An UNC-40 pathway directs postsynaptic membrane extension in Caenorhabditis elegans

Development

Volumn 136, Issue 6, 2009, Pages 911-922

  Alexander, Mariam ^a   Chan, Kevin Ka Ming ^a   Byrme, Alexandra B ^a   Selman, Guillermo ^a   Lee, Teresa ^a   Ono, Jasmine ^a   Wong, Eric ^a   Puckrin, Rachel ^a   Dixon, Scott J ^a   Roy, Peter John ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Axon outgrowth; Caenorhabditis elegans; Dcc; GEX 2; GEX 3; Muscle arms; Trio; UNC 40; UNC 73; UNC 95; WAVE

Indexed keywords

GENE PRODUCT; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MEMBRANE PROTEIN; MUSCLE ARM DEVELOPMENT DEFECTIVE 2 PROTEIN; NETRIN; PROTEIN GEX 2; PROTEIN GEX 3; PROTEIN UNC 33; PROTEIN UNC 40; PROTEIN UNC 51; PROTEIN UNC 54; PROTEIN UNC 6; PROTEIN UNC 60B; PROTEIN UNC 73; PROTEIN UNC 93; PROTEIN UNC 95; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; CELL ADHESION MOLECULE; NERVE PROTEIN; UNC 40 PROTEIN, C ELEGANS; UNC 6 PROTEIN, C ELEGANS; UNC 73 PROTEIN, C ELEGANS; UNC-40 PROTEIN, C ELEGANS; UNC-6 PROTEIN, C ELEGANS; UNC-73 PROTEIN, C ELEGANS;

ACTIN POLYMERIZATION; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL EXPANSION; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENSE BODY; FOCAL ADHESION; GENE IDENTIFICATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC SCREENING; LARVAL DEVELOPMENT; MOTOR NERVE; MUSCLE FIBER MEMBRANE; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUSCLE; MUTATION; SYNAPSE;

CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION MOLECULES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MUSCLES; MUTATION; NERVE TISSUE PROTEINS; SYNAPSES;

EID: 66149104511     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.030759     Document Type: Article

References (67)

