Netrin 1 acts as an attractive or as a repulsive cue for distinct migrating neurons during the development of the cerebellar system

Development

Volumn 127, Issue 7, 2000, Pages 1359-1372

  Alcantara S ^a,b   Ruiz, M ^a   De Castro, F ^b   Soriano, E ^a   Sotelo, C ^b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

Cerebellum; Chemoattraction; Chemorepulsion; Migration; Netrin 1 receptors; Neuronal migration; Pontine nucleus

Indexed keywords

CHEMOTACTIC FACTOR; NETRIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CEREBELLUM; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EXPLANT; GRANULE CELL; MITOSIS; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; STEM CELL;

ANIMALS; AXONS; BODY PATTERNING; CELL MOVEMENT; CEREBELLUM; CULTURE TECHNIQUES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; IN SITU HYBRIDIZATION; MICE; NERVE GROWTH FACTORS; NEURITES; NEURONS; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA;

EID: 0343883509     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (78)

1. Ackerman, S., 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. Alcántara, S., Ruiz, M., D'Arcangelo, G., Ezan, F., de Lecea, L., Curran, T., Sotelo, C. and Soriano, E. (1998). Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J. Neurosci. 18, 7779-7799.
3. Altman, J. and Bayer, S. A. (1997). Development of Cerebellar System in Relation to its Evolution, Structure and Functions. Boca Raton, FL: CRC Press.
4. Anderson, S. A., Eisenstat, D. D., Shi, L. and Rubenstein, J. L. R. (1997). Interneuron migration from basal forebrain to neocortex: dependence on DLX genes. Science 278, 474-476.
5. Bloch-Gallego, E., Ezan, F., Tessier-Lavigne, M. and Sotelo, C. (1999). Floor plate and netrin-1 are involved in the migration and survival of inferior olivary neurons. J. Neurosci. 19, 4407-4420.
6. Bourrat, F. and Sotelo, C. (1988). Migratory pathways and neuritic differentiation of interior olivary neurons in the rat embryo: Axonal tracing study using the in vitro slab technique. Dev. Brain Res. 39, 19-37.
7. Bourrat, F. and Sotelo, C. (1990). Early development of the precerebellar system: Migratory routes, Selective aggregation and neuritic differentiation of the inferior olive and lateral reticular nucleus neurons. An overview. Arch. Ital. Biol. 128, 151-170.
8. Bourrat, F. and Sotelo, C. (1991). Relationships between neuronal birthdates and cytoarchitecture in the rat inferior olivary complex. J. Comp. Neurol. 313, 509-521.
9. Buttiglione, M., Revest, J. M., Rougon, G. and Faivre-Sarrailh, C. (1996). F3 neuronal adhesion molecule controls outgrowth and fasciculation of cerebellar granule cell neuntes: a cell type specific mediated by the Ig-like domains. Mol. Cell Neurosci. 8, 53-69.
10. Buttiglione, M., Revest, J. M., Pavlov, O., Karagogeos, D., Furley, A., Rougon, G. and Faivre-Sarrailh, C. (1998). A functional interaction between the neuronal adhesion molecules TAG-1 and F3 modulates neurite outgrowth and fasciculation of cerebellar granule cells. J. Neurosci. 17, 6853-6870.
11. Cho, K. R. and Fearon, E. R. (1995). DCC: linking tumor suppressor genes and altered cell surface interactions in cancer? Curr. Opin. Genet. Dev. 5, 72-78.
12. Colavita, A., Krishna, S., Zheng, H., Padget, R. W. and Culotti, J. G. (1998). Pioneer axon guidance by UNC-129, a C. elegans TGF-β. Science 281, 706-709.
13. Colamarino, S. A. and Tessier-Lavigne, M. (1995). The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81, 621-629.
14. Culotti, J. G. and Kolodkin, A. L. (1996). Functions of netrins and semaphorins in axon guidance. Curr. Opin. Neurobiol. 6, 81-88.
15. D'Arcangelo, G., Miao, G. G., Chen, S.-C., Soares, H. D., Morgan, J. I. and Curran, T. (1995). A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374, 719-723.
