Ifet-1 is a broad-scale translational repressor required for normal P granule formation in C. elegans

Journal of Cell Science

Volumn 126, Issue 3, 2013, Pages 850-859

  Sengupta, Madhu S ^a   Low, Wai Yee ^a   Patterson, Joseph R ^b   Kim, Hyun Min ^c   Traven, Ana ^a   Beilharz, Traude H ^a   Colaiácovo, Monica P ^b   Schisa, Jennifer A ^b   Boag, Peter R ^a  

^a MONASH UNIVERSITY   (Australia)

^b CENTRAL MICHIGAN UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Caenorhabditis elegans; Eif4E transporter; Germ granules; P granule; Translational regulation

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; IFET 1 PROTEIN; INITIATION FACTOR 4E; MESSENGER RNA; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL LINEAGE; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GERM CELL; GONAD; GRANULE CELL; NONHUMAN; OOCYTE DEVELOPMENT; P GRANULE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SEX DETERMINATION; SPERMATOGENESIS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELLS, CULTURED; CYTOPLASMIC GRANULES; EUKARYOTIC INITIATION FACTOR-4E; GERM CELLS; MUTATION; NUCLEAR PORE; OOGENESIS; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; REPRESSOR PROTEINS; RNA NUCLEOTIDYLTRANSFERASES; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SEX DETERMINATION PROCESSES;

CAENORHABDITIS ELEGANS;

EID: 84876337731     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.119834     Document Type: Article

References (54)

