Slit proteins: Key regulators of axon guidance, axonal branching, and cell migration

Current Opinion in Neurobiology

Volumn 10, Issue 1, 2000, Pages 95-102

  Brose, Katja ^a   Tessier Lavigne, Marc ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEOGLYCAN; RECEPTOR; SLIT PROTEIN; UNCLASSIFIED DRUG;

CELL MIGRATION; DROSOPHILA; INVERTEBRATE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; VERTEBRATE;

EID: 0033957068     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(99)00066-5     Document Type: Review

References (34)

1. Tessier-Lavigne M., Goodman C.S. The molecular biology of axon guidance. Science. 274:1996;1123-1133.
2. Mueller B.K. Growth cone guidance: first steps towards a deeper understanding. Annu Rev Neurosci. 22:1999;351-358.
3. Chisholm A., Tessier-Lavigne M. Conservation and divergence of axon guidance mechanisms. Curr Opin Neurobiol. 9:1999;603-615.
4. Seeger M., Tear G., Ferres-Marco D., Goodman C.S. Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron. 10:1993;409-426.
5. Kidd T., Brose K., Mitchell K.J., Fetter R.D., Tessier-Lavigne M., Goodman C.S., Tear G. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell. 92:1998;205-215. The authors use cloning and characterization of the Drosophila robo gene to demonstrate that its protein product, Robo, is an axonal receptor that detects a repulsive ligand at the midline. Midline-crossing is regulated by specific targeting of Robo to particular axonal domains.
6. Kidd T., Russell C., Goodman C.S., Tear G. Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron. 20:1998;25-33. The authors show that midline-crossing in Drosophila is controlled by the repulsive Robo receptor, whose expression on axons is shown to be downregulated by the Commissureless protein, allowing axonal passage across the midline.
7. Zallen J.A., Yi B.A., Bargmann C.I. The conserved immunoglobulin superfamily member SAX-3/Robo directs multiple aspects of axon guidance in C. elegans. Cell. 92:1998;217-227.
8. Bashaw G.J., Goodman C.S. Chimeric axon guidance receptors: the cytoplasmic domains of slit and netrin receptors specify attraction versus repulsion. Cell. 97:1999;917-926. The authors use chimeric guidance receptors composed of the extracellular and cytoplasmic domains of Robo and Frazzled in transgenic experiments to demonstrate that the nature of a response (attraction or repulsion) depends on the cytoplasmic domain of the receptor.
9. Battye R., Stevens A., Jacobs J.R. Axon repulsion from the midline of the Drosophila CNS requires slit function. Development. 126:1999;2475-2481. The authors confirm Slit's supposed repulsive effects in Drosophila by showing that ectopic Slit can disrupt axon projections and repel axons away from sites of ectopic expression.
10. Brose K., Bland K.S., Wang K.H., Arnott D., Henzel W., Goodman C.S., Tessier-Lavigne M., Kidd T. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell. 96:1999;795-806. The authors describe the cloning and expression of three mammalian Slit genes. They show that Slit binds Robo in vertebrates and Drosophila, and this binding is conserved across species. The authors also show that both human Slit2 and Drosophila Slit are proteolytically cleaved, that Robo and Slit binding is conserved across species, and that Slit2 can act as a chemorepellent for spinal motor neurons. A mammalian Slit is also shown to bind netrin-1.
11. Li H.S., Chen J.H., Wu W., Fagaly T., Zhou L., Yuan W., Dupuis S., Jiang Z.H., Nash W., Gick C.et al. Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell. 96:1999;807-818. This paper gives a description of several vertebrate Slit genes, and a demonstration that a Slit protein can repel olfactory bulb axons and bind to Robo receptors in vertebrates.
12. Nguyen Ba-Charvet K.T., Brose K., Marillat V., Kidd T., Goodman C.S., Tessier-Lavigne M., Sotelo C., Chedotal A. Slit2-mediated chemorepulsion and collapse of developing forebrain axons. Neuron. 22:1999;463-473. This paper gives a description of Robo and Slit expression in the forebrain. The authors provide further confirmation of the repulsive activities of a Slit protein by showing that human Slit2 can repel olfactory bulb and hippocampal axons. In addition, the authors provide the first demonstration that a Slit protein can cause collapse of growth cones - in this case, those of olfactory bulb axons.