16. Del Río, J. A., Heimrich, B., Borrell, V., Förster, E., Drakew, A., Alcántara, S., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K., Derer, P., Frotscher, M. and Soriano, E. (1997). An essential role for Cajal-Retzius cells and reelin in the layer-specific targeting of hippocampal afferents. Nature 385, 70-74.
17. Eickholt, B. J., Mackenzie, S. L., Graham A., Walsh, F. S. and Doherty, P. (1999). Evidence for collapsin-1 functioning in the control of neural crest migration in both trunk and hindbrain regions. Development 126, 2181-2189.
18. Ellerberger, C., Hanaway, J. and Netsky, M. G. (1969). Embryogenesis of the interior olivary nucleus in the rat: A radioautographic study and reevaluation of the rhombic lip. J. Comp. Neurol. 137, 71-88.
19. Engelkamp, D., Rashbas, P., Seawright, A. and van Heyningen, V. (1999). Role of Pax6 in development of the cerebellar system. Development 126, 3585-3596.
20. Fabre M., Martin, M., Ulloa, F. and Real, F. X. (1999). In vitro analysis of the role of DCC in mucus-secreting intestinal differentiation. Int. J. Cancer 81, 799-807.
21. Fazeli, A., Dickinson, S. L., Hermiston, M. L., Tighe, R. V., Steen, R. G., Small, R. G., Stoeckli, K. T., Keino-Masu, K., Masu M., Rayburn, H., Simons, J., Bronson, R. T., Gordon, J. I., Tessier-Lavigne, M. and Weinberg, R. A. (1997). Phenotype of mice lacking functional deleted in colorectal cancer (DCC) gene. Nature 386, 796-804.
22. Felsenfeld, D. P., Hynes M. A., Skoler, K. M., Furley, A. J. and Jessell, T. M. (1994). TAG-1 can mediate homophilic binding but neurite outgrowth on TAG-1 requires a L1-like molecule and β1 integrins. Neuron 12, 257-267.
23. Gao, W.-Q. and Hatten, M. E. (1994). Immortalizing oncogenes subvert the establishment of granule cell identity in developing cerebellum. Development 120, 1059-1070.
24. Goodman, C. S. (1996). Mechanisms and molecules that control growth cone guidance. Annu. Rev. Neurosci 19, 341-377.
25. Guthrie, S. and Pini, A. (1995). Chemorepulsion of developing motor axons by the floor plate. Neuron 14, 1117-1130.
26. Hamelin, M., Zhou, Y., Su, M. W. and Culotti, J. G. (1993). Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature 364, 327-330.
27. Harkmark, W. (1954). Cell migrations from the rhombic lip to the inferior olive, the nucleus raphe and the pons. A morphological and experimental investigation on chick embryos. J. Comp. Neurol. 100, 115-205.
28. Hatten, M. E. and Liem, R. K. H. (1981). Astroglia provide a template for the positioning of developing cerebellar neurons in vitro. J. Cell Biol. 90, 622-630.
29. His, W. (1891). Die Entwicklung des menschlichen Rautenhirns vom Ende des ersten bis zum Beginn des dritten Monats. I. Verlängertes Mark. Abhandlung der königlicher sächsischen Gesellschaft der Wissenschaften, Mathematischephysikalische Klasse 29, 1-74.
30. Hong, K., Hinck, L., Nishiyama, M., Poo, M., Tessier-Lavigne, M. and Stein, F. (1999). A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts Netrin-induced growth cone attraction to repulsion. Cell 97, 927-942.
31. Hu, H. (1999). Chemorepulsion of neuronal migration by Slit2 in the developing mammalian forebrain. Neuron 23, 703-711.
32. Hu, H. and Rutishauser, U. (1996), A septum-derived chemorepulsive factor for migrating olfactory interneuron precursors. Neuron 16, 933-940.
33. Hu, H., Tomasiewics, H., Magnuson, T. and Rutishauser, U. (1996). The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron 16, 735-743.
34. Hynes, R. O., Patel, R. and Miller, R. H. (1986). Migration of neuroblasts along preexisting axonal tracts during prenatal cerebellar development. J. Neurosci. 6, 867-876.
