Shared receptors in axon guidance: SAX-3/Robo signals via UNC-34/enabled and a Netrin-independent UNC-40/DCC function

Nature Neuroscience

Volumn 5, Issue 11, 2002, Pages 1147-1154

  Yu, Timothy W ^a   Hao, Joe C ^a   Lim, Wendell ^a   Tessier Lavigne, Marc ^a   Bargmann, Cornelia I ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE RECEPTOR; NETRIN; PROTEIN SAX 3; PROTEIN UNC 34; RECEPTOR PROTEIN; ROUNDABOUT RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL MIGRATION; CONTROLLED STUDY; DNA SEQUENCE; GENE MUTATION; GROWTH CONE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; RECEPTOR BINDING; VENTRAL ROOT;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION MOLECULES; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH CONES; HELMINTH PROTEINS; MUTATION; NERVE TISSUE PROTEINS; PHENOTYPE; RECEPTORS, CELL SURFACE; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION;

EID: 0036829004     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn956     Document Type: Article

References (50)

1. Tessier-Lavigne, M. & Goodman, C. S. The molecular biology of axon guidance. Science 274, 1123-1133 (1996).
2. Culotti, J. G. & Merz, D. C. DCC and netrins. Curr. Opin. Cell Biol. 10, 609-613 (1998).
3. Flanagan, J. G. & Van Vactor, D. Through the looking glass: Axon guidance at the midline choice point. Cell 92, 429-432 (1998).
4. Brose, K. & Tessier-Lavigne, M. Slit proteins: Key regulators of axon guidance, axonal branching, and cell migration. Curr. Opin. Neurobiol. 10, 95-102 (2000).
5. Flanagan, J. G. & Vanderhaeghen, P. The ephrins and Eph receptors in neural development. Annu. Rev. Neurosci. 21, 309-345 (1998).
6. Nakamura, F., Kalb, R. G. & Strittmatter, S. M. Molecular basis of semaphorin-mediated axon guidance. J. Neurobiol. 44, 219-229 (2000).
7. Bashaw, G. J. & Goodman, C. S. Chimeric axon guidance receptors: The cytoplasmic domains of slit and netrin receptors specify attraction versus repulsion. Cell 97, 917-926 (1999).
8. Stein, E. & Tessier-Lavigne, M. Hierarchical organization of guidance receptors: Silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 291, 1928-1938 (2001).
9. Chan, S. S. et al. UNC-40, a C. elegans homolog of DCC (Deleted in Colorectal Cancer), is required in motile cells responding to UNC-6 netrin cues. Cell 87, 187-195 (1996).
10. Colavita, A. & Culotti, J. G. Suppressors of ectopic UNC-5 growth cone steering identify eight genes involved in axon guidance in Caenorhabditis elegans. Dev. Biol. 194, 72-85 (1998).
11. Hamelin, M., Zhou, Y., Su, M. W., Scott, I. M. & Culotti, J. G. Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature 364, 327-330 (1993).
12. Hong, K. et al. 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 (1999).
13. Hedgecock, E. M., Culotti, J. G., Hall, D. H. & Stern, B. D. Genetics of cell and axon migrations in Caenorhabditis elegans. Development 100, 365-382 (1987).
14. Hedgecock, E. M., Culotti, J. G. & Hall, D. H. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4, 61-85 (1990).
15. Kim, S., Ren, X. C., Fox, E. & Wadsworth, W. G. SDQR migrations in Caenorhabditis elegans are controlled by multiple guidance cues and changing responses to netrin UNC-6. Development 126, 3881-3890 (1999).
16. Honigberg, L. & Kenyon, C. Establishment of left/right asymmetry in neuroblast migration by UNC-40/DCC, UNC-73/Trio and DPY-19 proteins in C. elegans. Development 127, 4655-4668 (2000).
17. 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, 217-227 (1998).
18. Kidd, T. et al. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92, 205-215 (1998).
19. Tear, G., Seeger, M. & Goodman, C. S. To cross or not to cross: A genetic analysis of guidance at the midline. Perspect. Dev. Neurobiol. 1, 183-194 (1993).
20. 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, 25-33 (1998).
21. Guthrie, S. Axon guidance: Robos make the rules. Curr. Biol. 11, R300-303 (2001).
22. Kidd, T., Bland, K. S. & Goodman, C. S. Slit is the midline repellent for the robo receptor in Drosophila. Cell 96, 785-794 (1999).
23. Zallen, J. A., Kirch, S. A. & Bargmann, C. I. Genes required for axon pathfinding and extension in the C. elegans nerve ring. Development 126, 3679-3692 (1999).
