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Phr1 is required for proper retinocollicular targeting of nasal–dorsal retinal ganglion cells

Published online by Cambridge University Press:  16 February 2011

BRADLY Q. VO ,
A. JOSEPH BLOOM  and
SUSAN M. CULICAN
BRADLY Q. VO
Affiliation:
Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, Saint Louis, Missouri
A. JOSEPH BLOOM
Affiliation:
Department of Psychiatry, Washington University School of Medicine, Saint Louis, Missouri
SUSAN M. CULICAN*
Affiliation:
Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, Saint Louis, Missouri
*
*Address correspondence and reprint requests to: Dr. Susan M. Culican, Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, 660 South Euclid Avenue, Ophthalmology Box 8096, Saint Louis, MO 63110. E-mail: [email protected]
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Abstract

Precise targeting of retinal projections is required for the normal development of topographic maps in the mammalian primary visual system. During development, retinal axons project to and occupy topographically appropriate positions in the dorsal lateral geniculate nucleus (dLGN) and superior colliculus (SC). Phr1 retinal mutant mice, which display mislocalization of the ipsilateral retinogeniculate projection independent of activity and ephrin-A signaling, were found to have a more global disruption of topographic specificity of retinofugal inputs. The retinocollicular projection lacks local refinement of terminal zones and multiple ectopic termination zones originate from the dorsal–nasal (DN) retinal quadrant. Similarly, in the dLGN, the inputs originating from the contralateral DN retina are poorly refined in the Phr1 mutant. These results show that Phr1 is an essential regulator of retinal ganglion cell projection during both dLGN and SC topographic map development.

Keywords

dLGNSuperior colliculusRetinocollicularTopographyDiI
Type
Brief Communication
Information
Visual Neuroscience , Volume 28 , Issue 2 , March 2011 , pp. 175 - 181
Copyright
Copyright © Cambridge University Press 2011