35. Jacobowitz, D. M. and Abbott, L. C. (1998). Chemoarchitectonic tectonic Atlas of the Developing Mouse Brain. Boca Raton. FL: CRC Press.
36. Jankovski, A. and Sotelo, C. (1996). Subventricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J. Comp. Neurol. 371, 376-396.
37. Karagogeos, D., Morton, S. B., Casano, F., Dodd, J. and Jessell, T. M. (1991). Developmental expression of the axonal glycoprotein TAG-1: Differential regulation by central and peripheral neurons in vitro. Development 112, 51-67.
38. Keino-Masu K., Masu, M., Hinck, L., Leonardo, E. D., Chan, S. S. Y., Culotti, J. G. and Tessier-Lavigne, M. (1996). Deleted in colorectal cancer (DCC) encodes a Netrin receptor. Cell 87, 175-185.
39. Kennedy, T. K., Serafini, T., de la Torre, J. and Tessier-Lavigne, M. (1994). Netrins are diffussible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78, 425-435.
40. Lemmon, V., Farr, K. L. and Lagenaur, C. (1989). L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron 2, 1597-1603.
41. 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, 833-837.
42. Leung-Hagesteijn, C., Spence, A. M., Stern, B. D., Zhou, Y., Su, M.-W., Edgecock, E. M. and Culotti, J. G. (1992). UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type I domains, guides cell and pioneer axon migrations in C. elegans. Cell 71, 289-299
43. Lois, C., García-Verdugo, J. M. and Alvarez-Buylla, A. (1996). Chain migration of neuronal precursors. Science 271, 978-981.
44. Lumsden, A. G. S. and Davies, A. M. (1986). Chemotropic effect of specific target epithelium in the development of the mammalian central nervous system. Nature 323, 538-539.
45. Mathis, L., Bonnerot, C., Puelles, L. and Nicolas, J.-F. (1997). Retrospective clonal analysis of the cerebellum using genetic lac Z/lacZ mouse mosaics. Development 124, 4089-4104.
46. Mehlen, P., Rubizadeh, S., Snipas, S. J., Ass-Munt, N., Salvesen, G. S. and Bredesen, D. E. (1998). The DCC gene product induces apoptosis by a mechanism requiring receptor proteolysis. Nature 395, 801-804.
47. Métin, C., Diléglise, D., Serafini, T., Kennedy, T. E. and Tessier-Lavigne, M. (1997). A role for netrin-1 in the guidance of cortical efferents. Development 124, 5063-5074.
48. Miale, I. and Sidmun, R. L. (1961). An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp. Neurol. 4, 277-296.
49. Moody, S. A., Quigg, M. S. and Frankfurter, A. (1989). Development of the peripheral trigeminal system in the chick revealed by an isotype-specific anti-beta-tubulin monoclonal antibody. J. Comp. Neurol. 279, 567-580.
50. Ono, K. and Kawamura, K. (1989). Migration of immature neurons along tangentially oriented fibers in the subpial part of the letal mouse medulla oblongata. Exp. Brain Res. 78, 290-300.
51. Ono, K. and Kawamura, K. (1990). Mode of neuronal migration of the pontine stream in fetal mice. Anat. Embryol. 182, 11-19.
52. Pearlman, A. L., Faust, P. L., Hatten, M. K. and Brunstrom, J. E. (1998). New directions for neuronal migration. Curr. Opin. Neurobiol. 8, 45-54.
53. Persohn, E., and Schachner, M. (1987). Immunoelectron microscopic localization of the neural adhesion molecules L1 and N-CAM during postnatal development of the rat cerebellum. J. Cell. Biol. 105, 569-576.
54. Placzek, M., Tessier-Lavigne, M., Jessell, T. M. and Dodd, J. (1990). Orientation of commisural axons in vitro in response to a floor plate-derived chemoattractant. Development 110, 19-30.
55. Przynorski, S. A., Knowles, B. B. and Ackerman, S. L. (1998). Embryonic phenotype of Unc5h3 mutant mice suggest chemorepulsion during the formation of the rostral cerebellar boundary. Development 125, 41-50.
