The netrin receptor UNC-40/DCC stimulates axon attraction and outgrowth through enabled and, in parallel, Rac and UNC-115/abLIM

Neuron

Volumn 37, Issue 1, 2003, Pages 53-65

  Gitai, Zemer ^a,c   Yu, Timothy W ^a   Lundquist, Erik A ^b   Tessier Lavigne, Marc ^c   Bargmann, Cornelia I ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF KANSAS   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; HYBRID PROTEIN; MEMBRANE RECEPTOR; MUTANT PROTEIN; NETRIN; RAC PROTEIN; RECEPTOR PROTEIN; UNC 40 DCC RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; MOLECULE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; STIMULATION;

EID: 0037426990     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(02)01149-2     Document Type: Article

References (79)

1. Aletta J.M., Greene L.A. Growth cone configuration and advance. a time-lapse study using video-enhanced differential interference contrast microscopy J. Neurosci. 8:1988;1425-1435.
2. Awasaki T., Saito M., Sone M., Suzuki E., Sakai R., Ito K., Hama C. The Drosophila trio plays an essential role in patterning of axons by regulating their directional extension. Neuron. 26:2000;119-131.
3. Bachmann C., Fischer L., Walter U., Reinhard M. The EVH2 domain of the vasodilator-stimulated phosphoprotein mediates tetramerization, F-actin binding, and actin bundle formation. J. Biol. Chem. 274:1999;23549-23557.
4. 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.
5. 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. 101:2000;703-715.
6. Baumeister R., Liu Y., Ruvkun G. Lineage-specific regulators couple cell lineage asymmetry to the transcription of the Caenorhabditis elegans POU gene unc-86 during neurogenesis. Genes Dev. 10:1996;1395-1410.
7. Bear J.E., Loureiro J.J., Libova I., Fassler R., Wehland J., Gertler F.B. Negative regulation of fibroblast motility by Ena/VASP proteins. Cell. 101:2000;717-728.
8. Bear J.E., Svitkina T.M., Krause M., Schafer D.A., Loureiro J.J., Strasser G.A., Maly I.V., Chaga O.Y., Cooper J.A., Borisy G.G., Gertler F.B. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell. 109:2002;509-521.
9. Bloom L., Horvitz H.R. The Caenorhabditis elegans gene unc-76 and its human homologs define a new gene family involved in axonal outgrowth and fasciculation. Proc. Natl. Acad. Sci. USA. 94:1997;3414-3419.
10. Branda C.S., Stern M.J. Cell migration and axon growth cone guidance in Caenorhabditis elegans. Curr. Opin. Genet. Dev. 9:1999;479-484.
11. Bray D., Hollenbeck P.J. Growth cone motility and guidance. Annu. Rev. Cell Biol. 4:1988;43-61.
12. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 77:1974;71-94.
13. Chan S.S., Zheng H., Su M.W., Wilk R., Killeen M.T., Hedgecock E.M., Culotti J.G. UNC-40, a C. elegans homolog of DCC (Deleted in Colorectal Cancer), is required in motile cells responding to UNC-6 netrin cues. Cell. 87:1996;187-195.
14. Colamarino S.A., Tessier-Lavigne M. The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell. 81:1995;621-629.
15. 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. 194:1998;72-85.
16. de la Torre J.R., Hopker V.H., Ming G.L., Poo M.M., Tessier-Lavigne M., Hemmati-Brivanlou A., Holt C.E. Turning of retinal growth cones in a netrin-1 gradient mediated by the netrin receptor DCC. Neuron. 19:1997;1211-1224.
17. Edwards D.C., Sanders L.C., Bokoch G.M., Gill G.N. Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat. Cell Biol. 1:1999;253-259.
18. Erkman L., Yates P.A., McLaughlin T., McEvilly R.J., Whisenhunt T., O'Connell S.M., Krones A.I., Kirby M.A., Rapaport D.H., Bermingham J.R.et al. A POU domain transcription factor-dependent program regulates axon pathfinding in the vertebrate visual system. Neuron. 28:2000;779-792.
19. Fazeli A., Dickinson S.L., Hermiston M.L., Tighe R.V., Steen R.G., Small C.G., Stoeckli E.T., Keino-Masu K., Masu M., Rayburn H.et al. Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature. 386:1997;796-804.
20. George S.E., Simokat K., Hardin J., Chisholm A.D. The VAB-1 Eph receptor tyrosine kinase functions in neural and epithelial morphogenesis in C. elegans. Cell. 92:1998;633-643.
21. Gertler F.B., Comer A.R., Juang J.L., Ahern S.M., Clark M.J., Liebl E.C., Hoffmann F.M. enabled, a dosage-sensitive suppressor of mutations in the Drosophila Abl tyrosine kinase, encodes an Abl substrate with SH3 domain-binding properties. Genes Dev. 9:1995;521-533.
22. Gertler F.B., Niebuhr K., Reinhard M., Wehland J., Soriano P. Mena, a relative of VASP and Drosophila Enabled, is implicated in the control of microfilament dynamics. Cell. 87:1996;227-239.
