Semaphorin signaling in vertebrate neural circuit assembly

Frontiers in Molecular Neuroscience

Volumn , Issue JUNE 2012, 2012, Pages

  Yoshida, Yutaka ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Axon guidance; Neuropilin; Plexin; Semaphorin; Synapse formation

Indexed keywords

NEUROPILIN; PLEXIN; SEMAPHORIN; VASCULOTROPIN;

ACTIN FILAMENT; ADRENERGIC NERVE CELL; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CORPUS CALLOSUM; CORPUS STRIATUM; DENDRITE; DENTATE GYRUS; DOPAMINERGIC NERVE CELL; ENTROPY; GROWTH CONE; HIPPOCAMPAL MOSSY FIBER; MICROTUBULE ASSEMBLY; MOTONEURON; NERVE CELL; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE FIBER; NERVE FIBER GROWTH; NERVE PROJECTION; NONHUMAN; OLFACTORY SYSTEM; OPTIC CHIASM; PHENOTYPE; POSTSYNAPTIC POTENTIAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PYRAMIDAL TRACT; RETINA GANGLION CELL; REVIEW; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPINAL GANGLION; SYNAPTIC TRANSMISSION; THALAMOCORTICAL TRACT; TOPOGRAPHY; VERTEBRATE;

EID: 85184644024     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2012.00071     Document Type: Review

References (114)

1. Artigiani, S., Conrotto, P., Fazzari, P., Gilestro, G. F., Barberis, D., Giordano, S., Comoglio, P. M., and Tam-agnone, L. (2004). Plexin-B3 is a functional receptor for semaphorin 5A. EMBO Rep. 5, 710-714.
2. Bagnard, D., Lohrum, M., Uziel, D., Puschel, A. W., and Bolz, J. (1998). Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections. Development 125, 5043-5053.
3. Bagri, A., Cheng, H. J., Yaron, A., Pleasure, S. J., and Tessier-Lavigne, M. (2003). Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 113, 285-299.
4. Baudet, M. L., Zivraj, K. H., Abreu-Goodger, C., Muldal, A., Armisen, J., Blenkiron, C., Goldstein, L. D., Miska, E. A., and Holt, C. E. (2011). miR-124 acts through CoREST to control onset of Sema3A sensitivity in navigating retinal growth cones. Nat. Neurosci. 15, 29-38.
5. Behar, O., Golden, J. A., Mashimo, H., Schoen, F. J., and Fishman, M. C. (1996). SemaphorinlII isneededfor normal patterning and growth of nerves, bones and heart. Nature 383, 525-528.
6. Bellon, A., Luchino, J., Haigh, K., Rougon, G., Haigh, J., Chauvet, S., and Mann, F. (2010). VEGFR2 (KDR/Flk1) signaling mediates axon growth in response to semaphorin 3E in the developing brain. Neuron 66, 205-219.
7. Bouzioukh, F., Daoudal, G., Falk, J., Debanne, D., Rougon, G., and Castellani, V. (2006). Semaphorin3A regulates synaptic function of differentiated hippocampal neurons. Eur. J. Neurosci. 23, 2247-2254.
8. Bron, R., Vermeren, M., Kokot, N., Andrews, W., Little, G. E., Mitchell, K. J., and Cohen, J. (2007). Boundary cap cells constrain spinal motor neuron somal migration at motor exit points by a semaphorin-plexin mechanism. Neural Dev. 22, 21.
9. Brown, A. G. (1981). Organization in the Spinal Cord. NewYork, NY: Springer.
10. Castellani, V., Chedotal, A., Schachner, M., Faivre-Sarrailh, C., and Rougon, G. (2000). Analysis of the L1-deficient mouse phenotype reveals crosstalk between Sema3A and L1 signaling pathways in axonal guidance. Neuron 27, 237-249.
11. Castellani, V., De Angelis, E., Ken-wrick, S., and Rougon, G. (2002). Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO J. 21, 6348-6357.
