Extrinsic factors as multifunctional regulators of retinal ganglion cell morphogenesis

Developmental Neurobiology

Volumn 71, Issue 12, 2011, Pages 1170-1185

  Atkinson Leadbeater, Karen ^a   Mcfarlane, Sarah ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Axon guidance; Dendrite development; Growth cone; Morphogenesis; Retinal ganglion cell

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; EPHRIN; FIBROBLAST GROWTH FACTOR; NETRIN; NUCLEOTIDE; ROUNDABOUT RECEPTOR; SLIT PROTEIN; SONIC HEDGEHOG PROTEIN;

CELL FUNCTION; CELL GROWTH; DENDRITE; MORPHOGENESIS; NERVE CELL; NERVE FIBER; NEURITE; NONHUMAN; OPTICS; PRIORITY JOURNAL; RETINA; RETINA GANGLION CELL; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; VISUAL SYSTEM;

ANIMALS; AXONS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DENDRITES; MORPHOGENESIS; RETINA; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; SYNAPSES; VISUAL PATHWAYS;

EID: 80755143251     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20924     Document Type: Review

References (122)

1. Alsina B, Vu T, Cohen-Cory S. 2001. Visualizing synapse formation in arborizing optic axons in vivo: Dynamics and modulation by BDNF. Nat Neurosci 4: 1093-1101.
2. Atkinson-Leadbeater K, Bertolesi GE, Hehr CL, Webber CA, Cechmanek PB, McFarlane S. 2010. Dynamic expression of axon guidance cues required for optic tract development is controlled by fibroblast growth factor signaling. J Neurosci 30: 685-693.
3. Baier H. 2000. Zebrafish on the move: Towards a behavior-genetic analysis of vertebrate vision. Curr Opin Neurobiol 10: 451-455.
4. Bao ZZ. 2008. Intraretinal projection of retinal ganglion cell axons as a model system for studying axon navigation. Brain Res 1192: 165-177.
5. Barresi MJ, Hutson LD, Chien CB, Karlstrom RO. 2005. Hedgehog regulated Slit expression determines commissure and glial cell position in the zebrafish forebrain. Development 132: 3643-3656.
6. Beug ST, Parks RJ, McBride HM, Wallace VA. 2010. Processing-dependent trafficking of Sonic hedgehog to the regulated secretory pathway in neurons. Mol Cell Neurosci 46: 583-596.
7. Birgbauer E, Cowan CA, Sretavan DW, Henkemeyer M. 2000. Kinase independent function of EphB receptors in retinal axon pathfinding to the optic disc from dorsal but not ventral retina. Development 127: 1231-1241.
8. Bovolenta P. 2005. Morphogen signaling at the vertebrate growth cone: A few cases or a general strategy? J Neurobiol 64: 405-416.
9. Callander DC, Lamont RE, Childs SJ, McFarlane S. 2007. Expression of multiple class three semaphorins in the retina and along the path of zebrafish retinal axons. Dev Dyn 236: 2918-2924.
10. Campbell DS, Regan AG, Lopez JS, Tannahill D, Harris WA, Holt CE. 2001. Semaphorin 3A elicits stage-dependentcollapse, turning, and branching in Xenopus retinal growth cones. J Neurosci 21: 8538-8547.
11. Campbell DS, Stringham SA, Timm A, Xiao T, Law MY, Baier H, Nonet ML, et al. 2007. Slit1a inhibits retinal ganglion cell arborization and synaptogenesis via Robo2-dependent and -independent pathways. Neuron 55: 231-245.
12. Charron F, Tessier-Lavigne M. 2005. Novel brain wiring functions for classical morphogens: A role as graded positional cues in axon guidance. Development 132: 2251-2262.
13. Chen Z, Gore BB, Long H, Ma L, Tessier-Lavigne M. 2008. Alternative splicing of the Robo3 axon guidance receptor governs the midline switch from attraction to repulsion. Neuron 58: 325-332.
14. Choi JH, Law MY, Chien CB, Link BA, Wong RO. 2010. In vivo development of dendritic orientation in wild-type and mislocalized retinal ganglion cells. Neural Dev 5: 29.