13. Wu W.W.K., Chen J-H., Jiang Z-H., Dupuis S., Wu J.Y., Rao Y. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature. 400:1999;331-336. The authors provide important evidence to support a role for Slit proteins in directing cell migration in the mammalian brain. They focus on the migration of subventricular zone (SVZ) cells of the olfactory bulb, and use explant culture experiments to establish a role for Slit proteins in mediating the known repulsive action of the septum on these neurons.
14. Hu H. Chemorepulsion of neuronal migration by slit-2 in the developing mammalian forebrain. Neuron. 23:1999;703-711. The authors show that a Slit protein can repel migrating neurons of the subventricular zone. This paper is particularly impressive because the author, who was the first to describe chemorepulsion of this population of migrating neurons, used a novel bioassay and purification strategy to identify Slit2 as a chemorepellent.
15. Zhu Y., Li H.S., Zhou L., Wu J.Y., Rao Y. Cellular and molecular guidance of GABAergic neuronal migration from an extracortical origin to the neocortex. Neuron. 23:1999;473-485. The authors provide another example of the repulsive effect of a Slit protein on migrating cells, in this case on GABAergic neurons originating in the ganglionic eminence.
16. Wang K.H., Brose K., Arnott D., Kidd T., Goodman C.S., Henzel W., Tessier-Lavigne M. Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell. 96:1999;771-784. The authors describe an activity in brain extracts that promotes the elongation and branching of spinal sensory axons and present the purification of this activity using a novel in vitro branching assay. By showing that this activity is the amino-terminal cleavage fragment of Slit2, the authors establish that this Slit protein is bifunctional, with both positive (branching), as well as negative (repulsive) effects. Slit2 represents the first example of a factor with branch-promoting activity for developing axons prior to target encounter.
17. Murray M., Whitington P. Effects of roundabout on growth cone dynamics, filopodial length, and growth cone morphology at the midline and throughout the neuropile. J Neurosci. 19:1999;1901-1912. Using time-lapse imaging to examine growth cone behavior at the midline in robo mutant and wild-type embryos, the authors show that growth cones in robo mutants have longer filopodia and more extensively branched morphologies. These results suggest that Robo both repels growth cones at the midline and inhibits their branching.
18. Rothberg J.M., Jacobs J.R., Goodman C.S., Artavanis-Tsakonas S. slit: an extracellular protein necessary for development of midline glia and commissural axon pathways contains both EGF and LRR domains. Genes Dev. 4:1990;2169-2187.
19. Sonnenfeld M.J., Jacobs J.R. Mesectodermal cell fate analysis in Drosophila midline mutants. Mech Dev. 46:1994;3-13.
20. Tear G., Harris R., Sutaria S., Kilomanski K., Goodman C.S., Seeger M.A. commissureless controls growth cone guidance across the CNS midline in Drosophila and encodes a novel membrane protein. Neuron. 16:1996;501-514.
21. Kidd T., Bland K.S., Goodman C.S. Slit is the midline repellent for the robo receptor in Drosophila. Cell. 96:1999;785-794. Using an extensive series of genetic interactions, the authors provide evidence that Slit is a ligand for Robo in Drosophila. The authors also provide the first indication that Slit can repel cell bodies by showing that midline expression of Slit is required for the repulsion of mesodermal precursors.
22. Hong K., Hinck L., Nishiyama M., Poo M.M., Tessier-Lavigne M., Stein E. A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell. 97:1999;927-941. The authors performed chimeric receptor experiments in order to show that the repulsive function of UNC5 netrin receptors is specified by the cytoplasmic domains of the proteins. Furthermore, it is shown that the conversion of netrin-mediated attraction to repulsion involves the formation of a receptor complex of UNC5 proteins with the attractive netrin-receptor DCC, and a direct interaction of their cytoplasmic domains.
