PAR-3 and PAR-1 inhibit LET-99 localization to generate a cortical band important for spindle positioning in Caenorhabditis elegans embryos

Molecular Biology of the Cell

Volumn 18, Issue 11, 2007, Pages 4470-4482

  Wu, Jui Ching ^a   Rose, Lesilee S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PROTEIN LET 99; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 3; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL DIVISION; CELL FATE; CELL SHAPE; CONTROLLED STUDY; EMBRYO; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANAPHASE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL NUCLEUS; CELL POLARITY; CELL SHAPE; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MITOTIC SPINDLE APPARATUS; MUTATION; PROTEIN-SERINE-THREONINE KINASES; SENSITIVITY AND SPECIFICITY;

CAENORHABDITIS ELEGANS;

EID: 35549011174     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-02-0105     Document Type: Article

References (56)

1. Afshar, K., Willard, F. S., Colombo, K., Johnston, C. A., McCudden, C. R., Siderovski, D. P., and Gönczy, P. (2004). RIC-8 is required for GPR-1/2-dependent Gα function during asymmetric division of C. elegans embryos. Cell 119, 219-230.
2. Afshar, K., Willard, F. S., Colombo, K., Siderovski, D. P., and Gönczy, P. (2005). Cortical localization of the Gα protein GPA-16 requires RIC-8 function during C. elegans asymmetric cell division. Development 132, 4449-4459.
3. Bellaiche, Y., and Gotta, M. (2005). Heterotrimeric G proteins and regulation of size asymmetry during cell division. Curr. Opin. Cell Biol. 17, 658-663.
4. Benton, R., and St. Johnston, D. (2003). Drosophila PAR-1 and 14-3-3 inhibit Bazooka/PAR-3 to establish complementary cortical domains in polarized cells. Cell 115, 691-704.
5. Betschinger, J., Eisenhaber, F., and Knoblich, J. A. (2005). Phosphorylation-induced autoinhibition regulates the cytoskeletal protein Lethal (2) giant larvae. Curr. Biol. 15, 276-282.
6. Betschinger, J., and Knoblich, J. A. (2004). Dare to be different: asymmetric cell division in Drosophila, C. elegans and vertebrates. Curr. Biol. 14, R674-R685.
7. Boyd, L., Guo, S., Levitan, D., Stinchcomb, D., and Kemphues, K. (1996). PAR-2 is asymmetrically distributed and promotes association of P granules and PAR-1 with the cortex in C. elegans embryos. Development 122, 3075-3084.
8. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
9. Bringmann, H., Cowan, C. R., Kong, J., and Hyman, A. A. (2007). LET-99, GOA-1/GPA-16, and GPR-1/2 are required for aster-positioned cytokinesis. Curr. Biol. 17, 185-191.
10. Cheeks, R. J., Canman, J. C., Gabriel, W. N., Meyer, N., Strome, S., and Goldstein, B. (2004). C. elegans PAR proteins function by mobilizing and stabilizing asymmetrically localized protein complexes. Curr. Biol. 14, 851-862.
11. Church, D., Guan, K., and Lambie, E. (1995). Three genes of the MAP kinase cascade, mek-2, mpk-1/sur-1 and let-60 ras, are required for meiotic cell cycle progression in Caenorhabditis elegans. Development 121, 2525-2535.
12. Colombo, K., Grill, S. W., Kimple, R. J., Willard, F. S., Siderovski, D. P., and Gönczy, P. (2003). Translation of polarity cues into asymmetric spindle positioning in Caenorhabditis elegans embryos. Science 300, 1957-1961.
13. Couwenbergs, C., Spilker, A. C., and Gotta, M. (2004). Control of embryonic spindle positioning and Gα activity by C. elegans RIC-8. Curr. Biol. 14, 1871-1876.
14. Cowan, C. R., and Hyman, A. A. (2004). Asymmetric cell division in C. elegans: cortical polarity and spindle positioning. Annu. Rev. Cell Dev. Biol. 20, 427-453.
15. Cuenca, A. A., Schetter, A., Aceto, D., Kemphues, K., and Seydoux, G. (2003). Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 130, 1255-1265.