12. Chauvet, S., Cohen, S., Yoshida, Y., Fekrane, L., Livet, J., Gayet, O., Segu, L., Buhot, M. C., Jessell, T. M., Henderson, C. E., and Mann, F. (2007). Gating of Sema3E/PlexinD1 signaling by neuropilin-1 switches axonal repulsion to attraction during brain development. Neuron 56, 807-822.
13. Chen, G., Sima, J., Jin, M., Wang, K. Y., Xue, X. J., Zheng, W., Ding, Y. Q., and Yuan, X. B. (2008). Semaphorin-3A guides radial migration of cortical neurons during development. Nat. Neurosci. 11, 36-44.
14. Cheng, H. J., Bagri, A., Yaron, A., Stein, E., Pleasure, S. J., and Tessier-Lavigne, M. (2001). Plexin-A3 mediates semaphorin signaling and regulates the development of hippocampal axonal projections. Neuron 32, 249-263.
15. Coburn, C. M., and Bargmann, C. I. (1996). A putative cyclic nucleotide-gated channel is required for sen-sorydevelopment andfunctionin C. elegans. Neuron 17, 695-706.
16. Cohen, S., Funkelstein, L., Livet, J., Rougon, G., Henderson, C. E., Castellani, V., and Mann, F. (2005). A semaphorin code defines subpopulations of spinal motor neurons during mouse development. Eur. J. Neurosci. 21, 1767-1776.
17. de Winter, F., Cui, Q., Symons, N., Ver-haagen, J., and Harvey, A. R. (2004). Expression of class-3 semaphorins and their receptors in the neonatal and adult rat retina. Invest. Ophthalmol. Vis. Sci. 45, 4554-4562.
18. Ding, J. B., Oh, W. J., Sabatini, B. L., and Gu, C. (2012). Semaphorin 3E-Plexin-D1 signaling controls pathway-specific synapse formation in the striatum. Nat. Neurosci. 15, 215-223.
19. Erskine, L., Reijntjes, S., Pratt, T., Denti, L., Schwarz, Q., Vieira, J. M., Alakakone, B., Shewan, D., and Ruhrberg, C. (2011). VEGF signaling through neuropilin 1 guides commissural axon crossing at the optic chiasm. Neuron 70, 951-965.
20. Falk, J., Bechara, A., Fiore, R., Nawabi, H., Zhou, H., Hoyo-Becerra, C., Bozon, M., Rougon, G., Grumet, M., Püschel, A. W., Sanes, J. R., and Castellani, V. (2005). Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron 48, 63-75.
21. Faulkner, R. L., Low, L. K., Liu, X. B., Coble, J., Jones, E. G., and Cheng, H. J. (2008). Dorsal turning of motor corticospinal axons at the pyramidal decussation requires plexin signaling. Neural Dev. 3, 21.
22. Fenstermaker, V., Chen, Y., Ghosh, A., and Yuste, R. (2004). Regulation of dendritic length and branching by semaphorin 3A. J. Neurobiol. 58, 403-412.
23. Friedel, R. H., Kerjan, G., Rayburn, H., Schüller, U., Sotelo, C., Tessier-Lavigne, M., and Chédotal, A. (2007). Plexin-B2 controls the development of cerebellar granule cells. J. Neurosci. 27, 3921-3932.
24. Fu, S. Y., Sharma, K., Luo, Y., Raper, J. A., and Frank, E. (2000). SEMA3A regulates developing sensory projections in the chicken spinal cord. J. Neurobiol. 45, 227-236.
25. Gu, C., Rodriguez, E. R., Reimert, D. V., Shu, T., Fritzsch, B., Richards, L. J., Kolodkin, A. L., and Ginty, D. D. (2003). Neuropilin-1 conveys sema-phorin and VEGF signaling during neural and cardiovascular development. Dev. Cell 5, 45-57.