23. Gordon-Weeks P.R. The cytoskeletons of isolated, neuronal growth cones. Neuroscience. 21:1987;977-989.
24. Hakeda-Suzuki S., Ng J., Tzu J., Dietzl G., Sun Y., Harms M., Nardine T., Luo L., Dickson B.J. Rac function and regulation during Drosophila development. Nature. 416:2002;438-442.
25. 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. 11:1992;2885-2893.
26. 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. 364:1993;327-330.
27. Hao J.C., Yu T.W., Fujisawa K., Culotti J.G., Gengyo-Ando K., Mitani S., Moulder G., Barstead R., Tessier-Lavigne M., Bargmann C.I. C. elegans slit acts in midline, dorsal-ventral, and anterior-posterior guidance via the SAX-3/Robo receptor. Neuron. 32:2001;25-38.
28. Hedgecock E.M., Culotti J.G., Thomson J.N., Perkins L.A. Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev. Biol. 111:1985;158-170.
29. 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. 4:1990;61-85.
30. 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.
31. Hong K., Nishiyama M., Henley J., Tessier-Lavigne M., Poo M. Calcium signalling in the guidance of nerve growth by netrin-1. Nature. 403:2000;93-98.
32. Hu H., Marton T.F., Goodman C.S. Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron. 32:2001;39-51.
33. Huttelmaier S., Harbeck B., Steffens O., Messerschmidt T., Illenberger S., Jockusch B.M. Characterization of the actin binding properties of the vasodilator-stimulated phosphoprotein VASP. FEBS Lett. 451:1999;68-74.
34. Ishii N., Wadsworth W.G., Stern B.D., Culotti J.G., Hedgecock E.M. UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans. Neuron. 9:1992;873-881.
35. Jin Z., Strittmatter S.M. Rac1 mediates collapsin-1-induced growth cone collapse. J. Neurosci. 17:1997;6256-6263.
36. Jin Y., Jorgensen E., Hartwieg E., Horvitz H.R. The Caenorhabditis elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development. J. Neurosci. 19:1999;539-548.
37. Kamps M.P., Buss J.E., Sefton B.M. Mutation of NH2-terminal glycine of p60src prevents both myristoylation and morphological transformation. Proc. Natl. Acad. Sci. USA. 82:1985;4625-4628.
38. Keino-Masu K., Masu M., Hinck L., Leonardo E.D., Chan S.S., Culotti J.G., Tessier-Lavigne M. Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell. 87:1996;175-185.
39. 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. 78:1994;425-435.
40. Kishore R.S., Sundaram M.V. ced-10 Rac and mig-2 function redundantly and act with unc-73 trio to control the orientation of vulval cell divisions and migrations in Caenorhabditis elegans. Dev. Biol. 241:2002;339-348.
41. Kolodziej P.A., Timpe L.C., Mitchell K.J., Fried S.R., Goodman C.S., Jan L.Y., Jan Y.N. frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell. 87:1996;197-204.
42. Korey C.A., Van Vactor D. From the growth cone surface to the cytoskeleton. one journey, many paths J. Neurobiol. 44:2000;184-193.
43. Lambrechts A., Kwiatkowski A.V., Lanier L.M., Bear J.E., Vandekerckhove J., Ampe C., Gertler F.B. cAMP-dependent protein kinase phosphorylation of EVL, a Mena/VASP relative, regulates its interaction with actin and SH3 domains. J. Biol. Chem. 275:2000;36143-36151.
44. Laurent V., Loisel T.P., Harbeck B., Wehman A., Grobe L., Jockusch B.M., Wehland J., Gertler F.B., Carlier M.F. Role of proteins of the Ena/VASP family in actin-based motility of Listeria monocytogenes. J. Cell Biol. 144:1999;1245-1258.
45. Leonardo E.D., Hinck L., Masu M., Keino-Masu K., Ackerman S.L., Tessier-Lavigne M. Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature. 386:1997;833-838.
46. Leung-Hagesteijn C., Spence A.M., Stern B.D., Zhou Y., Su M.W., Hedgecock E.M., Culotti J.G. UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell. 71:1992;289-299.
47. Lundquist E.A., Herman R.K., Shaw J.E., Bargmann C.I. UNC-115, a conserved protein with predicted LIM and actin-binding domains, mediates axon guidance in C. elegans. Neuron. 21:1998;385-392.
48. Lundquist E.A., Reddien P.W., Hartwieg E., Horvitz H.R., Bargmann C.I. Three C. elegans Rac proteins and several alternative Rac regulators control axon guidance, cell migration and apoptotic cell phagocytosis. Development. 128:2001;4475-4488.
49. Luo L., Liao Y.J., Jan L.Y., Jan Y.N. Distinct morphogenetic functions of similar small GTPases. Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion Genes Dev. 8:1994;1787-1802.
50. McIntire S.L., Garriga G., White J., Jacobson D., Horvitz H.R. Genes necessary for directed axonal elongation or fasciculation in C. elegans. Neuron. 8:1992;307-322.
