Conversion of cell movement responses to Semaphorin-1 and Plexin-1 from attraction to repulsion by lowered levels of specific RAC GTPases in C. elegans

Development

Volumn 131, Issue 9, 2004, Pages 2073-2088

  Dalpé, Gratien ^a   Zhang, Lijia W ^a   Zheng, Hong ^a   Culotti, Joseph G ^a,b  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

C. elegans; Migration; Plexins; RHO GTPases

Indexed keywords

GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; MUTANT PROTEIN; PROTEIN PLEXIN 1; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RNA; SEMAPHORIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL MIGRATION; CELL MOTION; CONTROLLED STUDY; ENZYME SPECIFICITY; GENETIC ANALYSIS; GENETIC CODE; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN FUNCTION; RNA ANALYSIS; RNA INTERFERENCE; TAIL; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; BODY PATTERNING; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION MOLECULES; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; COS CELLS; GENES, REPORTER; MALE; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PROTEIN BIOSYNTHESIS; RAC GTP-BINDING PROTEINS; RECOMBINANT FUSION PROTEINS; RHO GTP-BINDING PROTEINS; RNA INTERFERENCE; SEMAPHORINS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSGENES;

CAENORHABDITIS; CAENORHABDITIS ELEGANS; INVERTEBRATA; NEMATODA;

EID: 2542633389     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01063     Document Type: Article

References (61)

