C. elegans VAB-8 and UNC-73 regulate the SAX-3 receptor to direct cell and growth-cone migrations

Nature Neuroscience

Volumn 10, Issue 2, 2007, Pages 169-176

  Watari Goshima, Natsuko ^a   Ogura, Ken Ichi ^b   Wolf, Fred W ^a,d   Goshima, Yoshio ^b,c   Garriga, Gian ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; KINESIN; NETRIN; PROTEIN; PROTEIN SAX 3; PROTEIN SLT 1; PROTEIN UNC 73; PROTEIN VAB 8L; ROUNDABOUT RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL MIGRATION; GENETICS; GROWTH CONE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL DIFFERENTIATION; CELL MOVEMENT; CUES; GROWTH CONES; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; RAC GTP-BINDING PROTEINS; RECEPTORS, IMMUNOLOGIC;

EID: 33846625269     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1834     Document Type: Article

References (50)

1. Dickson, B.J. Molecular mechanisms of axon guidance. Science 298, 1959-1964 (2002).
2. Tessier-Lavigne, M. & Goodman, C.S. The molecular biology of axon guidance. Science 274, 1123-1133 (1996).
3. 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).
4. 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).
5. Serafini, T. et al. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424 (1994).
6. Kennedy, T.E., Serafini, T., de la Torre, J.R. & Tessier-Lavigne, M. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78, 425-435 (1994).
7. Keino-Masu, K. et al. Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 87, 175-185 (1996).
8. Kolodziej, P.A. et al. frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 87, 197-204 (1996).
9. Mitchell, K.J. et al. Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 17, 203-215 (1996).
10. 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).
11. 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).
12. Leung-Hagesteijn, C. et al. UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell 71, 289-299 (1992).
13. 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).
14. Sabatier, C. et al. The divergent Robo family protein rig-1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell 117, 157-169 (2004).
15. Keleman, K. et al. Comm sorts robo to control axon guidance at the Drosophila midline. Cell 110, 415-427 (2002).
16. Keleman, K., Ribeiro, C. & Dickson, B.J. Comm function in commissural axon guidance: cell-autonomous sorting of Robo in vivo. Nat. Neurosci. 8, 156-163 (2005).
17. Lyuksyutova, A.I. et al. Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science 302, 1984-1988 (2003).
18. Pan, C.-L. et al. Multiple Wnt and Frizzled receptors regulate anteriorly directed cell and growth cone migrations in Caenorhabditis elegans. Dev. Cell 10, 367-377 (2006).
19. Wightman, B. et al. The C. elegans gene vab-8 guides posteriorly directed axon outgrowth and cell migration. Development 122, 671-682 (1996).
20. Wolf, F.W., Hung, M.S., Wightman, B., Way, J. & Garriga, G. vab-8 is a key regulator of posteriorly directed migrations in C. elegans and encodes a novel protein with kinesin motor similarity. Neuron 20, 655-666 (1998).
21. Levy-Strumpf, N. & Culotti, J. VAB-8, UNC-73 and MIG-2 regulate axon polarity and cell migration functions ofUNC-40 in C. elegans. Nat. Neurosci. advance online publication, 21 January 2007 (doi:10.1038/nn1835).
22. Chalfie, M. & Sulston, J. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev. Biol. 82, 358-370 (1981).
23. 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 314, 1-340 (1986).
24. Debant, A. et al. The multidomain protein Trio binds the LAR transmembrane tyrosine phosphatase, contains a protein kinase domain, and has separate rac-specific and rhospecific guanine nucleotide exchange factor domains. Proc. Natl. Acad. Sci. USA 93, 5466-5471 (1996).
25. Newsome, T.P. et al. Trio combines with dock to regulate Pak activity during photoreceptor axon pathfinding in Drosophila. Cell 101, 283-294 (2000).
26. Steven, R. et al. UNC-73 activates the Rac GTPase and is required for cell and growth cone migrations in C. elegans. Cell 92, 785-795 (1998).