16. Etemad-Moghadam, B., Guo, S., and Kemphues, K. J. (1995). Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell 83, 743-752.
17. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., and Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811.
18. Golden, A. (2000). Cytoplasmic flow and the establishment of polarity in C. elegans 1-cell embryos. Curr. Opin. Genet. Dev. 10, 414-420.
19. Gönczy, P., Pichler, S., Kirkham, M., and Hyman, A. A. (1999). Cytoplasmic dynein is required for distinct aspects of MTOC positioning, including centrosome separation, in the one cell stage Caenorhabditis elegans embryo. J. Cell Biol. 147, 135-150.
20. Gönczy, P., and Rose, L. S. (2005). Asymmetric cell division and axis formation in the embryo. In: WormBook, ed. T.C.e.R. Community: WormBook, doi/10.1895/wormbook. 1.30.1, http://www.wormbook.org.
21. Gotta, M., and Ahringer, J. (2001). Distinct roles for Gα and Gβγ in regulating spindle position and orientation in Caenorhabditis elegans embryos. Nat. Cell Biol. 3, 297-300.
22. Gotta, M., Dong, Y., Peterson, Y. K., Lanier, S. M., and Ahringer, J. (2003). Asymmetrically distributed C. elegans homologs of AGS3/PINS control spindle position in the early embryo. Curr. Biol. 13, 1029-1037.
23. Grill, S. W., Howard, J., Schaffer, E., Stelzer, E. H., and Hyman, A. A. (2003). The distribution of active force generators controls mitotic spindle position. Science 301, 518-521.
24. Guo, S., and Kemphues, K. J. (1995). par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81, 611-620.
25. Hao, Y., Boyd, L., and Seydoux, G. (2006). Stabilization of cell polarity by the C. elegans RING protein PAR-2. Dev. Cell 10, 199-208.
26. Hung, T. J., and Kemphues, K. J. (1999). PAR-6 is a conserved PDZ domain-containing protein that colocalizes with PAR-3 in Caenorhabditis elegans embryos. Development 126, 127-135.
27. Hurov, J. B., Watkins, J. L., and Piwnica-Worms, H. (2004). Atypical PKC phosphorylates PAR-1 kinases to regulate localization and activity. Curr. Biol. 14, 736-741.
28. Kemphues, K. J., Priess, J. R., Morton, D. G., and Cheng, N. S. (1988). Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52, 311-320.
29. Kimura, A., and Onami, S. (2005). Computer simulations and image processing reveal length-dependent pulling force as the primary mechanism for C. elegans male pronuclear migration. Dev. Cell 8, 765-775.
30. Lewis, J. A., and Fleming, J. T. (1995). Basic culture methods of Caenorhabditis elegans. In: Modern Biological Analysis of an Organism, ed. H. F. Epstein and D. C. Shakes, San Diego: Academic Press, 3-29.
31. Macara, I. G. (2004). Parsing the polarity code. Nat. Rev. Mol. Cell Biol. 5, 220-231.
32. Miller, D. M., and Shakes, D. C. (1995). Immunofluorescence microscopy in Caenorhabditis elegans. In: Modern Biological Analysis of an Organism, ed. H. F. Epstein and D. C. Shakes, San Diego: Academic Press, 365-394.
33. Morton, D. G., Roos, J. M., and Kemphues, K. J. (1992). par-4, a gene required for cytoplasmic localization and determination of specific cell types in Caenorhabditis elegans embryogenesis. Genetics 130, 771-790.
34. Munro, E., Nance, J., and Priess, J. R. (2004). Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Dev. Cell 7, 413-424.
35. Nagai-Tamai, Y., Mizuno, K., Hirose, T., Suzuki, A., and Ohno, S. (2002). Regulated protein-protein interaction between aPKC and PAR-3 plays an essential role in the polarization of epithelial cells. Genes Cells 7, 1161-1171.
36. Nance, J. (2005). PAR proteins and the establishment of cell polarity during C. elegans development. BioEssays 27, 126-135.