51. McKim K.S., Matheson C., Marra M.A., Wakarchuk M.F., Baillie D.L. The Caenorhabditis elegans unc-60 gene encodes proteins homologous to a family of actin-binding proteins. Mol. Gen. Genet. 242:1994;346-357.
52. Mello C., Fire A. DNA transformation. Methods Cell Biol. 48:1995;451-482.
53. 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. 158:2001;1071-1080.
54. Ming G.L., Song H.J., Berninger B., Holt C.E., Tessier-Lavigne M., Poo M.M. cAMP-dependent growth cone guidance by netrin-1. Neuron. 19:1997;1225-1235.
55. Ng J., Nardine T., Harms M., Tzu J., Goldstein A., Sun Y., Dietzl G., Dickson B.J., Luo L. Rac GTPases control axon growth, guidance and branching. Nature. 416:2002;442-447.
56. Niebuhr K., Ebel F., Frank R., Reinhard M., Domann E., Carl U.D., Walter U., Gertler F.B., Wehland J., Chakraborty T. A novel proline-rich motif present in ActA of Listeria monocytogenes and cytoskeletal proteins is the ligand for the EVH1 domain, a protein module present in the Ena/VASP family. EMBO J. 16:1997;5433-5444.
57. Nobes C.D., Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 81:1995;53-62.
58. Ogura K., Wicky C., Magnenat L., Tobler H., Mori I., Muller F., Ohshima Y. Caenorhabditis elegans unc-51 gene required for axonal elongation encodes a novel serine/threonine kinase. Genes Dev. 8:1994;2389-2400.
59. Otsuka A.J., Franco R., Yang B., Shim K.H., Tang L.Z., Zhang Y.Y., Boontrakulpoontawee P., Jeyaprakash A., Hedgecock E., Wheaton V.I.et al. An ankyrin-related gene (unc-44) is necessary for proper axonal guidance in Caenorhabditis elegans. J. Cell Biol. 129:1995;1081-1092.
60. Reddien P.W., Horvitz H.R. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat. Cell Biol. 2:2000;131-136.
61. Roof D.J., Hayes A., Adamian M., Chishti A.H., Li T. Molecular characterization of abLIM, a novel actin-binding and double zinc finger protein. J. Cell Biol. 138:1997;575-588.
62. Serafini T., Kennedy T.E., Galko M.J., Mirzayan C., Jessell 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.
63. Serafini T., Colamarino S.A., Leonardo E.D., Wang H., Beddington R., Skarnes W.C., Tessier-Lavigne M. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell. 87:1996;1001-1014.
64. Shamah S.M., Lin M.Z., Goldberg J.L., Estrach S., Sahin M., Hu L., Bazalakova M., Neve R.L., Corfas G., Debant A., Greenberg M.E. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell. 105:2001;233-244.
65. Shekarabi M., Kennedy T.E. The netrin-1 receptor DCC promotes filopodia formation and cell spreading by activating Cdc42 and Rac1. Mol. Cell. Neurosci. 19:2002;1-17.
66. Stein E., Tessier-Lavigne M. Hierarchical organization of guidance receptors. silencing of netrin attraction by slit through a Robo/DCC receptor complex Science. 291:2001;1928-1938.
67. 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. 291:2001;1976-1982.
68. Steven R., Kubiseski T.J., Zheng H., Kulkarni S., Mancillas J., Ruiz Morales A., Hogue C.W., Pawson T., Culotti J. UNC-73 activates the Rac GTPase and is required for cell and growth cone migrations in C. elegans. Cell. 92:1998;785-795.
69. Su M., Merz D.C., Killeen M.T., Zhou Y., Zheng H., Kramer J.M., Hedgecock E.M., Culotti J.G. Regulation of the UNC-5 netrin receptor initiates the first reorientation of migrating distal tip cells in Caenorhabditis elegans. Development. 127:2000;585-594.
70. Tessier-Lavigne M., Goodman C.S. The molecular biology of axon guidance. Science. 274:1996;1123-1133.
71. Ullrich A., Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell. 61:1990;203-212.
72. Vikis H.G., Li W., He Z., Guan K.L. The semaphorin receptor plexin-B1 specifically interacts with active Rac in a ligand-dependent manner. Proc. Natl. Acad. Sci. USA. 97:2000;12457-12462.
73. 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. 16:1996;35-46.
74. Wightman B., Baran R., Garriga G. Genes that guide growth cones along the C. elegans ventral nerve cord. Development. 124:1997;2571-2580.
75. Wong K., Ren X.R., Huang Y.Z., Xie Y., Liu G., Saito H., Tang H., Wen L., Brady-Kalnay S.M., Mei L.et al. Signal transduction in neuronal migration. roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway Cell. 107:2001;209-221.
76. 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. 5:2002;1147-1154.
77. 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.
78. Zallen J.A., Kirch S.A., Bargmann C.I. Genes required for axon pathfinding and extension in the C. elegans nerve ring. Development. 126:1999;3679-3692.
79. Zipkin I.D., Kindt R.M., Kenyon C.J. Role of a new Rho family member in cell migration and axon guidance in C. elegans. Cell. 90:1997;883-894.