The Xenopus ELAV protein ElrB represses Vg1 mRNA translation during oogenesis

Molecular and Cellular Biology

Volumn 25, Issue 20, 2005, Pages 9028-9039

  Colegrove Otero, Lucy J ^a   Devaux, Agathe ^a   Standart, Nancy ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HUR PROTEIN; MESSENGER RNA; MONOCLONAL ANTIBODY; PROTEIN; PROTEIN ELRB; PROTEIN VG1; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; BINDING SITE; COMPLEX FORMATION; GENE EXPRESSION REGULATION; GENE REPRESSION; IMMUNOPRECIPITATION; MUTAGENESIS; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA TRANSLATION; TRANSLATION REGULATION; XENOPUS;

3' UNTRANSLATED REGIONS; ANIMALS; ANTIGENS, SURFACE; BASE SEQUENCE; DNA; FEMALE; GLYCOPROTEINS; OOCYTES; OOGENESIS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; REPRESSOR PROTEINS; RIBONUCLEOPROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSFORMING GROWTH FACTOR BETA; XENOPUS LAEVIS; XENOPUS PROTEINS;

XENOPUS LAEVIS;

EID: 26444435752     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.20.9028-9039.2005     Document Type: Article

References (64)

1. Antic, D., and J. D. Keene. 1997. Embryonic lethal abnormal visual RNA-binding proteins involved in growth, differentiation and posttranscriptional gene expression. Am. J. Hum. Genet. 61:273-278.
2. Antic, D., N. Lu, and J. D. Keene. 1999. ELAV tumor antigen, Hel-N1, increases translation of neurofilament M mRNA and induces formation of neurites in human teratocarcinoma cells. Genes Dev. 13:449-461.
3. Atasoy, U., J. Watson, D. Patel, and J. D. Keene. 1998. ELAV protein HuA (HuR) can redistribute between nucleus and cytoplasm and is upregulated during serum stimulation and T cell activation. J. Cell Sci. 111:3145-3156.
4. Campos, A. R., D. Grossman, and K. White. 1985. Mutant alleles at the locus elav in Drosophila melanogaster lead to nervous system defects. A developmental-genetic analysis. J. Neurogenet. 2:197-218.
5. Chen, C.-Y., and A.-B. Shyu. 1995. AU-rich elements: characterisation and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
6. Colegrove-Otero, L. J., N. Minshall, and N. Standart. 2005. RNA-binding proteins in early development. Crit. Rev. Biochem. Mol. Biol. 40:21-73.
7. Cooperstock, R. L., and H. D. Lipshitz. 2001. RNA localization and translational regulation during axis specification in the Drosophila oocyte. Int. Rev. Cytol. 2001:541-566.
8. Copeland, P. R., and M. Wormington. 2001. The mechanism and regulation of deadenylation: identification and characterisation of Xenopus PARN. RNA 7:875-886.
9. Dahanukar, A., J. A. Walker, and R. P. Wharton. 1999. Smaug, a novel RNA-binding protein that operates a translational switch in Drosophila. Mol. Cell 4:209-218.
10. Dale, L., G. Matthews, L. Tabe, and A. Colman. 1989. Developmental expression of the protein product of Vg1, a localised maternal mRNA in the frog Xenopus laevis. EMBO J. 8:1057-1065.
11. de Moor, C., and J. D. Richter. 1999. Cytoplasmic polyadenylation elements mediate masking and unmasking of cyclin B1 mRNA. EMBO J. 18:2294-2303.
12. Dixon, D. A., G. C. Balch, N. Kedersha, P. Anderson, G. A. Zimmerman, R. D. Beauchamp, and S. M. Prescott. 2003. Regulation of cyclooxygenase-2 expression by the translational silencer TIA-1. J. Exp. Med. 198:475-481.
13. Espel, E. 2005. The role of the AU-rich elements of mRNAs in controlling translation. Semin. Cell Dev. Biol. 16:59-67.
14. Evdokimova, V., P. Ruzanov, H. Imataka, B. Raught, Y. Svitkin, L. P. Ovchinnikov, and N. Sonenberg. 2001. The major mRNA-associated protein YB-1 is a potent 5′ cap-dependent mRNA stabilizer. EMBO J. 20:5491-5502.
15. Fan, X. C., and J. A. Steitz. 1998. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17:3448-3460.
16. Gallouzi, I. E., C. M. Brennan, M. G. Stenberg, M. S. Swanson, A. Eversole, N. Maizels, and J. A. Steitz. 2000. HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc. Natl. Acad. Sci. USA 97:3073-3078.
17. Gao, F.-B., C. Carson, T. Levine, and J. Keene. 1994. Selection of a subset of mRNAs from combinatorial 3′ untranslated region libraries using neuronal RNA-binding protein Hel-N1. Proc. Natl. Acad. Sci. USA 91:11207-11211.