15. Cohen-Cory S, Escandón E, Fraser SE. 1996. The cellular patterns of BDNF and trkB expression suggest multiple roles for BDNF during Xenopus visual system development. Dev Biol 179: 102-115.
16. Cohen-Cory S, Fraser SE. 1995. Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378: 192-196.
17. Cohen-Cory S, Lom B. 2004. Neurotrophic regulation of retinal ganglion cell synaptic connectivity: From axons and dendrites to synapses. Int J Dev Biol 48: 947-956.
18. Culverwell J, Karlstrom RO. 2002. Making the connection: Retinal axon guidance in the zebrafish. Semin Cell Dev Biol 13: 497-506.
19. Dakubo GD, Wang YP, Mazerolle C, Campsall K, McMahon AP, Wallace VA. 2003. Retinal ganglion cell-derived sonic hedgehog signaling is required for optic disc and stalk neuroepithelial cell development. Development 130: 2967-2980.
20. de la Torre JR, Höpker VH, Ming GL, Poo MM, Tessier-Lavigne M, Hemmati-Brivanlou A, Holt CE. 1997. Turning of retinal growth cones in a netrin-1 gradient mediated by the netrin receptor DCC. Neuron 19: 1211-1224.
21. Deiner MS, Kennedy TE, Fazeli A, Serafini T, Tessier-Lavigne M, Sretavan DW. 1997. Netrin-1 and DCC mediate axon guidance locally at the optic disc: Loss of function leads to optic nerve hypoplasia. Neuron 19: 575-589.
22. Deiner MS, Sretavan DW. 1999. Altered midline axon pathways and ectopic neurons in the developing hypothalamus of netrin-1- and DCC-deficient mice. J Neurosci 19: 9900-9912.
23. Dickson BJ. 2002. Molecular mechanisms of axon guidance. Science 298: 1959-1964.
24. Dickson BJ, Gilestro GF. 2006. Regulation of commissural axon pathfinding by slit and its Robo receptors. Annu Rev Cell Dev Biol 22: 651-675.
25. Dickson BJ, Zou Y. 2010. Navigating intermediate targets: The nervous system midline. Cold Spring Harb Perspect Biol 2: a002055.
26. Erskine L, Herrera E. 2007. The retinal ganglion cell axon's journey: Insights into molecular mechanisms of axon guidance. Dev Biol 308: 1-14.
27. Erskine L, Williams SE, Brose K, Kidd T, Rachel RA, Goodman CS, Tessier-Lavigne M, et al. 2000. Retinal ganglion cell axon guidance in the mouse optic chiasm: Expression and function of robos and slits. J Neurosci 20: 4975-4982.
28. Esteve P, Bovolenta P. 2006. Secreted inducers in vertebrate eye development: More functions for old morphogens. Curr Opin Neurobiol 16: 13-19.
29. Fabre PJ, Shimogori T, Charron F. 2010. Segregation of ipsilateral retinal ganglion cell axons at the optic chiasm requires the Shh receptor Boc. J Neurosci 30: 266-275.
30. Feldheim DA, O'Leary DD. 2010. Visual map development: bidirectional signaling, bifunctional guidance molecules, and competition. Cold Spring Harb Perspect Biol 2: a001768
31. Fricke C, Lee JS, Geiger-Rudolph S, Bonhoeffer F, Chien CB. 2001. Astray, a zebrafish roundabout homolog required for retinal axon guidance. Science 292: 507-510.
32. Furrer MP, Kim S, Wolf B, Chiba A. 2003. Robo and Frazzled/DCC mediate dendritic guidance at the CNS midline. Nat Neurosci 6: 223-230.
33. Furrer MP, Vasenkova I, Kamiyama D, Rosado Y, Chiba A. 2007. Slit and Robo control the development of dendrites in Drosophila CNS. Development 134: 3795-3804.
34. Gaze RM, Wilson MA, Taylor JS. 1993. Optic synapses are found in diencephalic neuropils before development of the tectum in Xenopus. Anat Embryol (Berl) 187: 27-35.