56. Rakic, P. (1971). Neuron-glia relationship during cell migration in developing cerebellar cortex: A Golgi and electron microscopic study in Macacus rhesus. J. Comp. Neurol. 141, 283-312
57. Rakic, P. (1981). Neuron-glial interaction during brain development. Trends Neurosci. 4, 184-187.
58. Rakic, P. (1985). Contact regulation of neuronal migration. In The Cell in Contact. (eds. G. E. Edelman and J. P.Thiery). pp 67-90. New York: J. Wiley.
59. Rakic, P. (1990). Principles of neural migration. Experientia 46, 882-891.
60. Ramón y Cajal, S. (1911). Histologie du Système Nerveux de l'Homme et des Vértébres. Maloine, Paris.
61. Richards, L. J., Koester, S. E., Tuttle, R. and O'Leary, D. D. M. (1997). Directed growth of early cortical axons is influenced by a chemoattractant released from an intermediate target. J. Neurosci. 17, 2445-2458.
62. 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, 1011-1029.
63. 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.
64. Serafini, T., Colamarino, S. A., Leonardo, E. D., Wang, E., 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.
65. Shirasaki, R., Tamada, A., Katsumata, R. and Murakami, F. (1995). Guidanee of cerebellofugal axons in the rat embryo: Directed growth toward the floor plate and subsequent elongation along the longitudinal axis. Neuron 14, 961-972.
66. Shirasaki, R., Mirzayan, C., Tessier-Lavigne, M. and Murakami, F. (1996). Guidance of circumferentially growing axons by Netrin-dependent and -independent floor plate chemotropism in the vertebrate brain. Neuron 17, 1079-1088.
67. Soriano, E., Alvarado-Mallart, R. M., Dumesnil, N., Del Río, J. A. and Sotelo, C. (1997). Cajal-Retzius cells regulate the radial glia phenotype in the adult and developing cerebellum and alter granule cell migration. Neuron 18, 563-577.
68. Stoeckli, E. T. and Landmesser, L. T (1995). Axonin-1, Nr.CAM and Ng-CAM play different roles in the in vivo guidance of chick commissural neurons. Neuron 14, 1165-1179.
69. Taber-Pierce, E. (1966). Histogenesis of the nuclei griseum pontis, corporis pontobulbaris and reticularis tegmenti pontis (Bechterew) in the mouse. J. Comp. Neurol. 129, 219-240.
70. Tamada, A., Shirasaki, R. and Murakami, F. (1995). Floor plate chemoattracts crossed axons and chemorepels uncrossed axons in the vertebrate brain. Neuron 14, 1083-1093.
71. Tessier-Lavigne, M. and Goodman, C. S. (1996). The moloecular biology of axon guidance. Science 274, 1123-1132.
72. Varela-Echevarría, A., Tucker, A., Püschel, A. W. and Guthrie, S. (1997). Motor axon subpopulations respond differentially to the chemorepellents netrin-1 and semaphorin D. Neuron 18, 193-207.
73. Walsh, F. S. and Doherty, P. (1997). Neural cell adhesion molecules of the immunoglubulin superfamily: Role in axon growth and guidance. Ann. Rev. Cell Dev. Biol. 13, 425-456.
74. Wassef, M., Zanetta, J. P., Brehier, A. and Sotelo, C. (1985). Transient biochemical compartmentalization of Purkinje cells during early cerebellar development. Dev. Biol. 111, 129-137.
75. Wichterle, H., García-Verdugo, J. and Alvarez-Buylla, A. (1997). Direct evidence for homotypic, glia-independent neuronal migration. Neuron 18, 779-791.
76. Wolfer, D. P., Henehan-Beatty, A., Stoeckli, E. T., Sondererger, P. and Lipp, H. P. (1994). Distribution of TAG-1/Axonin-1 in fibre tracts and migratory streams of the developing mouse nervous system. J. Comp. Neurol. 345, 1-32.
77. Wu, W., Wong, K., Chen, J-h., Jiang Z-h, Dupuis, S., Wu, J. and Rao, Y. (1999). Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 400, 331-336.
78. Yamamoto, M., Hassinger, L. and Crandall, J. K. (1990). Ultrastructural localisation of stage-specific neurite associated proteins in the developing rat cerebral and cerebellar cortices. J. Neurocytol. 19, 619-627.