37. Nance, J., Munro, E. M., and Priess, J. R. (2003). C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation. Development 130, 5339-5350.
38. Oegema, K., Desai, A., Rybina, S., Kirkham, M., and Hyman, A. A. (2001). Functional analysis of kinetochore assembly in Caenorhabditis elegans. J. Cell Biol. 153, 1209-1226.
39. Pecreaux, J., Roper, J.-C., Kruse, K., Julicher, F., Hyman, A. A., Grill, S. W., and Howard, J. (2006). Spindle oscillations during asymmetric cell division require a threshold number of active cortical force generators. Curr. Biol. 16, 2111-2122.
40. Riechmann, V., Gutierrez, G. J., Filardo, P., Nebreda, A. R., and Ephrussi, A. (2002). Par-1 regulates stability of the posterior determinant Oskar by phosphorylation. Nat. Cell Biol. 4, 337-342.
41. Rose, L. S., and Kemphues, K. (1998). The let-99 gene is required for proper spindle orientation during cleavage of the C. elegans embryo. Development 125, 1337-1346.
42. Sato, M., Blumer, J. B., Simon, V., and Lanier, S. M. (2006). Accessory proteins for G proteins: partners in signaling. Annu. Rev. Pharmacol. Toxicol. 46, 151-187.
43. Schmidt, D. J., Rose, D. J., Saxton, W. M., and Strome, S. (2005). Functional analysis of cytoplasmic dynein heavy chain in Caenorhabditis elegans with fast-acting temperature-sensitive mutations. Mol. Biol. Cell 16, 1200-1212.
44. Schneider, S. Q., and Bowerman, B. (2003). Cell polarity and the cytoskeleton in the Caenorhabditis elegans zygote. Annu. Rev. Genet. 37, 221-249.
45. Schubert, C. M., Lin, R., de Vries, C. J., Plasterk, R.H.A., and Priess, J. R. (2000). MEX-5 and MEX-6 function to establish soma/germline asymmetry in early C. elegans embryos. Mol. Cell 5, 671-682.
46. Severson, A. F., and Bowerman, B. (2003). Myosin and the PAR proteins polarize microfilament-dependent forces that shape and position mitotic spindles in Caenorhabditis elegans. J. Cell Biol. 161, 21-26.
47. Skop, A. R., and White, J. G. (1998). The dynactin complex is required for cleavage plane specification in early Caenorhabditis elegans embryos. Curr. Biol. 8, 1110-1117.
48. Srinivasan, D. G., Fisk, R. M., Xu, H., and van den Heuvel, S. (2003). A complex of LIN-5 and GPR proteins regulates G protein signaling and spindle function in C. elegans. Genes Dev. 17, 1225-1239.
49. Suzuki, A. et al. (2004). aPKC acts upstream of PAR-1b in both the establishment and maintenance of mammalian epithelial polarity. Curr. Biol. 14, 1425-1435.
50. Tabara, H., Grishok, A., and Mello, C. C. (1998). RNAi in C. elegans: soaking in the genome sequence. Science 282, 430-431.
51. Tabuse, Y., Izumi, Y., Piano, F., Kemphues, K., Miwa, J., and Ohno, S. (1998). Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125, 3607-3614.
52. Timmons, L., and Fire, A. (1998). Specific interference by ingested dsRNA. Nature 395, 854.
53. Tsou, M. F., Hayashi, A., DeBella, L. R., McGrath, G., and Rose, L. S. (2002). LET-99 determines spindle position and is asymmetrically enriched in response to PAR polarity cues in C. elegans embryos. Development 129, 4469-4481.
54. Tsou, M. F., Hayashi, A., and Rose, L. S. (2003a). LET-99 opposes Gα/GPR signaling to generate asymmetry for spindle positioning in response to PAR and MES-1/SRC-1 signaling. Development 130, 5717-5730.
55. Tsou, M.F.B., Ku, W., Hayashi, A., and Rose, L. S. (2003b). PAR-dependent and geometry-dependent mechanisms of spindle positioning. J. Cell Biol. 160, 845-855.
56. Watts, J. L., Morton, D. G., Bestman, J., and Kemphues, K. J. (2000). The C. elegans par-4 gene encodes a putative serine-threonine kinase required for establishing embryonic asymmetry. Development 127, 1467-1475.