35. Gosse NJ, Baier H. 2009. An essential role for Radar (Gdf6a) in inducing dorsal fate in the zebrafish retina. Proc Natl Acad Sci USA 106: 2236-2241.
36. Harada T, Harada C, Parada LF. 2007. Molecular regulation of visual system development: More than meets the eye. Genes Dev 21: 367-378.
37. Hatakeyama J, Kageyama R. 2004. Retinal cell fate determination and bHLH factors. Semin Cell Dev Biol 15: 83-89.
38. Haupt C, Huber AB. 2008. How axons see their way-Axonal guidance in the visual system. Front Biosci 13: 3136-3149.
39. Hindges R, McLaughlin T, Genoud N, Henkemeyer M, O'Leary DD. 2002. EphB forward signaling controls directional branch extension and arborization required for dorsal-ventral retinotopic mapping. Neuron 35: 475-487.
40. Hocking JC, Hehr CL, Bertolesi GE, Wu JY, McFarlane S. 2010. Distinct roles for Robo2 in the regulation of axon and dendrite growth by retinal ganglion cells. Mech Dev 127: 36-48.
41. Hocking JC, Hehr CL, Chang RY, Johnston J, McFarlane S. 2008. TGFbeta ligands promote the initiation of retinal ganglion cell dendrites in vitro and in vivo. Mol Cell Neurosci 37: 247-260.
42. Holt CE. 1989. A single-cell analysis of early retinal ganglion cell differentiation in Xenopus: From soma to axon tip. J Neurosci 9: 3123-3145.
43. Höpker VH, Shewan D, Tessier-Lavigne M, Poo M, Holt C. 1999. Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401: 69-73.
44. Hu B, Nikolakopoulou AM, Cohen-Cory S. 2005. BDNF stabilizes synapses and maintains the structural complexity of optic axons in vivo. Development 132: 4285-4298.
45. Huberman AD, Feller MB, Chapman B. 2008. Mechanisms underlying development of visual maps and receptive fields. Annu Rev Neurosci 31: 479-509.
46. Hutson LD, Chien CB. 2002. Pathfinding and error correction by retinal axons: The role of astray/robo2. Neuron 33: 205-217.
47. Hutson LD, Jurynec MJ, Yeo SY, Okamoto H, Chien CB. 2003. Two divergent slit1 genes in zebrafish. Dev Dyn 228: 358-369.
48. Josten NJ, Huberman AD. 2010. Milestones and mechanisms for generating specific synaptic connections between the eyes and the brain. Curr Top Dev Biol 93: 229-259.
49. Kania A, Jessell TM. 2003. Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 38: 581-596.
50. Kania A, Johnson RL, Jessell TM. 2000. Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell 102: 161-173.
51. Kennedy TE, Serafini T, de la Torre JR, Tessier-Lavigne M. 1994. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78: 425-435.
52. Klein R. 2004. Eph/ephrin signaling in morphogenesis, neural development and plasticity. Curr Opin Cell Biol 16: 580-589.
53. Koestner U, Shnitsar I, Linnemannstöns K, Hufton AL, Borchers A. 2008. Semaphorin and neuropilin expression during early morphogenesis of Xenopus laevis. Dev Dyn 237: 3853-3863.
54. Kolodkin AL, Tessier-Lavigne M. 2011. Mechanisms and molecules of neuronal wiring: A primer. Cold Spring Harb Perspect Biol Jun 1;3(6).
55. Kolpak A, Zhang J, Bao ZZ. 2005. Sonic hedgehog has a dual effect on the growth of retinal ganglion axons depending on its concentration. J Neurosci 25: 3432-3441.
56. Koshiba-Takeuchi K, Takeuchi JK, Matsumoto K, Momose T, Uno K, Hoepker V, Ogura K, et al. 2000. Tbx5 and the retinotectum projection. Science 287: 134-137.
57. Lee SM, Danielian PS, Fritzsch B, McMahon AP. 1997. Evidence that FGF8 signalling from the midbrain-hindbrain junction regulates growth and polarity in the developing midbrain. Development 124: 959-969.
