A genomewide screen for suppressors of par-2 uncovers potential regulators of PAR protein-dependent cell polarity in Caenorhabditis elegans

Genetics

Volumn 174, Issue 1, 2006, Pages 285-295

  Labbé, Jean Claude ^a,b   Pacquelet, Anne ^a,c   Marty, Thomas ^a,c   Gotta, Monica ^a  

^a ETH ZURICH   (Switzerland)

^b INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINASE ACTIVATED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 2;

ARTICLE; CAENORHABDITIS ELEGANS; CELL POLARITY; CONTROLLED STUDY; GENE; GENE FUNCTION; GENE REPRESSION; GENOME ANALYSIS; NONHUMAN; NOS 3 GENE; PRIORITY JOURNAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL POLARITY; CHROMOSOME MAPPING; DISORDERS OF SEX DEVELOPMENT; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, LETHAL; GENES, SUPPRESSOR; HERMAPHRODITISM; MALE; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SUPPRESSION, GENETIC; TISSUE DISTRIBUTION;

ANIMALIA; CAENORHABDITIS ELEGANS; DROSOPHILA NANOS;

EID: 33748908963     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.106.060517     Document Type: Article

References (53)

1. BETSCHINGER, J., and J. A. KNOBLICH, 2004 Dare to be different: asymmetric cell division in Drosophila, C. elegans and vertebrates. Curr. Biol. 14: R674-R685.
2. BOYD, L., S. GUO, D. LEVITAN, D. T. STINCHCOMB and K. J. KEMPHUES, 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.
3. BRENNER, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
4. CHEEKS, R. J., J. C. CANMAN, W. N. GABRIEL, N. MEYER, S. STROME et al., 2004 C. elegans PAR proteins function by mobilizing and stabilizing asymmetrically localized protein complexes. Curr. Biol. 14: 851-862.
5. COX, D. N., S. A. SEYFRIED, L. Y. JAN and Y. N. JAN, 2001 Bazooka and atypical protein kinase C are required to regulate oocyte differentiation in the Drosophila ovary. Proc. Natl. Acad. Sci. USA 98: 14475-14480.
6. CRITTENDEN, S. L., D. S. BERNSTEIN, J. L. BACHORIK, B. E. THOMPSON, M. GALLEGOS et al., 2002 A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417: 660-663.
7. CUENCA, A. A., A. SCHETTER, D. ACETO, K. KEMPHUES and G. SEYDOUX, 2003 Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 130: 1255-1265.
8. DAVY, A., P. BELLO, N. THIERRY-MIEG, P. VAGLIO, J. HITTI et al., 2001 A protein-protein interaction map of the Caenorhabditis elegans 26S proteasome. EMBO Rep. 2: 821-828.
9. EDGAR, L. G., 1995 Blastomere culture and analysis. Methods Cell Biol. 48: 303-321.
10. ETEMAD-MOGHADAM, B., S. GUO and K. J. KEMPHUES, 1995 Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell 83: 743-752.
11. ETIENNE-MANNEVILLE, S., and A. HALL, 2001 Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCζ. Cell 106: 489-498.
12. ETIENNE-MANNEVILLE, S., and A. HALL, 2003 Cell polarity: Par6, aPKC and cytoskeletal crosstalk. Curr. Opin. Cell Biol. 15: 67-72.
13. FIRE, A., S. XU, M. K. MONTGOMERY, S. A. KOSTAS, S. E. DRIVER et al., 1998 Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811.
14. FORMAN, M. S., J. Q. TROJANOWSKI and V. M. LEE, 2004 Neurodegenerative diseases: a decade of discoveries paves the way for therapeutic breakthroughs. Nat. Med. 10: 1055-1063.
15. GLICKMAN, M. H., and A. CIECHANOVER, 2002 The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82: 373-428.
16. GONCZY, P., J. M. BELLANGER, M. KIRKHAM, A. POZNIAKOWSKI, K. BAUMER et al., 2001 zyg-8, a gene required for spindle positioning in C. elegans, encodes a doublecortin-related kinase that promotes microtubule assembly. Dev. Cell 1: 363-375.
17. GOTTA, M., M. C. ABRAHAM and J. AHRINGER, 2001 CDC-42 controls early cell polarity and spindle orientation in C. elegans. Curr. Biol. 11: 482-488.
18. GREENSTEIN, D., S. HIRD, R. H. PLASTERK, Y. ANDACHI, Y. KOHARA et al., 1994 Targeted mutations in the Caenorhabditis elegans POU homeo box gene ceh-18 cause defects in oocyte cell cycle arrest, gonad migration, and epidermal differentiation. Genes Dev. 8: 1935-1948.
19. GUO, S., and K. J. KEMPHUES, 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.
20. HANSEN, D., L. WILSON-BERRY, T. DANG and T. SCHEDL, 2004 Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 131: 93-104.
21. HAO, Y., L. BOYD and G. SEYDOUX, 2006 Stabilization of cell polarity by the C. elegans RING protein PAR-2. Dev. Cell 10: 199-208.
22. HULSKAMP, M., C. SCHRODER, C. PFEIFLE, H. JACKLE and D. TAUTZ, 1989 Posterior segmentation of the Drosophila embryo in the absence of a maternal posterior organizer gene. Nature 338: 629-632.
23. HUNG, T. J., and K. J. KEMPHUES, 1999 PAR-6 is a conserved PDZ domain-containing protein that colocalizes with PAR-3 in Caenorhabditis elegans embryos. Development 126: 127-135.
24. HURD, T. W., L. GAO, M. H. ROH, I. G. MACARA and B. MARGOLIS, 2003 Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat. Cell Biol. 5: 137-142.
