A germline-specific isoform of eIF4E (IFE-1) is required for efficient translation of stored mRNAs and maturation of both oocytes and sperm

Journal of Cell Science

Volumn 122, Issue 10, 2009, Pages 1529-1539

  Henderson, Melissa A ^a   Croniand, Elizabeth ^a   Dunkelbarger, Steve ^b   Contreras, Vince ^a   Strome, Susan ^b   Keiper, Brett D ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CED 4 Apaf 1; Germ line; Maternal mRNAs; Meiosis; Oogenesis; Polysomes; Protein synthesis; Spermatogenesis

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; INITIATION FACTOR 4E; MESSENGER RNA; CAENORHABDITIS ELEGANS PROTEIN; ISOPROTEIN; MESSENGER RIBONUCLEOPROTEIN; RIBONUCLEOPROTEIN;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CYTOKINESIS; FERTILITY; GAMETOGENESIS; MEIOSIS; MITOSIS; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RNA TRANSLATION; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOZOON MATURATION; WILD TYPE; ANIMAL; APOPTOSIS; GENE DELETION; GENETICS; GENOTYPE; HUMAN; MALE; METABOLISM; OOCYTE; PATHOLOGY; PHENOTYPE; SPERMATOZOON; TEMPERATURE; TIME;

CAENORHABDITIS ELEGANS;

ANIMALS; APOPTOSIS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CYTOKINESIS; EUKARYOTIC INITIATION FACTOR-4E; FERTILITY; GENOTYPE; HUMANS; MALE; MEIOSIS; MITOSIS; OOCYTES; OOGENESIS; PHENOTYPE; PROTEIN BIOSYNTHESIS; PROTEIN ISOFORMS; RIBONUCLEOPROTEINS; RNA, MESSENGER; SEQUENCE DELETION; SPERM-OVUM INTERACTIONS; SPERMATOGENESIS; SPERMATOZOA; TEMPERATURE; TIME FACTORS;

EID: 67649988022     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.046771     Document Type: Article

References (57)

