The Early Isoform of Disabled-1 Functions Independently of Reelin-Mediated Tyrosine Phosphorylation in Chick Retina

REFERENCES

• Altshuler, D., and C. Cepko. 1992. A temporally regulated, diffusible activity is required for rod photoreceptor development in vitro. Development 114:947–957.
   PubMed Web of Science ®Google Scholar
• Andrade, N., V. Komnenovic, S. M. Blake, Y. Jossin, B. Howell, A. Goffinet, W. J. Schneider, and J. Nimpf. 2007. ApoER2/VLDL receptor and Dab1 in the rostral migratory stream function in postnatal neuronal migration independently of Reelin. Proc. Natl. Acad. Sci. U. S. A. 104:8508–8513.
   PubMedGoogle Scholar
• Arnaud, L., B. A. Ballif, E. Forster, and J. A. Cooper. 2003. Fyn tyrosine kinase is a critical regulator of disabled-1 during brain development. Curr. Biol. 13:9–17.
   PubMed Web of Science ®Google Scholar
• Austin, C. P., D. E. Feldman, J. A. Ida, Jr., and C. L. Cepko. 1995. Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. Development 121:3637–3650.
   PubMed Web of Science ®Google Scholar
• Ballif, B. A., L. Arnaud, W. T. Arthur, D. Guris, A. Imamoto, and J. A. Cooper. 2004. Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelin-stimulated neurons. Curr. Biol. 14:606–610.
   PubMed Web of Science ®Google Scholar
• Bar, I., F. Tissir, C. Lambert de Rouvroit, O. De Backer, and A. M. Goffinet. 2003. The gene encoding disabled-1 (DAB1), the intracellular adaptor of the Reelin pathway, reveals unusual complexity in human and mouse. J. Biol. Chem. 278:5802–5812.
   PubMedGoogle Scholar
• Baye, L. M., and B. A. Link. 2008. Nuclear migration during retinal development. Brain Res. 1192:29–36.
   PubMedGoogle Scholar
• Belecky-Adams, T., S. Tomarev, H. S. Li, L. Ploder, R. R. McInnes, O. Sundin, and R. Adler. 1997. Pax-6, Prox 1, and Chx10 homeobox gene expression correlates with phenotypic fate of retinal precursor cells. Invest. Ophthalmol. Vis. Sci. 38:1293–1303.
   PubMedGoogle Scholar
• Bernier, B., I. Bar, G. D'Arcangelo, T. Curran, and A. M. Goffinet. 2000. Reelin mRNA expression during embryonic brain development in the chick. J. Comp. Neurol. 422:448–463.
   PubMedGoogle Scholar
• Bock, H. H., and J. Herz. 2003. Reelin activates SRC family tyrosine kinases in neurons. Curr. Biol. 13:18–26.
   PubMed Web of Science ®Google Scholar
• Bock, H. H., Y. Jossin, P. Liu, E. Forster, P. May, A. M. Goffinet, and J. Herz. 2003. Phosphatidylinositol 3-kinase interacts with the adaptor protein Dab1 in response to Reelin signaling and is required for normal cortical lamination. J. Biol. Chem. 278:38772–38779.
   PubMed Web of Science ®Google Scholar
• Boije, H., P. H. Edqvist, and F. Hallbook. 2009. Horizontal cell progenitors arrest in G2-phase and undergo terminal mitosis on the vitreal side of the chick retina. Dev. Biol. 330:105–113.
   PubMedGoogle 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. U. S. A. 93:589–595.
   PubMed Web of Science ®Google Scholar
• Chai, X., E. Forster, S. Zhao, H. H. Bock, and M. Frotscher. 2009. Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n-cofilin phosphorylation at serine3. J. Neurosci. 29:288–299.
   PubMed Web of Science ®Google Scholar
• Chen, K., P. G. Ochalski, T. S. Tran, N. Sahir, M. Schubert, A. Pramatarova, and B. W. Howell. 2004. Interaction between Dab1 and CrkII is promoted by Reelin signaling. J. Cell Sci. 117:4527–4536.
   PubMedGoogle Scholar
• Costagli, A., B. Felice, A. Guffanti, S. W. Wilson, and M. Mione. 2006. Identification of alternatively spliced dab1 isoforms in zebrafish. Dev. Genes Evol. 216:291–299.
   PubMedGoogle Scholar
• D'Arcangelo, G., G. G. Miao, S. C. Chen, H. D. Soares, J. I. Morgan, and T. Curran. 1995. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719–723.
   PubMed Web of Science ®Google Scholar
• Del Bene, F., A. M. Wehman, B. A. Link, and H. Baier. 2008. Regulation of neurogenesis by interkinetic nuclear migration through an apical-basal notch gradient. Cell 134:1055–1065.
   PubMed Web of Science ®Google Scholar
• Dutting, D., A. Gierer, and G. Hansmann. 1983. Self-renewal of stem cells and differentiation of nerve cells in the developing chick retina. Brain Res. 312:21–32.
