Development, Vol 127, Issue 7 1359-1372, Copyright © 2000 by Company of Biologists

JOURNAL ARTICLES

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

S Alcantara, M Ruiz, F De Castro, E Soriano and C Sotelo
Department of Animal and Plant Cell Biology, Faculty of Biology, University of Barcelona, Barcelona E 08028, Spain. sole@porthos.bio. ub.es.

Netrin 1 is a long-range diffusible factor that exerts chemoattractive or chemorepulsive effects on developing axons growing to or away from the neural midline. Here we used tissue explants to study the action of netrin 1 in the migration of several cerebellar and precerebellar cell progenitors. We show that netrin 1 exerts a strong chemoattractive effect on migrating neurons from the embryonic lower rhombic lip at E12-E14, which give rise to precerebellar nuclei. Netrin 1 promotes the exit of postmitotic migrating neurons from the embryonic lower rhombic lip and upregulates the expression of TAG-1 in these neurons. In addition, in the presence of netrin 1, the migrating neurons are not isolated but are associated with thick fascicles of neurites, typical of the neurophilic way of migration. In contrast, the embryonic upper rhombic lip, which contains tangentially migrating granule cell progenitors, did not respond to netrin 1. Finally, in the postnatal cerebellum, netrin 1 repels both the parallel fibres and migrating granule cells growing out from explants taken from the external germinal layer. The developmental patterns of expression in vivo of netrin 1 and its receptors are consistent with the notion that netrin 1 secreted in the midline acts as chemoattractive cue for precerebellar neurons migrating circumferentially along the extramural stream. Similarly, the pattern of expression in the postnatal cerebellum suggests that netrin 1 could regulate the tangential migration of postmitotic premigratory granule cells. Thus, molecular mechanisms considered as primarily involved in axonal guidance appear also to steer neuronal cell migration.

This article has been cited by other articles:

				C. H. Faux and J. G. Parnavelas The Role of Intracellular Calcium and RhoA in Neuronal Migration Sci. Signal., November 13, 2007; 2007(412): pe62 - pe62. [Abstract] [Full Text] [PDF]

				P. G. Barth, C. B. Majoie, M. W.A. Caan, M. A.J. Weterman, M. Kyllerman, L. M.E. Smit, R. A. Kaplan, R. H. Haas, F. Baas, J.-M. Cobben, et al. Pontine tegmental cap dysplasia: a novel brain malformation with a defect in axonal guidance Brain, September 1, 2007; 130(9): 2258 - 2266. [Abstract] [Full Text] [PDF]

				M. Pascual, I. Abasolo, A. Mingorance-Le Meur, A. Martinez, J. A. Del Rio, C. V. E. Wright, F. X. Real, and E. Soriano Cerebellar GABAergic progenitors adopt an external granule cell-like phenotype in the absence of Ptf1a transcription factor expression PNAS, March 20, 2007; 104(12): 5193 - 5198. [Abstract] [Full Text] [PDF]

				E. Charrier, B. Mosinger, C. Meissirel, M. Aguera, V. Rogemond, S. Reibel, P. Salin, N. Chounlamountri, V. Perrot, M.-F. Belin, et al. Transient alterations in granule cell proliferation, apoptosis and migration in postnatal developing cerebellum of CRMP1-/- mice Genes Cells, December 1, 2006; 11(12): 1337 - 1352. [Abstract] [Full Text] [PDF]

				H. Taniguchi, D. Kawauchi, K. Nishida, and F. Murakami Classic cadherins regulate tangential migration of precerebellar neurons in the caudal hindbrain Development, May 15, 2006; 133(10): 1923 - 1931. [Abstract] [Full Text] [PDF]

				J. L. Bartoe, W. L. McKenna, T. K. Quan, B. K. Stafford, J. A. Moore, J. Xia, K. Takamiya, R. L. Huganir, and L. Hinck Protein interacting with C-kinase 1/protein kinase Calpha-mediated endocytosis converts netrin-1-mediated repulsion to attraction. J. Neurosci., March 22, 2006; 26(12): 3192 - 3205. [Abstract] [Full Text] [PDF]

				T. Kawasaki, K. Ito, and T. Hirata Netrin 1 regulates ventral tangential migration of guidepost neurons in the lateral olfactory tract Development, March 1, 2006; 133(5): 845 - 853. [Abstract] [Full Text] [PDF]

				A. K. Dillon, S. C. Fujita, M. P. Matise, A. A. Jarjour, T. E. Kennedy, H. Kollmus, H.-H. Arnold, J. A. Weiner, J. R. Sanes, and Z. Kaprielian Molecular Control of Spinal Accessory Motor Neuron/Axon Development in the Mouse Spinal Cord J. Neurosci., November 2, 2005; 25(44): 10119 - 10130. [Abstract] [Full Text] [PDF]

