Conditional Deletion of Activating Protein 2α (AP-2α) in the Developing Retina Demonstrates Non-Cell-Autonomous Roles for AP-2α in Optic Cup Development

REFERENCES

• Akagawa, K., M. Takada, H. Hayashi, and K. Uyemura. 1990. Calcium- and voltage-dependent potassium channel in the rat retinal amacrine cells identified in vitro using a cell type-specific monoclonal antibody. Brain Res. 518:1–5.
   PubMedGoogle Scholar
• Baumer, N., T. Marquardt, A. Stoykova, R. Ashery-Padan, K. Chowdhury, and P. Gruss. 2002. Pax6 is required for establishing naso-temporal and dorsal characteristics of the optic vesicle. Development 129:4535–4545.
   PubMedGoogle Scholar
• Bisgrove, D. A., and R. Godbout. 1999. Differential expression of AP-2α and AP-2β in the developing chick retina: repression of R-FABP promoter activity by AP-2. Dev. Dyn. 214:195–206.
   PubMedGoogle Scholar
• Bisgrove, D. A., E. A. Monckton, and R. Godbout. 1997. Involvement of AP-2 in regulation of the R-FABP gene in the developing chick retina. Mol. Cell. Biol. 17:5935–5945.
   PubMedGoogle Scholar
• Bosher, J. M., N. F. Totty, J. J. Hsuan, T. Williams, and H. C. Hurst. 1996. A family of AP-2 proteins regulates c-erbB-2 expression in mammary carcinoma. Oncogene 13:1701–1707.
   PubMedGoogle Scholar
• Brewer, S., W. Feng, J. Huang, S. Sullivan, and T. Williams. 2004. Wnt1-Cre-mediated deletion of AP-2α causes multiple neural crest-related defects. Dev. Biol. 267:135–152.
   PubMedGoogle Scholar
• Brewer, S., X. Jiang, S. Donaldson, T. Williams, and H. M. Sucov. 2002. Requirement for AP-2α in cardiac outflow tract morphogenesis. Mech. Dev. 110:139–149.
   PubMedGoogle Scholar
• Buettner, R., M. Moser, A. Pscherer, A. Imhof, R. Bauer, and F. Hofstaedter. 1994. Molecular cloning of a new AP-2 transcription factor, AP-2beta, and its function in cell differentiation. Verh. Dtsch. Ges. Pathol. 78:38–42. (In German.)
   PubMedGoogle Scholar
• Burmeister, M., J. Novak, M. Y. Liang, S. Basu, L. Ploder, N. L. Hawes, D. Vidgen, F. Hoover, D. Goldman, V. I. Kalnins, T. H. Roderick, B. A. Taylor, M. H. Hankin, and R. R. McInnes. 1996. Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation. Nat. Genet. 12:376–384.
   PubMed Web of Science ®Google Scholar
• Cepko, C. L. 1999. The roles of intrinsic and extrinsic cues and bHLH genes in the determination of retinal cell fates. Curr. Opin. Neurobiol. 9:37–46.
   PubMed Web of Science ®Google Scholar
• Cepko, C. L., C. P. Austin, X. Yang, M. Alexiades, and D. Ezzeddine. 1996. Cell fate determination in the vertebrate retina. Proc. Natl. Acad. Sci. USA 93:589–595.
   PubMed Web of Science ®Google Scholar
• Chen, D., I. Livne-bar, J. L. Vanderluit, R. S. Slack, M. Agochiya, and R. Bremner. 2004. Cell-specific effects of RB or RB/p107 loss on retinal development implicate an intrinsically death-resistant cell-of-origin in retinoblastoma. Cancer Cell 5:539–551.
   PubMedGoogle Scholar
• Chow, R. L., and R. A. Lang. 2001. Early eye development in vertebrates. Annu. Rev. Cell Dev. Biol. 17:255–296.