   PubMedGoogle Scholar
• Edqvist, P. H., and F. Hallbook. 2004. Newborn horizontal cells migrate bi-directionally across the neuroepithelium during retinal development. Development 131:1343–1351.
   PubMedGoogle Scholar
• Federspiel, M. J., and S. H. Hughes. 1997. Retroviral gene delivery. Methods Cell Biol. 52:179–214.
   PubMedGoogle Scholar
• Feng, L., and J. A. Cooper. 2009. Dual functions of Dab1 during brain development. Mol. Cell. Biol. 29:324–332.
   PubMedGoogle Scholar
• Gertler, F. B., K. K. Hill, M. J. Clark, and F. M. Hoffmann. 1993. Dosage-sensitive modifiers of Drosophila abl tyrosine kinase function: prospero, a regulator of axonal outgrowth, and disabled, a novel tyrosine kinase substrate. Genes Dev. 7:441–453.
   PubMed Web of Science ®Google Scholar
• Giniger, E. 1998. A role for Abl in Notch signaling. Neuron 20:667–681.
   PubMedGoogle Scholar
• Goldowitz, D., R. C. Cushing, E. Laywell, G. D'Arcangelo, M. Sheldon, H. O. Sweet, M. Davisson, D. Steindler, and T. Curran. 1997. Cerebellar disorganization characteristic of reeler in scrambler mutant mice despite presence of reelin. J. Neurosci. 17:8767–8777.
   PubMedGoogle Scholar
• Hamburger, V., and H. L. Hamilton. 1951. A series of normal stages in the development of the chick embryo. J. Morphol. 88:49–92.
   PubMed Web of Science ®Google Scholar
• Hashimoto-Torii, K., M. Torii, M. R. Sarkisian, C. M. Bartley, J. Shen, F. Radtke, T. Gridley, N. Sestan, and P. Rakic. 2008. Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex. Neuron 60:273–284.
   PubMed Web of Science ®Google Scholar
• Henrique, D., E. Hirsinger, J. Adam, I. Le Roux, O. Pourquie, D. Ish-Horowicz, and J. Lewis. 1997. Maintenance of neuroepithelial progenitor cells by Delta-Notch signalling in the embryonic chick retina. Curr. Biol. 7:661–670.
   PubMedGoogle Scholar
• Herrick, T. M., and J. A. Cooper. 2002. A hypomorphic allele of dab1 reveals regional differences in reelin-Dab1 signaling during brain development. Development 129:787–796.
   PubMedGoogle Scholar
• Hiesberger, T., M. Trommsdorff, B. W. Howell, A. Goffinet, M. C. Mumby, J. A. Cooper, and J. Herz. 1999. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24:481–489.
   PubMed Web of Science ®Google Scholar
• Holt, C. E., T. W. Bertsch, H. M. Ellis, and W. A. Harris. 1988. Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1:15–26.
   PubMed Web of Science ®Google Scholar
• Homayouni, R., D. S. Rice, M. Sheldon, and T. Curran. 1999. Disabled-1 binds to the cytoplasmic domain of amyloid precursor-like protein 1. J. Neurosci. 19:7507–7515.
   PubMedGoogle Scholar
• Howell, B. W., F. B. Gertler, and J. A. Cooper. 1997. Mouse disabled (mDab1): a Src binding protein implicated in neuronal development. EMBO J. 16:121–132.
   PubMed Web of Science ®Google Scholar
• Howell, B. W., R. Hawkes, P. Soriano, and J. A. Cooper. 1997. Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389:733–737.
   PubMed Web of Science ®Google Scholar
• Howell, B. W., T. M. Herrick, and J. A. Cooper. 1999. Reelin-induced tryosine phosphorylation of disabled 1 during neuronal positioning. Genes Dev. 13:643–648.
   PubMed Web of Science ®Google Scholar
• Howell, B. W., T. M. Herrick, J. D. Hildebrand, Y. Zhang, and J. A. Cooper. 2000. Dab1 tyrosine phosphorylation sites relay positional signals during mouse brain development. Curr. Biol. 10:877–885.
   PubMedGoogle Scholar
• Hughes, S. H., J. J. Greenhouse, C. J. Petropoulos, and P. Sutrave. 1987. Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J. Virol. 61:3004–3012.
   PubMed Web of Science ®Google Scholar
• Iijima, H., M. Miyazawa, J. Sakai, K. Magoori, M. R. Ito, H. Suzuki, M. Nose, Y. Kawarabayasi, and T. T. Yamamoto. 1998. Expression and characterization of a very low density lipoprotein receptor variant lacking the O-linked sugar region generated by alternative splicing. J. Biochem. 124:747–755.
   PubMedGoogle Scholar
• Jossin, Y., and A. M. Goffinet. 2007. Reelin signals through phosphatidylinositol 3-kinase and Akt to control cortical development and through mTor to regulate dendritic growth. Mol. Cell. Biol. 27:7113–7124.
   PubMed Web of Science ®Google Scholar
• Kahn, A. J. 1974. An autoradiographic analysis of the time of appearance of neurons in the developing chick neural retina. Dev. Biol. 38:30–40.