1. Abe, T., Kato, M., Miki, H., Takenawa, T. and Endo, T. (2003). Small GTPase Tc10 and its homologue RhoT induce N-WASP-mediated long process formation and neurite outgrowth. J. Cell Sci. 116, 155-168.
2. Adler, C. E., Fetter, R. D. and Bargmann, C. I. (2006). UNC-6/ Netrin induces neuronal asymmetry and defines the site of axon formation. Nat. Neurosci. 9, 511-518.
3. Baumeister, R., Liu, Y. and Ruvkun, G. (1996). Lineage-specific regulators couple cell lineage asymmetry to the transcription of the Caenorhabditis elegans POU gene unc-86 during neurogenesis. Genes Dev. 10, 1395-1410.
4. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
5. Broday, L., Kolotuev, I., Didier, C., Bhoumik, A., Podbilewicz, B. and Ronai, Z. (2004). The LIM domain protein UNC-95 is required for the assembly of muscle attachment structures and is regulated by the RING finger protein RNF-5 in C. elegans. J. Cell Biol. 165, 857-867.
6. Chan, S. S., Zheng, H., Su, M. W., Wilk, R., Killeen, M. T., Hedgecock, E. M. and Culotti, J. G. (1996). 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.
7. Clark, S. G. and Chiu, C. (2003). C. elegans ZAG-1, a Zn-finger-homeodomain protein, regulates axonal development and neuronal differentiation. Development 130, 3781-3794.
8. DeMali, K. A., Barlow, C. A. and Burridge, K. (2002). Recruitment of the Arp2/3 complex to vinculin: coupling membrane protrusion to matrix adhesion. J. Cell Biol. 159, 881-891.
9. Desai, C., Garriga, G., McIntire, S. L. and Horvitz, H. R. (1988). A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336, 638-646.
10. Dixon, S. J. and Roy, P. J. (2005). Muscle arm development in Caenorhabditis elegans. Development 132, 3079-3092.
11. Dixon, S. J., Alexander, M., Fernandes, R., Ricker, N. and Roy, P. J. (2006). FGF negatively regulates muscle membrane extension in Caenorhabditis elegans. Development 133, 1263-1275.
12. Eden, S., Rohatgi, R., Podtelejnikov, A. V., Mann, M. and Kirschner, M. W. (2002). Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418, 790-793.
13. Farrer, T., Roller, A. B., Kent, W. J. and Zahler, A. M. (2002). Analysis of the role of Caenorhabditis elegans GC-AG introns in regulated splicing. Nucleic Acids Res. 30, 3360-3367.
14. Forrester, W. C. and Garriga, G. (1997). Genes necessary for C. elegans cell and growth cone migrations. Development 124, 1831-1843.
15. Forsthoefel, D. J., Liebl, E. C., Kolodziej, P. A. and Seeger, M. A. (2005). The Abelson tyrosine kinase, the Trio GEF and Enabled interact with the Netrin receptor Frazzled in Drosophila. Development 132, 1983-1994.
16. Fukata, Y., Itoh, T. J., Kimura, T., Menager, C., Nishimura, T., Shiromizu, T., Watanabe, H., Inagaki, N., Iwamatsu, A., Hotani, H. et al. (2002). CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat. Cell Biol. 4, 583-591.
17. Gitai, Z., Yu, T. W., Lundquist, E. A., Tessier-Lavigne, M. and Bargmann, C. I. (2003). 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.
18. Gorczyca, D., Ashley, J., Speese, S., Gherbesi, N., Thomas, U., Gundelfinger, E., Gramates, L. S. and Budnik, V. (2007). Postsynaptic membrane addition depends on the Discs-Large-interacting t-SNARE Gtaxin. J. Neurosci. 27, 1033-1044.
19. Guan, B., Hartmann, B., Kho, Y. H., Gorczyca, M. and Budnik, V. (1996). The Drosophila tumor suppressor gene, dlg, is involved in structural plasticity at a glutamatergic synapse. Curr. Biol. 6, 695-706.
20. Hedgecock, E. M., Culotti, J. G., Thomson, J. N. and Perkins, L. A. (1985). Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev. Biol. 111, 158-170.
21. Hedgecock, E. M., Culotti, J. G., Hall, D. H. and Stern, B. D. (1987). Genetics of cell and axon migrations in Caenorhabditis elegans. Development 100, 365-382.
22. Hedgecock, E. M., Culotti, J. G. and Hall, D. H. (1990). 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.