   PubMed Web of Science ®Google Scholar
• de Melo, J., G. Du, M. Fonseca, L. A. Gillespie, W. J. Turk, J. L. Rubenstein, and D. D. Eisenstat. 2005. Dlx1 and Dlx2 function is necessary for terminal differentiation and survival of late-born retinal ganglion cells in the developing mouse retina. Development 132:311–322.
   PubMedGoogle Scholar
• de Melo, J., X. Qiu, G. Du, L. Cristante, and D. D. Eisenstat. 2003. Dlx1, Dlx2, Pax6, Brn3b, and Chx10 homeobox gene expression defines the retinal ganglion and inner nuclear layers of the developing and adult mouse retina. J. Comp. Neurol. 461:187–204.
   PubMedGoogle Scholar
• Dwivedi, D. J., G. F. Pontoriero, R. Ashery-Padan, S. Sullivan, T. Williams, and J. A. West-Mays. 2005. Targeted deletion of AP-2alpha leads to disruption in corneal epithelial cell integrity and defects in the corneal stroma. Investig. Ophthalmol. Vis. Sci. 46:3623–3630.
   PubMedGoogle Scholar
• Eckert, D., S. Buhl, S. Weber, R. Jager, and H. Schorle. 2005. The AP-2 family of transcription factors. Genome Biol. 6:246.
   PubMed Web of Science ®Google Scholar
• Feng, W., and T. Williams. 2003. Cloning and characterization of the mouse AP-2 epsilon gene: a novel family member expressed in the developing olfactory bulb. Mol. Cell Neurosci. 24:460–475.
   PubMedGoogle Scholar
• Galli-Resta, L., G. Resta, S. S. Tan, and B. E. Reese. 1997. Mosaics of islet-1-expressing amacrine cells assembled by short-range cellular interactions. J. Neurosci. 17:7831–7838.
   PubMed Web of Science ®Google Scholar
• Gan, L., S. W. Wang, Z. Huang, and W. H. Klein. 1999. POU domain factor Brn-3b is essential for retinal ganglion cell differentiation and survival but not for initial cell fate specification. Dev. Biol. 210:469–480.
   PubMedGoogle Scholar
• Gan, L., M. Xiang, L. Zhou, D. S. Wagner, W. H. Klein, and J. Nathans. 1996. POU domain factor Brn-3b is required for the development of a large set of retinal ganglion cells. Proc. Natl. Acad. Sci. USA 93:3920–3925.
   PubMedGoogle Scholar
• Hatakeyama, J., and R. Kageyama. 2004. Retinal cell fate determination and bHLH factors. Semin. Cell Dev. Biol. 15:83–89.
   PubMed Web of Science ®Google Scholar
• Haverkamp, S., F. Haeseleer, and A. Hendrickson. 2003. A comparison of immunocytochemical markers to identify bipolar cell types in human and monkey retina. Vis. Neurosci. 20:589–600.
   PubMed Web of Science ®Google Scholar
• Hilger-Eversheim, K., M. Moser, H. Schorle, and R. Buettner. 2000. Regulatory roles of AP-2 transcription factors in vertebrate development, apoptosis and cell-cycle control. Gene 260:1–12.
   PubMed Web of Science ®Google Scholar
• Hinds, J. W., and P. L. Hinds. 1978. Early development of amacrine cells in the mouse retina: an electron microscopic, serial section analysis. J. Comp. Neurol. 179:277–300.
   PubMedGoogle Scholar
• Hu, M., and S. S. Easter. 1999. Retinal neurogenesis: the formation of the initial central patch of postmitotic cells. Dev. Biol. 207:309–321.
   PubMed Web of Science ®Google Scholar
• Inoue, T., M. Hojo, Y. Bessho, Y. Tano, J. E. Lee, and R. Kageyama. 2002. Math3 and NeuroD regulate amacrine cell fate specification in the retina. Development 129:831–842.