26. Gu, C., Yoshida, Y., Livet, J., Reimert, D. V., Mann, F., Merte, J., Henderson, C. E., Jessell, T. M., Kolodkin, A. L., and Ginty, D. D. (2005). Semaphorin 3E and plexin-Dl control vascular pattern independently of neuropilins. Science 307, 265-268.
27. Hernández-Miranda, L. R., Cariboni, A., Faux, C., Ruhrberg, C., Cho, J. H., Cloutier, J. F., Eickholt, B. J., Par-navelas, J. G., and Andrews, W. D. (2011). Robol regulates semaphorin signaling to guide the migration of cortical interneurons through the ventral forebrain. J. Neurosci. 31, 6174-6187.
28. Huber, A. B., Kania, A., Tran, T. S., Gu, C., De Marco Garcia, N., Lieberam, I., Johnson, D., Jessell, T. M., Ginty, D. D., and Kolodkin, A. L. (2005). Distinct roles for secreted sema-phorin signaling in spinal motor axon guidance. Neuron 48, 949-964.
29. Huettl, R. E., Soellner, H., Bianchi, E., Novitch, B. G., and Huber, A. B. (2011). Npn-1 contributes to axon-axon interactions that differentially control sensory and motor innervation of the limb. PLoS Biol. 9, e1001020. doi:10.1371/journal.pbio.1001020
30. Imai, T., Suzuki, M., and Sakano, H. (2006). Odorant receptor-derived cAMP signals direct axonal targeting. Science 314, 657-661.
31. Imai, T., Yamazaki, T., Kobayakawa, R., Kobayakawa, K., Abe, T., Suzuki, M., and Sakano, H. (2009). Pretarget axon sorting establishes the neural map topography. Science 325, 585-590.
32. Jan, Y. N., and Jan, L. Y. (2003). The control of dendrite development. Neuron 40, 229-242.
33. Kerjan, G., Dolan, J., Haumaitre, C., Schneider-Maunoury, S., Fujisawa, H., Mitchell, K. J., and Chédotal, A. (2005). The transmembrane sema-phorin Sema6A controls cerebellar granule cell migration. Nat. Neurosci. 8, 1516-1524.
34. Kikutani, H., and Kumanogoh, A. (2003). Semaphorins in interactions between T cells and antigen-presenting cells. Nat. Rev. Immunol. 3, 159-167.
35. Kitsukawa, T., Shimizu, M., Sanbo, M., Hirata, T., Taniguchi, M., Bekku, Y., Yagi, T., and Fujisawa, H. (1997). Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19, 995-1005.
36. Koerber, H. R., and Mendell, L. M. (1992). "Functional heterogeneity of dorsal root ganglion cells, "in Sensory Neurons: Diversity, Developmentand Plasticity, ed. S. A. Scott (New York: Oxford University Press), 77-96.
37. Kolk, S. M., Gunput, R. A., Tran, T. S., van den Heuvel, D. M., Prasad, A. A., Hellemons, A. J., Adolfs, Y., Ginty, D. D., Kolodkin, A. L., Burbach, J. P., Smidt, M. P., and Pasterkamp, R. J. (2009). Semaphorin 3F is a bifunctional guidance cue for dopaminergic axons and controls their fascic-ulation, channeling, rostral growth, and intracortical targeting. J. Neu-rosci. 29, 12542-12557.
38. Komatsu, H., Mori, I., Rhee, J. S., Akaike, N., and Ohshima, Y. (1996). Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17, 707-718.
39. Komuro, H., Yacubova, E., Yacubova, E., and Rakic, P. (2001). Mode and tempo of tangential cell migration in the cerebellar external granular layer. J. Neurosci. 21, 527-540.
40. Kumanogoh, A., Marukawa, S., Suzuki, K., Takegahara, N., Watanabe, C., Ch'Ng, E., Ishida, I., Fujimura, H., Sakoda, S., Yoshida, K., and Kiku-tani, H. (2002). Class IV semaphorin Sema4A enhances T-cell activation and interacts with Tim-2. Nature 419, 629-633.
