Semaphorin 5B is a repellent cue for sensory afferents projecting into the developing spinal cord

Development (Cambridge)

Volumn 141, Issue 9, 2014, Pages 1940-1949

  Liu, Rachel Q ^a,b   Wang, Wenyan ^a   Legg, Arthur ^a   Abramyan, John ^a   O'Connor, Timothy P ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b INTERNATIONAL COLLABORATION ON REPAIR DISCOVERIES   (Canada)

Author keywords

Chick; Dorsal root entry zone; Repulsion; Sema5B

Indexed keywords

CELL ADHESION MOLECULE; NERVE GROWTH FACTOR; SEMAPHORIN; SEMAPHORIN 5B; TAG 1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CHICK; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; GRAY MATTER; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SENSORY NERVE; SPINAL CORD; SPINAL CORD DORSAL HORN; VENTRAL ROOT;

CHICK; DORSAL ROOT ENTRY ZONE; REPULSION; SEMA5B;

ANIMALS; AVIAN PROTEINS; AXONS; BODY PATTERNING; CHICK EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; NEURONS, AFFERENT; NOCICEPTION; PROPRIOCEPTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SEMAPHORINS; SENSORY RECEPTOR CELLS; SPINAL CORD;

EID: 84899619113     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.103630     Document Type: Article

References (42)

