A semaphorin code defines subpopulations of spinal motor neurons during mouse development

European Journal of Neuroscience

Volumn 21, Issue 7, 2005, Pages 1767-1776

  Cohen, Samia ^a   Funkelstein, Lydiane ^b   Livet, Jean ^a,c   Rougon, Geneviève ^b   Henderson, Christopher E ^a   Castellani, Valerie ^b,d   Mann, Fanny ^a  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c HARVARD UNIVERSITY   (United States)

^d CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Axon guidance; Growth cone collapse; Motor pool; Neuropilin; Plexin

Indexed keywords

CELL SURFACE PROTEIN; MESSENGER RNA; NEUROPILIN; PLEXIN; SEMAPHORIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; EFFERENT NERVE; EMBRYO; GROWTH CONE; IN SITU HYBRIDIZATION; LUMBAR SPINAL CORD; MOTONEURON; MOUSE; NERVE FIBER; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; SENSORY NERVE; SPINAL CORD; SPINAL CORD MOTONEURON;

ANIMALS; AXONS; CELL ADHESION MOLECULES; DNA-BINDING PROTEINS; EMBRYO; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICE; MOTOR NEURONS; NERVE TISSUE PROTEINS; NEUROPILINS; NUCLEAR PROTEINS; PREGNANCY; SEMAPHORINS; SPINAL CORD;

EID: 18844448730     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04021.x     Document Type: Article

References (48)