58. Li L. 2001. Zebrafish mutants: Behavioral genetic studies of visual system defects. Dev Dyn 221: 365-372.
59. Liu J, Wilson S, Reh T. 2003. BMP receptor 1b is required for axon guidance and cell survival in the developing retina. Dev Biol 256: 34-48.
60. Liu Y, Berndt J, Su F, Tawarayama H, Shoji W, Kuwada JY, Halloran MC. 2004. Semaphorin3D guides retinal axons along the dorsoventral axis of the tectum. J Neurosci 24: 310-318.
61. Livesey FJ, Cepko CL. 2001. Vertebrate neural cell-fate determination: Lessons from the retina. Nat Rev Neurosci 2: 109-118.
62. Lom B, Cogen J, Sanchez AL, Vu T, Cohen-Cory S. 2002. Local and target-derived brain-derived neurotrophic factor exert opposing effects on the dendritic arborization of retinal ganglion cells in vivo. J Neurosci 22: 7639-7649.
63. Lom B, Cohen-Cory S. 1999. Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arborization in vivo. J Neurosci 19: 9928-9938.
64. Lom B, Höpker V, McFarlane S, Bixby JL, Holt CE. 1998. Fibroblast growth factor receptor signaling in Xenopus retinal axon extension. J Neurobiol 37: 633-641.
65. Lowery LA, Van Vactor D. 2009. The trip of the tip: understanding the growth cone machinery. Nat Rev Mol Cell Biol 10: 332-343.
66. Lupo G, Liu Y, Qiu R, Chandraratna RA, Barsacchi G, He RQ, Harris WA. 2005. Dorsoventral patterning of the Xenopus eye: A collaboration of Retinoid, Hedgehog and FGF receptor signaling. Development 132: 1737-1748.
67. Manitt C, Nikolakopoulou AM, Almario DR, Nguyen SA, Cohen-Cory S. 2009. Netrin participates in the development of retinotectal synaptic connectivity by modulating axon arborization and synapse formation in the developing brain. J Neurosci 29: 11065-11077.
68. Mann F, Harris WA, Holt CE. 2004. New views on retinal axon development: A navigation guide. Int J Dev Biol 48: 957-964.
69. Mann F, Ray S, Harris W, Holt C. 2002. Topographic mapping in dorsoventral axis of the Xenopus retinotectal system depends on signaling through ephrin-B ligands. Neuron 35: 461-473.
70. Martinez-Morales JR, Del Bene F, Nica G, Hammerschmidt M, Bovolenta P, Wittbrodt J. 2005. Differentiation of the vertebrate retina is coordinated by an FGF signaling center. Dev Cell 8: 565-574.
71. McAllister AK. 2002. Neurotrophins and cortical development. Results Probl Cell Differ 39: 89-112.
72. McFarlane S, Cornel E, Amaya E, Holt CE. 1996. Inhibition of FGF receptor activity in retinal ganglion cell axons causes errors in target recognition. Neuron 17: 245-254.
73. McFarlane S, McNeill L, Holt CE. 1995. FGF signaling and target recognition in the developing Xenopus visual system. Neuron 15: 1017-1028.
74. McLaughlin T, Hindges R, O'Leary DD. 2003. Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr Opin Neurobiol 13: 57-69.
75. McLaughlin T, Hindges R, Yates PA, O'Leary DD. 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.
76. McLaughlin T, O'Leary DD. 2005. Molecular gradients and development of retinotopic maps. Annu Rev Neurosci 28: 327-355.
77. Merchán P, Bribián A, Sánchez-Camacho C, Lezameta M, Bovolenta P, de Castro F. 2007. Sonic hedgehog promotes the migration and proliferation of optic nerve oligodendrocyte precursors. Mol Cell Neurosci 36: 355-368.
78. Ming GL, Song HJ, Berninger B, Holt CE, Tessier-Lavigne M, Poo MM. 1997. cAMP-dependent growth cone guidance by netrin-1. Neuron 19: 1225-1235.
79. Morcillo J, Martínez-Morales JR, Trousse F, Fermin Y, Sowden JC, Bovolenta P. 2006. Proper patterning of the optic fissure requires the sequential activity of BMP7 and SHH. Development 133: 3179-3190.