23. Hobert, O., Moerman, D. G., Clark, K. A., Beckerle, M. C. and Ruvkun, G. (1999). A conserved LIM protein that affects muscular adherens junction integrity and mechanosensory function in Caenorhabditis elegans. J. Cell Biol. 144, 45-57.
24. Honigberg, L. and Kenyon, C. (2000). 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.
25. Ishii, N., Wadsworth, W. G., Stern, B. D., Culotti, J. G. and Hedgecock, E. M. (1992). UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans. Neuron 9, 873-881.
26. Keino-Masu, K., Masu, M., Hinck, L., Leonardo, E. D., Chan, S. S., Culotti, J. G. and Tessier-Lavigne, M. (1996). Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 87, 175-185.
27. Kunda, P., Craig, G., Dominguez, V. and Baum, B. (2003). Abi, Sra1, and Kette control the stability and localization of SCAR/WAVE to regulate the formation of actin-based protrusions. Curr. Biol. 13, 1867-1875.
28. Lahey, T., Gorczyca, M., Jia, X. X. and Budnik, V. (1994). The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron 13, 823-835.
29. Lecroisey, C., Segalat, L. and Gieseler, K. (2007). The C. elegans dense body: anchoring and signaling structure of the muscle. J. Muscle Res. Cell Motil. 28, 79-87.
30. Leung-Hagesteijn, C., Spence, A. M., Stern, B. D., Zhou, Y., Su, M. W., Hedgecock, E. M. and Culotti, J. G. (1992). 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.
31. Levin, J. Z. and Horvitz, H. R. (1992). The Caenorhabditis elegans unc-93 gene encodes a putative transmembrane protein that regulates muscle contraction. J. Cell Biol. 117, 143-155.
32. Levy-Strumpf, N. and Culotti, J. G. (2007). VAB-8, UNC-73 and MIG-2 regulate axon polarity and cell migration functions of UNC-40 in C. elegans. Nat. Neurosci. 10, 161-168.
33. Lewis, J. A. and Fleming, J. T. (1995). Basic culture methods. Methods Cell Biol. 48, 3-29.
34. McIntire, S. L., Garriga, G., White, J., Jacobson, D. and Horvitz, H. R. (1992). Genes necessary for directed axonal elongation or fasciculation in C. elegans. Neuron 8, 307-322.
35. Mello, C. C., Kramer, J. M., Stinchcomb, D. and Ambros, V. (1991). Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970.
36. Mercer, K. B., Flaherty, D. B., Miller, R. K., Qadota, H., Tinley, T. L., Moerman, D. G. and Benian, G. M. (2003). Caenorhabditis elegans UNC-98, a C2H2 Zn finger protein, is a novel partner of UNC-97/PINCH in muscle adhesion complexes. Mol. Biol. Cell 14, 2492-2507.
37. Miki, H., Suetsugu, S. and Takenawa, T. (1998). WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J. 17, 6932-6941.
38. Misgeld, T., Burgess, R. W., Lewis, R. M., Cunningham, J. M., Lichtman, J. W. and Sanes, J. R. (2002). Roles of neurotransmitter in synapse formation: development of neuromuscular junctions lacking choline acetyltransferase. Neuron 36, 635-648.
39. Ogura, K., Wicky, C., Magnenat, L., Tobler, H., Mori, I., Muller, F. and Ohshima, Y. (1994). Caenorhabditis elegans unc-51 gene required for axonal elongation encodes a novel serine/threonine kinase. Genes Dev. 8, 2389-2400.
40. Raftopoulou, M. and Hall, A. (2004). Cell migration: Rho GTPases lead the way. Dev. Biol. 265, 23-32.
41. Ritzenthaler, S. and Chiba, A. (2003). Myopodia (postsynaptic filopodia) participate in synaptic target recognition. J. Neurobiol. 55, 31-40.
42. Ritzenthaler, S., Suzuki, E. and Chiba, A. (2000). Postsynaptic filopodia in muscle cells interact with innervating motoneuron axons. Nat. Neurosci. 3, 1012-1017.
43. Rudolphi, K. A. (1808). Entozoorum, sive vermium intestinalium, historia naturalis, vol. 1, p. 218, Amstelaedami [as cited in Debell, J. T. (1965). A long look at neuromuscular junctions in nematodes. Q. Rev. Biol. 40, 233-251].
44. Sawa, M., Suetsugu, S., Sugimoto, A., Miki, H., Yamamoto, M. and Takenawa, T. (2003). Essential role of the C. elegans Arp2/3 complex in cell migration during ventral enclosure. J. Cell Sci. 116, 1505-1518.
45. Serafini, T., Kennedy, T. E., Galko, M. J., Mirzayan, C., Jessell, T. M. and Tessier-Lavigne, M. (1994). The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424.