   PubMed Web of Science ®Google Scholar
• Kageyama, R., J. Hatakeyama, and T. Ohtsuka. 2006. Roles of Hes bHLH factors in neural development, p. 3–22. In G. Thiel (ed.), Transcription factors in the nervous system: development, brain function, and diseases. Wiley, Hoboken, NJ.
   Google Scholar
• Kageyama, R., T. Ohtsuka, J. Hatakeyama, and R. Ohsawa. 2005. Roles of bHLH genes in neural stem cell differentiation. Exp. Cell Res. 306:343–348.
   PubMed Web of Science ®Google Scholar
• Kammandel, B., K. Chowdhury, A. Stoykova, S. Aparicio, S. Brenner, and P. Gruss. 1999. Distinct cis-essential modules direct the time-space pattern of the Pax6 gene activity. Dev. Biol. 205:79–97.
   PubMedGoogle Scholar
• Li, S., Z. Mo, X. Yang, S. M. Price, M. M. Shen, and M. Xiang. 2004. Foxn4 controls the genesis of amacrine and horizontal cells by retinal progenitors. Neuron 43:795–807.
   PubMedGoogle Scholar
• Livesey, F. J., and C. L. Cepko. 2001. Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2:109–118.
   PubMed Web of Science ®Google Scholar
• Marquardt, T. 2003. Transcriptional control of neuronal diversification in the retina. Prog. Retin. Eye Res. 22:567–577.
   PubMed Web of Science ®Google Scholar
• Marquardt, T., R. Ashery-Padan, N. Andrejewski, R. Scardigli, F. Guillemot, and P. Gruss. 2001. Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105:43–55.
   PubMed Web of Science ®Google Scholar
• Marquardt, T., and P. Gruss. 2002. Generating neuronal diversity in the retina: one for nearly all. Trends Neurosci. 25:32–38.
   PubMed Web of Science ®Google Scholar
• Masland, R. H. 1988. Amacrine cells. Trends Neurosci. 11:405–410.
   PubMed Web of Science ®Google Scholar
• McCabe, K. L., E. C. Gunther, and T. A. Reh. 1999. The development of the pattern of retinal ganglion cells in the chick retina: mechanisms that control differentiation. Development 126:5713–5724.
   PubMedGoogle Scholar
• Mitchell, P. J., P. M. Timmons, J. M. Hebert, P. W. Rigby, and R. Tjian. 1991. Transcription factor AP-2 is expressed in neural crest cell lineages during mouse embryogenesis. Genes Dev. 5:105–119.
   PubMed Web of Science ®Google Scholar
• Mo, Z., S. Li, X. Yang, and M. Xiang. 2004. Role of the Barhl2 homeobox gene in the specification of glycinergic amacrine cells. Development 131:1607–1618.
   PubMedGoogle Scholar
• Morrow, E. M., T. Furukawa, J. E. Lee, and C. L. Cepko. 1999. NeuroD regulates multiple functions in the developing neural retina in rodent. Development 126:23–36.
   PubMed Web of Science ®Google Scholar
• Moser, M., A. Imhof, A. Pscherer, R. Bauer, W. Amselgruber, F. Sinowatz, F. Hofstadter, R. Schule, and R. Buettner. 1995. Cloning and characterization of a second AP-2 transcription factor: AP-2β. Development 121:2779–2788.
   PubMed Web of Science ®Google Scholar
• Moser, M., A. Pscherer, C. Roth, J. Becker, G. Mucher, K. Zerres, C. Dixkens, J. Weis, L. Guay-Woodford, R. Buettner, and R. Fassler. 1997. Enhanced apoptotic cell death of renal epithelial cells in mice lacking transcription factor AP-2β. Genes Dev. 11:1938–1948.
   PubMed Web of Science ®Google Scholar
• Moser, M., J. Ruschoff, and R. Buettner. 1997. Comparative analysis of AP-2α and AP-2β gene expression during murine embryogenesis. Dev. Dyn. 208:115–124.
