Dorsally derived netrin 1 provides an inhibitory cue and elaborates the 'waiting period' for primary sensory axons in the developing spinal cord

Development

Volumn 133, Issue 7, 2006, Pages 1379-1387

  Watanabe, Keisuke ^a,b   Tamamaki, Nobuaki ^c,d   Furuta, Takahiro ^d   Ackerman, Susan L ^e   Ikenaka, Kazuhiro ^a,b   Ono, Katsuhiko ^a,b  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

^d KYOTO UNIVERSITY   (Japan)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Dcc; Dorsal funiculus; DRG; Mouse; Network formation; RCM; Unc5c

Indexed keywords

NERVE PROTEIN; NETRIN 1; PROTEIN UNC5A; PROTEIN UNC5B; PROTEIN UNC5C; UNCLASSIFIED DRUG;

ALPHA NERVE FIBER; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CELL MIGRATION; CONTROLLED STUDY; DORSAL ROOT; EMBRYO; EMBRYO PATTERN FORMATION; GENE EXPRESSION REGULATION; GROWTH INHIBITION; MOUSE; NERVE CELL NETWORK; NERVE FIBER; NERVE SPROUTING; NERVOUS SYSTEM DEVELOPMENT; NEUROBIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SENSORY NERVE; SKIN NERVE; SPINAL CORD; SPINAL GANGLION;

ANIMALS; AXONS; CELL LINE; CRICETINAE; EPIDERMAL GROWTH FACTOR; FEMALE; GALACTOSIDES; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INDOLES; MICE; MICE, INBRED ICR; MODELS, BIOLOGICAL; MUTATION; NERVE GROWTH FACTORS; NEURONS, AFFERENT; ORGAN CULTURE TECHNIQUES; PREGNANCY; SPINAL CORD; TUMOR SUPPRESSOR PROTEINS;

EID: 33646158916     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02312     Document Type: Article

References (49)

