P granules extend the nuclear pore complex environment in the C. elegans germ line

Journal of Cell Biology

Volumn 192, Issue 6, 2011, Pages 939-948

  Updike, Dustin L ^a   Hachey, Stephanie J ^a   Kreher, Jeremy ^a   Strome, Susan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLH1 PROTEIN; GLH2 PROTEIN; GLH4 PROTEIN; GLYCINE; PHENYLALANINE; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL NUCLEUS; CELL STRUCTURE; CONCENTRATION (PARAMETERS); GERM LINE; HYDROPHOBICITY; INTESTINE; NONHUMAN; NUCLEAR PORE COMPLEX; P GRANULE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CYTOPLASMIC GRANULES; DEAD-BOX RNA HELICASES; GERM CELLS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; RNA-BINDING PROTEINS;

CAENORHABDITIS ELEGANS;

EID: 79955497151     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201010104     Document Type: Article

References (44)

1. Amiri, A., B.D. Keiper, I. Kawasaki, Y. Fan, Y. Kohara, R.E. Rhoads, S. Strome. 2001. An isoform of eIF4E is a component of germ granules and is required for spermatogenesis in C. elegans. Development. 128:3899-3912.
2. Aoyama, J., Y. Nakayama, D. Sugiyama, S. Saburi, D. Nadano, M.N. Fukuda, N. Yamaguchi. 2005. Apical cell adhesion molecule, trophinin, localizes to the nuclear envelope. FEBS Lett. 579:6326-6332.
3. Batista, P.J., J.G. Ruby, J.M. Claycomb, R. Chiang, N. Fahlgren, K.D. Kasschau, D.A. Chaves, W. Gu, J.J. Vasale, S. Duan, et al. 2008. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol. Cell. 31:67-78.
4. Blobel, G. 1985. Gene gating: a hypothesis. Proc. Natl. Acad. Sci. USA. 82:8527-8529.
5. Bontems, F., A. Stein, F. Marlow, J. Lyautey, T. Gupta, M.C. Mullins, R. Dosch. 2009. Bucky ball organizes germ plasm assembly in zebrafish. Curr. Biol. 19:414-422.
6. Brangwynne, C.P., C.R. Eckmann, D.S. Courson, A. Rybarska, C. Hoege, J. Gharakhani, F. Jülicher, A.A. Hyman. 2009. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science. 324:1729-1732.
7. Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics. 77:71-94.
8. Cheeks, R.J., J.C. Canman, W.N. Gabriel, N. Meyer, S. Strome, B. Goldstein. 2004. C. elegans PAR proteins function by mobilizing and stabilizing asymmetrically localized protein complexes. Curr. Biol. 14:851-862.
9. Chuma, S., M. Hosokawa, T. Tanaka, N. Nakatsuji. 2009. Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: germinal granules in mammals. Mol. Cell. Endocrinol. 306:17-23.
10. Claycomb, J.M., P.J. Batista, K.M. Pang, W. Gu, J.J. Vasale, J.C. van Wolfswinkel, D.A. Chaves, M. Shirayama, S. Mitani, R.F. Ketting, et al. 2009. The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell. 139:123-134.
11. Conine, C.C., P.J. Batista, W. Gu, J.M. Claycomb, D.A. Chaves, M. Shirayama, C.C. Mello. 2010. Argonautes ALG-3 and ALG-4 are required for spermatogenesis-specific 26G-RNAs and thermotolerant sperm in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 107:3588-3593.
12. Coustham, V., C. Bedet, K. Monier, S. Schott, M. Karali, F. Palladino. 2006. The C. elegans HP1 homologue HPL-2 and the LIN-13 zinc finger protein form a complex implicated in vulval development. Dev. Biol. 297:308-322.
13. DeRenzo, C., K.J. Reese, G. Seydoux. 2003. Exclusion of germ plasm proteins from somatic lineages by cullin-dependent degradation. Nature. 424:685-689.
14. Eddy, E.M. 1975. Germ plasm and the differentiation of the germ cell line. Int. Rev. Cytol. 43:229-280.
15. Ephrussi, A., R. Lehmann. 1992. Induction of germ cell formation by oskar. Nature. 358:387-392.
16. Eulalio, A., F. Tritschler, E. Izaurralde. 2009. The GW182 protein family in animal cells: new insights into domains required for miRNA-mediated gene silencing. RNA. 15:1433-1442.
17. Extavour, C.G., M. Akam. 2003. Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development. 130:5869-5884.
18. Galy, V., I.W. Mattaj, P. Askjaer. 2003. Caenorhabditis elegans nucleoporins Nup93 and Nup205 determine the limit of nuclear pore complex size exclusion in vivo. Mol. Biol. Cell. 14:5104-5115.
19. Gruidl, M.E., P.A. Smith, K.A. Kuznicki, J.S. McCrone, J. Kirchner, D.L. Roussell, S. Strome, K.L. Bennett. 1996. Multiple potential germ-line helicases are components of the germ-line-specific P granules of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 93:13837-13842.
