Translational control in early development: CPEB, P-bodies and germinal granules

Biochemical Society Transactions

Volumn 36, Issue 4, 2008, Pages 671-676

  Standart, Nancy ^a   Minshall, Nicola ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cap binding; Cytoplasmic polyadenylation element binding protein (CPEB); Processing body (P body); RNA decay; Stress granule; Translation initiation

Indexed keywords

CAP BINDING PROTEIN; CYTOPLASMIC POLYADENYLATION ELEMENT BINDING PROTEIN; FROG GERM CELL SPECIFIC Y BOX PROTEIN 2; INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN; MESSENGER RNA; PAT1 PROTEIN; POLYADENYLIC ACID BINDING PROTEIN; PROTEIN DERIVATIVE; RIBONUCLEOPROTEIN; RNA ASSOCIATED PROTEIN 55; RNA BINDING PROTEIN; RNA HELICASE;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CELL FATE; CELL GRANULE; CELL MATURATION; COMPLEX FORMATION; CYTOPLASM; DEVELOPMENTAL BIOLOGY; EMBRYO AXIS; EMBRYO DEVELOPMENT; GEL FILTRATION; GERM CELL; IMMUNOPRECIPITATION; MEIOSIS; MITOSIS; NERVE CELL; OOCYTE DEVELOPMENT; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SOMATIC CELL; TRANSLATION INITIATION; TRANSLATION REGULATION; XENOPUS;

ANIMALS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYTOPLASMIC STRUCTURES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; PROTEIN BIOSYNTHESIS; RIBONUCLEOPROTEINS; TIME FACTORS;

ANURA; EUKARYOTA;

EID: 49349088194     PISSN: 03005127     EISSN: None     Source Type: Journal    
DOI: 10.1042/BST0360671     Document Type: Article

References (71)