1. Amiri, A., Keiper, B. D., Kawasaki, I., Fan, Y., Kohara, Y., Rhoads, R. E. and Strome, S. (2001). An isoform of eIF4E is a component of germ granules and is required for spermatogenesis in C. elegans. Development 128, 3899-3912.
2. Arama, E., Agapite, J. and Steller, H. (2003). Caspase activity and a specific cytochrome C are required for sperm differentiation in Drosophila. Dev. Cell 4, 687-697.
3. Baker, C. C. and Fuller, M. T. (2007). Translational control of meiotic cell cycle progression and spermatid differentiation in male germ cells by a novel eIF4G homolog. Development 134, 2863-2869.
4. Barnard, D. C., Cao, Q. and Richter, J. D. (2005). Differential phosphorylation controls Maskin association with eukaryotic translation initiation factor 4E and localization on the mitotic apparatus. Mol. Cell. Biol. 25, 7605-7615.
5. Baum, J. S., St George, J. P. and McCall, K. (2005). Programmed cell death in the germline. Semin. Cell Dev. Biol. 16, 245-259.
6. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-74.
7. Cagan, R. L. (2003). Spermatogenesis: borrowing the apoptotic machinery. Curr. Biol. 13, R600-R602.
8. Contreras, V., Richardson, M. A., Hao, E. and Keiper, B. D. (2008). Depletion of the cap-associated isoform of translation factor eIF4G induces germline apoptosis in C. elegans. Cell Death Differ. 15, 1232-1242.
9. Crittenden, S. L., Eckmann, C. R., Wang, L., Bernstein, D. S., Wickens, M. and Kimble, J. (2003). Regulation of the mitosis/meiosis decision in the Caenorhabditis elegans germline. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 1359-1362.
10. Curtis, D., Lehmann, R. and Zamore, P. D. (1995). Translational regulation in development. Cell 81, 171-178.
11. Dahanukar, A., Walker, J. A. and Wharton, R. P. (1999). Smaug, a novel RNA-binding protein that operates a translational switch in Drosophila. Mol. Cell 4, 209-218.
12. 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.
13. Dinkova, T. D., Keiper, B. D., Korneeva, N. L., Aamodt, E. J. and Rhoads, R. E. (2005). Translation of a small subset of Caenorhabditis elegans mRNAs is dependent on a specific eukaryotic translation initiation factor 4E isoform. Mol. Cell. Biol. 25, 100-113.
14. Edgar, L. G. (1995). Blastomere culture and analysis. Methods Cell Biol. 48, 303-321.
15. Edgley, M. K., Baillie, D. L., Riddle, D. L. and Rose, A. M. (2006). Genetic balancers. In WormBook (ed. The C. elegans Research Community): WormBook.
16. Evans, T. C., Crittenden, S. L., Kodoyianni, V. and Kimble, J. (1994). Translational control of maternal glp-1 mRNA establishes an asymmetry in the C. elegans embryo. Cell 77, 183-194.
17. Evsikov, A. V., Graber, J. H., Brockman, J. M., Hampl, A., Holbrook, A. E., Singh, P., Eppig, J. J., Solter, D. and Knowles, B. B. (2006). Cracking the egg: molecular dynamics and evolutionary aspects of the transition from the fully grown oocyte to embryo. Genes Dev. 20, 2713-2727.
18. Franklin-Dumont, T. M., Chatterjee, C., Wasserman, S. A. and Dinardo, S. (2007). A novel eIF4G homolog, Off-schedule, couples translational control to meiosis and differentiation in Drosophila spermatocytes. Development 134, 2851-2861.
19. Gingras, A.-C., Raught, B. and Sonenberg, N. (1999). eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68, 913-963.
20. Goodwin, E. B. and Evans, T. C. (1997). Translational control of development in C. elegans. Semin. Cell. Dev. Biol. 8, 551-559.
21. Guedes, S. and Priess, J. R. (1997). The C. elegans MEX-1 protein is present in germline blastomeres and is a P granule component. Development 124, 731-739.
22. Gumienny, T. L., Lambie, E., Hartwieg, E., Horvitz, H. R. and Hengartner, M. O. (1999). Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126, 1011-1022.
23. Honarpour, N., Du, C., Richardson, J. A., Hammer, R. E., Wang, X. and Herz, J. (2000). Adult Apaf-1-deficient mice exhibit male infertility. Dev. Biol. 218, 248-258.
24. Huh, J. R., Vernooy, S. Y., Yu, H., Yan, N., Shi, Y., Guo, M. and Hay, B. A. (2004). Multiple apoptotic caspase cascades are required in nonapoptotic roles for Drosophila spermatid individualization. PLoS Biol. 2, E15.
25. Hunter, C. P. and Kenyon, C. (1996). Spatial and temporal controls target pal-1 blastomere-specification activity to a single blastomere lineage in C. elegans embryos. Cell 87, 217-226.
26. Jud, M., Razelun, J., Bickel, J., Czerwinski, M. and Schisa, J. A. (2007). Conservation of large foci formation in arrested oocytes of Caenorhabditis nematodes. Dev. Genes Evol. 217, 221-226.
27. Jud, M. C., Czerwinski, M. J., Wood, M. P., Young, R. A., Gallo, C. M., Bickel, J. S., Petty, E. L., Mason, J. M., Little, B. A., Padilla, P. A. et al. (2008). Large P body-like RNPs form in C. elegans oocytes in response to arrested ovulation, heat shock, osmotic stress, and anoxia and are regulated by the major sperm protein pathway. Dev. Biol. 318, 38-51.