23. Yuan S.S., Cox L.A., Dasika G.K., Lee E.Y. Cloning and functional studies of a novel gene aberrantly expressed in RB-deficient embryos. Dev Biol. 207:1999;62-75. The authors describe the cloning of a third vertebrate Robo, Rig-1.
24. Yuan W., Zhou L., Chen J., Rao Y., Ornitz D. The mouse Slit family: secreted ligands for ROBO expression in patterns that suggest a role in morphogenesis and axon guidance. Dev Biol. 212:1999;290-306. The authors describe the expression patterns of the mouse Robo and Slit genes in the central nervous system and other developing tissues. The complementary expression patterns of Robo and Slit suggest a role for these proteins in neural crest cell migration and limb bud development, as well as in axon pathfinding.
25. Itoh A., Miyabayashi T., Ohno M., Sakano S. Cloning and expressions of three mammalian homologues of Drosophila slit suggest possible roles for Slit in the formation and maintenance of the nervous system. Brain Res Mol Brain Res. 62:1998;175-186. The authors provide a description of three mammalian Slit proteins.
26. Taguchi A., Wanaka A., Mori T., Matsumoto K., Imai Y., Tagaki T., Tohyama M. Molecular cloning of novel leucine-rich repeat proteins and their expression in the developing mouse nervous system. Brain Res Mol Brain Res. 35:1996;31-40.
27. Holmes G.P., Negus K., Burridge L., Raman S., Algar E., Yamada T., Little M.H. Distinct but overlapping expression patterns of two vertebrate slit homologs implies functional roles in CNS development and organogenesis. Mech Dev. 79:1998;57-72. The authors provide a description of two mammalian Slit proteins.
28. Nakayama M., Nakajima D., Nagase T., Nomura N., Seki N., Ohara O. Identification of high-molecular-weight proteins with multiple EGF-like motifs by motif-trap screening. Genomics. 51:1998;27-34. The authors provide a description of two mammalian Slit proteins.
29. O'Leary D.D., Heffener C.D., Kutka L., Lopez-Mascaraque L., Missias A., Reinoso B.S. A target-derived chemoattractant controls the development of the corticopontine projection by a novel mechanism of axon targeting. Development. (Suppl 2):1991;123-130.
30. Serafini T., Kennedy T.E., Galko M.J., Mirzayan C., Jessel T.M., Tessier-Lavigne M. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell. 78:1994;409-424.
31. Davenport R.W., Thies E., Cohen M.L. Neuronal growth cone collapse triggers lateral extensions along trailing axons. Nat Neurosci. 2:1999;254-259. [published erratum appears in Nat Neurosci 1999, 2:485] The authors demonstrate a potential connection between growth cone collapse and axon branching. They show that primary growth cone collapse often results in the formation of lateral filopodial and lamellopodial extensions from the axon shaft. Although some of these extensions seem to be a result of defasciculation, many result from true interstitial branching.
32. Liang Y., Annan R.S., Carr S.A., Popp S., Mevissen M., Margolis R.K., Margolis R.U. Mammalian homologues of the Drosophila Slit Protein are ligands of the heparan sulfate proteoglycan glypican-1 in brain. J Biol Chem. 274:1999;17885-17892. The authors used affinity chromatography to isolate a glypican-1 binding protein, which they identified as the ~200 kDa full-length Slit2 protein. This study raises the possibility that glypicans might modulate the localization or bioactivity of Slit proteins in vivo.
33. Rudenko G., Tguyen T., Chelliah Y., Sudhof T.C., Deisenhofer J. The structure of the ligand-binding domain of neurexin I beta: regulation of LNS domain by alternative splicing. Cell. 99:1999;93-101. Description of the structure of the LNS domain of neurexin 1β, a domain also found in Slit, as well as laminin A and agrin. The authors also report that alternative splicing of the NLS domain of neurexin is able to modulate the protein's affinity for ligands in a neuron-specific manner, suggesting a potentially novel mechanism for regulating neurexin function.
34. Rakic P. Discriminating migrations. Nature. 400:1999;315-316.