41. Kumanogoh, A., Watanabe, C., Lee, I., Wang, X., Shi, W., Araki, H., Hirata, H., Iwahori, K., Uchida, J., Yasui, T., Matsumoto, M., Yoshida, K., Yakura, H., Pan, C., Parnes, J. R., and Kikutani, H. (2000). Identification of CD72 as a lymphocyte receptor for the class IV semaphorin CD100: a novel mechanism for regulating B cell signaling. Immunity 13, 621-631.
42. Kuwajima, T., Yoshida, Y., Takegahara, N., Kumanogoh, A., Petros, T. J., Jessell, T. M., Sakurai, T., and Mason, C. (2012). Optic chiasm presentation of Semaphorin6D in the context of Plexin-A1 and Nr-CAM promotes retinal axon midline crossing. Neuron 74, 676-690.
43. Ladle, D. R., Pecho-Vrieseling, E., and Arber, S. (2007). Assembly of motor circuits in the spinal cord: driven to function by genetic and experience-dependent mechanisms. Neuron 56, 270-283.
44. Landmesser, L. (1978). The development of motor projection patterns in the chick hind limb. J. Physiol. (Lond.) 284, 391-414.
45. Leighton, P. A., Mitchell, K. J., Goodrich, L. V., Lu, X., Pinson, K., Scherz, P., Skarnes, W. C., and Tessier-Lavigne, M. (2001). Defining brain wiring patterns and mechanisms through gene trapping in mice. Nature 410, 174-179.
46. Leslie, J. R., Imai, F., Fukuhara, K., Takegahara, N., Rizvi, T. A., Friedel, R. H., Wang, F., Kumanogoh, A., and Yoshida, Y. (2011). Ectopic myelinating oligodendrocytes in the dorsal spinal cord as a consequence of altered semaphorin 6D signaling inhibit synapse formation. Development 138, 4085-4095.
47. Little, G. E., López-Bendito, G., Rünker, A. E., García, N., Piñon, M. C., Chédotal, A., Molnár, Z., and Mitchell, K. J. (2009). Specificity and plasticity of thalamocortical connections in Sema6A mutant mice. PLoS Biol. 7, e98. doi:10.1371/journal.pbio.1000098
48. Liu, X. B., Low, L. K., Jones, E. G., and Cheng, H. J. (2005). Stereotyped axon pruning via plexin signaling is associated with synaptic complex elimination in the hippocampus. J. Neurosci. 25, 9124-9134.
49. Low, L. K., Liu, X. B., Faulkner, R. L., Coble, J., and Cheng, H. J. (2008). Plexin signaling selectively regulates the stereotyped pruning of corticospinal axons from visual cortex. Proc. Natl. Acad. Sci. U.S.A. 105, 8136-8141.
50. Maier, V., Jolicoeur, C., Rayburn, H., Takegahara, N., Kumanogoh, A., Kikutani, H., Tessier-Lavigne, M., Wurst, W., and Friedel, R. H. (2011). Semaphorin 4C and 4G are ligands of Plexin-B2 required in cerebellar development. Mol. Cell. Neurosci. 46, 419-431.
51. Mann, F., Chauvet, S., and Rougon, G. (2007). Semaphorins in development and adult brain: implication for neurological diseases. Prog. Neurobiol. 82, 57-79.
52. Marín, O., Yaron, A., Bagri, A., Tessier-Lavigne, M., and Rubenstein, J. L. (2001). Sorting of striatal and cortical interneurons regulated by semaphorin-neuropilin interactions. Science 293, 872-875.
53. Matsuoka, R. L., Chivatakarn, O., Badea, T. C., Samuels, I. S., Cahill, H., Katayama, K., Kumar, S. R., Suto, F., Chédotal, A., Peachey, N. S., Nathans, J., Yoshida, Y., Giger, R. J., and Kolodkin, A. L. (2011a). Class 5 transmembrane semaphorins control selective Mammalian retinal lamination and function. Neuron 71, 460-473.