1. Andrei, M. A., Ingelfinger, D., Heintzmann, R., Achsel, T., Rivera-Pomar, R. and Lührmann, R. (2005). A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA 11, 717-727.
2. Audhya, A., Hyndman, F., McLeod, I. X., Maddox, A. S., Yates, J. R., 3rd, Desai, A. and Oegema, K. (2005). A complex containing the Sm protein CAR-1 and the RNA helicase CGH-1 is required for embryonic cytokinesis in Caenorhabditis elegans. J. Cell Biol. 171, 267-279.
3. Boag, P. R., Nakamura, A. and Blackwell, T. K. (2005). A conserved RNA-protein complex component involved in physiological germline apoptosis regulation in C. elegans. Development 132, 4975-4986.
4. Boag, P. R., Atalay, A., Robida, S., Reinke, V. and Blackwell, T. K. (2008). Protection of specific maternal messenger RNAs by the P body protein CGH-1 (Dhh1/ RCK) during Caenorhabditis elegans oogenesis. J. Cell Biol. 182, 543-557.
5. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
6. Cao, Q. and Richter, J. D. (2002). Dissolution of the maskin-eIF4E complex by cytoplasmic polyadenylation and poly(A)-binding protein controls cyclin B1 mRNA translation and oocyte maturation. EMBO J. 21, 3852-3862.
7. Coller, J. and Parker, R. (2005). General translational repression by activators of mRNA decapping. Cell 122, 875-886.
8. Culjkovic, B., Topisirovic, I., Skrabanek, L., Ruiz-Gutierrez, M. and Borden, K. L. (2005). eIF4E promotes nuclear export of cyclin D1 mRNAs via an element in the 39UTR. J. Cell Biol. 169, 245-256.
9. Detwiler, M. R., Reuben, M., Li, X., Rogers, E. and Lin, R. (2001). Two zinc finger proteins, OMA-1 and OMA-2, are redundantly required for oocyte maturation in C. elegans. Dev. Cell 1, 187-199.
10. Dostie, J., Ferraiuolo, M., Pause, A., Adam, S. A. and Sonenberg, N. (2000). A novel shuttling protein, 4E-T, mediates the nuclear import of the mRNA 59 cap-binding protein, eIF4E. EMBO J. 19, 3142-3156.
11. Ellis, R. E. (2008). Sex determination in the Caenorhabditis elegans germ line. Curr. Top. Dev. Biol. 83, 41-64.
12. Ferraiuolo, M. A., Basak, S., Dostie, J., Murray, E. L., Schoenberg, D. R. and Sonenberg, N. (2005). A role for the eIF4E-binding protein 4E-T in P-body formation and mRNA decay. J. Cell Biol. 170, 913-924.
13. Garneau, N. L., Wilusz, J. and Wilusz, C. J. (2007). The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 8, 113-126.
14. Goldstrohm, A. C. and Wickens, M. (2008). Multifunctional deadenylase complexes diversify mRNA control. Nat. Rev. Mol. Cell Biol. 9, 337-344.
15. Gruidl, M. E., Smith, P. A., Kuznicki, K. A., McCrone, J. S., Kirchner, J., Roussell, D. L., Strome, S. and Bennett, K. L. (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.
16. Guven-Ozkan, T., Robertson, S. M., Nishi, Y. and Lin, R. (2010). zif-1 translational repression defines a second, mutually exclusive OMA function in germline transcriptional repression. Development 137, 3373-3382.
17. Igreja, C. and Izaurralde, E. (2011). CUP promotes deadenylation and inhibits decapping of mRNA targets. Genes Dev. 25, 1955-1967.
18. Jänicke, A., Vancuylenberg, J., Boag, P. R., Traven, A. and Beilharz, T. H. (2012). ePAT: a simple method to tag adenylated RNA to measure poly(A)-tail length and other 39 RACE applications. RNA 18, 1289-1295.
19. Kamath, R. S. and Ahringer, J. (2003). Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313-321.
20. Kawasaki, I., Shim, Y. H., Kirchner, J., Kaminker, J., Wood, W. B. and Strome, S. (1998). PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell 94, 635-645.
21. Kim, K. W., Wilson, T. L. and Kimble, J. (2010). GLD-2/RNP-8 cytoplasmic poly(A) polymerase is a broad-spectrum regulator of the oogenesis program. Proc. Natl. Acad. Sci. USA 107, 17445-17450.
22. la Cour, T., Kiemer, L., Mølgaard, A., Gupta, R., Skriver, K. and Brunak, S. (2004). Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 17, 527-536.
23. Li, W., DeBella, L. R., Guven-Ozkan, T., Lin, R. and Rose, L. S. (2009). An eIF4Ebinding protein regulates katanin protein levels in C. elegans embryos. J. Cell Biol. 187, 33-42.
24. Matsumoto, K., Kwon, O. Y., Kim, H. and Akao, Y. (2005). Expression of rck/p54, a DEAD-box RNA helicase, in gametogenesis and early embryogenesis of mice. Dev. Dyn. 233, 1149-1156.
25. Merritt, C., Rasoloson, D., Ko, D. and Seydoux, G. (2008). 39 UTRs are the primary regulators of gene expression in the C. elegans germline. Curr. Biol. 18, 1476-1482. Minshall, N., Reiter, M. H., Weil, D. and Standart, N. (2007). CPEB interacts with an ovary-specific eIF4E and 4E-T in early Xenopus oocytes. J. Biol. Chem. 282, 37389- 37401.
26. Minshall, N., Reiter, M. H., Weil, D. and Standart, N. (2007). CPEB interacts with an ovary-specific eIF4E and 4E-T in early Xenopus oocytes. J. Biol. Chem. 282, 37389- 37401.