28. Keiper, B. D., Lamphear, B. J., Deshpande, A. M., Jankowska-Anyszka, M., Aamodt, E. J., Blumenthal, T. and Rhoads, R. E. (2000). Functional characterization of five eIF4E isoforms in Caenorhabditis elegans. J. Biol. Chem. 275, 10590-10596.
29. Kimble, J. and Crittenden, S. L. (2007). Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu. Rev. Cell Dev. Biol. 23, 405-433.
30. Kimble, J., Edgar, L. and Hirsh, D. (1984). Specification of male development in Caenorhabditis elegans: the fem genes. Dev. Biol. 105, 234-239.
31. L'Hernault, S. W. (2006). Spermatogenesis. In WormBook (ed. The C. elegans Research Community): WormBook.
32. Luitjens, C., Gallegos, M., Kraemer, B., Kimble, J. and Wickens, M. (2000). CPEB proteins control two key steps in spermatogenesis in C. elegans. Genes Dev. 14, 2596-2609.
33. Macdonald, P. M. and Smibert, C. A. (1996). Translational regulation of maternal mRNAs. Curr. Opin. Genet. Dev. 6, 403-407.
34. Mendez, R. and Richter, J. D. (2001). Translational control by CPEB: a means to the end. Nat. Rev. Mol. Cell. Biol. 2, 521-529.
35. Miller, M. A., Nguyen, V. Q., Lee, M. H., Kosinski, M., Schedl, T., Caprioli, R. M. and Greenstein, D. (2001). A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291, 2144-2147.
36. 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.
37. Morales, J., Mulner-Lorillon, O., Cosson, B., Morin, E., Belle, R., Bradham, C. A., Beane, W. S. and Cormier, P. (2006). Translational control genes in the sea urchin genome. Dev. Biol. 300, 293-307.
38. Ogura, K., Kishimoto, N., Mitani, S., Gengyo-Ando, K. and Kohara, Y. (2003). Translational control of maternal glp-1 mRNA by POS-1 and its interacting protein SPN-4 in Caenorhabditis elegans. Development 130, 2495-2503.
39. 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.
40. Portman, D. S. (2006). Profiling C. elegans gene expression with DNA microarrays. In WormBook (ed. The C. elegans Research Community): WormBook.
41. Proud, C. G. (2006). Regulation of protein synthesis by insulin. Biochem. Soc. Trans. 34, 213-216.
42. Richter, J. D. (1991). Translational control during early development. BioEssays 13, 179-183.
43. Richter, J. D. (2007). CPEB: a life in translation. Trends Biochem. Sci. 32, 279-285.
44. Robalino, J., Joshi, B., Fahrenkrug, S. C. and Jagus, R. (2004). Two zebrafish eIF4E family members are differentially expressed and functionally divergent. J. Biol. Chem. 279, 10532-10541.
45. Rodriguez, C. M., Freire, M. A., Camilleri, C. and Robaglia, C. (1998). The Arabidopsis thaliana cDNAs coding for eIF4E and eIF(iso)4E are not functionally equivalent for yeast complementation and are differentially expressed during plant development. Plant J. 13, 465-473.
46. 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.
47. Seydoux, G. and Strome, S. (1999). Launching the germline in Caenorhabditis elegans: regulation of gene expression in early germ cells. Development 126, 3275-3283.
48. Shimada, M., Yokosawa, H. and Kawahara, H. (2006). OMA-1 is a P granules-associated protein that is required for germline specification in Caenorhabditis elegans embryos. Genes Cells 11, 383-396.
49. Syntichaki, P., Troulinaki, K. and Tavernarakis, N. (2007). eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans. Nature 445, 922-926.
50. Tabara, H., Hill, R. J., Mello, C. C., Priess, J. R. and Kohara, Y. (1999). pos-1 encodes a cytoplasmic zinc-finger protein essential for germline specification in C. elegans. Development 126, 1-11.
51. Tadros, W. and Lipshitz, H. D. (2005). Setting the stage for development: mRNA translation and stability during oocyte maturation and egg activation in Drosophila. Dev. Dyn. 232, 593-608.
52. Wickens, M., Anderson, P. and Jackson, R. J. (1997). Life and death in the cytoplasm: messages from the 3′ end. Curr. Opin. Genet. Dev. 7, 220-232.
53. Wilhelm, J. E. and Smibert, C. A. (2005). Mechanisms of translational regulation in Drosophila. Biol. Cell 97, 235-252.
54. Yamamoto, I., Kosinski, M. E. and Greenstein, D. (2006). Start me up: cell signaling and the journey from oocyte to embryo in C. elegans. Dev. Dyn. 235, 571-585.
55. Yu, X., Vought, V. E., Conradt, B. and Maine, E. M. (2006). Eukaryotic translation initiation factor 5B activity regulates larval growth rate and germline development in Caenorhabditis elegans. Genesis 44, 412-418.
56. Zannoni, S., L'Hernault, S. W. and Singson, A. W. (2003). Dynamic localization of SPE-9 in sperm: a protein required for sperm-oocyte interactions in Caenorhabditis elegans. BMC Dev. Biol. 3, 10-15.
57. Zhou, Z., Hartwieg, E. and Horvitz, H. R. (2001). CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104, 43-56.