				T. Yabe, T. Hata, J. He, and N. Maeda Developmental and regional expression of heparan sulfate sulfotransferase genes in the mouse brain Glycobiology, October 1, 2005; 15(10): 982 - 993. [Abstract] [Full Text] [PDF]

				S. Li, F. Qiu, A. Xu, S. M. Price, and M. Xiang Barhl1 Regulates Migration and Survival of Cerebellar Granule Cells by Controlling Expression of the Neurotrophin-3 Gene J. Neurosci., March 24, 2004; 24(12): 3104 - 3114. [Abstract] [Full Text] [PDF]

				H.-t. Xu, X.-b. Yuan, C.-b. Guan, S. Duan, C.-p. Wu, and L. Feng Calcium signaling in chemorepellant Slit2-dependent regulation of neuronal migration PNAS, March 23, 2004; 101(12): 4296 - 4301. [Abstract] [Full Text] [PDF]

				M. E. Williams, S. C.-Y. Wu, W. L. McKenna, and L. Hinck Surface Expression of the Netrin Receptor UNC5H1 Is Regulated through a Protein Kinase C-Interacting Protein/Protein Kinase-Dependent Mechanism J. Neurosci., December 10, 2003; 23(36): 11279 - 11288. [Abstract] [Full Text] [PDF]

				M. Muller, N. Jabs, D. E. Lork, B. Fritzsch, and M. Sander Nkx6.1 controls migration and axon pathfinding of cranial branchio-motoneurons Development, December 1, 2003; 130(23): 5815 - 5826. [Abstract] [Full Text] [PDF]

				A. Louvi, P. Alexandre, C. Metin, W. Wurst, and M. Wassef The isthmic neuroepithelium is essential for cerebellar midline fusion Development, November 15, 2003; 130(22): 5319 - 5330. [Abstract] [Full Text] [PDF]

				G. Liu and Y. Rao Neuronal Migration from the Forebrain to the Olfactory Bulb Requires a New Attractant Persistent in the Olfactory Bulb J. Neurosci., July 23, 2003; 23(16): 6651 - 6659. [Abstract] [Full Text] [PDF]

				H.-H. Tsai, M. Tessier-Lavigne, and R. H. Miller Netrin 1 mediates spinal cord oligodendrocyte precursor dispersal Development, May 15, 2003; 130(10): 2095 - 2105. [Abstract] [Full Text] [PDF]

				A. A. Jarjour, C. Manitt, S. W. Moore, K. M. Thompson, S.-J. Yuh, and T. E. Kennedy Netrin-1 Is a Chemorepellent for Oligodendrocyte Precursor Cells in the Embryonic Spinal Cord J. Neurosci., May 1, 2003; 23(9): 3735 - 3744. [Abstract] [Full Text] [PDF]

				O. Marin, A. S. Plump, N. Flames, C. Sanchez-Camacho, M. Tessier-Lavigne, and J. L. R. Rubenstein Directional guidance of interneuron migration to the cerebral cortex relies on subcortical Slit1/2-independent repulsion and cortical attraction Development, May 1, 2003; 130(9): 1889 - 1901. [Abstract] [Full Text] [PDF]

				J. D. Gilthorpe, E.-K. Papantoniou, A. Chedotal, A. Lumsden, and R. J. T. Wingate The migration of cerebellar rhombic lip derivatives Development, March 12, 2003; 129(20): 4719 - 4728. [Abstract] [Full Text] [PDF]

				K. Kyriakopoulou, I. de Diego, M. Wassef, and D. Karagogeos A combination of chain and neurophilic migration involving the adhesion molecule TAG-1 in the caudal medulla Development, March 3, 2003; 129(2): 287 - 296. [Abstract] [Full Text] [PDF]

				I. de Diego, K. Kyriakopoulou, D. Karagogeos, and M. Wassef Multiple influences on the migration of precerebellar neurons in the caudal medulla Development, March 3, 2003; 129(2): 297 - 306. [Abstract] [Full Text] [PDF]

				R. J. Wechsler-Reya Analysis of Gene Expression in the Normal and Malignant Cerebellum Recent Prog. Horm. Res., January 1, 2003; 58(1): 227 - 248. [Abstract] [Full Text] [PDF]

				Y. Rao, K. Wong, M. Ward, C. Jurgensen, and J. Y. Wu Neuronal migration and molecular conservation with leukocyte chemotaxis Genes & Dev., December 1, 2002; 16(23): 2973 - 2984. [Full Text] [PDF]

				M. E. Hatten New Directions in Neuronal Migration Science, September 6, 2002; 297(5587): 1660 - 1663. [Abstract] [Full Text] [PDF]