1. Pestova, T.V., Lorsch, J.R. and Hellen, C.U.T. (2007) The mechanism of translation initiation in eukaryotes. In Translational Control in Biology and Medicine (Mathews, M.B., Sonenberg, N., Hershey, J.W.B., eds), Cold Spring Harbor Laboratory Press, Cold Spring Harbor 87-128
2. Goodfellow, I.G. and Roberts, L.O. (2007) Eukaryotic initiation factor 4E. Int. J. Biochem. Cell Biol., doi:10.1016/J.biocel.2007.10.023
3. Hernández, G., Altmann, M., Sierra, J.M., Urlaub, H., del Corral, R.D., Schwartz, P. and Rivera-Pomar, R. (2005) Functional analysis of seven genes encoding eight translation initiation factor 4E (eIF4E) isoforms in Drosophila. Mech. Dev. 122, 529-543
4. lankowska-Anyszka, M., Lamphear, B.J., Aamodt, E.J., Harrington, T., Darzynkiewicz, E., Stolarski, R. and Rhoads, R.E. (1998) Multiple isoforms of eukaryotic protein synthesis initiation factor 4E in Coenorhobditis elegans can distinguish between mono- and trimethylated mRNA cap structures. J. Biol. Chem. 269, 10538-10542
5. Dhalia, R., Reis, C.R., Freire, E.R., Rocha, P.O., Katz, R., Muniz, J.R., Standart, N. and de Melo Neto, O.P. (2005) Translation initiation in Leishmania mojor: characterisation of multiple eIF4F subunit homologues. Mol. Biochem. Parasitol. 140, 23-41
6. Yoffe, Y., Zuberek, J., Lerer, A., Lewdorowicz, M., Stepinski, J., Altmann, M., Darzynkiewicz, E. and Shapira, M. (2006) Binding specificities and potential roles of isoforms of eukaryotic initiation factor 4E in Leishmania. Eukaryotic Cell 5, 1969-1979
7. Ptushkina, M., Berthelot, K., von der Haar, T., Geffers, L., Warwicker, J. and McCarthy, J.F. (2001) A second eIF4F protein in Schizosscchafomyces pombe has distinct eIF4G-binding properties. Nucleic Acids Res. 29, 4561-4569
8. Miyoshi, H., Dwyer, D.S., Keiper, B.D., Jankowska-Anyszka, M., Darzynkiewicz, E. and Rhoads, R.E. (2002) Discrimination between mono- and trimethylated cap structures by two isoforms of Caenorhabditis elegans eIF4E. EMBO J. 21, 4680-4690
9. Joshi, B., Lee, K., Maeder, D.L. and Jagus, R. (2005) Phylogenetic analysis of eIF4E-family members. BMC Evol. Biol. 5, 48
10. Joshi, B., Cameron, A. and Jagus, R. (2004) Characterization of mammalian eIF4E-family members. Eur. J. Biochem. 271, 2189-2203
11. 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 5' cap-binding protein, eIF4E. EMBO J. 19, 3142-3156
12. Cho, P.F., Poulin, F., Cho-Park, Y.A., Cho-Park, I.B., Chicoine, J.D., Lasko, P. and Sonenberg, N. (2005) A new paradigm for translational control: inhibition via 5'-3' mRNA tethering by Bicoid and the eIF4E cognate 4EHP. Cell 121, 411-423
13. Colegrove-Otero, L.J., Minshall, N. and Standart, N. (2005) RNA-binding proteins in early development. Crit. Rev. Biochem. Mol. Biol. 40, 21-73
14. de Moor, C.H., Meijer, H. and Lissenden, S. (2005) Mechanisms of translational control by the 3' UTR in development and differentiation. Semin. Cell Dev. Biol. 16, 49-58
15. Thompson, B., Wickens, M. and Kimble, J. (2007) Translational control in development. in Translational Control in Biology and Medicine (Mathews, M.B., Sonenberg, N. and Hershey, J.W.B., eds.), pp. 507-544, Cold Spring Harbor Laboratory Press, Cold Spring Harbor
16. Abaza, I. and Gebauer, F. (2008) Trading translation with RNA-binding proteins. RNA 14, 404-409
17. Radford, H.F., Meijer, H.A. and de Moor, C.H. (2008) Translational control by cytoplasmic polyadenylation in Xenopus oocytes. Biochim. Biophys. Acta 1779, 217-229
18. Huang, Y.S., Kan, M.C., Lin, C.L. and Richter, J.D. (2006) CPEB3 and CPEB4 in neurons: analysis of RNA-binding specificity and translational control of AMPA receptor GluR2 mRNA. EMBO J. 25, 4865-4876
19. Theis, M., Si, K. and Kandel, E.R. (2003) Two previously undescribed members of the mouse CPEB family of genes and their inducible expression in the principal cell layers of the hippocampus. Proc. Natl. Acad. Sci. U,S.A. 100, 9602-9607
20. Rouhana, L., Wang, L., Buter, N., Kwak, J.E., Schiltz, C.A., Gonzalez, T., Kelley, A.E., Landry, C.F. and Wickens, M. (2005) Vertebrate GLD2 poly(A) polymerases in the germline and the brain. RNA. 11, 1117-1130
21. Minshall, N., Walker, J., Dale, M. and Standart, N. (1999) Dual roles of p82, the clam CPEB homolog, in cytoplasmic polyadenylation and translational masking. RNA 5, 27-38
22. de Moor, C. and Richter, J.D. (1999) Cytoplasmic polyadenylation elements mediate masking and unmasking of cyclin B1 mRNA. EMBO J. 18, 2294-2303
23. Méndez, R. and Richter, J.D. (2001) Translational control by CPEB: a means to the end. Nat. Rev. Mol. Cell Biol. 2, 521-529