1. Awasaki, T., Saito, M., Sone, M., Suzuki, E., Sakai, R., Ito, K. and Hama, C. (2000). The Drosophila trio plays an essential role in patterning of axons by regulating their directional extension. Neuron 26, 119-131.
2. Baird, S. E., Fitch, D. H., Kassem, I. A. and Emmons, S. W. (1991). Pattern formation in the nematode epidermis: determination of the arrangement of peripheral sense organs in the C. elegans male tail. Development 113, 515-526.
3. Bateman, J., Shu, H. and Van Vactor, A (2000). The guanine nucleotide exchange factor trio mediates axonal development in the Drosophila embryo. Neuron 26, 93-106.
4. Buck, K. B. and Zheng, J. Q. (2002). Growth cone turning induced by direct local modification of microtubule dynamics. J. Neurosci. 22, 9358-9367.
5. da Silva, J. S. and Dotti, C. G. (2002). Breaking the neuronal sphere: regulation of the action cytoskeleton in neurogenesis. Nat. Rev. Neurosci. 3, 694-704.
6. 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.
7. Dickson, B. J. (2001). Rho GTPases in growth cone guidance. Curr. Opin. Neurobiol. 11, 103-110.
8. Dickson, B. J., Cline, H., Polleux, F. and Ghosh, A. (2001b). Making connections. Meeting: axon guidance and neural plasticity. EMBO Rep. 2, 182-186.
9. Driessens, M. H., Hu, H., Nobes, C. D., Self, A., Jordens, L, Goodman, C. S. and Hall, A. (2001). Plexin-B semaphorin receptors interact directly with active Rac and regulate the actin cytoskeleton by activating Rho. Curr. Biol. 11, 339-344.
10. Eickholt, B. J., Mackenzie, S. L., Graham, A., Walsh, F. S. and Doherty, P. (1999). Evidence for collapsin-1 functioning in the control of neural crest migration in both trunk and hindbrain regions. Development 126, 2181-2189.
11. Ellis, R. E., Jacobson, D. M. and Horvitz, H. R. (1991). Genes required for the engulfment of cell corpses during programmed cell death in Caenorhabditis elegans. Genetics 129, 79-94.
12. Fitch, D. H. and Emmons, S. W. (1995). Variable cell positions and cell contacts underlie morphological evolution of the rays in the male tails of nematodes related to Caenorhabditis elegans. Dev. Biol. 170, 564-582.
13. Forrester, W. C. and Garriga, G. (1997). Genes necessary for C. elegans cell and growth cone migrations. Development 124, 1831-1843.
14. Francis, G. R. and Waterston, R. H. (1985). Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization. J. Cell Biol. 101, 1532-1549.
15. Fujii, T., Nakao, F., Shibata, Y., Shioi, G., Kodama, E., Fujisawa, H. and Takagi, S. (2002). Caenorhabditis elegans PlexinA, PLX-1, interacts with transmembrane semaphorins and regulates epidermal morphogenesis. Development 129, 2053-2063.
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. Ginzburg, V. E., Roy, P. J. and Culotti, J. G. (2002). Semaphorin 1a and semaphorin 1b are required for correct epidermal cell positioning and adhesion during morphogenesis in C. elegans. Development 129, 2065-2078.
18. Goshima, Y., Nakamura, F., Strittmatter, P. and Strittmatter, S. M. (1995). Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 376, 509-514.
19. Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
20. Hall, C., Brown, M., Jacobs, T., Ferrari, G., Cann, N., Teo, M., Monfries, C. and Lim, L. (2001). Collapsin response mediator protein switches RhoA and Rac1 morphology in N1E-115 neuroblastoma cells and is regulated by Rho kinase. J. Biol. Chem. 276, 43482-43486.
21. Hodgkin, J., Horvitz, H. R. and Brenner, S. (1979). Nondisjunction mutants of the nematode C. elegans. Genetics 91, 67-94.
22. Hu, H., Marton, T. F. and Goodman, C. S. (2001). Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron 32, 39-51.
23. Jalink, K., van Corven, E. J., Hengeveld, T., Morii, N., Narumiya, S. and Moolenaar, W. H. (1994). Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell Biol. 126, 801-810.
24. Jin, Z. and Strittmatter, S. M. (1997). Rac1 mediates collapsin-1-induced growth cone collapse. J. Neurosci. 17, 6256-6263.
25. Kamath, R. S., Martinez-Campos, M., Zipperlen, P., Fraser, A. G. and Ahringer, J. (2001). Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2, RESEARCH0002.
26. Kimble, J., Sulston, J. and White, J. G. (1979). Regulative development in the post-embryonic lineages of C. elegans. In Cell Lineage, Stem Cells and Cell Determinations (ed. N. Le Douarin), pp. 59-68. New York: Elsevier.
27. Kishore, R. S. and Sundaram, M. V. (2002). 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, 339-348.
28. Koppen, M., Simske, J. S., Sims, P. A., Firestein, B. L., Hall, D. H., Radice, A. D., Rongo, C. and Hardin, J. D. (2001). Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat. Cell Biol. 3, 983-991.
29. Kuhn, T. B., Brown, M. D., Wilcox, C. L., Raper, J. A. and Bamburg, J. R. (1999). Myelin and collapsin-1 induce motor neuron growth cone collapse through different pathways: inhibition of collapse by opposing mutants of rac1. J. Neurosci. 19, 1965-1975.
30. Letunic, I., Goodstadt, L., Dickens, N. J., Doerks, T., Schultz, J., Mott, R., Ciccarelli, F., Copley, R. R., Ponting, C. P. and Bork, P. (2002). Recent improvements to the SMART domain-based sequence annotation resource. Nucl. Acids Res. 30, 242-244.