24. Hao, J. C. et al. C. elegans Slit acts in midline, dorsal-ventral, and anterior-posterior guidance via the SAX-3/Robo receptor. Neuron 32, 25-38 (2001).
25. Brose, K. et al. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96, 795-806 (1999).
26. Zou, Y., Stoeckli, E., Chen, H. & Tessier-Lavigne, M. Squeezing axons out of the gray matter: A role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 102, 363-375 (2000).
27. Fricke, C., Lee, J. S., Geiger-Rudolph, S., Bonhoeffer, F. & Chien, C. B. astray, a zebrafish roundabout homolog required for retinal axon guidance. Science 292, 507-510 (2001).
28. Bagri, A. et al. Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 33, 233-248 (2002).
29. Plump, A. S. et al. Slit1 and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 33, 219-232 (2002).
30. Gallo, G. & Letourneau, P. C. Axon guidance: A balance of signals sets axons on the right track. Curr. Biol. 9, R490-R492 (1999).
31. Merz, D. C. & Culotti, J. G. Genetic analysis of growth cone migrations in Caenorhabditis elegans. J. Neurobiol. 44, 281-288 (2000).
32. Lin, M. Z. & Greenberg, M. E. Orchestral maneuvers in the axon: Trio and the control of axon guidance. Cell 101, 239-242 (2000).
33. Gertler, F. B., Doctor, J. S. & Hoffmann, F. M. Genetic suppression of mutations in the Drosophila abl proto-oncogene homolog. Science 248, 857-860 (1990).
34. Gertler, F. B. et al. enabled, a dosage-sensitive suppressor of mutations in the Drosophila Abl tyrosine kinase, encodes an Abl substrate with SH3 domain-binding properties. Genes and Development 9, 521-533 (1995).
35. Wills, Z., Bateman, J., Korey, C. A., Comer, A. & Van Vactor, D. The tyrosine kinase Abl and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron 22, 301-312 (1999).
36. Bashaw, G. J., Kidd, T., Murray, D., Pawson, T. & Goodman, C. S. Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101, 703-715 (2000).
37. Fire, A. et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811 (1998).
38. Forrester, W. C. & Garriga, G. Genes necessary for C. elegans cell and growth cone migrations. Development 124, 1831-1843 (1997).
39. McIntire, S. L., Garriga, G., White, J., Jacobson, D. & Horvitz, H. R. Genes necessary for directed axonal elongation or fasciculation in C. elegans. Neuron 8,307-322 (1992).
40. White, J. G., Southgate, E., Thomson, J. N. & Brenner, S. The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. B Biol. Sci. 314, 1-340 (1986).
41. Wadsworth, W. G., Bhatt, H. & Hedgecock, E. M. Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 16, 35-46 (1996).
42. Hiramoto, M., Hiromi, Y, Giniger, E. & Hotta, Y. The Drosophila Netrin receptor Frazzled guides axons by controlling Netrin distribution. Nature 406, 886-889 (2000).
43. Chakraborty, T. et al. A focal adhesion factor directly linking intracellularly motile Listeria monocytogenes and Listeria ivanovii to the actin-based cytoskeleton of mammalian cells. EMBO J. 14, 1314-1321 (1995).
44. Stein, E., Zou, Y., Poo, M. & Tessier-Lavigne, M. Binding of DCC by netrin-1 to mediate axon guidance independent of adenosine A2B receptor activation. Science 291, 1976-1982 (2001).
45. Laurent, V. et al. Role of proteins of the Ena/VASP family in actin-based motility of Listeria monocytogenes. J. Cell. Biol. 144, 1245-1258 (1999).
46. Bear, J. E. et al. Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 101, 717-728 (2000).
47. Sun, Q., Bahri, S., Schmid, A., Chia, W. & Zinn, K. Receptor tyrosine phosphatases regulate axon guidance across the midline of the Drosophila embryo. Development 127, 801-812 (2000).
48. Fritz, J. L. & VanBerkum, M. F. Calmodulin and son of sevenless dependent signaling pathways regulate midline crossing of axons in the Drosophila CNS. Development 127, 1991-2000 (2000).
49. Fazeli, A. et al. Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386, 796-804 (1997).
50. Hamelin, M., Scott, I. M., Way, J. C. & Culotti, J. G. The mec-7 beta-tubulin gene of Caenorhabditis elegans is expressed primarily in the touch receptor neurons. EMBO J. 11, 2885-2893 (1992).