25. HUROV, J. B., J. L. WATKINS and H. PIWNICA-WORMS, 2004 Atypical PKC phosphorylates PAR-1 kinases to regulate localization and activity. Curr. Biol. 14: 736-741.
26. HUYNH, J. R., M. PETRONCZKI, J. A. KNOBLICH and D. ST JOHNSTON, 2001 Bazooka and PAR-6 are required with PAR-1 for the maintenance of oocyte fate in Drosophila. Curr. Biol. 11: 901-906.
27. IRISH, V., R. LEHMANN and M. AKAM, 1989 The Drosophila posterior-group gene nanos functions by repressing hunchback activity. Nature 338: 646-648.
28. KAMATH, R. S., A. G. FRASER, Y. DONG, G. POULIN, R. DURBIN et al., 2003 Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237.
29. KAWASAKI, I., A. AMIRI, Y. FAN, N. MEYER, S. DUNKELBARGER et al., 2004 The PGL family proteins associate with germ granules and function redundantly in Caenorhabditis elegans germline development. Genetics 167: 645-661.
30. KEMPHUES, K., and S. STROME, 1997 Fertilization and establishment of polarity in the embryo, pp. 335-359 in C. elegans II, edited by D. L. RIDDLE, T. BLUMENTHAL, B. J. MEYER and J. R. PRIESS. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. KRAEMER, B., S. CRITTENDEN, M. GALLEGOS, G. MOULDER, R. BARSTEAD et al., 1999 NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans. Curr. Biol. 9: 1009-1018.
32. LEVITAN, D. J., L. BOYD, C. C. MELLO, K. J. KEMPHUES and D. T. STINCHCOMB, 1994 par-2, a gene required for blastomere asymmetry in Caenorhabditis elegans, encodes zinc-finger and ATP-binding motifs. Proc. Natl. Acad. Sci. USA 91: 6108-6112.
33. LIN, D., A. S. EDWARDS, J. P. FAWCETT, G. MBAMALU, J. D. SCOTT et al., 2000 A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat. Cell Biol. 2: 540-547.
34. MACARA, I. G., 2004 Parsing the polarity code. Nat. Rev. Mol. Cell Biol. 5: 220-231.
35. MICHELITSCH, M. D., and J. S. WEISSMAN, 2000 A census of glutamine/asparagine-rich regions: implications for their conserved function and the prediction of novel prions. Proc. Natl. Acad. Sci. USA 97: 11910-11915.
36. MILLER, M. A., P. J. RUEST, M. KOSINSKI, S. K. HANKS and D. GREENSTEIN, 2003 An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans. Genes Dev. 17: 187-200.
37. NAKAHATA, S., T. KOTANI, K. MITA, T. KAWASAKI, Y. KATSU et al., 2003 Involvement of Xenopus Pumilio in the translational regulation that is specific to cyclin B1 mRNA during oocyte maturation. Mech. Dev. 120: 865-880.
38. NANCE, J., 2005 PAR proteins and the establishment of cell polarity during C. elegans development. BioEssays 27: 126-135.
39. PETROSKI, M. D., and R. J. DESHAIES, 2005 Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6: 9-20.
40. QIU, R. G., A. ABO and G. STEVEN MARTIN, 2000 A human homolog of the C. elegans polarity determinant Par-6 links Rac and Cdc42 to PKCzeta signaling and cell transformation. Curr. Biol. 10: 697-707.
41. ROEGIERS, F., and Y. N. JAN, 2004 Asymmetric cell division. Curr. Opin. Cell Biol. 16: 195-205.
42. SHI, S. H., L. Y. JAN and Y. N. JAN, 2003 Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112: 63-75.
43. SONNICHSEN, B., L. B. KOSKI, A. WALSH, P. MARSCHALL, B. NEUMANN et al., 2005 Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434: 462-469.
44. SONODA, J., and R. P. WHARTON, 2001 Drosophila Brain Tumor is a translational repressor. Genes Dev. 15: 762-773.
45. SUBRAMANIAM, K., and G. SEYDOUX, 1999 nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans. Development 126: 4861-4871.
46. TABUSE, Y., Y. IZUMI, F. PIANO, K. J. KEMPHUES, J. MIWA et al., 1998 Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125: 3607-3614.
47. TAKAHASHI, M., H. IWASAKI, H. INOUE and K. TAKAHASHI, 2002 Reverse genetic analysis of the Caenorhabditis elegans 26S proteasome subunits by RNA interference. Biol. Chem. 383: 1263-1266.
48. WATTS, J. L., and J. BROWSE, 2002 Genetic dissection of polyunsaturated fatty acid synthesis in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 99: 5854-5859.
49. WATTS, J. L., B. ETEMAD-MOGHADAM, S. GUO, L. BOYD, B. W. DRAPER et al., 1996 par-6, a gene involved in the establishment of asymmetry in early C. elegans embryos, mediates the asymmetric localization of PAR-3. Development 122: 3133-3140.
50. WICKENS, M., D. S. BERNSTEIN, J. KIMBLE and R. PARKER, 2002 A PUF family portrait: 3′UTR regulation as a way of life. Trends Genet. 18: 150-157.
51. WILHELM, J. E., and C. A. SMIBERT, 2005 Mechanisms of translational regulation in Drosophila. Biol. Cell. 97: 235-252.
52. WILKINSON, C. R., K. FERRELL, M. PENNEY, M. WALLACE, W. DUBIEL et al., 2000 Analysis of a gene encoding Rpn10 of the fission yeast proteasome reveals that the polyubiquitin-binding site of this subunit is essential when Rpn12/Mts3 activity is compromised. J. Biol. Chem. 275: 15182-15192.
53. ZHANG, B., M. GALLEGOS, A. PUOTI, E. DURKIN, S. FIELDS et al., 1997 A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 390: 477-484.