54. Matsuoka, R. L., Nguyen-Ba-Charvet, K. T., Parray, A., Badea, T. C., Chédotal, A., and Kolodkin, A. L. (2011b). Transmembrane sem-aphorin signalling controls laminar stratification in the mammalian retina. Nature 470, 259-263.
55. Mauti, O., Domanitskaya, E., Ander-matt, I., Sadhu, R., and Stoeckli, E. T. (2007). Semaphorin6A acts as a gate keeper between the central and the peripheral nervous system. Neural Dev. 2, 28.
56. Messersmith, E. K., Leonardo, E. D., Shatz, C. J., Tessier-Lavigne, M., Goodman, C. S., and Kolodkin, A. L. (1995). Semaphorin III can function as a selective chemorepellent to pattern sensoryprojections in the spinal cord. Neuron 14, 949-959.
57. Mombaerts, P. (2006). Axonal wiring in the mouse olfactory system. Annu. Rev. Cell Dev. Biol. 22, 713-737.
58. Moret, F., Renaudot, C., Bozon, M., and Castellani, V. (2007). Semaphorin and neuropilin co-expression in motoneurons sets axon sensitivity to environmental semaphorinsources during motor axon pathfinding. Development 134, 4491-4501.
59. Mori, K., and Sakano, H. (2011). How is the olfactory map formed and interpreted in the mammalian brain? Annu. Rev. Neurosci. 34, 467-499.
60. Mumm, J. S., Williams, P. R., God-inho, L., Koerber, A., Pittman, A. J., Roeser, T., Chien, C. B., Baier, H., and Wong, R. O. (2006). In vivo imaging reveals dendritic targeting of laminated afferents by zebrafish retinal ganglion cells. Neuron 52, 609-621.
61. Nawabi, H., Briançon-Marjollet, A., Clark, C., Sanyas, I., Takamatsu, H., Okuno, T., Kumanogoh, A., Bozon, M., Takeshima, K., Yoshida, Y., Moret, F., Abouzid, K., and Castel-lani, V. (2010). A midline switch of receptor processing regulates commissural axon guidance in vertebrates. Genes Dev. 24, 396-410.
62. Niquille, M., Garel, S., Mann, F., Hor-nung, J. P., Otsmane, B., Chevalley, 5., Parras, C., Guillemot, F., Gas-par, P., Yanagawa, Y., and Lebrand, C. (2009). Transient neuronal populations are required to guide callosal axons: a role for sema-phorin 3C. PLoS Biol. 7, e1000230. doi:10.1371/journal.pbio.1000230
63. Nishiyama, M., Togashi, K., von Schim-melmann, M. J., Lim, C. S., Maeda, S., Yamashita, N., Goshima, Y., Ishii, 5., and Hong, K. (2011). Semaphorin 3A induces CaV2.3 channel-dependent conversion of axons to dendrites. Nat. Cell Biol. 13, 676-685.
64. O'Connor, T. P., Cockburn, K., Wang, W., Tapia, L., Currie, E., and Bamji, S. X. (2009). Semaphorin 5B mediates synapse elimination in hippocampal neurons. Neural Dev. 4, 18.
65. Okado, N., Homma, S., Ishihara, R., and Kohno, K. (1990). Distribution patterns of dendrites in motor neuron pools of lumbosacral spinal cord of the chicken. Anat. Embryol. 182, 113-121.
66. Paradis, S., Harrar, D. B., Lin, Y., Koon, A. C., Hauser, J. L., Griffith, E. C., Zhu, L., Brass, L. F., Chen, C., and Greenberg, M. E. (2007). An RNAi-based approach identifies molecules required for glutamater-gic and GABAergic synapse development. Neuron 53, 217-232.
67. Parra, L. M., and Zou, Y. (2010). Sonic hedgehog induces response of commissural axons to Semaphorin repulsion during midline crossing. Nat. Neurosci. 13, 29-35.