24. Kwalk, J.E., Wang, L., Ballantyne, S., Kimble, J. and Wickens, M. (2004) Mammalian GLD-2 homologs are poly(A) polymerases. Proc. Natl. Acad. Sci. U.S.A. 101, 4407-4412
25. Barnard, D.C., Ryan, K., Manley, J.L. and Richter, J.D. (2004) Symplekin and xGLD-2 are required for CPEB-mediated cytoplasmic polyadenylation. Cell 24, 641-651
26. Pique, M., Lopez, J.M., Foissac, S., Guigo, R. and Méndez, R. (2008) A combinatorial code for CPE-mediated translational control. Cell 132, 434-448
27. Belloc, E. and Méndez, R. (2008) A deadenylation negative feedback mechanism governs meiotic metaphase arrest. Nature 452, 1017-1021
28. Belloc, E., Piqué, M. and Méndez, R. (2008) Sequential waves of polyadenylation and deadenylation define a translation circuit that drives meiotic progression. Biochem. Soc. Trans. 36, 665-670
29. Stebbins-Boaz, B., Cao, Q., de Moor, C.H., Méndez, R. and Richter, J.D. (1999) Maskin is a CPEB-associated factor that transiently interacts with elF-4E. Mol. Cell 4, 1017-1027
30. Groisman, I., Huang, Y.-S., Méndez, R., Cao, Q., Therkauf, W. and Richter, J. (2000) CPEB, maskin, and cyclin B1 mRNA at the mitotic apparatus: implications for local translational control of cell division. Cell 103, 435-447
31. Meijer, H.A., Radford, H.E., Wilson, L.S., Lissenden, S. and de Moor, C.H. (2007) Translational control of maskin mRNA by its 3' untranslated region. Biol. Cell 99, 239-2SO
32. Minshall, N., Reiter, M.-H., Weil, D. and Standart, N. (2007) CPEB interacts with an ovary-specific elF4E and 4E-T in early Xenopus oocytes. J. Biol. Chem. 282, 37389-37401
33. Kim, J.H. and Richter, J.D. (2006) opposing polymerase-deadenylase activities regulate cytoplasmic polyadenylation. Mol. Cell 24, 173-183
34. Wormington, M., Searfoss, A. and Hurney, C. (1996) Overexpression of poly(A) binding protein prevents maturation-specific deadenylation and translational inactivation in Xenopus oocytes. EMBO J. 15, 900-909
35. Copeland, P.R. and Wormington, M. (2001) The mechanism and regulation of deadenylation: identification and characterisation of Xenopus PARN. RNA 7, 875-886
36. Yamashita, A., Chang, T.C., Yamashita, Y., Zhu, W., Zhong, Z., Chen, C.Y. and Shyu, A.B. (2005) Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat. Struct. Mol. Biol. 12, 1054-1063
37. Minshall, N., Thorn, G. and Standart, N. (2001) A conserved role of a DEAD box helicase in mRNA masking. RNA. 7, 1728-1742
38. Minshall, N. and Standart, N. (2004) The active form of Xp54 RNA helicase in translational repression is an RNA-mediated oligomer. Nucleic Acids Res. 32, 1325-1334
39. Ferraiuolo, M.A., Basak, S., Dostie, J., Murray, E.L., Schoenberg, D.R. and Sonenberg, N. (2005) A role for the elF4E-binding protein in P-body formation and mRNA decay. J. Cell Biol. 170, 913-924
40. Lee, H.C., Cho, H. and Kim, Y.K. (2008) Ectopic expression of elF4E-transporter triggers the movement of elF4E into P-bodies, inhibiting steady-State translation but not the pioneer round of translation. Biochem. Biophys. Res. Commun. 369, 1160-1165
41. Andrei, M.A., Ingelfinger, D., Heintzmann, R., Achsel, T., Rivera-Pomar, R. and Lührmann, R. (2005) A role for eIF4E and elF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA 11, 717-727
42. Robalino, J., Joshi, B., Fahrenkrug, S.C. and Jagus, R. (2004) Two zebrafish elF4E family members are differentially expressed and functionally divergent. J. Biol. Chem. 279, 10532-10541
43. 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
44. Wilhelm, J.E., Hilton, M., Amos, Q. and Henzel, W. (2003) Cup is an elF4E binding protein required for both the translational repression of oskor and the recruitment of Barentsz. J. Cell Biol. 163, 1197-1204
45. Nakamura, A., Sato, K. and Hanyu-Nakamura, K. (2004) Drosophilo Cup is an elF4E binding protein that associates with Bruno and regulates oskor mRNA translation in oogenesis. Dev. Cell 6, 69-78
46. Chekulaeva, M., Hentze, M.W. and Ephrussi, A. (2006) Bruno acts as a dual repressor of oskor translation, promoting mRNA oligomerization and formation of silencing particles. Cell 124, 521-533
47. Cho, P.F., Gamberi, C., Cho-Park, Y.A., Cho-Park, I.B., Lasko, P. and Sonenberg, N. (2006) Cap-dependent translational inhibition establishes two opposing morphogen gradients in Drosophilo embryos. Curr. Biol. 16, 2035-2041
48. Zuberek, J., Kubacka, D., Jablonowska, A., Jemielity, J., Stepinski, J., Sonenberg, N. and Darzynkiewicz, E. (2007) Weak binding affinity of human 4EHP for mRNA cap analogs. RNA 13, 691-697