18. Gavis, E. R., L. Lunsford, S. E. Bergsten, and R. Lehmann. 1996. A conserved 90 nucleotide element mediates translational repression of nanos RNA. Development 122:2791-2800.
19. Good, P. 1995. A conserved family of elav-like genes in vertebrates. Proc. Natl. Acad. Sci. USA 92:4557-4561.
20. Gueydan, C., L. Droogmans, P. Chalon, G. Huez, D. Caput, and V. Kruys. 1999. Identification of TIAR as a protein binding to the translational regulatory AU-rich element of tumor necrosis factor α mRNA. J. Biol. Chem. 274:2322-2326.
21. Hake, L. E., and J. D. Richter. 1994. CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell 79:617-627.
22. Hyatt, B. A., and H. J. Yost. 1998. The left-right coordinator: the role of Vg1 in organising left-right axis formation. Cell 93:37-46.
23. Jain, R. G., L. G. Andrews, K. M. McGowan, P. H. Pekala, and J. D. Keene. 1997. Ectopic expression of Hel-N1, an RNA-binding protein, increases glucose transporter (GLUT1) expression in 3T3-L1 adipocytes. Mol. Cell. Biol. 17:954-962.
24. Johnstone, O., and P. Lasko. 2001. Translational regulation and RNA localization in Drosophila oocytes and embryos. Annu. Rev. Genet. 35:365-406.
25. Kawai, T., J. Fan, K. Mazan-Mamczarz, and M. Gorospe. 2004. Global mRNA stabilization preferentially linked to translational repression during the endoplasmic reticulum stress response. Mol. Cell. Biol. 24:6773-6787.
26. Kedersha, N. L., M. Gupta, W. Li, I. Miller, and P. Anderson. 1999. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2α to the assembly of mammalian stress granules. J. Cell Biol. 147:1431-1441.
27. Kim-Ha, J., K. Kerr, and P. Macdonald. 1995. Translational regulation of oskar mRNA by Bruno, an ovarian RNA-binding protein, is essential. Cell 81:403-412.
28. Kruys, V., O. Marinx, G. Shaw, J. Deschamps, and G. Huez. 1989. Translational blockade imposed by cytokine-derived UA-rich sequences. Science 245:852-855.
29. Kuersten, S., and E. B. Goodwin. 2003. The power of the 3′ UTR: translational control and development. Nat. Rev. Genet. 4:626-637.
30. Kullmann, M., U. Gopfert, B. Siewe, and L. Hengst. 2002. ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5′ UTR. Genes Dev. 16:3087-3099.
31. Ladomery, M., E. Wade, and J. Sommerville. 1997. Xp54, the Xenopus homologue of human RNA helicase p54, is an integral component of stored mRNP particles in oocytes. Nucleic Acids Res. 25:965-973.
32. Lal, A., T. Kawai, X. Yang, K. Mazan-Mamczarz, and M. Gorospe. 2005. Antiapoptotic function of RNA-binding protein HuR effected through prothymosin alpha. EMBO J. 24:1852-1862.
33. Lal, A., K. Mazan-Mamczarz, T. Kawai, X. Yang, J. L. Martindale, and M. Gorospe. 2004. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23:3092-3102.
34. Loflin, P., C. Chen, and A. Shyu. 1999. Unraveling a Cytoplasmic role for hnRNP D in the in vivo mRNA destabilization directed by the AU-rich element. Genes Dev. 13:1884-1897.
35. Mazan-Mamczarz, K., S. Galban, I. Lopez de Silanes, J. L. Martindale, U. Atasoy, J. D. Keene, and M. Gorospe. 2003. RNA-binding protein HuR enhances p53 translation in response to ultraviolet irradiation. Proc. Natl. Acad. Sci. USA 100:8354-8359.
36. Melton, D. 1987. Translocation of a localised maternal mRNA to the vegetal pole of Xenopus oocytes. Nature 328:80-82.
37. Mendez, R., D. Barnard, and J. D. Richter. 2002. Differential mRNA translation and meiotic progression require Cdc2-mediated CPEB destruction. EMBO J. 21:1833-1844.
38. Minshall, N., J. Walker, M. Dale, and N. Standart. 1999. Dual roles of p82, the clam CPEB homolog, in cytoplasmic polyadenylation and translational masking. RNA 5:27-38.
39. Mowry, K. L., and D. A. Melton. 1992. Vegetal messenger RNA localisation directed by a 340-nt RNA sequence element in Xenopus oocytes. Science 255:991-994.
40. 39a. Mowry, K. L. 1996. Complex formation between stage-specific oocyte factors and a Xenopus mRNA localization element. Proc. Natl. Acad. Sci. USA 93:14608-14613.