46. Serrels, B., Serrels, A., Brunton, V. G., Holt, M., McLean, G. W., Gray, C. H., Jones, G. E. and Frame, M. C. (2007). Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat. Cell Biol. 9, 1046-1056.
47. Shakir, M. A., Jiang, K., Struckhoff, E. C., Demarco, R. S., Patel, F. B., Soto, M. C. and Lundquist, E. A. (2008). The Arp2/3 activators WAVE and WASP have distinct genetic interactions with Rac GTPases in Caenorhabditis elegans axon guidance. Genetics 179, 1957-1971.
48. Slater, C. R. (2007). Structural factors influencing the efficacy of neuromuscular transmission. Ann. New York Acad. Sci. 1132, 1-12.
49. Small, T. M., Gernert, K. M., Flaherty, D. B., Mercer, K. B., Borodovsky, M. and Benian, G. M. (2004). Three new isoforms of Caenorhabditis elegans UNC-89 containing MLCK-like protein kinase domains. J. Mol. Biol. 342, 91-108.
50. Soto, M. C., Qadota, H., Kasuya, K., Inoue, M., Tsuboi, D., Mello, C. C. and Kaibuchi, K. (2002). The GEX-2 and GEX-3 proteins are required for tissue morphogenesis and cell migrations in C. elegans. Genes Dev. 16, 620-632.
51. Spencer, A. G., Orita, S., Malone, C. J. and Han, M. (2001). A RHO GTPase-mediated pathway is required during P cell migration in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 98, 13132-13137.
52. Steffen, A., Rottner, K., Ehinger, J., Innocenti, M., Scita, G., Wehland, J. and Stradal, T. E. (2004). Sra-1 and Nap1 link Rac to actin assembly driving lamellipodia formation. EMBO J. 23, 749-759.
53. Steven, R., Kubiseski, T. J., Zheng, H., Kulkarni, S., Mancillas, J., Ruiz Morales, A., Hogue, C. W., Pawson, T. and Culotti, J. (1998). UNC-73 activates the Rac GTPase and is required for cell and growth cone migrations in C. elegans. Cell 92, 785-795.
54. Steven, R., Zhang, L., Culotti, J. and Pawson, T. (2005). 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.
55. Sulston, J. E. and Horvitz, H. R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110-156.
56. Symons, M., Derry, J. M., Karlak, B., Jiang, S., Lemahieu, V., McCormick, F., Francke, U. and Abo, A. (1996). Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization. Cell 84, 723-734.
57. Sze, J. Y., Victor, M., Loer, C., Shi, Y. and Ruvkun, G. (2000). Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403, 560-564.
58. Timmons, L. and Fire, A. (1998). Specific interference by ingested dsRNA. Nature 395, 854.
59. Tu, Y., Li, F., Goicoechea, S. and Wu, C. (1999). The LIM-only protein PINCH directly interacts with integrin-linked kinase and is recruited to integrin-rich sites in spreading cells. Mol. Cell. Biol. 19, 2425-2434.
60. Wadsworth, W. G., Bhatt, H. and Hedgecock, E. M. (1996). Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 16, 35-46.
61. Watari-Goshima, N., Ogura, K., Wolf, F. W., Goshima, Y. and Garriga, G. (2007). C. elegans VAB-8 and UNC-73 regulate the SAX-3 receptor to direct cell and growth-cone migrations. Nat. Neurosci. 10, 169-176.
62. Weaver, A. M., Young, M. E., Lee, W. L. and Cooper, J. A. (2003). Integration of signals to the Arp2/3 complex. Curr. Opin. Cell Biol. 15, 23-30.
63. White, J. G., Southgate, E., Thomson, J. N. and Brenner, S. (1986). The structure of the nervous system of the nematode C. elegans. Philos. Trans. R. Soc. London Ser. B 314, 1-340.
64. Wicks, S. R., Yeh, R. T., Gish, W. R., Waterston, R. H. and Plasterk, R. H. (2001). Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 28, 160-164.
65. Withee, J., Galligan, B., Hawkins, N. and Garriga, G. (2004). Caenorhabditis elegans WASP and Ena/VASP proteins play compensatory roles in morphogenesis and neuronal cell migration. Genetics 167, 1165-1176.
66. Yook, K. J., Proulx, S. R. and Jorgensen, E. M. (2001). Rules of nonallelic noncomplementation at the synapse in Caenorhabditis elegans. Genetics 158, 209-220.
67. Yu, T. W., Hao, J. C., Lim, W., Tessier-Lavigne, M. and Bargmann, C. I. (2002). 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.