31. Leung, T., Ng, Y., Cheong, A., Ng, C. H., Tan, I., Hall, C. and Lim, L. (2002). p80 ROKalpha binding protein is a novel splice variant of CRMP-1 which associates with CRMP-2 and modulates RhoA-induced neuronal morphology. FEBS Lett. 532, 445-449.
32. Li, W., Herman, R. K. and Shaw, J. E. (1992). Analysis of the Caenorhabditis elegans axonal guidance and outgrowth gene unc-33. Genetics 132, 675-689.
33. Liebl, E. C., Forsthoefel, D. J., Franco, L. S., Sample, S. H., Hess, J. E., Cowger, J. A., Chandler, M. P., Shupert, A. M. and Seeger, M. A. (2000). Dosage-sensitive, reciprocal genetic interactions between the Abl tyrosine kinase and the putative GEF trio reveal trio's role in axon pathfinding. Neuron 26, 107-118.
34. Lundquist, E. A., Reddien, P. W., Hartwieg, E., Horvitz, H. R. and Bargmann, C. I. (2001). Three C. elegans Rac proteins and several alternative Rac regulators control axon guidance, cell migration and apoptotic cell phagocytosis. Development 128, 4475-4488.
35. Luo, L. (2000). Rho GTPases in neuronal morphogenesis. Nat. Rev. Neurosci. 1, 173-180.
36. Mello, C. and Fire, A. (1995). DNA transformation. Methods Cell Biol. 48, 451-482.
37. Mitani, S. (1995). Integration of extrachromosomal DNA arrays into a chromosome by UV-irradiation. Worm Breeder's Gazette 14, 22.
38. Mitsui, N., Inatome, R., Takahashi, S., Goshima, Y., Yamamura, H. and Yanagi, S. (2002). Involvement of Fes/Fps tyrosine kinase in semaphorin3A signaling. EMBO J. 21, 3274-3285.
39. Moon, I. S. and Krause, M. O. (1991). Common RNA polymerase I, II, and III upstream elements in mouse 7SK gene locus revealed by the inverse polymerase chain reaction. DNA Cell Biol. 10, 23-32.
40. Moore, D. S. and McCabe, G. P. (1998). Introduction to the Practice of Statistics. New York, NY: W. H. Freeman.
41. Mueller, B. K. (1999). Growth cone guidance: first steps towards a deeper understanding. Annu. Rev. Neurosci. 22, 351-388.
42. Newsome, T. P., Schmidt, S., Dietzl, G., Keleman, K., Asling, B., Debant, A. and Dickson, B. J. (2000). Trio combines with dock to regulate Pak activity during photoreceptor axon pathfinding in Drosophila. Cell 101, 283-294.
43. Rohm, B., Rahim, B., Kleiber, B., Hovatta, I. and Puschel, A. W. (2000). The semaphorin 3A receptor may directly regulate the activity of small GTPases. FEBS Lett. 486, 68-72.
44. Roy, P. J., Zheng, H., Warren, C. E. and Culotti, J. G. (2000). mab-20 encodes Semaphorin-2a and is required to prevent ectopic cell contacts during epidermal morphogenesis in Caenorhabditis elegans. Development 127, 755-767.
45. Sambrook, J., Fristsch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
46. Schultz, J., Milpetz, F., Bork, P. and Ponting, C. P. (1998). SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. USA 95, 5857-5864.
47. Simske, J. S. and Hardin, J. (2001). Getting into shape: epidermal morphogenesis in Caenorhabditis elegans embryos. BioEssays 23, 12-23.
48. Song, H., Ming, G., He, Z., Lehmann, M., McKerracher, L., Tessier-Lavigne, M. and Poo, M. (1998). Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281, 1515-1518.
49. 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.
50. 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 Rae GTPase and is required for cell and growth cone migrations in C. elegans. Cell 92, 785-795.
51. Sulston, J. E. and Horvitz, H. R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110-156.
52. Sulston, J. E. and Horvitz, H. R. (1981). Abnormal cell lineages in mutants of the nematode Caenorhabditis elegans. Dev. Biol. 82, 41-55.
53. Suter, D. M. and Forscher, P. (1998). An emerging link between cytoskeletal dynamics and cell adhesion molecules in growth cone guidance. Curr. Opin. Neurobiol. 8, 106-116.
54. Timmons, L., Court, D. L. and Fire, A. (2001). Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112.
55. Vikis, H. G., Li, W., He, Z. and Guan, K. L. (2000). The semaphorin receptor plexin-B1 specifically interacts with active Rac in a ligand-dependent manner. Proc. Natl. Acad. Sci. USA 97, 12457-12462.
56. Vikis, H. G., Li, W. and Guan, K. L. (2002). The plexin-B1/Rac interaction inhibits PAK activation and enhances Sema4D ligand binding. Genes Dev. 16, 836-845.
57. Winberg, M. L., Noordermeer, J. N., Tamagnone, L., Comoglio, P. M., Spriggs, M. K., Tessier-Lavigne, M. and Goodman, C. S. (1998). Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95, 903-916.
58. Wood, W. B. (1988). The Nematode Caenorhabditis elegans. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
59. Yuan, X.-b., Jin, M., Xu, X., Song, Y.-q., Wu, C.-p., Poo, M.-m. and Duan, S. (2003). Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat. Cell Biol. 5, 1-8.
60. Zipkin, I. D., Kindt, R. M. and Kenyon, C. J. (1997). Role of a new Rho family member in cell migration and axon guidance in C. elegans. Cell 90, 883-894.
61. Zwaal, R. R., Broeks, A., van Meurs, J., Groenen, J. T. and Plasterk, R. H. (1993). Target-selected gene inactivation in Caenorhabditis elegans by using a frozen transposon insertion mutant bank. Proc. Natl. Acad. Sci. USA 90, 7431-7435.