20. Gu, W., M. Shirayama, D. Conte Jr, J. Vasale, P.J. Batista, J.M. Claycomb, J.J. Moresco, E.M. Youngman, J. Keys, M.J. Stoltz, et al. 2009. Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol. Cell. 36:231-244.
21. Hanazawa, M., Y. Masafumi, A. Sugimoto. 2011. PGL proteins self-associate and bind RNPs to mediate germ granule assembly in C. elegans. J. Cell Biol. 192:929-937.
22. Ikenishi, K., S. Nakazato, T. Okuda. 1986. Direct evidence for the presence of germ cell determinant in vegetal pole cytoplasm of Xenopus laevis and in a subcellular fraction of it. Dev. Growth Differ. 28:563-568.
23. Illmensee, K., A.P. Mahowald. 1974. Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc. Natl. Acad. Sci. USA. 71:1016-1020.
24. Kawasaki, I., A. Amiri, Y. Fan, N. Meyer, S. Dunkelbarger, T. Motohashi, T. Karashima, O. Bossinger, S. Strome. 2004. The PGL family proteins associate with germ granules and function redundantly in Caenorhabditis elegans germline development. Genetics. 167:645-661.
25. Kawasaki, I., Y.H. Shim, J. Kirchner, J. Kaminker, W.B. Wood, S. Strome. 1998. PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell. 94:635-645.
26. Kuznicki, K.A., P.A. Smith, W.M. Leung-Chiu, A.O. Estevez, H.C. Scott, K.L. Bennett. 2000. Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C. elegans. Development. 127:2907-2916.
27. Pappu, R.V., X. Wang, A. Vitalis, S.L. Crick. 2008. A polymer physics perspective on driving forces and mechanisms for protein aggregation. Arch. Biochem. Biophys. 469:132-141.
28. Patel, S.S., B.J. Belmont, J.M. Sante, M.F. Rexach. 2007. Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell. 129:83-96.
29. Peters, R. 1986. Fluorescence microphotolysis to measure nucleocytoplasmic transport and intracellular mobility. Biochim. Biophys. Acta. 864:305-359.
30. Petrella, L., W. Wang, C.A. Spike, A. Rechsteiner, V. Reinke, S. Strome. 2011. synMuvB proteins antagonize germline fate in the intestine and ensure C. elegans survival. Development. 138:1069-1079.
31. Pitt, J.N., J.A. Schisa, J.R. Priess. 2000. P granules in the germ cells of Caenorhabditis elegans adults are associated with clusters of nuclear pores and contain RNA. Dev. Biol. 219:315-333.
32. Ribbeck, K., D. Görlich. 2002. The permeability barrier of nuclear pore complexes appears to operate via hydrophobic exclusion. EMBO J. 21:2664-2671.
33. Sarov, M., S. Schneider, A. Pozniakovski, A. Roguev, S. Ernst, Y. Zhang, A.A. Hyman, A.F. Stewart. 2006. A recombineering pipeline for functional genomics applied to Caenorhabditis elegans. Nat. Methods. 3:839-844.
34. Schisa, J.A., J.N. Pitt, J.R. Priess. 2001. Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development. 128:1287-1298.
35. Sheth, U., J. Pitt, S. Dennis, J.R. Priess. 2010. Perinuclear P granules are the principal sites of mRNA export in adult C. elegans germ cells. Development. 137:1305-1314.
36. Shulga, N., D.S. Goldfarb. 2003. Binding dynamics of structural nucleoporins govern nuclear pore complex permeability and may mediate channel gating. Mol. Cell. Biol. 23:534-542.
37. Spike, C., N. Meyer, E. Racen, A. Orsborn, J. Kirchner, K. Kuznicki, C. Yee, K. Bennett, S. Strome. 2008. Genetic analysis of the Caenorhabditis elegans GLH family of P-granule proteins. Genetics. 178:1973-1987.
38. Strome, S., W.B. Wood. 1983. Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell. 35:15-25.
39. Updike, D.L., S. Strome. 2009. A genomewide RNAi screen for genes that affect the stability, distribution and function of P granules in Caenorhabditis elegans. Genetics. 183:1397-1419.
40. Updike, D.L., S. Strome. 2010. P granule assembly and function in Caenorhabditis elegans germ cells. J. Androl. 31:53-60.
41. Voronina, E., G. Seydoux. 2010. The C. elegans homolog of nucleoporin Nup98 is required for the integrity and function of germline P granules. Development. 137:1441-1450.
42. Wang, D., S. Kennedy, D. Conte Jr, J.K. Kim, H.W. Gabel, R.S. Kamath, C.C. Mello, G. Ruvkun. 2005. Somatic misexpression of germline P granules and enhanced RNA interference in retinoblastoma pathway mutants. Nature. 436:593-597.
43. Weis, K. 2007. The nuclear pore complex: oily spaghetti or gummy bear? Cell. 130:405-407.
44. Zhang, Y., L. Yan, Z. Zhou, P. Yang, E. Tian, K. Zhang, Y. Zhao, Z. Li, B. Song, J. Han, et al. 2009. SEPA-1 mediates the specific recognition and degradation of P granule components by autophagy in C. elegans. Cell. 136:308-321.