Slit1 and slit2 proteins control the development of the lateral olfactory tract

Journal of Neuroscience

Volumn 22, Issue 13, 2002, Pages 5473-5480

  Nguyen Ba Charvet, Kim T ^a   Plump, Andrew S ^b   Tessier Lavigne, Marc ^b   Chédotal, Alain ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Axon guidance; Chemorepulsion; Molecular cues; Olfactory bulb; Robo; Slit

Indexed keywords

CELL PROTEIN; SLIT1 PROTEIN; SLIT2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; DOSE RESPONSE; EMBRYO DEVELOPMENT; GENE DELETION; GENE EXPRESSION REGULATION; GENE TARGETING; MOUSE; NERVE FIBER GROWTH; NERVE FIBER TRANSPORT; NONHUMAN; NOSE SEPTUM; OLFACTORY BULB; OLFACTORY CORTEX; OLFACTORY TRACT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION;

EID: 0036662891     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-13-05473.2002     Document Type: Article

References (62)

1. Bagri A, Marin O, Plump AS, Mak J, Pleasure SJ, Rubenstein JLR, Tessier-Lavigne M (2002) Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 33:233-248.
2. Brose K, Tessier-Lavigne M (2000) Slit proteins: Key regulators of axon guidance, axonal branching, and cell migration. Curr Opin Neurobiol 10:95-102.
3. Brose K, Bland KS, Wang K-H, Arnott D, Henzel W, Goodman CS, Tessier-Lavigne M, Kidd T (1999) Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96:795-806.
4. Chédotal A, Del Rio JA, Ruiz M He Z, Borrell V, de Castro F, Ezan F, Goodman CS, Tessier-Lavigne M, Sotelo C, Soriano E (1998) Semaphorins III, IV repel hippocampal axons via two distinct receptors. Development 125:4313-4323.
5. Chen H, Bagri A, Zupicich JA, Zou Y, Stoeckli E, Pleasure SJ, Lowenstein DH, Skarnes WC, Chedotal A, Tessier-Lavigne M (2000) Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections. Neuron 25:43-56.
6. Chen J-H, Wen L, Dupuis S, Wu JY, Rao Y (2001) The N-terminal leucine-rich regions in slit are sufficient to repel olfactory bulb axons and subventricular zone neurons. J Neurosci 21:1548-1556,
7. de Castro F, Hu L, Drabkin H, Sotelo C, Chédotal A (1999) Chemoattraction and chemorepulsion of olfactory bulb axons by different secreted Semaphorins. J Neurosci 19:4428-4436.
8. Derer P, Caviness Jr VS, Sidman RL (1977) Early cortical histogenesis in the primary olfactory cortex of the mouse. Brain Res 123:27
9. Devor M (1976) Fiber trajectories of olfactory bulb efferents in the hamster. J Comp Neurol 166:31-47.
10. Erskine L, Williams SE, Brose K, Kidd T, Rachel RA, Goodman CS, Tessier-Lavigne M, Mason CA (2000) Retinal ganglion cell axon guidance in the mouse optic chiasm: Expression and function of Robos and Slits. J Neurosci 20:4975-4982.
11. Fricke C, Lee J-S, Geiger-Rudolph S, Bonhoeffer F, Chien C-B (2001) astray, a zebrafish roundabout homolog required for retinal axon guidance. Science 292:507-510.
12. Hadjantonakis A-K, Gertsenstein M, Ikawa M, Okabe M, Nagy A (1998) Generating green fluorescent mice by germline transmission of green fluorescent ES cells. Mech Dev 76:79-90.
13. Hirata T, Fujisawa H (1997) Cortex-specific distribution of membrane-bound factors that promote neurite outgrowth of mitral cells in culture. J Neurobiol 32:415-425.
14. Hirata T, Fujisawa H (1999) Environmental control of collateral branching and target invasion of mitral cell axons during development. J Neurobiol 38:93-104.
15. Hirata T, Fujisawa H, Wu JY, Rao Y (2001) Short-range guidance of olfactory bulb axons is independent of repulsive factor slit. J Neurosci 21:2373-2379.
16. Holmes GP, Negus K, Burridge L, Raman S, Algar E, Yamada T, Little MH (1998) Distinct but overlapping expression patterns of two vertebrate slit homologs implies functional roles in CNS development and organogenesis. Mech Dev 79:57-72.
17. Hu H (1999) Chemorepulsion of neuronal migration by slit2 in the developing mammalian forebrain. Neuron 23:703-711.