1. Adams, R.H., Betz, H. & Puschel, 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. Arber, S., Ladle, D.R., Lin, J.H., Frank, E. & Jessell, T.M. (2000) ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell, 101, 485-498.
3. Arce, V., Garces, A., de Bovis, B., Filippi, P., Henderson, C., Pettmann, B. & deLapeyriere, O. (1999) Cardiotrophin-1 requires LIFRbeta to promote survival of mouse motoneurons purified by a novel technique. J. Neurosci. Res., 55, 119-126.
4. Carroll, P., Gayet, O., Feuillet, C., Kallenbach, S., de Bovis, B., Dudley, K. & Alonso, S. (2001) Juxtaposition of CNR protocadherins and reelin expression in the developing spinal cord. Mol. Cell Neurosci., 17, 611-623.
5. Castellani, V. & Rougon, G. (2002) Control of semaphorin signaling. Curr. Opin. Neurobiol., 12, 532-541.
6. Chedotal, A., Del Rio, J.A., Ruiz, M., He, Z., Borrell, V., de Castro, F., Ezan, F., Goodman, C.S., Tessier-Lavigne, M., Sotelo, C. & Soriano, E. (1998) Semaphorins III and IV repel hippocampal axons via two distinct receptors. Development, 125, 4313-4323.
7. Chen, H., Chedotal, A., He, Z., Goodman, C.S. & Tessier-Lavigne, M. (1997) Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron, 19, 547-559.
8. Cheng, H.J., Bagri, A., Yaron, A., Stein, E., Pleasure, S.J. & Tessier-Lavigne, M. (2001) Plexin-A3 mediates semaphorin signaling and regulates the development of hippocampal axonal projections. Neuron, 32, 249-263.
9. Chilton, J.K. & Guthrie, S. (2003) Cranial expression of class 3 secreted semaphorins and their neuropilin receptors. Dev. Dyn., 228, 726-733.
10. Cloutier, J.F., Giger, R.J., Koentges, G., Dulac, C., Kolodkin, A.L. & Ginty, D.D. (2002) Neuropilin-2 mediates axonal fasciculation, zonal segregation, but not axonal convergence, of primary accessory olfactory neurons. Neuron, 33, 877-892.
11. Eberhart, J., Swartz, M.E., Koblar, S.A., Pasquale, E.B. & Krull, C.E. (2002) EphA4 constitutes a population-specific guidance cue for motor neurons. Dev. Biol., 247, 89-101.
12. Eberhart, J., Barr, J., O'Connell, S., Flagg, A., Swartz, M.E., Cramer, K.S., Tosney, K.W., Pasquale, E.B. & Krull, C.E. (2004) Ephrin-A5 exerts positive or inhibitory effects on distinct subsets of EphA4-positive motor neurons. J. Neurosci., 24, 1070-1078.
13. Eckhardt, F. & Meyerhans, A. (1998) Cloning and expression pattern of a murine semaphorin homologous to H-sema IV. Neuroreport, 9, 3975-3979.
14. Giger, R.J., Clouter, J.F., Sahay, A., Prinjha, R.K., Levengood, D.V., Moore, S.E., Pickering, S., Simmons, D., Rastan, S., Walsh, F.S., Kolodkin, A.L., Ginty, D.D. & Geppert, M. (2000) Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron, 25, 29-41.
15. Gu, C., Rodriguez, E.R., Reimert, D.V., Shu, T., Fritzsch, B., Richards, L.J., Kolodkin, A.L. & Ginty, D.D. (2003) Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev. Cell. 5, 45-57.
16. Helmbacher, F., Schneider-Maunoury, S., Topilko, P., Tiret, L. & Charnay, P. (2000) Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons. Development, 127, 3313-3324.
17. Hu, H., Marton, T.F. & Goodman, C.S. (2001) Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron. 32, 39-51.
18. Jessell, T.M. (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet., 1, 20-29.
19. Kania, A. & Jessell, T.M. (2003) Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron, 38, 581-596.
20. Kapfhammer, J.P. & Raper, J.A. (1987) Collapse of growth cone structure on contact with specific neuntes in culture. J. Neurosci., 7, 201-212.
21. Kawakami, A., Kitsukawa, T., Takagi, S. & Fujisawa, H. (1996) Developmentally regulated expression of a cell surface protein, neuropilin, in the mouse nervous system. J. Neurobiol., 29, 1-17.
22. Kitsukawa, T., Shimono, A., Kawakami, A., Kondoh, H. & Fujisawa, H. (1995) Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs. Development, 121, 4309-4318.
23. Kitsukawa, T., Shimizu, M., Sanbo, M., Hirata, T., Taniguchi, M., Bekku, Y., Yagi, T. & Fujisawa, H. (1997) Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron, 19, 995-1005.
24. Lance-Jones, C. & Landmesser, L. (1980) Motoneurone projection patterns in the chick hind limb following early partial reversals of the spinal cord. J. Physiol. (Lond.), 302, 581-602.
25. Lance-Jones, C. & Landmesser, L. (1981) Pathway selection by chick lumbosacral motoneurons during normal development. Proc. R. Soc. Lond. B Biol. Sci., 214, 1-18.
26. Landmesser, L. (1978) The development of motor projection patterns in the chick hind limb. J. Physiol. (Lond.), 284, 391-414.
27. Livet, J., Sigrist, M., Stroebel, S., De Paola, V., Price, S.R., Henderson, C.E., Jessell, T.M. & Arber, S. (2002) ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools. Neuron, 35, 877-892.
28. Marin, O., Yaron, A., Bagri, A., Tessier-Lavigne, M. & Rubenstein, J.L. (2001) Sorting of striatal and cortical interneurons regulated by semaphorin-neuropilin interactions. Science, 293, 872-875.
29. Matthes, D.J., Sink, H., Kolodkin, A.L. & Goodman, C.S. (1995) Semaphorin II can function as a selective inhibitor of specific synaptic arborizations. Cell, 81, 631-639.
30. Messersmith, E.K., Leonardo, E.D., Shatz, C.J., Tessier-Lavigne, M., Goodman, C.S. & Kolodkin, A.L. (1995) Semaphorin III can function as a selective chemorepellent to pattern sensory projections in the spinal cord. Neuron, 14, 949-959.
31. Pasterkamp, R.J. & Kolodkin, A.L. (2003) Semaphorin junction: making tracks toward neural connectivity. Curr. Opin. Neurobiol., 13, 79-89.
32. Pasterkamp, R.J., Peschon, J.J., Spriggs, M.K. & Kolodkin, A.L. (2003) Semaphorin 7A promotes axon outgrowth through integrins and MAPKs. Nature, 424, 398-405.
33. Price, S.R., De Marco Garcia, N.V., Ranscht, B. & Jessell, T.M. (2002) Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell, 109, 205-216.
34. Puschel, A.W., Adams, R.H. & Betz, H. (1996) The sensory innervation of the mouse spinal cord may be patterned by differential expression of and differential responsiveness to semaphorins. Mol. Cell Neurosci., 7, 419-431.
35. Raper, J.A. (2000) Semaphorins and their receptors in vertebrates and invertebrates. Curr. Opin. Neurobiol., 10, 88-94.
36. Semaphorin Nomenclature Committee (1999) Unified nomenclature for the semaphorins/collapsins. Cell, 97, 551-552.
37. Shimamura, K., Hirano, S., McMahon, A.P. & Takeichi, M. (1994) Wnt-1-dependent regulation of local E-cadherin and alpha N-catenin expression in the embryonic mouse brain. Development, 120, 2225-2234.
38. Shirasaki, R. & Pfaff, S.L. (2002) Transcriptional codes and the control of neuronal identity. Annu. Rev. Neurosci., 25, 251-281.
39. Tamagnone, L. & Comoglio, P.M. (2004) To move or not to move? EMBO Rep., 5, 356-361.
40. 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. & Comoglio, P.M. (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell, 99, 71-80.
41. Tamamaki, N., Fujimori, K., Nojyo, Y., Kaneko, T. & Takauji, R. (2003) Evidence that Sema3A and Sema3F regulate the migration of GABAergic neurons in the developing neocortex. J. Comp. Neurol., 455, 238-248.
42. Taniguchi, M., Yuasa, S., Fujisawa, H., Naruse, I., Saga, S., Mishina, M. & Yagi, T. (1997) Disruption of Semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron, 19, 519-530.
43. Tarantino, L.M., Feiner, L., Alavizadeh, A., Wiltshire, T., Hurle, B., Ornitz, D.M., Webber, A.L., Raper, J., Lengeling, A., Rowe, L.B. & Bucan, M. (2000) A high-resolution radiation hybrid map of the proximal portion of mouse chromosome 5. Genomics, 66, 55-64.
44. Varela-Echavarria, A., Tucker, A., Puschel, A.W. & Guthrie, S. (1997) Motor axon subpopulations respond differentially to the chemorepellents netrin-1 and semaphorin D. Neuron, 18, 193-207.
45. Watanabe, Y., Toyoda, R. & Nakamura, H. (2004) Navigation of trochlear motor axons along the midbrain-hindbrain boundary by neuropilin 2. Development, 131, 681-692.
46. Winberg, M.L., Noordermeer, J.N., Tamagnone, L., Comoglio, P.M., Spriggs, M.K., Tessier-Lavigne & Goodman, C.S. (1998) Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell, 23, 903-916.
47. Yu, H.H., Araj, H.H., Ralls, S.A. & Kolodkin, A.L. (1998) The transmembrane semaphorin Sema I is required in Drosophila for embryonic motor and CNS axon guidance. Neuron, 20, 207-220.
48. Yu, H.H., Huang, A.S. & Kolodkin, A.L. (2000) Semaphorin-1a acts in concert with the cell adhesion molecules fasciclin II and connectin to regulate axon fasciculation in Drosophila. Genetics, 156, 723-731.