68. Pasterkamp, R. J., and Giger, R. J. (2009). Semaphorin function in neural plasticity and disease. Curr. Opin. Neu-robiol. 19, 263-274.
69. Pasterkamp, R. J., Peschon, J. J., Spriggs, M. K., and Kolodkin, A. L. (2003). Semaphorin 7A promotes axon outgrowth through integrins and MAPKs. Nature 424, 398-405.
70. Pecho-Vrieseling, E., Sigrist, M., Yoshida, Y., Jessell, T. M., and Arber, S. (2009). Specificity of sensory-motor connections encoded by Sema3e-Plxnd1 recognition. Nature 459, 842-826.
71. Polleux, F., Morrow, T., and Ghosh, A. (2000). Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404, 567-573.
72. Porter, L. L., and White, E. L. (1983). Afferent and efferent pathways of the vibrissal region of primary motor cortexinthemouse. J. Comp. Neurol. 214, 279-289.
73. Renaud, J., Kerjan, G., Sumita, I., Zagar, Y., Georget, V., Kim, D., Fouquet, C., Suda, K., Sanbo, M., Suto, F., Ackerman, S. L., Mitchell, K. J., Fujisawa, H., and Chédotal, A. (2008). Plexin-A2 and its ligand, Sema6A, control nucleus-centrosome coupling in migrating granule cells. Nat. Neu-rosci. 11, 440-409.
74. Ruhrberg, C., Gerhardt, H., Golding, M., Watson, R., Ioannidou, S., Fujisawa, H., Betsholtz, C., and Shima, D. T. (2002). Spatiallyrestricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 16, 2684-2698.
75. Rünker, A. E., Little, G. E., Suto, F., Fujisawa, H., and Mitchell, K. J. (2008). Semaphorin-6A controls guidance of corticospinal tract axons at multiple choice points. Neural Dev. 3, 34.
76. Ryder, E. F., and Cepko, C. L. (1994). Migration patterns of clonally related granule cells and their progenitors in the developing chick cerebellum. Neuron 12, 1011-1028.
77. Sahay, A., Kim, C. H., Sepkuty, J. P., Cho, E., Huganir, R. L., Ginty, D. D., and Kolodkin, A. L. (2005). Secreted semaphorins modulate synaptic transmission in the adult hippocampus. J. Neurosci. 25, 3613-3620.
78. Sanes, J. R., and Zipursky, S. L. (2010). Design principles of insect and vertebrate visual systems. Neuron 66, 15-36.
79. Schwarz, Q., Gu, C., Fujisawa, H., Sabelko, K., Gertsenstein, M., Nagy, A., Taniguchi, M., Kolodkin, A. L., Ginty, D. D., Shima, D. T., and Ruhrberg, C. (2004). Vascular endothelial growth factor controls neuronal migration and cooperates with Sema3A to pattern distinct compartments of the facial nerve. GenesDev. 18, 2822-2834.
80. Shelly, M., Cancedda, L., Heilshorn, S., Sumbre, G., and Poo, M. M. (2007). LKB1/STRAD promotes axon initiation during neuronal polarization. Cell 129, 565-577.
81. Shelly, M., Cancedda, L., Lim, B. K., Popescu, A. T., Cheng, P. L., Gao, H., and Poo, M. M. (2011). Sema-phorin3A regulates neuronal polarization by suppressing axon formation and promoting dendrite growth. Neuron 71, 433-446.
82. Shelly, M., Lim, B. K., Cancedda, L., Heilshorn, S. C., Gao, H., and Poo, M. M. (2010). Local and long-range reciprocal regulation of cAMP and cGMP in axon/dendrite formation. Science 327, 547-552.
83. Song, H., Ming, G., He, Z., Lehmann, M., McKerracher, L., Tessier-Lavigne, M., and Poo, M. (1998). Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281, 1515-1518.