18. Hu H (2001) Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein. Nat Neurosci 4:695-701.
19. Hu H, Rutishauser U (1996) A septum-derived chemorepulsive factor for migrating olfactory interneuron precursors. Neuron 16:933-940.
20. Hutson LD, Chien CB (2002) Pathfinding and error correction by retinal axons: The role of astray/robo2. Neuron 33:205-217.
21. Itoh A, Miyabayashi T, Ohno M, Sakano S (1998) Cloning and expressions of three mammalian homologues of Drosophila slit suggest possible roles for slit in the formation and maintenance of the nervous system. Mol Brain Res 62:175-186.
22. 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.
23. Kidd T, Brose K, Mitchell KJ, Fetter RD, Tessier-Lavigne M, Goodman CS, Tear G (1998) Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92:205-215.
24. Kidd T, Bland KS, Goodman CS (1999) Slit is the midline repellent for the robo receptor in Drosophila. Cell 96:785-794.
25. 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.
26. Kolodkin AL, Levengood DV, Rowe EG, Tai YT, Giger RJ, Ginty DD (1997) Neuropilin is a Semaphorin III receptor. Cell 90:753-762.
27. Li H-S, Chen J-H, Wu W, Fagaly T, Zhou L, Yuan W, Dupuis S, Jiang Z-H, Nash W, Gick C, Ornitz DM, Wu JY, Rao Y (1999) Vertebrate Slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 96:807-818.
28. Liang Y, Annan RS, Carr SA, Popp S, Mevissen M, Margolis RK, Margolis RU (1999) Mammalian homologues of the Drosophila slit protein are ligands of the heparan sulfate proteoglycan glypican-1 in brain. J Biol Chem 274:17885-17892.
29. Lopez-Mascaraque L, De Carlos JA, Valverde F (1996) Early onset of the rat olfactory bulb projections. Neuroscience 70:255-266.
30. Luskin MB, Price JL (1982) The distribution of axon collaterals from the olfactory bulb and the nucleus of the horizontal limb of the diagonal band to the olfactory cortex, demonstrated by double retrograde labeling techniques. J Comp Neurol 209:249-263.
31. Marillat V, Cases O, Nguyen-Ba-Charvet KT, Tessier-Lavigne M, Sotelo C, Chédotal A (2002) Spatiotemporal expression patterns of slit and robo genes in the rat brain. J Comp Neurol 442:130-155.
32. Moody SA, Quigg MS, Frankfurter A (1989) Development of the peripheral trigeminal system in the chick revealed by an isotype-specific anti-β-tubulin monoclonal antibody. J Comp Neurol 346:97-118.
33. Nguyen-Ba-Charvet KT, Brose K, Marillat V, Kidd T, Goodman CS, Tessier-Lavigne M, Sotelo C, Chédotal A (1999) Slit2-mediated chemorepulsion and collapse of developing forebrain axons. Neuron 22:463-473.
34. Nguyen-Ba-Charvet KT, Brose K, Ma L, Wang KH, Marillat V, Sotelo C, Tessier-Lavigne M, Chédotal A (2001) Diversity and specificity of actions of Slit2 proteolytic fragments in axon guidance. J Neurosci 21:4281-4289.
35. Niclou SP, Jia L, Raper JA (2000) Slit2 is a repellent for retinal ganglion cell axons. J Neurosci 20:4962-4974.
36. O'Connor R, Tessier-Lavigne M (1999) Identification of maxillary factor, a maxillary process-derived chemoattractant for developing trigeminal sensory axons. Neuron 24:165-178.
37. Patel K, Nash JAB, Itoh A, Liu Z, Sundaresan V, Pini A (2001) Slit proteins are dominant chemorepellents for olfactory tract and spinal motor axons. Development 128:5031-5037.
38. Pini A (1993) Chemorepulsion of axons in the developing mammalian central nervous system. Science 261:34-98.
39. Plump AS, Erskine L, Sabatier C, Brose K, Epstein CJ, Goodman CS, Mason C, Tessier-Lavigne M (2002) Slitl and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 33:219-232.
40. Pozas E, Pascual M, Nguyen-Ba-Charvet KT, Guijarro P, Sotelo C, Chédotal A, Del Rio JA, Soriano E (2001) Age-dependent effects of secreted sempahorines 3A, 3F, and 3E on developing hippocampal axons: In vitro effects and phenotype of semaphorin 3A (-/-) mice. Mol Cell Neurosci 18:26-43.
41. Rajagopalan S, Vivancos V, Nicolas E, Dickson BJ (2000a) Selecting a longitudinal pathway: Robo receptors specify the lateral position of axons in the Drosophila CNS. Cell 103:1033-1045.