27. Spencer, A.G., Orita, S., Malone, C.J. & Han, M.A. RHO GTPase-mediated pathway is required during P cell migration in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 98, 13132-13137 (2001).
28. Steven, R., Zhang, L., Culotti, J. & Pawson, T. The UNC-73/Trio RhoGEF-2 domain is required in separate isoforms for the regulation of pharynx pumping and normal neurotransmission in C. elegans. Genes Dev. 19, 2016-2029 (2005).
29. Jantsch-Plunger, V. et al. CYK-4: A Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis. J. Cell Biol. 149, 1391-1404 (2000).
30. 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).
31. 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).
32. Merz, D.C., Zheng, H., Killeen, M.T., Krizus, A. & Culotti, J.G. Multiple signaling mechanisms of the UNC-6/netrin receptors UNC-5 and UNC-40/DCC in vivo. Genetics 158, 1071-1080 (2001).
33. 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).
34. Yu, T.W., Hao, J.C., Lim, W., Tessier-Lavigne, M. & Bargmann, C.I. Shared receptors in axon guidance: SAX-3/Robo signals via UNC-34/Enabled and a Netrin-independent UNC-40/DCC function. Nat. Neurosci. 5, 1147-1154 (2002).
35. Forrester, W.C. & Garriga, G. Genes necessary for C. elegans cell and growth cone migrations. Development 124, 1831-1843 (1997).
36. Manser, J. & Wood, W.B. Mutations affecting embryonic cell migrations in Caenorhabditis elegans. Dev. Genet. 11, 49-64 (1990).
37. Fleming, T.C.,Wolf, F.W. & Garriga, G. Sensitized genetic backgrounds reveal a role for C. elegans FGF EGL-17 as a repellent for migrating CAN neurons. Development 132, 4857-4867 (2005).
38. 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).
39. Fan, X., Labrador, J.P., Hing, H. & Bashaw, G.J. Slit stimulation recruits Dock and Pak to the roundabout receptor and increases Rac activity to regulate axon repulsion at the CNS midline. Neuron 40, 113-127 (2003).
40. Hu, H. et al. Cross GTPase-activating protein (CrossGAP)/Vilse links the Roundabout receptor to Rac to regulate midline repulsion. Proc. Natl. Acad. Sci. USA 102, 4613-4618 (2005).
41. Gitai, Z., Yu, T.W., Lundquist, E.A., Tessier-Lavigne, M. & Bargmann, C.I. The netrin receptor UNC-40/DCC stimulates axon attraction and outgrowth through enabled and, in parallel, Rac and UNC-115/AbLIM. Neuron 37, 53-65 (2003).
42. Lundstrom, A. et al. Vilse, a conserved Rac/Cdc42 GAP mediating Robo repulsion in tracheal cells and axons. Genes Dev. 18, 2161-2171 (2004).
43. Lamaze, C., Chuang, T.H., Terlecky, L.J., Bokoch, G.M. & Schmid, S.L. Regulation of receptor-mediated endocytosis by Rho and Rac. Nature 382, 177-179 (1996).
44. Jou, T.S. et al. Selective alterations in biosynthetic and endocytic protein traffic in Madin-Darby canine kidney epithelial cells expressing mutants of the small GTPase Rac1. Mol. Biol. Cell 11, 287-304 (2000).
45. Kiosses, W.B., Shattil, S.J., Pampori, N. & Schwartz, M.A. Rac recruits high-affinity integrin alphavbeta3 to lamellipodia in endothelial cell migration. Nat. Cell Biol. 3, 316-320 (2001).
46. Forsthoefel, D.J., Liebl, E.C., Kolodziej, P.A. & Seeger, M.A. The Abelson tyrosine kinase, the Trio GEF and Enabled interact with the Netrin receptor Frazzled in Drosophila. Development 132, 1983-1994 (2005).
47. Su, M. et al. Regulation of the UNC-5 netrin receptor initiates the first reorientation of migrating distal tip cells in Caenorhabditis elegans. Development 127, 585-594 (2000).
48. Ogura, K. & Goshima, Y. The autophagy-related kinase UNC-51 and its binding partner UNC-14 regulate the subcellular localization of the Netrin receptor UNC-5 in Caenorhabditis elegans. Development 133, 3441-3450 (2006).
49. Lai, T. & Garriga, G. The conserved kinase UNC-51 acts with VAB-8 and UNC-14 to regulate axon outgrowth in C. elegans. Development 131, 5991-6000 (2004).
50. Georgiou, M. & Tear, G. Commissureless is required both in commissural neurones and midline cells for axon guidance across the midline. Development 129, 2947-2956 (2002)