mau-2 acts cell-autonomously to guide axonal migrations in Caenorhabditis elegans

Development

Volumn 131, Issue 23, 2004, Pages 5947-5958

  Bénard, Claire Y ^a   Kébir, Hania ^a   Takagi, Shin ^a   Hekimi, Siegfried ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Caenorhabditis elegans; Cell autonomous; Guidance; Maternal effect; mau 2; Migration; slit; slt 1

Indexed keywords

HYBRID PROTEIN; PROTEIN MAU 2; SLIT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL MIGRATION; CONTROLLED STUDY; CYTOPLASM; EMBRYO DEVELOPMENT; GASTRULATION; GENE EXPRESSION; LARVAL STAGE; MUTANT; NERVE CELL; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ALLELES; AMINO ACID SEQUENCE; ANIMALS; AXONS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL MOVEMENT; CLONING, MOLECULAR; CONSERVED SEQUENCE; CYTOPLASM; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; GENETIC COMPLEMENTATION TEST; GREEN FLUORESCENT PROTEINS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTATION; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; NEURONS; PHENOTYPE; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; TRANSGENES;

ANIMALIA; CAENORHABDITIS; CAENORHABDITIS ELEGANS; NEMATODA;

EID: 12344302590     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01433     Document Type: Article

References (51)