42. Rajagopalan S, Nicolas E, Vivancos V, Berger J, Dickson BJ (2000b) Crossing the midline: Roles and regulation of robo receptors. Neuron 28:767-777.
43. Ringstedt T, Braisted JE, Brose K, Kidd T, Goodman C, Tessier-Lavigne M, O'Leary DD (2000) Slit inhibition of retinal axon growth and its role in retinal axon pathfinding and innervation patterns in the diencephalon. J Neurosci 20:4983-4991.
44. Ronca F, Brose K, Andersen JS, Paech V, Tessier-Lavigne M, Margolis RU (2001) Characterization of Slit protein interactions with glypican-1. J Biol Chem 26:29141-29147.
45. Rothberg JM, Jacobs JR, Goodman CS, Artavanis-Tsakonas S (1990) Slit: An extracellular protein necessary for development of midline glia and commissural axon pathways contains both EGF, LRR domains. Genes Dev 4:2169-2187.
46. Sato Y, Hirata T, Ogawa M, Fujisawa H (1998) Requirement for early-generated neurons recognized by monoclonal antibody Lot1 in the formation of lateral olfactory tract. J Neurosci 18:7800-7810.
47. Schwob JE, Price JL (1984) The development of axonal connections in the central olfactory system of rats. J Comp Neurol 223:177-202.
48. Scott JW, McBride RL, Schneider SP (1980) The organization of projections from the olfactory bulb to the piriform cortex and olfactory tubercle in the rat. J Comp Neurol 194:519-534.
49. Shipley MT, Ennis M (1996) Functional organization of olfactory system. J Neurobiol 30:123-176.
50. Shu T, Richards LJ (2001) Cortical axon guidance by the glial wedge during the development of the corpus callosum. J Neurosci 21:2749-2758.
51. Simpson JH, Bland KS, Fetter RD, Goodman CS (2000a) Short-range and long-range guidance by slit and its robo receptors: A combinatorial code of Robo receptors controls lateral position. Cell 103:1019-1032.
52. Simpson JH, Kidd T, Bland KS, Goodman CS (2000b) Short-range and long-range guidance by slit and its robo receptors: Robo and Robo2 play distinct roles in midline guidance. Neuron 28:753-766.
53. Soussi-Yanicostas N, de Castro F, Julliard K, Perfettini I, Chédotal A, Petit C (2002) Anosmin-1, defective in the X-linked form of Kallmann syndrome, promotes axonal branch formation from olfactory bulb output neurons. Cell 109:217-228.
54. Sugisaki N, Hirata T, Naruse I, Kawakami A, Kitsukawa T, Fujisawa H (1996) Positional cues that are strictly localized in the telencephalon induce preferential growth of mitral cell axons. J Neurobiol 29:127-137.
55. Tomioka N, Osumi N, Sato Y, Inoue T, Nakamura S, Fujisawa H, Hirata T (2000) Neocortical origin and tangential migration of guidepost neurons in the lateral olfactory tract. J Neurosci 20:5802-5812.
56. Wang KH, Brose K, Arnott D, Kidd T, Goodman C, Henzel W, 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.
57. Whitford KL, Marillat V, Stein E, Goodman CS, Tessier-Lavigne M, Chédotal A, Ghosh A (2002) Regulation of cortical dendrite development by Slit-Robo interactions. Neuron 33:47-61.
58. Wu W, Wong K, Chen J-H, Jiang Z-H, Dupuis S, Wu JY, Rao Y (1999) Directional guidance of neuronal migration in the olfactory system by the protein slit. Nature 400:331-336.
59. Yuan S-S, Cox LA, Dasika GK, Lee EY (1999a) Cloning and functional studies of a novel gene aberrantly expressed in RB-deficient embryos. Dev Biol 207:62-75.
60. Yuan W, Zhou L, Chen J-H, Wu JY, Rao Y, Ornitz DM (1999b) The mouse SLIT family: Secreted ligands for ROBO expressed in patterns that suggest a role in morphogenesis and axon guidance. Dev Biol 212:290-306.
61. Zou Y, Stoeckli E, Chen H, Tessier-Lavigne M (2000) Squeezing axons out of the gray matter: A role for slit and semaphorin proteins from the midline and ventral spinal cord. Cell 102:363-375.
62. Zou Z, Horowitz LF, Montmayeur JP, Snapper S, Buck LB (2001) Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 414:173-179.