   PubMed Web of Science ®Google Scholar
• Katyal, S., Z. Gao, E. Monckton, D. Glubrecht, and R. Godbout. 2007. Hierarchical disabled-1 tyrosine phosphorylation in Src family kinase activation and neurite formation. J. Mol. Biol. 368:349–364.
   PubMedGoogle Scholar
• Katyal, S., and R. Godbout. 2004. Alternative splicing modulates Disabled-1 (Dab1) function in the developing chick retina. EMBO J. 23:1878–1888.
   PubMedGoogle Scholar
• Keshvara, L., D. Benhayon, S. Magdaleno, and T. Curran. 2001. Identification of reelin-induced sites of tyrosyl phosphorylation on disabled 1. J. Biol. Chem. 276:16008–16014.
   PubMedGoogle Scholar
• Lambert de Rouvroit, C., V. de Bergeyck, C. Cortvrindt, I. Bar, Y. Eeckhout, and A. M. Goffinet. 1999. Reelin, the extracellular matrix protein deficient in reeler mutant mice, is processed by a metalloproteinase. Exp. Neurol. 156:214–217.
   PubMedGoogle Scholar
• Le Gall, M., C. De Mattei, and E. Giniger. 2008. Molecular separation of two signaling pathways for the receptor, Notch. Dev. Biol. 313:556–567.
   PubMedGoogle Scholar
• Le, N., and M. A. Simon. 1998. Disabled is a putative adaptor protein that functions during signaling by the sevenless receptor tyrosine kinase. Mol. Cell. Biol. 18:4844–4854.
   PubMedGoogle Scholar
• Li, X., D. D. Glubrecht, R. Mita, and R. Godbout. 2008. Expression of AP-2delta in the developing chick retina. Dev. Dyn. 237:3210–3221.
   PubMedGoogle Scholar
• Nabi, N. U., E. Mezer, S. I. Blaser, A. A. Levin, and J. R. Buncic. 2003. Ocular findings in lissencephaly. J. AAPOS 7:178–184.
   PubMedGoogle Scholar
• Park, T. J., and T. Curran. 2008. Crk and Crk-like play essential overlapping roles downstream of Disabled-1 in the Reelin pathway. J. Neurosci. 28:13551–13562.
   PubMed Web of Science ®Google Scholar
• Prada, C., J. Puga, L. Perez-Mendez, R. Lopez, and G. Ramirez. 1991. Spatial and temporal patterns of neurogenesis in the chick retina. Eur. J. Neurosci. 3:559–569.
   PubMed Web of Science ®Google Scholar
• Reh, T. A., and I. J. Kljavin. 1989. Age of differentiation determines rat retinal germinal cell phenotype: induction of differentiation by dissociation. J. Neurosci. 9:4179–4189.
   PubMed Web of Science ®Google Scholar
• Rice, D. S., and T. Curran. 2000. Disabled-1 is expressed in type AII amacrine cells in the mouse retina. J. Comp. Neurol. 424:327–338.
   PubMedGoogle Scholar
• Rice, D. S., S. Nusinowitz, A. M. Azimi, A. Martinez, E. Soriano, and T. Curran. 2001. The Reelin pathway modulates the structure and function of retinal synaptic circuitry. Neuron 31:929–941.
   PubMedGoogle Scholar
• Schiffmann, S. N., B. Bernier, and A. M. Goffinet. 1997. Reelin mRNA expression during mouse brain development. Eur. J. Neurosci. 9:1055–1071.
   PubMed Web of Science ®Google Scholar
• Sheldon, M., D. S. Rice, G. D'Arcangelo, H. Yoneshima, K. Nakajima, K. Mikoshiba, B. W. Howell, J. A. Cooper, D. Goldowitz, and T. Curran. 1997. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389:730–733.
   PubMed Web of Science ®Google Scholar
• Songyang, Z., S. E. Shoelson, M. Chaudhuri, G. Gish, T. Pawson, W. G. Haser, F. King, T. Roberts, S. Ratnofsky, R. J. Lechleider, et al. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72:767–778.
   PubMed Web of Science ®Google Scholar
• Sun, X. M., and A. K. Soutar. 1999. Expression in vitro of alternatively spliced variants of the messenger RNA for human apolipoprotein E receptor-2 identified in human tissues by ribonuclease protection assays. Eur. J. Biochem. 262:230–239.
   PubMedGoogle Scholar
• Trommsdorff, M., J. P. Borg, B. Margolis, and J. Herz. 1998. Interaction of cytosolic adaptor proteins with neuronal apolipoprotein E receptors and the amyloid precursor protein. J. Biol. Chem. 273:33556–33560.
   PubMed Web of Science ®Google Scholar
• Trommsdorff, M., M. Gotthardt, T. Hiesberger, J. Shelton, W. Stockinger, J. Nimpf, R. E. Hammer, J. A. Richardson, and J. Herz. 1999. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97:689–701.
   PubMed Web of Science ®Google Scholar
• Turner, D. L., and C. L. Cepko. 1987. A common progenitor for neurons and glia persists in rat retina late in development. Nature 328:131–136.
   PubMed Web of Science ®Google 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