The RNA recognition motif of eukaryotic translation initiation factor 3g (eIF3g) is required for resumption of scanning of posttermination ribosomes for reinitiation on GCN4 and together with eif3i stimulates linear scanning

Molecular and Cellular Biology

Volumn 30, Issue 19, 2010, Pages 4671-4686

  Cuchalová, Lucie ^a   Kouba, Tomáš ^a   Herrmannová, Anna ^a   Dányi, István ^a   Chiu, Wen Ling ^b   Valášek, Leoš ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 3; INITIATION FACTOR 3G; INITIATION FACTOR 3I; MESSENGER RNA; RNA; TRANSCRIPTION FACTOR GCN4; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; RIBOSOME; SACCHAROMYCES CEREVISIAE; TRANSLATION INITIATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; BLOTTING, WESTERN; EUKARYOTIC INITIATION FACTOR-3; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RIBOSOMAL PROTEINS; RIBOSOMES; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 77956657467     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00430-10     Document Type: Article

References (62)

1. Abastado, J. P., P. F. Miller, B. M. Jackson, and A. G. