Molecular mechanisms of translational control

Nature Reviews Molecular Cell Biology

Volumn 5, Issue 10, 2004, Pages 827-835

  Gebauer, Fátima ^a   Hentze, Matthias W ^b  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 2; INITIATION FACTOR 4E; INITIATION FACTOR 4F; IRON REGULATORY FACTOR; MESSENGER RNA; MICRORNA; PROTEIN SERINE THREONINE KINASE; RNA;

GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; RNA TRANSLATION; TRANSLATION INITIATION; TRANSLATION REGULATION; UNTRANSLATED REGION;

ANIMALS; EUKARYOTIC INITIATION FACTOR-2; EUKARYOTIC INITIATION FACTOR-4E; GENE EXPRESSION REGULATION; MACROMOLECULAR SUBSTANCES; MICRORNAS; MODELS, GENETIC; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER;

EID: 5044229348     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1488     Document Type: Review

References (65)

1. Kuersten, S. & Goodwin, E. B. The power of the 3′ UTR: translational control and development. Nature Rev. Genet. 4, 626-637 (2003).
2. Wickens, M., Goodwin, E., Kimble, J., Strickland S. & Hentze, M. in Translational control of gene expression (eds Sonenberg, N., Hershey, J. W. & Mathews, B. M. B.) 295 (Cold Spring Harbour Laboratory Press, New York, USA, 2000).
3. Johnstone, O. & Lasko, P. Translational regulation and RNA localization in Drosophila oocytes and embryos. Annu. Rev. Genet. 35, 365-406 (2001).
4. Hershey, J. W. B. & Merrick, W. C. in Translational control of gene expression (eds Sonenberg, N., Hershey, J. W. & Mathews, B. M. B.) 33 (Cold Spring Harbour Laboratory Press, New York, USA, 2000).
5. Pestova, T. V. et al. Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl Acad. Sci. USA 98, 7029-7036 (2001).
6. Preiss, T. & Hentze, M. W. Starting the protein synthesis machine: eukaryotic translation initiation. Bioessays 25, 1201-1211 (2003).
7. Lamphear, B. J., Kirchweger, R., Skern, T. & Rhoads R. E. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. J. Biol. Chem. 270, 21975-21983 (1995).
8. Asano, K. et al. Multiple roles for the C-terminal domain of eIF5 in translation initiation complex assembly and GTPase activation. EMBO J. 20, 2326-2337 (2001).
9. Wells, S. E., Hillner, P. E., Vale, R. D. & Sachs, A. B. Circularisation of mRNA by eukaryotic translation initiation factors. Mol. Cell 2, 135-140 (1998). The authors visualize the circularization of capped and polyadenylated RNA mediated by eIF4E, eIF4G and PABP by atomic force microscopy, and provide the first detailed example of molecular interactions that enable 5′-3′-end communication of mRNAs.
10. Kozak, M. Pushing the limits of the scanning mechanism for initiation of translation. Gene 299, 1-34 (2002).
11. Pestova, T. V. & Kolupaeva, V. G. The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev. 16, 2906-2922 (2002).
12. Pestova, T. V., Borukhov, S. I. & Hellen, C. U. T. Eukaryotic ribosomes require initiation factors 1 and 1A to locate initiation codons. Nature 394, 854-859 (1998). Defines the role of eIF1 and eIF1A in translation initiation using a reconstituted translation-initiation system with highly purified factors and a reverse-transcription-based toe-printing assay.
13. Pestova, T. V. et al. The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature 403, 332-335 (2000). Identification of a second GTP-dependent step in 80S ribosome formation, which shows that eIF5B is a ribosome-stimulated GTPase.
14. Shin, B. S. et al. Uncoupling of initiation factor eIF5B/IF2 GTPase and translational activities by mutations that lower ribosome affinity. Cell 111, 1015-1025 (2002).
15. Hinnebusch, A. G. in Translational control of gene expression (eds Sonenberg, N., Hershey, J. W. & Mathews, B. M. B.) 185 (Cold Spring Harbour Laboratory Press, New York, USA, 2000).
16. Rowlands, A. G., Panniers, R. & Henshaw, E. C. The catalytic mechanism of guanine nucleotide exchange factor action and competitive inhibition by phosphorylated eukaryotic initiation factor 2. J. Biol. Chem. 263, 5526-5533 (1988).
17. de Haro, C., Mendez, R. & Santoyo, J. The eIF-2α kinases and the control of protein synthesis. FASEB J. 10, 1378-1387 (1996).
18. Dever, T. E. Gene-specific regulation by general translation factors. Cell 108, 545-556 (2002).
19. Gingras, A. C., Raught, B. & Sonenberg, N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68, 913-963 (1999).
20. Pause, A. et al. Insulin-dependent stimulation of protein synthesis by phosphorylation of 5′ cap function. Nature 371, 762-767 (1994). Reports the discovery of a new class of global translational regulators - the 4E-BPs.
21. Bushell, M. et al. Cleavage of polypeptide chain initiation factor eIF4GI during apoptosis in lymphoma cells: characterisation of an internal fragment generated by caspase-3-mediated cleavage. Cell Death Differ. 7, 628-636 (2000).
22. Marissen, W. E., Triyoso, D., Younan, P. & Lloyd, R. E. Degradation of poly(A)-binding protein in apoptotic cells and linkage to translation regulation. Apoptosis 9, 67-75 (2004).
23. Schneider, R. J. & Mohr, I. Translation initiation and viral tricks. Trends Biochem. Sci. 28, 130-136 (2003).
24. Gray, N. K. & Hentze, M. W. Iron regulatory protein prevents binding of the 43S translation pre-initiation complex to ferritin and eALAS mRNAs. EMBO J. 13, 3882-3891 (1994).
25. Muckenthaler, M., Gray, N. K. & Hentze, M. W. IRP-1 binding to ferritin mRNA prevents the recruitment of the small ribosomal subunit by the cap-binding complex eIF4F. Mol. Cell 2, 383-388 (1998). Molecular explanation of translational regulation by the IRE/IRP system by showing that eIF4F bound to the cap structure fails to form the subsequent bridging interactions to recruit the small ribosomal subunit when IRP is bound to the IRE.
26. Goossen, B., Caughman, S. W., Harford, J. B., Klausner, R. D. & Hentze, M. W. Translational repression by a complex between the iron-responsive element of ferritin mRNA and its specific cytoplasmic binding protein is position-dependent in vivo. EMBO J. 9, 4127-4133 (1990).
27. Paraskeva, E., Gray, N. K., Schlager, B., Wehr, K. & Hentze, M. W. Ribosomal pausing and scanning arrest as mechanisms of translational regulation from cap-distal iron-responsive elements. Mol. Cell. Biol. 19, 807-816 (1999).
28. Stripecke, R., Oliveira, C. C., McCarthy, J. E. & Hentze, M. W. Proteins binding to 5′ untranslated region sites: a general mechanism for translational regulation of mRNAs in human and yeast cells. Mol. Cell. Biol. 14, 5898-5909 (1994).
29. Mendez, R. & Richter, J. D. Translational control by CPEB: a means to the end. Nature Rev. Mol. Cell Biol. 2, 521-529 (2001).
30. Stebbins-Boaz, B., Cao, Q., de Moor, C. H., Mendez, R. & Richter, J. D. Maskin is a CPEB-associated factor that transiently interacts with eIF-4E. Mol. Cell 4, 1017-1027 (1999). Reports the identification of the first 'message-specific' 4E-BP.
31. Nelson, M. R., Leidal, A. M. & Smibert, C. A. Drosophila Cup is an eIF4E binding protein that functions in Smaug-mediated translational repression. EMBO J. 23, 150-159 (2004).
32. Wilhelm, J. E., Hilton, M., Amos, Q. & Henzel, W. J. 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 (2003).
33. Nakamura, A., Sato, K. & Hanyu-Nakamura, K. Drosophila Cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev. Cell 6, 69-78 (2004).
34. Clark, I. E., Wyckoff, D. & Gavis, E. R. Synthesis of the posterior determinant Nanos is spatially restricted by a novel cotranslational regulatory mechanism. Curr. Biol. 10, 1311-1314 (2000).
35. Niessing, D., Blanke, S. & Jackle, H. Bicoid associates with the 5′-cap-bound complex of caudal mRNA and represses translation. Genes Dev. 16, 2576-2582 (2002).
36. Gebauer, F., Grskovic, M. & Hentze, M. W. Drosophila sex-lethal inhibits the stable association of the 40S ribosomal subunit with msl-2 mRNA. Mol. Cell 11, 1397-1404 (2003).
37. Grskovic, M., Hentze, M. W. & Gebauer, F. A co-repressor assembly nucleated by Sex-lethal in the 3′ UTR mediates translational control of Drosophila msl-2 mRNA. EMBO J. 22, 5571-5581 (2003).
38. Gebauer, F., Corona, D. F., Preiss, T., Becker, P. B. & Hentze, M. W. Translational control of dosage compensation in Drosophila by Sex-lethal: cooperative silencing via the 5′ and 3′ UTRs of msl-2 mRNA is independent of the poly(A) tail. EMBO J. 18, 6146-6154 (1999).
39. Mazumder, B. & Fox, P. L. Delayed translational silencing of ceruloplasmin transcript in γ-interferon-activated U937 monocytic cells: role of the 3′ untranslated region. Mol. Cell. Biol. 19, 6898-6905 (1999).
40. Sampath, P., Mazumder, B., Seshadri, V. & Fox, P. L. Transcript-selective translational silencing by γ-interferon is directed by a novel structural element in the ceruloplasmin mRNA 3′ untranslated region. Mol. Cell. Biol. 23, 1509-1519 (2003).
41. Mazumder, B. et al. Regulated release of L13a from the 60S ribosomal subunit as a mechanism of transcript-specific translational control. Cell 115, 187-198 (2003). Reports a new role for a ribosomal protein in mRNA-specific translational control.
42. Mazumder, B., Seshadri, V., Imataka, H., Sonenberg, N. & Fox, P. L. Translational silencing of ceruloplasmin requires the essential elements of mRNA circularization: poly(A) tail, poly(A)-binding protein, and eukaryotic translation initiation factor 4G. Mol. Cell. Biol. 21, 6440-6449 (2001).
43. Ostareck, D. H. et al. mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3′ end. Cell 89, 597-606 (1997).
44. Ostareck, D. H., Ostareck-Lederer, A., Shatsky, I. N. & Hentze, M. W. Lipoxygenase mRNA silencing in erythroid differentiation: the 3′ UTR regulatory complex controls 60S ribosomal subunit joining. Cell 104, 281-290 (2001). Identifies 60S ribosomal subunit joining as a regulated step in translation and shows that hnRNP K and E1 inhibit lipoxygenase mRNA translation by a mechanism that probably involves interference with one or more translation-initiation factors.
45. Hinnebusch, A. G. Translational regulation of yeast GCN4. A window on factors that control initiator-tRNA binding to the ribosome. J. Biol. Chem. 272, 21661-21664 (1997). An excellent summary of one of the most intensively studied models of translational control in eukaryotes.
46. Harding, H. P. et al. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6, 1099-1108 (2000).
47. Lee, R. C., Feinbaum, R. L. & Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843-854 (1993). References 47 and 48 are the first reports of a regulatory miRNA.
48. Wightman, B., Ha, I. & Ruvkun, G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855-862 (1993).
49. Carrington, J. C. & Ambros, V. Role of microRNAs in plant and animal development. Science 301, 336-338 (2003).
50. Ambros, V. MicroRNA pathways in flies and worms: growth, death, fat, stress, and timing. Cell 113, 673-676 (2003).
51. Stark, A., Brennecke, J., Russell, R. B. & Cohen, S. M. Identification of Drosophila microRNA targets. PLoS Biol. 1, 397-409 (2003).
52. Enright, A. J. et al. MicroRNA targets in Drosophila. Genome Biol. 5, R1 (2003).
53. Zamore, P. D. Ancient pathways programmed by small RNAs. Science 296, 1265-1269 (2002).
54. Hutvagner, G. & Zamore, P. D. A microRNA in a multiple-turnover RNAi enzyme complex. Science 297, 2056-2060 (2002). Shows that the degree of complementarity between the miRNA and the target mRNA critically influences whether an mRNA is subject to degradation or translational repression.
55. Zeng, Y., Yi, R. & Cullen, B. R. MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc. Natl Acad. Sci. USA 19, 9779-9784 (2003).
56. Mourelatos, Z. et al. miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev. 16, 720-728 (2002).
57. Olsen, P. H. & Ambros, V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216, 671-680 (1999).
58. Seggerson, K., Tang, L. & Moss, E. G. Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev. Biol. 243, 215-225 (2002).
59. Lee, Y. et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419 (2003).
60. Hutvagner, G. et al. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293, 834-838 (2001).
61. Ketting, R. F. et al. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev. 15, 2654-2659 (2001).
62. Grishok, A. et al. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106, 23-34 (2001).
63. Bernstein, E., Caudy, A. A., Hammond, S. M., Hannon, G. J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363-366 (2001).
64. Hammond, S. M., Bernstein, E., Beach, D. & Hannon, G. J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404, 293-296 (2000).
65. Hammond, S. M., Boettcher, S., Caudy, A. A., Kobayashi, R. & Hannon, G. J. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293, 1146-1150 (2001).