27. Nabeshima, K., Villeneuve, A. M. and Colaiácovo, M. P. (2005). Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J. Cell Biol. 168, 683-689.
28. Nakai, K. and Horton, P. (1999). PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 24, 34-35. Nakamura, A., Amikura, R., Hanyu, K. and Kobayashi, S. (2001). Me31B silences translation of oocyte-localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis. Development 128, 3233-3242.
29. Nakamura, A., Amikura, R., Hanyu, K. and Kobayashi, S. (2001). Me31B silences translation of oocyte-localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis. Development 128, 3233-3242.
30. Nakamura, A., Sato, K. and Hanyu-Nakamura, K. (2004). Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev. Cell 6, 69-78.
31. Navarro, R. E., Shim, E. Y., Kohara, Y., Singson, A. and Blackwell, T. K. (2001). cgh-1, a conserved predicted RNA helicase required for gametogenesis and protection from physiological germline apoptosis in C. elegans. Development 128, 3221-3232.
32. Nelson, M. R., Leidal, A. M. and Smibert, C. A. (2004). Drosophila Cup is an eIF4Ebinding protein that functions in Smaug-mediated translational repression. EMBO J. 23, 150-159.
33. Nissan, T., Rajyaguru, P., She, M., Song, H. and Parker, R. (2010). Decapping activators in Saccharomyces cerevisiae act by multiple mechanisms. Mol. Cell 39, 773-783.
34. Parker, R. and Sheth, U. (2007). P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635-646.
35. Paynton, B. V. (1998). RNA-binding proteins in mouse oocytes and embryos: expression of genes encoding Y box, DEAD box RNA helicase, and polyA binding proteins. Dev. Genet. 23, 285-298.
36. Pepling, M. E., Wilhelm, J. E., O'Hara, A. L., Gephardt, G. W. and Spradling, A. C. (2007). Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body. Proc. Natl. Acad. Sci. USA 104, 187-192.
37. Pitt, J. N., Schisa, J. A. and Priess, J. R. (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.
38. Reinke, V., Gil, I. S., Ward, S. and Kazmer, K. (2004). Genome-wide germlineenriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131, 311-323.
39. Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-212.
40. Rong, L., Livingstone, M., Sukarieh, R., Petroulakis, E., Gingras, A. C., Crosby, K., Smith, B., Polakiewicz, R. D., Pelletier, J., Ferraiuolo, M. A. et al. (2008). Control of eIF4E cellular localization by eIF4E-binding proteins, 4E-BPs. RNA 14, 1318- 1327.
41. Schisa, J. A., Pitt, J. N. and Priess, J. R. (2001). Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development 128, 1287-1298.
42. Sheth, U. and Parker, R. (2003). Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300, 805-808.
43. Sheth, U., Pitt, J., Dennis, S. and Priess, J. R. (2010). Perinuclear P granules are the principal sites of mRNA export in adult C. elegans germ cells. Development 137, 1305-1314.
44. Sonenberg, N. and Hinnebusch, A. G. (2009). Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745.
45. Spike, C., Meyer, N., Racen, E., Orsborn, A., Kirchner, J., Kuznicki, K., Yee, C., Bennett, K. and Strome, S. (2008). Genetic analysis of the Caenorhabditis elegans GLH family of P-granule proteins. Genetics 178, 1973-1987.
46. Spurr, A. R. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31-43.
47. Strome, S. and Lehmann, R. (2007). Germ versus soma decisions: lessons from flies and worms. Science 316, 392-393.
48. Strome, S. and Wood, W. B. (1983). Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell 35, 15-25.
49. Updike, D. L. and Strome, S. (2009). A genomewide RNAi screen for genes that affect the stability, distribution and function of P granules in Caenorhabditis elegans. Genetics 183, 1397-1419.
50. Updike, D. L., Hachey, S. J., Kreher, J. and Strome, S. (2011). P granules extend the nuclear pore complex environment in the C. elegans germ line. J. Cell Biol. 192, 939- 948.
51. Villaescusa, J. C., Allard, P., Carminati, E., Kontogiannea, M., Talarico, D., Blasi, F., Farookhi, R. and Verrotti, A. C. (2006). Clast4, the murine homologue of human eIF4E-Transporter, is highly expressed in developing oocytes and post-translationally modified at meiotic maturation. Gene 367, 101-109.
52. Voronina, E., Seydoux, G., Sassone-Corsi, P. and Nagamori, I. (2011). RNA granules in germ cells. Cold Spring Harb. Perspect. Biol. 3, a002774.
53. Wilhelm, J. E., Hilton, M., Amos, Q. and Henzel, W. J. (2003). Cup is an eIF4E binding protein required for both the translational repression of oskar and the recruitment of Barentsz. J. Cell Biol. 163, 1197-1204.
54. Zappavigna, V., Piccioni, F., Villaescusa, J. C. and Verrotti, A. C. (2004). Cup is a nucleocytoplasmic shuttling protein that interacts with the eukaryotic translation initiation factor 4E to modulate Drosophila ovary development. Proc. Natl. Acad. Sci. USA 101, 14800-14805.