41. Nakamura, A., K. Sato, and K. Hanyu-Nakamura. 2004. Drosophila Cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev. Cell 6:69-78.
42. Nelson, M. R., A. M. Leidal, and C. A. Smibert. 2004. Drosophila Cup is an eIF4E-binding protein that functions in Smaug-mediated translational repression. EMBO J. 23:150-159.
43. Otero, L. J., A. Devaux, and N. Standart. 2001. A 250-nucleotide UA-rich element in the 3′ untranslated region of Xenopus laevis Vg1 mRNA represses translation both in vivo and in vitro. RNA 7:1-15.
44. Palacios, I. M., and D. St. Johnston. 2001. Getting the message across: the intracellular localisation of mRNAs in higher eukaryotes. Annu. Rev. Cell Dev. Biol. 17:569-614.
45. Parker, R., and H. Song. 2004. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11:121-127.
46. Peng, S. S.-Y., C.-Y. A. Chen, N. Xu, and A.-B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17:3461-3470.
47. Piecyk, M., S. Wax, A. R. P. Beck, N. Kedersha, M. Gupta, B. Maritim, S. Chen, C. Gueydan, V. Kruys, M. Streuli, and P. Anderson. 2000. TIA-1 is a translational silencer that selectively regulates the expression of TNF-α. EMBO J. 19:4154-4163.
48. Preiss, T., and M. W. Hentze. 2003. Starting the protein synthesis machine: eukaryotic translation initiation. BioEssays 25:1201-1211.
49. Reverte, C. G., M. D. Ahearn, and L. E. Hake. 2001. CPEB degradation during Xenopus oocyte maturation requires a PEST domain and the 26S proteasome. Dev. Biol. 231:447-458.
50. Richter, J. D. 2000. Influence of polyadenylation-induced translation on metazoan development and neuronal synaptic function, p. 785-806. In N. Sonenberg, J. Hershey, and M. Mathews (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.
51. Smibert, C., Y. Lie, W. Shillinglaw, W. Henzel, and P. Macdonald. 1999. Smaug, a novel and conserved protein, contributes to repression of nanos mRNA translation in vitro. RNA 5:1535-1547.
52. Stebbins-Boaz, B., Q. Cao, C. H. de Moor, R. Mendez, and J. D. Richter. 1999. Maskin is a CPEB-associated factor that transiently interacts with eIF-4E. Mol. Cell 4:1017-1027.
53. Stebbins-Boaz, B., L. E. Hake, and J. D. Richter. 1996. CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocyte maturation in Xenopus. EMBO J. 15:2582-2592.
54. Tannahill, D., and D. A. Melton. 1989. Localized synthesis of the Vg1 protein during early Xenopus development. Development 106:775-785.
55. Tay, J., R. Hodgman, and J. Richter. 2000. The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev. Biol. 221:1-9.
56. Thom, G., N. Minshall, A. Git, J. Argasinska, and N. Standart. 2003. Role of cdc2 kinase phosphorylation and conserved N-terminal proteolysis motifs in cytoplasmic polyadenylation-element-binding protein (CPEB) complex dissociation and degradation. Biochem. J. 370:91-100.
57. Voeltz, G. K., and J. A. Steitz. 1998. AUUUA sequences direct mRNA deadenylation uncoupled from decay during Xenopus early development. Mol. Cell. Biol. 18:7537-7545.
58. Walker, J., C. Minshall, L. Hake, J. Richter, and N. Standart. 1999. The clam 3′ UTR masking element-binding protein p82 is a member of the CPEB family. RNA 5:14-26.
59. Weeks, D. L., and D. A. Melton. 1987. A maternal mRNA localized to the vegetal hemisphere in Xenopus eggs codes for a growth factor related to TGF-β. Cell 51:861-867.
60. Wickens, M., E. Goodwill, J. Kimble, S. Strickland, and M. Hentze. 2000. Translational control of developmental decisions, p. 295-370. In N. Sonenberg, J. Hershey, and M. Mathews (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
61. Wilhelm, J., R. Vale, and R. Hegde. 2000. Coordinate control of translation and localization of Vg1 mRNA in Xenopus oocytes. Proc. Natl. Acad. Sci. USA 97:13132-13137.
62. Wilhelm, J. E, M. Hilton, Q. Amos, and W. Henzel. 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.
63. Wilkie, G. S., K. S. Dickson, and N. K. Gray. 2003. Regulation of mRNA translation by 5′- and 3′-UTR-binding factors. Trends Biochem. Sci. 28:182-188.
64. Zhang, S., C. J. Williams, M. Wormington, A. Stevens, and S. W. Peltz. 1999. Monitoring mRNA decapping activity. Methods Companion Methods Enzymol. 17:46-51.