   PubMed Web of Science ®Google Scholar
• Oulad-Abdelghani, M., P. Bouillet, C. Chazaud, P. Dolle, and P. Chambon. 1996. AP-2.2: a novel AP-2-related transcription factor induced by retinoic acid during differentiation of P19 embryonal carcinoma cells. Exp. Cell Res. 225:338–347.
   PubMed Web of Science ®Google Scholar
• Pak, W., R. Hindges, Y. S. Lim, S. L. Pfaff, and D. D. O'Leary. 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.
   PubMedGoogle Scholar
• Pan, L., Z. Yang, L. Feng, and L. Gan. 2005. Functional equivalence of Brn3 POU-domain transcription factors in mouse retinal neurogenesis. Development 132:703–712.
   PubMedGoogle Scholar
• Rapaport, D. H., L. L. Wong, E. D. Wood, D. Yasumura, and M. M. LaVail. 2004. Timing and topography of cell genesis in the rat retina. J. Comp. Neurol. 474:304–324.
   PubMedGoogle Scholar
• Reese, B. E., and L. Galli-Resta. 2002. The role of tangential dispersion in retinal mosaic formation. Prog. Retin. Eye Res. 21:153–168.
   PubMedGoogle Scholar
• Reese, B. E., A. R. Harvey, and S. S. Tan. 1995. Radial and tangential dispersion patterns in the mouse retina are cell-class specific. Proc. Natl. Acad. Sci. USA 92:2494–2498.
   PubMed Web of Science ®Google Scholar
• Reese, B. E., B. D. Necessary, P. P. Tam, B. Faulkner-Jones, and S. S. Tan. 1999. Clonal expansion and cell dispersion in the developing mouse retina. Eur. J. Neurosci. 11:2965–2978.
   PubMed Web of Science ®Google Scholar
• Reese, B. E., and S. S. Tan. 1998. Clonal boundary analysis in the developing retina using X-inactivation transgenic mosaic mice. Semin. Cell Dev. Biol. 9:285–292.
   PubMed Web of Science ®Google Scholar
• Schaeren-Wiemers, N., and A. Gerfin-Moser. 1993. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labeled cRNA probes. Histochemistry 100:431–440.
   PubMedGoogle Scholar
• Soriano, P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21:70–71.
   PubMed Web of Science ®Google Scholar
• Stewart, L., M. A. Potok, S. A. Camper, and S. Stifani. 2005. Runx1 expression defines a subpopulation of displaced amacrine cells in the developing mouse retina. J. Neurochem. 94:1739–1745.
   PubMedGoogle Scholar
• Strettoi, E., and R. H. Masland. 1996. The number of unidentified amacrine cells in the mammalian retina. Proc. Natl. Acad. Sci. USA 93:14906–14911.
   PubMed Web of Science ®Google Scholar
• Tomita, K., K. Moriyoshi, S. Nakanishi, F. Guillemot, and R. Kageyama. 2000. Mammalian achaete-scute and atonal homologs regulate neuronal versus glial fate determination in the central nervous system. EMBO J. 19:5460–5472.
   PubMedGoogle Scholar
• Tsonis, P. A., and K. Del Rio-Tsonis. 2004. Lens and retina regeneration: transdifferentiation, stem cells, and clinical applications. Exp. Eye Res. 78:161–172.
   PubMed Web of Science ®Google Scholar
• Tsuchida, T., M. Ensini, S. B. Morton, M. Baldassare, T. Edlund, T. M. Jessell, and S. L. Pfaff. 1994. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79:957–970.
   PubMed Web of Science ®Google Scholar
• Vaney, D. I. 1990. The mosaic of amacrine cells in the mammalian retina. Prog. Ret Res. 9:49–100.