1. Adams, R. H., Betz, H. and Püschel, A. W. (1996). A novel class of murine semaphorins with homology to thrombospondin is differentially expressed during early embryogenesis. Mech. Dev. 57, 33-45.
2. Behar, O., Golden, J. A., Mashimo, H., Schoen, F. J. and Fishman, M. C. (1996). Semaphorin III is needed for normal patterning and growth of nerves, bones and heart. Nature 383, 525-528.
3. Browne, K., Wang, W., Liu, R. Q., Piva, M. and O'Connor, T. P. (2012). Transmembrane semaphorin5B is proteolytically processed into a repulsive neural guidance cue. J. Neurochem. 123, 135-146.
4. Chan, C. C. M., Roberts, C. R., Steeves, J. D. and Tetzlaff, W. (2008). Aggrecan components differentially modulate nerve growth factor-responsive and neurotrophin-3-responsive dorsal root ganglion neurite growth. J. Neurosci. Res. 86, 581-592.
5. Dang, P., Smythe, E. and Furley, A. J. W. (2012). TAG1 regulates the endocytic trafficking and signaling of the semaphorin3A receptor complex. J. Neurosci. 32, 10370-10382.
6. Davis, B. M., Frank, E., Johnson, F. A. and Scott, S. A. (1989). Development of central projections of lumbosacral sensory neurons in the chick. J. Comp. Neurol. 279, 556-566.
7. Eide, A. L. and Glover, J. C. (1995). Development of the longitudinal projection patterns of lumbar primary sensory afferents in the chicken embryo. J. Comp. Neurol. 353, 247-259.
8. Eide, A. L. and Glover, J. C. (1996). Development of an identified spinal commissural interneuron population in an amniote: neurons of the avian Hofmann nuclei. J. Neurosci. 16, 5749-5761.
9. Eide, A. L. and Glover, J. C. (1997). Developmental dynamics of functionally specific primary sensory afferent projections in the chicken embryo. Anat. Embryol. 195, 237-250.
10. Freigang, J., Proba, K., Leder, L., Diederichs, K., Sonderegger, P. andWelte, W. (2000). The crystal structure of the ligand binding module of axonin-1/TAG-1 suggests a zipper mechanism for neural cell adhesion. Cell 101, 425-433.
11. 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.
12. Furley, A. J., Morton, S. B., Manalo, D., Karagogeos, D., Dodd, J. and Jessell, T. M. (1990). The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell 61, 157-170.
13. 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 semaphorin and VEGF signaling during neural and cardiovascular development. Dev. Cell 5, 45-57.
14. Guan, W. and Condic, M. L. (2003). Characterization of Netrin-1, Neogenin and cUNC-5H3 expression during chick dorsal root ganglia development. Gene Expr. Patterns 3, 369-373.
15. Hamburger, V. and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
16. 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.
17. Law, C. O., Kirby, R. J., Aghamohammadzadeh, S. and Furley, A. J. W. (2008). The neural adhesion molecule TAG-1 modulates responses of sensory axons to diffusible guidance signals. Development 135, 2361-2371.
18. Lefcort, F., Clary, D. O., Rusoff, A. C. and Reichardt, L. F. (1996). Inhibition of the NT-3 receptor TrkC, early in chick embryogenesis, results in severe reductions in multiple neuronal subpopulations in the dorsal root ganglia. J. Neurosci. 16, 3704-3713.
19. Lett, R. L. M., Wang, W. and O'Connor, T. P. (2009). Semaphorin 5B is a novel inhibitory cue for corticofugal axons. Cereb. Cortex 19, 1408-1421.
20. Masuda, T. and Shiga, T. (2005). Chemorepulsion and cell adhesion molecules in patterning initial trajectories of sensory axons. Neurosci. Res. 51, 337-347.
21. Masuda, T., Tsuji, H., Taniguchi, M., Yagi, T., Tessier-Lavigne, M., Fujisawa, H., Okado, N. and Shiga, T. (2003). Differential non-target-derived repulsive signals play a critical role in shaping initial axonal growth of dorsal root ganglion neurons. Dev. Biol. 254, 289-302.
22. Matsuoka, R. L., Chivatakarn, O., Badea, T. C., Samuels, I. S., Cahill, H., Katayama, K.-I., Kumar, S. R., Suto, F., Chédotal, A., Peachey, N. S. et al. (2011). Class 5 transmembrane semaphorins control selective Mammalian retinal lamination and function. Neuron 71, 460-473.
23. Mauti, O., Domanitskaya, E., Andermatt, I., Sadhu, R. and Stoeckli, E. T. (2007). Semaphorin 6A acts as a gate keeper between the central and the peripheral nervous system. Neural Dev. 2, 28.
24. Mendelson, B., Koerber, H. R. and Frank, E. (1992). Development of cutaneous and proprioceptive afferent projections in the chick spinal cord. Neurosci. Lett. 138, 72-76.
25. 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 sensory projections in the spinal cord. Neuron 14, 949-959.
26. Nakamura, H. and Funahashi, J.-I. (2001). Introduction of DNA into chick embryos by in ovo electroporation. Methods 24, 43-48.
27. 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.
28. Perrin, F. E., Rathjen, F. G. and Stoeckli, E. T. (2001). Distinct subpopulations of sensory afferents require F11 or axonin-1 for growth to their target layers within the spinal cord of the chick. Neuron 30, 707-723.
29. Rader, C., Stoeckli, E. T., Ziegler, U., Osterwalder, T., Kunz, B. and Sonderegger, P. (1993). Cell-cell adhesion by homophilic interaction of the neuronal recognition molecule axonin-1. Eur. J. Biochem. 215, 133-141.
30. Reynolds, A., Leake, D., Boese, Q., Scaringe, S., Marshall, W. S. and Khvorova, A. (2004). Rational siRNA design for RNA interference. Nat. Biotechnol. 22, 326-330.
31. Schmidt, H., Stonkute, A., Juttner, R., Schaffer, S., Buttgereit, J., Feil, R., Hofmann, F. and Rathjen, F. G. (2007). The receptor guanylyl cyclase Npr2 is essential for sensory axon bifurcation within the spinal cord. J. Cell Biol. 179, 331-340.
32. Sharma, K. and Frank, E. (1998). Sensory axons are guided by local cues in the developing dorsal spinal cord. Development 125, 635-643.
33. Shepherd, I., Luo, Y., Raper, J. A. and Chang, S. (1996). The distribution of collapsin-1 mRNA in the developing chick nervous system. Dev. Biol. 173, 185-199.
34. Shepherd, I. T., Luo, Y., Lefcort, F., Reichardt, L. F. and Raper, J. A. (1997). A sensory axon repellent secreted from ventral spinal cord explants is neutralized by antibodies raised against collapsin-1. Development 124, 1377-1385.
35. Snider, W. D. and Silos-Santiago, I. (1996). Dorsal root ganglion neurons require functional neurotrophin receptors for survival during development. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351, 395-403.
36. Sprague, J. M. (1958). The distribution of dorsal root fibres on motor cells in the lumbosacral spinal cord of the cat, and the site of excitatory and inhibitory terminals in monosynaptic pathways. Proc. R. Soc. Lond. B Biol. Sci. 149, 534-556.
37. 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.
38. To, K. C. W., Church, J. and O'Connor, T. P. (2007). Combined activation of calpain and calcineurin during ligand-induced growth cone collapse. Mol. Cell. Neurosci. 36, 425-434.
39. Wang, H., Copeland, N. G., Gilbert, D. J., Jenkins, N. A. and Tessier-Lavigne, M. (1999). Netrin-3, a mouse homolog of human NTN2L, is highly expressed in sensory ganglia and shows differential binding to netrin receptors. J. Neurosci. 19, 4938-4947.
40. Watanabe, K., Tamamaki, N., Furuta, T., Ackerman, S. L., Ikenaka, K. and Ono, K. (2006). Dorsally derived netrin 1 provides an inhibitory cue and elaborates the 'waiting period' for primary sensory axons in the developing spinal cord. Development 133, 1379-1387.
41. Wright, D. E., White, F. A., Gerfen, R. W., Silos-Santiago, I. and Snider, W. D. (1995). The guidance molecule semaphorin III is expressed in regions of spinal cord and periphery avoided by growing sensory axons. J. Comp. Neurol. 361, 321-333.
42. Zuellig, R. A., Rader, C., Schroeder, A., Kalousek, M. B., Von Bohlen und Halbach, F., Osterwalder, T., Inan, C., Stoeckli, E. T., Affolter, H.-U., Fritz, A. et al. (1992). The axonally secreted cell adhesion molecule, axonin-1. Primary structure, immunoglobulin-like and fibronectin-type-III-like domains and glycosyl-phosphatidylinositol anchorage. Eur. J. Biochem. 204, 453-463.