84. Stacy, R. C., and Wong, R. O. (2003). Developmental relationship between cholinergic amacrine cell processes and ganglion cell dendrites of the mouse retina. J. Comp. Neurol. 456, 154-166.
85. Stanfield, B. B. (1992). The development of the corticospinal projection. Prog. Neurobiol. 38, 169-202.
86. Surmeier, D. J., Ding, J., Day, M., Wang, Z., and Shen, W. (2007). D1 and D2 dopamine-receptor modulation of striatal glutamater-gic signaling in striatal medium spiny neurons. Trends Neurosci. 30, 228-235.
87. Suto, F., Ito, K., Uemura, M., Shimizu, M., Shinkawa, Y., Sanbo, M., Shin-oda, T., Tsuboi, M., Takashima, S., Yagi, T., and Fujisawa, H. (2005). Plexin-a4 mediates axon-repulsive activities ofboth secreted and transmembrane semaphorins and plays roles in nerve fiber guidance. J. Neu-rosci. 25, 3628-3637.
88. Suto, F., Tsuboi, M., Kamiya, H., Mizuno, H., Kiyama, Y., Komai, S., Shimizu, M., Sanbo, M., Yagi, T., Hiromi, Y., Chédotal, A., Mitchell, K. J., Manabe, T., and Fujisawa, H. (2007). Interactions between plexin-A2, plexin-A4, and semaphorin 6A control lamina-restricted projection of hippocampal mossy fibers. Neuron 53, 535-547.
89. Suzuki, K., Kumanogoh, A., and Kiku-tani, H. (2008). Semaphorins and their receptors in immune cell interactions. Nat. Immunol. 9, 17-23.
90. Takahashi, T., Fournier, A., Nakamura, F., Wang, L. H., Murakami, Y., Kalb, R. G., Fujisawa, H., and Strittmatter, S. M. (1999). Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99, 59-69.
91. Takamatsu, H., and Kumanogoh, A. (2012). Diverse roles for semaphorin-plexin signaling in the immune system. Trends Immunol. 33, 127-135.
92. Takeuchi, H., Inokuchi, K., Aoki, M., Suto, F., Tsuboi, A., Matsuda, I., Suzuki, M., Aiba, A., Serizawa, S., Yoshihara, Y., Fujisawa, H., and Sakano, H. (2010). Sequentialarrival and graded secretion of Sema3F by olfactory neuron axons specify map topography at the bulb. Cell 141, 1056-1067.
93. Tamagnone, L., Artigiani, S., Chen, H., He, Z., Ming, G. I., Song, H., Chedotal, A., Winberg, M. L., Goodman, C. S., Poo, M., Tessier-Lavigne, M., and Comoglio, P. M. (1999). Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored sem-aphorins in vertebrates. Cell 99, 71-80.
94. Taniguchi, M., Yuasa, S., Fujisawa, H., Naruse, I., Saga, S., Mishina, M., and Yagi, T. (1997). Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron 19, 519-530.
95. Tawarayama, H., Yoshida, Y., Suto, F., Mitchell, K. J., and Fujisawa, H. (2010). Roles ofsemaphorin-6B and plexin-A2 in lamina-restricted pro-jectionofhippocampalmossyfibers. J. Neurosci. 30, 7049-7060.
96. Thong, I. G., and Dreher, B. (1987). The development of the corticotec-tal pathway in the albino rat: transient projections from the visual and motor cortices. Neurosci. Lett. 80, 275-282.
97. Togashi, K., von Schimmelmann, M. J., Nishiyama, M., Lim, C. S., Yoshida, N., Yun, B., Molday, R. S., Goshima, Y., and Hong, K. (2008). Cyclic GMP-gated CNG channels function in Sema3A-induced growth cone repulsion. Neuron 58, 694-707.
98. Toyofuku, T., Yoshida, J., Sugimoto, T., Zhang, H., Kumanogoh, A., Hori, M., and Kikutani, H. (2005). FARP2 triggers signals for Sema3A-mediated axonal repulsion. Nat. Neurosci. 8, 1712-1719.