1. Ackerman, S. L., Kozak, L. P., Przyborski, S. A., Rund, L. A., Boyer, B. B. and Knowles, B. B. (1997). The mouse rostral cerebellar malformation gene encodes an UNC-5-like protein. Nature 386, 838-842.
2. Akazawa, C., Ishibashi, M., Shimizu, C., Nakanishi, S. and Kageyama, R. (1995). A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J. Biol. Chem. 270, 8730-8738.
3. Arber, S., Ladle, D. R., Lin, J. H., Frank, E. and Jessell, T. M. (2000). ETS gene Er81 controls the formation of functional connections between group la sensory afferents and motor neurons. Cell 101, 485-498.
4. Caspary, T. and Anderson, K. V. (2003). Patterning cell types in the dorsal spinal cord: what the mouse mutants say. Nat. Rev. Neurosci. 4, 289-297.
5. Charron, F., Stein, E., Jeong, J., McMahon, A. P. and Tessier-Lavigne, M. (2003). The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 113, 11-23.
6. Chen, H., Lun, Y., Ovchinnikov, D., Kokubo, H., Oberg, K. C., Pepicelli, C. V., Gan, L., Lee, B. and Johnson, R. L. (1998). Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nat. Genet. 19, 51-55.
7. Chen, Z. F., Rebelo, S., White, F, Malmberg, A. B., Baba, H., Lima, D., Woolf, C. J., Basbaum, A. I. and Anderson, D. J. (2001). The paired homeodomain protein DRG11 is required for the projection of cutaneous sensory afferent fibers to the dorsal spinal cord. Neuron 31, 59-73.
8. Colamarino, S. A. and Tessier-Lavigne, M. (1995a). The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81, 621-629.
9. Colamarino, S. A. and Tessier-Lavigne, M. (1995b). The role of the floor plate in axon guidance. Annu. Rev. Neurosci. 18, 497-529.
10. Ding, L., Takebayashi, H., Watanabe, K., Ohtsuki, T., Tanaka, K. F., Nabeshima, Y., Chisaka, O., Ikenaka, K. and Ono, K. (2005a). Short-term lineage analysis of dorsally derived Olig3 cells in the developing spinal cord. Dev. Dyn. 234, 622-632.
11. Ding, Y. Q., Kim, J. Y., Xu, Y. S., Rao, Y. and Chen, Z. F. (2005b). Ventral migration of early-born neurons requires Dcc and is essential for the projections of primary afferents in the spinal cord. Development 132, 2047-2056.
12. Fazeli, A., Dickinson, S. L., Hermiston, M. L., Tighe, R. V, Steen, R. G., Small, C. G., Stoeckli, E. T., Keino-Masu, K., Masu, M., Rayburn, H. et al. (1997). Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386, 796-804.
13. Finger, J. H., Bronson, R. T., Harris, B., Johnson, K., Przyborski, S. A. and Ackerman, S. L. (2002). The netrin 1 receptors Unc5h3 and Dcc are necessary at multiple choice points for the guidance of corticospinal tract axons. J. Neurosci. 22, 10346-10356.
14. Furuta, T., Tomioka, R., Taki, K., Nakamura, K., Tamamaki, N. and Kaneko, T. (2001). In vivo transduction of central neurons using recombinant Sindbis virus: Golgi-like labeling of dendrites and axons with membrane-targeted fluorescent proteins. J. Histochem. Cytochem. 49, 1497-1508.
15. Ghosh, A. and Shatz, C. J. (1992). Pathfinding and target selection by developing geniculocortical axons. J. Neurosci. 12, 39-55.
16. Goulding, M. D., Chalepakis, G., Deutsch, U., Erselius, J. R. and Gruss, P. (1991). Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J. 10, 1135-1147.
17. Helms, A. W. and Johnson, J. E. (2003). Specification of dorsal spinal cord interneurons. Curr. Opin. Neurobiol. 13, 42-49.
18. Hong, K., Hinck, L., Nishiyama, M., Poo, M. M., Tessier-Lavigne, M. and Stein, E. (1999). A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 97, 927-941.
19. Huang, E. J. and Reichardt, L. F. (2001). Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736.
20. Inoue, K., Ozaki, S., Shiga, T., Ito, K., Masuda, T., Okado, N., Iseda, T., Kawaguchi, S., Ogawa, M., Bae, S. C. et al. (2002). Runx3 controls the axonal projection of proprioceptive dorsal root ganglion neurons. Nat. Neurosci. 5,946-954.
21. Keino-Masu, K., Masu, M., Hinck, L., Leonardo, E. D., Chan, S. S., Culotti, J. G. and Tessier-Lavigne, M. (1996). Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 87, 175-185.
22. Keleman, K. and Dickson, B. J. (2001). Short- and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron 32, 605-617.
23. Kennedy, T. E., Serafini, T., de la Torre, J. R. and Tessier-Lavigne, M. (1994). Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78, 425-435.
24. 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.
25. Leonardo, E. D., Hinck, L., Masu, M., Keino-Masu, K., Ackerman, S. L. and Tessier-Lavigne, M. (1997). Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 386, 833-838.
26. Liu, Y., Shi, J., Lu, C. C., Wang, Z. B., Lyuksyutova, A. I., Song, X. and Zou, Y. (2005). Ryk-mediated Wnt repulsion regulates posterior-directed growth of corticospinal tract. Nat Neurosci. 8, 1151-1159.
27. 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.
28. Matise, M. P., Lustig, M., Sakurai, T., Grumet, M. and Joyner, A. L. (1999). Ventral midline cells are required for the local control of commissural axon guidance in the mouse spinal cord. Development 126, 3649-3659.
29. 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.
30. Mo, R., Freer, A. M., Zinyk, D. L., Crackower, M. A., Michaud, J., Heng, H. H., Chik, K. W., Shi, X. M., Tsui, L. C., Cheng, S. H. et al. (1997). Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 124, 113-123.
31. Ninkina, N. N., Stevens, G. E., Wood, J. N. and Richardson, W. D. (1993). A novel Brn3-like POU transcription factor expressed in subsets of rat sensory and spinal cord neurons. Nucleic Acids Res. 21, 3175-3182.
32. Ono, K., Yasui, Y. and Ikenaka, K. (2004). Lower rhombic lip-derived cells undergo transmedian tangential migration followed by radial migration in the chick embryo brainstem. Eur. J. Neurosci. 20, 914-922.
33. Ozaki, S. and Snider, W. D. (11997). Initial trajectories of sensory axons toward laminar targets in the developing mouse spinal cord. J. Comp. Neurol. 380, 215-229.
34. 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.
35. Renzi, M. J., Wexler, T. L. and Raper, J. A. (2000). Olfactory sensory axons expressing a dominant-negative semaphorin receptor enter the CNS early and overshoot their target. Neuron 28, 437-447.
36. Schreyer, D. J. and Jones, E. G. (1982). Growth and target finding by axons of the corticospinal tract in prenatal and postnatal rats. Neuroscience 7, 1837-1853.
37. Serafini, T., Kennedy, T. E., Galko, M. J., Mirzayan, C., Jessell, T. M. and Tessier-Lavigne, M. (1994). The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424.
38. Serafini, T., Colamarino, S. A., Leonardo, E. D., Wang, H., Beddington, R., Skarnes, W. C. and Tessier-Lavigne, M. (1996). Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87, 1001-1014.
39. 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.
40. Snider, W. D. (1994). Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77, 627-638.
41. 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.
42. Sugimoto, Y., Taniguchi, M., Yagi, T., Akagi, Y., Nojyo, Y. and Tamamaki, N. (2001). Guidance of glial precursor cell migration by secreted cues in the developing optic nerve. Development 128, 3321-3330.
43. 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.
44. Tessier-Lavigne, M. and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
45. Tessier-Lavigne, M., Placzek, M., Lumsden, A. G., Dodd, J. and Jessell, T. M. (1988). Chemotropic guidance of developing axons in the mammalian central nervous system. Nature 336, 775-778.
46. Wang, G. and Scott, S. A. (2000). The "waiting period" of sensory and motor axons in early chick hindlimb: its role in axon pathfinding and neuronal maturation. J. Neurosci. 20, 5358-5366.
47. Wang, K. H., Brose, K., Arnott, D., Kidd, T., Goodman, C. S., Henzel, W. and Tessier-Lavigne, M. (1999). Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 96, 771-784.
48. Wang, S. S., Tsai, R. Y. and Reed, R. R. (1997). The characterization of the Olf-1/EBF-like HLH transcription factor family: implications in olfactory gene regulation and neuronal development. J. Neurosci. 17, 4149-4158.
49. Yee, K. T., Simon, H. H., Tessier-Lavigne, M. and O'Leary, D. M. (1999). Extension of long leading processes and neuronal migration in the mammalian brain directed by the chemoattractant netrin-1. Neuron 24, 607-622.