   Google Scholar
• Wang, S. W., X. Mu, W. J. Bowers, D. S. Kim, D. J. Plas, M. C. Crair, H. J. Federoff, L. Gan, and W. H. Klein. 2002. Brn3b/Brn3c double knockout mice reveal an unsuspected role for Brn3c in retinal ganglion cell axon outgrowth. Development 129:467–477.
   PubMedGoogle Scholar
• Wang, Y., G. D. Dakubo, S. Thurig, C. J. Mazerolle, and V. A. Wallace. 2005. Retinal ganglion cell-derived sonic hedgehog locally controls proliferation and the timing of RGC development in the embryonic mouse retina. Development 132:5103–5113.
   PubMedGoogle Scholar
• West-Mays, J. A., B. M. Coyle, J. Piatigorsky, S. Papagiotas, and D. Libby. 2002. Ectopic expression of AP-2α transcription factor in the lens disrupts fiber cell differentiation. Dev. Biol. 245:13–27.
   PubMedGoogle Scholar
• West-Mays, J. A., J. Zhang, T. Nottoli, S. Hagopian-Donaldson, D. Libby, K. J. Strissel, and T. Williams. 1999. AP-2alpha transcription factor is required for early morphogenesis of the lens vesicle. Dev. Biol. 206:46–62.
   PubMedGoogle Scholar
• Williams, T., A. Admon, B. Luscher, and R. Tjian. 1988. Cloning and expression of AP-2, a cell-type-specific transcription factor that activates inducible enhancer elements. Genes Dev. 2:1557–1569.
   PubMed Web of Science ®Google Scholar
• Williams, T., and R. Tjian. 1991. Analysis of the DNA-binding and activation properties of the human transcription factor AP-2. Genes Dev. 5:670–682.
   PubMed Web of Science ®Google Scholar
• Williams, T., and R. Tjian. 1991. Characterization of a dimerization motif in AP-2 and its function in heterologous DNA-binding proteins. Science 251:1067–1071.
   PubMedGoogle Scholar
• Xiang, M., L. Zhou, J. P. Macke, T. Yoshioka, S. H. Hendry, R. L. Eddy, T. B. Shows, and J. Nathans. 1995. The Brn-3 family of POU-domain factors: primary structure, binding specificity, and expression in subsets of retinal ganglion cells and somatosensory neurons. J. Neurosci. 15:4762–4785.
   PubMed Web of Science ®Google Scholar
• Xiang, M., L. Zhou, Y. W. Peng, R. L. Eddy, T. B. Shows, and J. Nathans. 1993. Brn-3b: a POU domain gene expressed in a subset of retinal ganglion cells. Neuron 11:689–701.
   PubMedGoogle Scholar
• Young, R. W. 1985. Cell differentiation in the retina of the mouse. Anat. Rec. 212:199–205.
   PubMedGoogle Scholar
• Zhao, F., T. Lufkin, and B. D. Gelb. 2003. Expression of Tfap2d, the gene encoding the transcription factor Ap-2 delta, during mouse embryogenesis. Gene Expr. Patterns 3:213–217.
   PubMedGoogle Scholar
• Zhao, F., M. Satoda, J. D. Licht, Y. Hayashizaki, and B. D. Gelb. 2001. Cloning and characterization of a novel mouse AP-2 transcription factor, AP-2δ, with unique DNA binding and transactivation properties. J. Biol. Chem. 276:40755–40760.
   PubMedGoogle Scholar
• Zhou, J., and D. M. Kochhar. 2003. Regulation of AP-2 and apoptosis in developing eye in a vitamin A-deficiency model. Birth Defects Res. A Clin. Mol. Teratol. 67:41–53.
   PubMedGoogle Scholar
• Zhu, C. H., Y. Huang, L. W. Oberley, and F. E. Domann. 2001. A family of AP-2 proteins downregulate manganese superoxide dismutase expression. J. Biol. Chem. 276:14407–14413.
   PubMedGoogle Scholar