99. Toyofuku, T., Zhang, H., Kumanogoh, A., Takegahara, N., Suto, F., Kamei, J., Aoki, K., Yabuki, M., Hori, M., Fujisawa, H., and Kikutani, H. (2004). Dual roles of Sema6D in cardiac morphogenesis through region-specific association of its receptor, Plexin-A1, with off-track and vascular endothelial growth factor receptor type 2. Genes Dev. 18, 435-447.
100. Tran, T. S., Kolodkin, A. L., and Bharad-waj, R. (2007). Semaphorin regulation of cellular morphology. Annu. Rev. CellDev. Biol. 23, 263-292.
101. Tran, T. S., Rubio, M. E., Clem, R. L., Johnson, D., Case, L., Tessier-Lavigne, M., Huganir, R. L., Ginty, D. D., and Kolodkin, A. L. (2009). Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS. Nature 462, 1065-1069.
102. Vermeren, M., Maro, G. S., Bron, R., McGonnell, I. M., Charnay, P., Topilko, P., and Cohen, J. (2003). Integrity of developing spinal motor columns is regulated by neural crest derivatives at motor exit points. Neuron 37, 403-415.
103. Vrieseling, E., and Arber, S. (2006). Target-induced transcriptional control of dendritic patterning and connectivity in motor neurons by the ETS gene Pea3. Cell 127, 1439-1452.
104. Wässle, H. (2004). Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 5, 747-757.
105. Williams, S. E., Grumet, M., Colman, D. R., Henkemeyer, M., Mason, C. A., and Sakurai, T. (2006). A role for Nr-CAM in the patterning of binocular visual pathways. Neuron 50, 535-547.
106. Wingate, R. J. (2001). The rhombic lip and early cerebellar development. Curr. Opin. Neurobiol. 11, 82-88.
107. Wolman, M. A., Liu, Y., Tawarayama, H., Shoji, W., and Halloran, M. C. (2004). Repulsion and attraction of axons by semaphorin3D are mediated by different neuropilins in vivo. J. Neurosci. 24, 8428-8435.
108. Wu, Z., Sweeney, L. B., Ayoob, J. C., Chak, K., Andreone, B. J., Ohyama, T., Kerr, R., Luo, L., Zlatic, M., and Kolodkin, A. L. (2011). A combinatorial semaphorin code instructs the initial steps of sensory circuit assembly in the Drosophila CNS. Neuron 70, 281-298.
109. Yamauchi, K., Mizushima, S., Tamada, A., Yamamoto, N., Takashima, S., and Murakami, F. (2009). FGF8 signaling regulates growth of midbrain dopaminergic axons by inducing semaphorin 3F. J. Neurosci. 29, 4044-4055.
110. Yorke, C. H. Jr., and Caviness, V. S. Jr. (1975). Interhemispheric neocorti-cal connections of the corpus callosum in the normal mouse: a study based on anterograde and retrograde methods. J. Comp. Neurol. 164, 233-245.
111. Yoshida, Y., Han, B., Mendelsohn, M., and Jessell, T. M. (2006). PlexinA1 signaling directs the segregation of proprioceptive sensory axons in the developing spinal cord. Neuron 52, 775-788.
112. Zheng, C., Feinstein, P., Bozza, T., Rodriguez, I., and Mom-baerts, P. (2000). Peripheral olfactory projections are differentially affected in mice deficient in a cyclic nucleotide-gated channel subunit. Neuron 26, 81-91.
113. Zhuang, B., Su, Y. S., and Sock-anathan, S. (2009). FARP1 promotes the dendritic growth of spinal motor neuron subtypes through transmembrane Semaphorin6A and PlexinA4 signaling. Neuron 61, 359-372.
114. Zou, Y., Stoeckli, E., Chen, H., and Tessier-Lavigne, M. (2000). Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 102, 363-375.