwiler, S.R. and van Dyke, R.H. (1953) The induction of neural retina from the pigment epithelial layer of the eye. J. Exp. Zool., 122, 367-383.
71. Dragomirov, N. (1937) The influence of neighboring ectoderm on the organization of eye rudiment. Dokl. Akad. Nauk SSSR, 15, 61-64.
72. Lopashov, G.V. and Stroeva, O.G. (1964) Development of the Eye: Experimental Studies, Davey & Co, New York.
73. Donner, A.L., Lachke, S.A. and Maas, R.L. (2006) Lens induction in vertebrates: variations on a conserved theme of signaling events. Semin. Cell Dev. Biol., 17, 676-685.
74. Chauhan, B.K., Disanza, A., Choi, S.Y., Faber, S.C., Lou, M., Beggs, H.E., Scita, G., Zheng, Y. and Lang, R.A. (2009) Cdc42-and IRSp53-dependent contractile filopodia tether presumptive lens and retina to coordinate epithelial invagination. Development, 136, 3657-3667.
75. McAvoy, J.W. (1980) Cytoplasmic processes interconnect lens placode and optic vesicle during eye morphogenesis. Exp. Eye Res., 31, 527-534.
76. Harris, M.J. and Juriloff, D.M. (1999) Mini-review: toward understanding mechanisms of genetic neural tube defects in mice. Teratology, 60, 292-305.
77. Harris, M.J. and Juriloff, D.M. (2007) Mouse mutants with neural tube closure defects and their role in understanding human neural tube defects. Birth Defects Res. A Clin. Mol. Teratol., 79, 187-210.
78. Kaufman, M. (1979) Cephalic neurulation and optic vesicle formation in the early mouse embryo. Am. J. Anat., 155, 425-443.
79. Milenkovic, L., Goodrich, L.V., Higgins, K.M. and Scott, M.P. (1999) Mouse patched1 controls body size determination and limb patterning. Development, 126, 4431-4440.
80. Goodrich, L.V., Milenkovic, L., Higgins, K.M. and Scott, M.P. (1997) Altered neural cell fates and medulloblastoma in mouse patched mutants. Science, 277, 1109-1113.
81. Yamamoto, Y., Stock, D.W. and Jeffery, W.R. (2004) Hedgehog signalling controls eye degeneration in blind cavefish. Nature, 431, 844-847.
82. Matt, N., Ghyselinck, N.B., Pellerin, I. and Dupe, V. (2008) Impairing retinoic acid signalling in the neural crest cells is sufficient to alter entire eye morphogenesis. Dev. Biol., 320, 140-148.
83. Rodriguez-Gallardo,L., Lineros-Dominguez Mdel, C.,Francisco-Morcillo, J. and Martin-Partido, G. (2005) Macrophages during retina and optic nerve development in the mouse embryo: relationship to cell death and optic fibres. Anat. Embryol. (Berl)., 210, 303-316.
84. Davies, A.F., Mirza, G., Flinter, F. and Ragoussis, J. (1999) An interstitial deletion of 6p24-p25 proximal to the FKHL7 locus and including AP-2alpha that affects anterior eye chamber development. J. Med. Genet., 36, 708-710.
85. Davies, A.F., Mirza, G., Sekhon, G., Turnpenny, P., Leroy, F., Speleman, F., Law, C., van Regemorter, N., Vamos, E., Flinter, F. et al. (1999) Delineation of two distinct 6p deletion syndromes. Hum. Genet., 104, 64-72.
86. Moriarty, A.P. and Kerr-Muir, M.G. (1992) Sclerocornea and interstitial deletion of the short arm of chromosome 6-(46XY del[6] [p22 p24]). J. Pediatr. Ophthalmol. Strabismus, 29, 177-179.
87. Burns, C.J., Zhang, J., Brown, E.C., Van Bibber, A.M., Van Es, J., Clevers, H., Ishikawa, T.O., Taketo, M.M., Vetter, M.L. and Fuhrmann, S. (2008) Investigation of Frizzled-5 during embryonic neural development in mouse. Dev. Dyn., 237, 1614-1626.
88. Henrique, D., Adam, J., Myat, A., Chitnis, A., Lewis, J. and Ish-Horowicz, D. (1995) Expression of a Delta homologue in prospective neurons in the chick. Nature, 375, 787-790.