80. Nakagawa S, Brennan C, Johnson KG, Shewan D, Harris WA, Holt CE. 2000. Ephrin-B regulates the Ipsilateral routing of retinal axons at the optic chiasm. Neuron 25: 599-610.
81. Neuhauss SC. 2003. Behavioral genetic approaches to visual system development and function in zebrafish. J Neurobiol 54: 148-160.
82. Neumann CJ, Nuesslein-Volhard C. 2000. Patterning of the zebrafish retina by a wave of sonic hedgehog activity. Science 289: 2137-2139.
83. Palmer A, Klein R. 2003. Multiple roles of ephrins in morphogenesis, neuronal networking, and brain function. Genes Dev 17: 1429-1450.
84. Peters MA, Cepko CL. 2002. The dorsal-ventral axis of the neural retina is divided into multiple domains of restricted gene expression which exhibit features of lineage compartments. Dev Biol 251: 59-73.
85. Petros TJ, Rebsam A, Mason CA. 2008. Retinal axon growth at the optic chiasm: To cross or not to cross. Annu Rev Neurosci 31: 295-315.
86. Picker A, Brennan C, Reifers F, Clarke JD, Holder N, Brand M. 1999. Requirement for the zebrafish mid-hindbrain boundary in midbrain polarisation, mapping and confinement of the retinotectal projection. Development 126: 2967-2978.
87. Piper M, Anderson R, Dwivedy A, Weinl C, van Horck F, Leung KM, Cogill E, et al. 2006. Signaling mechanisms underlying Slit2-induced collapse of Xenopus retinal growth cones. Neuron 49: 215-228.
88. Plachez C, Andrews W, Liapi A, Knoell B, Drescher U, Mankoo B, Zhe L, et al. 2008. Robos are required for the correct targeting of retinal ganglion cell axons in thevisual pathway of the brain. Mol Cell Neurosci 37: 719-730.
89. Plas DT, Dhande OS, Lopez JE, Murali D, Thaller C, Henkemeyer M, Furuta Y, et al. 2008. Bone morphogenetic proteins, eye patterning, and retinocollicular map formation in the mouse. J Neurosci 28: 7057-7067.
90. Plump AS, Erskine L, Sabatier C, Brose K, Epstein CJ, Goodman CS, Mason CA, et al. 2002. Slit1 and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 33: 219-232.
91. Polleux F, Morrow T, Ghosh A. 2000. Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404: 567-573.
92. Portugues R, Engert F. 2009. The neural basis of visual behaviors in the larval zebrafish. Curr Opin Neurobiol 19: 644-647.
93. Raper JA. 2000. Semaphorins and their receptors in vertebrates and invertebrates. Curr Opin Neurobiol 10: 88-94.
94. Sakagami K, Gan L, Yang XJ. 2009. Distinct effects of Hedgehog signaling on neuronal fate specification and cell cycle progression in the embryonic mouse retina. JNeurosci 29: 6932-6944.
95. Sakai JA, Halloran MC. 2006. Semaphorin 3d guides laterality of retinal ganglion cell projections in zebrafish. Development 133: 1035-1044.
96. Sánchez-Camacho C, Bovolenta P. 2008. Autonomous and non-autonomous Shh signalling mediate the in vivo growth and guidance of mouse retinal ganglion cell axons. Development 135: 3531-3541.
97. Sanchez-Camacho C, Rodriguez J, Ruiz JM, Trousse F, Bovolenta P. 2005. Morphogens as growth cone signalling molecules. Brain Res Brain Res Rev 49: 242-252.
98. Sanes JR, Yamagata M. 2009. Many paths to synaptic specificity. Annu Rev Cell Dev Biol 25: 161-195.
99. Seth A, Culverwell J, Walkowicz M, Toro S, Rick JM, Neuhauss SC, Varga ZM, et al. 2006. belladonna/(Ihx2) is required for neural patterning and midline axon guidance in the zebrafish forebrain. Development 133: 725-735.