1. Antebi, A., Norris, C. and Hedgecock, E. M. (1997). Cell and growth cone migrations. In C. elegans II (ed. D. L. Riddle, T. Blumenthal, B. Meyer and J. Priess). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
2. Aparicio, S., Chapman, J., Stupka, E., Putnam, N., Chia, J. M., Dehal, P., Christoffels, A., Rash, S., Hoon, S., Smit, A. et al. (2002). Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297, 1301-1310.
3. Beanan, M. J. and Strome, S. (1992). Characterization of a germ-line proliferation mutation in C. elegans. Development 116, 755-766.
4. Blelloch, R., Newman, C. and Kimble, J. (1999). Control of cell migration during Caenorhabditis elegans development. Curr. Opin. Cell Biol. 11, 608-613.
5. Bloom, L. and Horvitz, H. R. (1997). 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, 3414-3419.
6. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
7. 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.
8. Chang, C., Yu, T. W., Bargmann, C. I. and Tessier-Lavigne, M. (2004). Inhibition of netrin-mediated axon attraction by a receptor protein tyrosine phosphatase. Science 305, 103-106.
9. D'Andrea, L. D. and Regan, L. (2003). TPR proteins: the versatile helix. TIBS 28, 655-662.
10. Edgar, L. G., Wolf, N. and Wood, W. B. (1994). Early transcription in Caenorhabditis elegans embryos. Development 120, 443-451.
11. Edgley, M., D'Souza, A., Moulder, G., McKay, S., Shen, B., Gilchrist, E., Moerman, D. and Barstead, R. (2002). Improved detection of small deletions in complex pools of DNA. Nucleic Acids Res. 30, E52.
12. Forrester, W. C., Perens, E., Zallen, J. A. and Garriga, G. (1998). Identification of Caenorhabditis elegans genes required for neuronal differentiation and migration. Genetics 148, 151-165.
13. Gilleard, J. S., Barry, J. D. and Johnstone, I. L. (1997). cis regulatory requirements for hypodermal cell-specific expression of the Caenorhabditis elegans cuticle coltagen gene dpy-7. Mol. Cell. Biol. 17, 2301-2311.
14. 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.
15. Gumienny, T. L., Brugnera, E., Tosello-Trampont, A. C., Kinchen, J. M., Haney, L. B., Nishiwaki, K., Walk, S. F., Nemergut, M. E., Macara, I. G., Francis, R. et al. (2001). CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, is required for phagocytosis and cell migration. Cell 107, 27-41.
16. Hamelin, M., Scott, I. M., Way, J. C. and Culotti, J. G. (1992). The mec-7 beta-tubulin gene of Caenorhabditis elegans is expressed primarily in the touch receptor neurons. EMBO J. 11, 2885-2893.
17. Hamelin, M., Zhou, Y., Su, M. W., Scott, I. M. and Culotti, J. G. (1993). Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature 364, 327-330.
18. Hao, J. C., Yu, T. W., Fujisawa, K., Culotti, J. G., Gengyo-Ando, K., Mitani, S., Moulder, G., Barstead, R., Tessier-Lavigne, M. and Bargmann, C. I. (2001). C. elegans slit acts in midline, dorsal-ventral, and anterior-posterior guidance via the SAX-3 /Robo receptor. Neuron 32, 25-38.
19. Harlow, E. and Lane, D. (1999). Using Antibodies: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
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. Hekimi, S., Boutis, P. and Lakowski, B. (1995). Viable maternal-effect mutations that affect the development of the nematode Caenorhabditis elegans. Genetics 141, 1351-1364.
24. 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.
25. Kaltenbach, L., Horner, M. A., Rothman, J. H. and Mango, S. E. (2000). The TBP-like factor CcTLF is required to activate RNA polymerase II transcription during C. elegans embryogenesis. Mol. Cell 6, 705-713.
26. Killeen, M., Tong, J., Krizus, A., Steven, R., Scott, I., Pawson, T. and Culotti, J. (2002). UNC-5 function requires phosphorylation of cytoplasmic tyrosine 482, but its UNC-40-independent functions also require a region between the ZU-5 and death domains. Dev. Biol. 251, 348-366.
27. Kim, S. and Wadsworth, W. G. (2000). Positioning of longitudinal nerves in C. elegans by nidogen. Science 288 150-154.
28. Lamb, J. R., Tugendreich, S. and Hieter, P. (1995). Tetratrico peptide repeat interactions: to TPR or not to TPR? Trends Biochem. Sci. 20, 257-259.
29. Lerner, K. and Goldstein, P. (1988). Electron microscopic autoradiographic analysis: evidence of RNA transcription along pachytene chromosomes of rad-4, him-4 and wild-type Caenorhabditis elegans. Cytobios 55, 51-61.
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. Lim, Y. S. and Wadsworth, W. G. (2002). Identification of domains of netrin UNC-6 that mediate attractive and repulsive guidance and responses from cells and growth cones. J. Neurosci. 22, 7080-7087.
32. Maduro, M. and Pilgrim, D. (1995). Identification and cloning of unc- 119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141, 977-988.
33. 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.
34. Mello, C. C. and Fire, A. (1995). DNA transformation. In Methods in Cell Biology: Caenorhabditis elegans: Modern Biological Analysis of an Organisms, Vol. 48 (ed. H. F. Epstein and D. C. Shakes), pp. 452-482. New York, NY: Academic Press.
35. Okkema, P. G., Harrison, S. W., Plunger, V., Aryana, A. and Fire, A. (1993). Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics 135, 385-404.
36. Powell-Coffman, J. A., Knight, J. and Wood, W. B. (1996). Onset of C. elegans gastrulation is blocked by inhibition of embryonic transcription with an RNA polymerase antisense RNA. Dev. Biol. 178, 472-483.
37. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
38. Stringham, E., Pujol, N., Vandekerckhove, J. and Bogaert, T. (2002). unc-53 controls longitudinal migration in C. elegans. Development 129, 3367-3379.
39. Su, M., Merz, D. C., Killeen, M. T., Zhou, Y., Zheng, H., Kramer, J. M., Hedgecock, E. M. and Culotti, J. G. (2000). Regulation of the UNC-5 netrin receptor initiates the first reorientation of migrating distal tip cells in Caenorhabditis elegans. Development 127, 585-594.
40. Sulston, J. E. and Horvitz, H. R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110-156.
41. Sym, M., Robinson, N. and Kenyon, C. (1999). MIG-13 positions migrating cells along the anteroposterior body axis of C. elegans. Cell 98, 25-36.
42. 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.
43. Takagi, S., Bénard, C., Pak, J., Livingstone, D. and Hekimi, S. (1997). Cellular and axonal migrations are misguided along both body axes in the maternal-effect mau-2 mutants of Caenorhabditis elegans. Development 124, 5115-5126.
44. 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.
45. White, J. G., Southgate, E., Thomson, J. N. and Brenner, S. (1986). The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314, 1-340.
46. Whitfield, C. W., Bénard, C., Barnes, T., Hekimi, S. and Kim, S. K. (1999). Basolateral localization of the Caenorhabditis elegans epidermal growth factor receptor in epithelial cells by the PDZ protein LIN-10. Mol. Biol. Cell 10, 2087-2100.
47. Wightman, B., Baran, R. and Garriga, G. (1997). Genes that guide growth cones along the C. elegans ventral nerve cord. Development 124, 2571-2580.
48. Wolf, F. W., Hung, M. S., Wightman, B., Way, J. and Garriga, G. (1998). 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.
49. Wood, W. B. (1988). The Nematode Caenorhabditis elegans. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
50. Yu, T. W., Han, 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.
51. Zallen, J. A., Yi, B. A. and Bargmann, C. I. (1998). The conserved immunoglobulin superfamily member SAX-3/Robo directs multiple aspects of axon guidance in C. elegans. Cell 92, 217-227.