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References

Bloom, A.J., Miller, B.R., Sanes, J.R. & DiAntonio, A. (2007). The requirement for Phr1 in CNS axon tract formation reveals the corticostriatal boundary as a choice point for cortical axons. Genes & Development 21, 2593–2606.Google Scholar
Burgess, R.W., Peterson, K.A., Johnson, M.J., Roix, J.J., Welsh, I.C. & O’Brien, T.P. (2004). Evidence for a conserved function in synapse formation reveals Phr1 as a candidate gene for respiratory failure in newborn mice. Molecular & Cellular Biology 24, 1096–1105.CrossRefGoogle ScholarPubMed
Chandrasekaran, A.R., Plas, D.T., Gonzalez, E. & Crair, M.C. (2005). Evidence for an instructive role of retinal activity in retinotopic map refinement in the superior colliculus of the mouse. The Journal of Neuroscience 25, 6929–6938.CrossRefGoogle ScholarPubMed
Culican, S.M., Bloom, A.J., Weiner, J.A. & DiAntionio, A. (2009). Phr1 regulates retinogeniculate targeting independent of activity and ephrin-A signaling. Molecular & Cellular Neurosciences 41, 304–312.CrossRefGoogle Scholar
DiAntonio, A., Haghighi, A.P., Portman, S.L., Lee, J.D., Amaranto, A.M. & Goodman, C.S. (2001) Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412, 449–452.Google Scholar
D’Souza, J., Hendricks, M., Le Guyader, S., Subburaju, S., Grunewald, B., Scholich, K. & Jesuthasan, S. (2005). Formation of the retinotectal projection requires Esrom, an ortholog of PAM (protein associated with Myc). Development 132, 247–256.CrossRefGoogle ScholarPubMed
Feldheim, D.A., Kim, Y.I., Bergemann, A.D., Frisen, J., Barbacid, M. & Flanagan, J.G. (2000). Genetic analysis of ephrin-a2 and ephrin-a5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25, 563–574.CrossRefGoogle ScholarPubMed
Feldheim, D.A., Vanderhaeghen, P., Hansen, M.J., Frisen, J., Lu, Q., Barbacid, M. & Flanagan, J.G. (1998). Topographic guidance labels in a sensory projection to the forebrain. Neuron 21, 1303–1313.CrossRefGoogle Scholar
Flanagan, J.G. (2006). Neural map specification by gradients. Current Opinion in Neurobiology 16, 59–66.CrossRefGoogle ScholarPubMed
Grubb, M.S., Rossi, F.M., Changeux, J.P. & Thompson, I.D. (2003). Abnormal functional organization in the dorsal lateral geniculate nucleus of mice lacking the beta 2 subunit of the nicotinic acetylcholine receptor. Neuron 40, 1161–1172.Google Scholar
Hindges, R., McLaughlin, T., Genoud, N., Henkemeyer, M. & O’Leary, D.D. (2002). EphB forward signaling controls directional branch extension and arborization required for dorsal-ventral retinotopic mapping. Neuron 35, 475–487.CrossRefGoogle ScholarPubMed
Hornberger, M.R., Dütting, D., Ciossek, T., Yamada, T., Handwerker, C., Lang, S., Weth, F., Huf, J., Webel, R., Logan, C., Tanaka, H. & Drescher, U. (1999). Modulation of EphA receptor function by coexpressed ephrinA ligands on retinal ganglion cell axons. Neuron 22, 731–742.CrossRefGoogle ScholarPubMed
Lewcock, J.W., Genoud, N., Lettieri, K. & Pfaff, A.L. (2007). The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics. Neuron 56, 604–620.CrossRefGoogle ScholarPubMed
Lim, Y., McLaughlin, T., Sung, T., Santiago, A., Lee, K. & O’Leary, D.M. (2008). p75(NTR) mediates ephrin-A reverse signaling required for axon repulsion and mapping. Neuron 59, 746–758.CrossRefGoogle ScholarPubMed
Luo, L. & Flanagan, J.G. (2007). Development of continuous and discrete neural maps. Neuron 56, 284–300.CrossRefGoogle ScholarPubMed
McLaughlin, T., Hindges, R., Yates, P.A. & O’leary, D.D. (2003). Bifunctional action of ephrin-B1 as a repellent and attractant to control bidirectional branch extension in dorsal-ventral retinotopic mapping. Development 130, 2407–2418.Google Scholar
McLaughlin, T. & O’Leary, D.D. (2005). Molecular gradients and development of retinotopic maps. Annual Review of Neuroscience 28, 327–355.Google Scholar
Pfeiffenberger, C., Yamada, J. & Feldheim, D.A. (2006). Ephrin-As and patterned retinal activity act together in the development of topographic Maps in the primary visual system. The Journal of Neuroscience 26, 12873–12884.CrossRefGoogle ScholarPubMed
Reese, B.E. (2010). Development of the retina and optic pathway. Vision Research doi: 10.1016/j.visres.2010.07.010.Google Scholar
Schaefer, A.M., Hadwiger, G.D. & Nonet, M.L. (2000). rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron 26, 345–356.Google Scholar
Simon, D.K. & O’Leary, D.D. (1991). Relationship of retinotopic ordering of axons in the optic pathway to the formation of visual maps in central targets. The Journal of Comparative Neurology 307, 393–404.CrossRefGoogle Scholar
Sperry, R.W. (1963). Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proceedings of the National Academy of Sciences of the United States of America 50, 703–710.Google Scholar
Torborg, C.L. & Feller, M.B. (2005). Spontaneous pattern retinal activity and the refinement of retinal projection. The Journal of Neuroscience 76, 213–235.Google Scholar
Wan, H.I., DiAntonio, A., Fetter, R.D., Bergstrom, K., Strauss, R. & Goodman, C.S. (2000). Highwire regulates synaptic growth in Drosophila. Neuron 26, 313–329.Google Scholar
Yang, Z., Ding, K., Pan, L., Deng, M. & Gan, L. (2003). Math5 determines the competence state of retinal ganglion cell progenitors. Developmental Biology 264, 240–254.Google Scholar
Zhen, M., Huang, X., Bamber, B. & Jin, Y. (2000). Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain. Neuron 26, 331–334.Google Scholar
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