100. Shamim H, Mahmood R, Logan C, Doherty P, Lumsden A, Mason I. 1999. Sequential roles for Fgf4, En1 and Fgf8 in specification and regionalisation of the midbrain. Development 126: 945-959.
101. Shewan D, Dwivedy A, Anderson R, Holt CE. 2002. Age-related changes underlie switch in netrin-1 responsiveness as growth cones advance along visual pathway. Nat Neurosci 5: 955-962.
102. Take-uchi M, Clarke JD, Wilson SW. 2003. Hedgehog signalling maintains the optic stalk-retinal interface through the regulation of Vax gene activity. Development 130: 955-968.
103. Thompson H, Andrews W, Parnavelas JG, Erskine L. 2009. Robo2 is required for Slit-mediated intraretinal axon guidance. Dev Biol 335: 418-426.
104. Thompson H, Barker D, Camand O, Erskine L. 2006a. Slits contribute to the guidance of retinal ganglion cell axons in the mammalian optic tract. Dev Biol 296: 476-484.
105. Thompson H, Camand O, Barker D, Erskine L. 2006b. Slit proteins regulate distinct aspects of retinal ganglion cell axon guidance within dorsal and ventral retina. J Neurosci 26: 8082-8091.
106. Torborg CL, Feller MB. 2005. Spontaneous patterned retinal activity and the refinement of retinal projections. Prog Neurobiol 76: 213-235.
107. Torres M, Gomez-Pardo E, Gruss P. 1996. Pax2 contributes to inner ear patterning and optic nerve trajectory. Development 122: 3381-3391.
108. Trousse F, Martí E, Gruss P, Torres M, Bovolenta P. 2001. Control of retinal ganglion cell axon growth: A new role for Sonic hedgehog. Development 128: 3927-3936.
109. Wallace VA, Raff MC. 1999. A role for Sonic hedgehog in axon-to-astrocyte signalling in the rodent optic nerve. Development 126: 2901-2909.
110. Wang Y, Dakubo GD, Thurig S, Mazerolle CJ, Wallace VA. 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.
111. Wang YP, Dakubo G, Howley P, Campsall KD, Mazarolle CJ, Shiga SA, Lewis PM, et al. 2002. Development of normal retinal organization depends on Sonic hedgehog signaling from ganglion cells. Nat Neurosci 5: 831-832.
112. Webber CA, Hyakutake MT, McFarlane S. 2003. Fibroblast growth factors redirect retinal axons in vitro and in vivo. Dev Biol 263: 24-34.
113. Whitford KL, Dijkhuizen P, Polleux F, Ghosh A. 2002. Molecular control of cortical dendrite development. Annu Rev Neurosci 25: 127-149.
114. Wilkinson DG. 2001. Multiple roles of EPH receptors and ephrins in neural development. Nat Rev Neurosci 2: 155-164.
115. Williams SE, Mann F, Erskine L, Sakurai T, Wei S, Rossi DJ, Gale NW, et al. 2003. Ephrin-B2 and EphB1 mediate retinal axon divergence at the optic chiasm. Neuron 39: 919-935.
116. Wong RO, Ghosh A. 2002. Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci 3: 803-812.
117. Yam PT, Langlois SD, Morin S, Charron F. 2009. Sonic hedgehog guides axons through a noncanonical, Src-family-kinase-dependent signaling pathway. Neuron 62: 349-362.
118. Yamauchi K, Mizushima S, Tamada A, Yamamoto N, Takashima S, Murakami F. 2009. FGF8 signaling regulates growth of midbrain dopaminergic axons by inducing semaphorin 3F. J Neurosci 29: 4044-4055.
119. Yang XJ. 2004. Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis. Semin Cell Dev Biol 15: 91-103.
120. Yazdani U, Terman JR. 2006. The semaphorins. Genome Biol 7: 211.
121. Zhang XM, Yang XJ. 2001. Temporal and spatial effects of Sonic hedgehog signaling in chick eye morphogenesis. Dev Biol 233: 271-290.
122. Zhou Y, Gunput RA, Pasterkamp RJ. 2008. Semaphorin signaling: Progress made and promises ahead. Trends Biochem Sci 33: 161-170.