49. Nakahata, S., Katsu, Y., Mita, K., Inoue, K., Nagahama, Y. and Yamashita, M. (2001) Biochemical identification of Xenopus Pumilio as a sequence-specific cyclin B1 mRNA-binding protein that physically interacts with a nanos homolog (Xcat-2) and a cytoplasmic polyadenylation element-binding protein (CPEB). J. Biol. Chem. 276, 20945-20953
50. Martínez, S.E., Yuan, L. Lacza, C., Ransom, H., Mahon, G.K., Whitehead, I.P. and Hake, L.E. (2005) XGef mediates early CPEB phosphorylation during Xenopus oocyte meiotic maturation. Mol. Biol. Cell 16, 1152-1164
51. Eulalio, A., Behm-Ansmant, I. and Izaurralde, E. (2007) P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 8, 9-22
52. Parker, R. and Sheth, U. (2007) P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635-646
53. Gillian-Daniel, D.L., Gray, N.K., Astrom, J., Barkoff, A- and Wickens, M. (1998) Modifications of the 5' cap of mRNAs during Xenopus oocyte maturation: independence from changes in poly(A) length and impact on translation. Mol. Cell. Biol. 18, 6152-6153
54. Zhang, S., Williams, C.J., Wormington, M., Stevens, A. and Peltz, S.W. (1999) Monitoring mRNA decapping activity. Methods 17, 46-51
55. Eulalio, A., Behm-Ansmant, I., Schweizer, D. and Izaurralde, E. (2007) P-body formation is a consequence, not the cause of RNA-mediated gene silencing. MoJ. Cell. Biol. 27, 3970-3981
56. Decker, C.J., Teixeira, D. and Parker, R. (2007) Edc3p and a glutamine/ asparagine-rich domain of Lsm4p function in processing body assembly in Socchoromyces cerevisicoe, J. Cell Biol. 179, 437-449
57. Yamasaki, S. and Anderson, P. (2008) Reprogramming mRNA translation during stress. Curr. Opin. Cell Biol. 20, 222-226
58. Wilczynska, A., Aigueperse, C., Kress, M., Dautry, F. and Weil, D. (2005) The translational regulator CPEB1 provides a link between Dcp1 bodies and stress granules. J. Cell Sci. 118, 981-992
59. Anderson, P. and Kedersha, N. (2008) Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33, 141-150
60. Hoyle, N.P., Castelli, L.M., Campbell, S.G., Holmes, L.F. and Ashe, M.P. (2007) Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies. J. Cell Biol. 179, 65-74
61. Holetz, F.B., Correa, A., Avila, A.R., Nakamura, C.V., Krieger, M.A. and Goldenberg, S. (2007) Evidence of P-body-like structures in Tryponosomo cruzi. Biochem. Biophys. Res. Commun. 356, 1062-1067
62. Cassola, A., De Gaudenzi, J.G. and Frasch, A.C. (2007) Recruitment of mRNAs to cytoplasmic ribonucleoprotein granules in trypanosomes. Mol. Microbiol. 65, 655-670
63. Kramer, S., Queiroz, R., Ellis, L., Webb, H., Hoheisel, J.D., Clayton, C. and Carrington, M. (2008) Heat shock causes a decrease in polysomes and appearance of stress granules in trypanosomes independently of elF2α phosphorylation at a position equivalent to sefine 51. J. Cell Sci., in the press
64. Hoyle, N.P. and Ashe, M. (2008) Subcellular localization of mRNA and factors involved in translation initiation. Biochem. Soc. Trans. 36, 648-652
65. Boag, P.R., Nakamura, A. and Blackwell, T.K. (2005) A conserved RNA-protein complex component involved in physiological germline apoptosis regulation in C. elegons. Development 132, 4975-4986
66. Barbee, S.A., Estes, P.S., Cziko, A.M., Hillebrand, J., Luedeman, R.A., Coller, J.M., Johnson, N., Howlett, I.C., Geng, C., Ueda, R. et al. (2006) Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron 52, 997-1009
67. Navarro, R.E. and Blackwell, T.K. (2005) Requirement for P granules and meiosis for accumulation of the germline RNA helicase CGH-1. Genesis 42, 172-180
68. Squirrell, J.M., Eggers, Z.T., Luedke, N., Saari, B., Grimson, A., Lyons, G.E., Anderson, P. and White, J.G. (2006) CAR-1, a protein that localizes with the mRNA decapping component DCAP-1, is required for cytokinesis and ER organization in C. elegons embryos. Mol, Biol. Cell 17, 336-344
69. Amiri, A., Keiper, B.D., Kawasaki, I., Fan, Y., Kohara, Y., Rhoads, R.E. and Strome, S. (2001) An isoform of elF4E is a component of germ granules and is required for spermatogenesis in C. elegons. Development 128, 3899-3912
70. Weston, A. and Sommerville, J. (2006) Xp54 and related (DDX6-like) RNA helicases: foles in messenger RNP assembly, translation regulation and RNA degradation. Nucleic Acids Res. 34, 3082-3094
71. Pepling, M.E., Wilhelm, J.E., O'Hara, A.L., Gephardt, G.W. and Spradling, A.C. (2006) Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body. Proc. Natl. Acad. Sci. U.S.A. 104, 187-192