				S. Patel and A. J. Barkovich Analysis and Classification of Cerebellar Malformations AJNR Am. J. Neuroradiol., August 1, 2002; 23(7): 1074 - 1087. [Abstract] [Full Text] [PDF]

				J.M. Soria and M. Valdeolmillos Receptor-activated Calcium Signals in Tangentially Migrating Cortical Cells Cereb Cortex, August 1, 2002; 12(8): 831 - 839. [Abstract] [Full Text] [PDF]

				E. Yacubova and H. Komuro Intrinsic Program for Migration of Cerebellar Granule Cells In Vitro J. Neurosci., July 15, 2002; 22(14): 5966 - 5981. [Abstract] [Full Text] [PDF]

				N. Spassky, F. de Castro, B. Le Bras, K. Heydon, F. Queraud-LeSaux, E. Bloch-Gallego, A. Chedotal, B. Zalc, and J.-L. Thomas Directional Guidance of Oligodendroglial Migration by Class 3 Semaphorins and Netrin-1 J. Neurosci., July 15, 2002; 22(14): 5992 - 6004. [Abstract] [Full Text] [PDF]

				A. B. Huber, O. Weinmann, C. Brosamle, T. Oertle, and M. E. Schwab Patterns of Nogo mRNA and Protein Expression in the Developing and Adult Rat and After CNS Lesions J. Neurosci., May 1, 2002; 22(9): 3553 - 3567. [Abstract] [Full Text] [PDF]

				M. Denaxa, C.-H. Chan, M. Schachner, J. G. Parnavelas, and D. Karagogeos The adhesion molecule TAG-1 mediates the migration of cortical interneurons from the ganglionic eminence along the corticofugal fiber system Development, November 15, 2001; 128(22): 4635 - 4644. [Abstract] [Full Text] [PDF]

				D. Caric, H. Raphael, J. Viti, A. Feathers, D. Wancio, and L. Lillien EGFRs mediate chemotactic migration in the developing telencephalon Development, November 1, 2001; 128(21): 4203 - 4216. [Abstract] [Full Text] [PDF]

				H. A. Mason, S. Ito, and G. Corfas Extracellular Signals That Regulate the Tangential Migration of Olfactory Bulb Neuronal Precursors: Inducers, Inhibitors, and Repellents J. Neurosci., October 1, 2001; 21(19): 7654 - 7663. [Abstract] [Full Text] [PDF]

				T. Hamasaki, S. Goto, S. Nishikawa, and Y. Ushio A Role of Netrin-1 in the Formation of the Subcortical Structure Striatum: Repulsive Action on the Migration of Late-Born Striatal Neurons J. Neurosci., June 15, 2001; 21(12): 4272 - 4280. [Abstract] [Full Text] [PDF]

				H. Komuro, E. Yacubova, E. Yacubova, and P. Rakic Mode and Tempo of Tangential Cell Migration in the Cerebellar External Granular Layer J. Neurosci., January 15, 2001; 21(2): 527 - 540. [Abstract] [Full Text] [PDF]

				J. C. Lin, L. Cai, and C. L. Cepko The External Granule Layer of the Developing Chick Cerebellum Generates Granule Cells and Cells of the Isthmus and Rostral Hindbrain J. Neurosci., January 1, 2001; 21(1): 159 - 168. [Abstract] [Full Text] [PDF]

				M. Koch, J. R. Murrell, D. D. Hunter, P. F. Olson, W. Jin, D. R. Keene, W. J. Brunken, and R. E. Burgeson A Novel Member of the Netrin Family, {beta}-Netrin, Shares Homology with the {beta} Chain of Laminin: Identification, Expression, and Functional Characterization J. Cell Biol., October 9, 2000; 151(2): 221 - 234. [Abstract] [Full Text] [PDF]

				H. Super, J. A. Del Rio, A. Martinez, P. Perez-Sust, and E. Soriano Disruption of Neuronal Migration and Radial Glia in the Developing Cerebral Cortex Following Ablation of Cajal-Retzius Cells Cereb Cortex, June 1, 2000; 10(6): 602 - 613. [Abstract] [Full Text] [PDF]

				S Garel, M Garcia-Dominguez, and P Charnay Control of the migratory pathway of facial branchiomotor neurones Development, January 12, 2000; 127(24): 5297 - 5307. [Abstract] [PDF]

				M. Barallobre, J. Del Rio, S Alcantara, V Borrell, F Aguado, M Ruiz, M. Carmona, M Martin, M Fabre, R Yuste, et al. Aberrant development of hippocampal circuits and altered neural activity in netrin 1-deficient mice Development, January 11, 2000; 127(22): 4797 - 4810. [Abstract] [PDF]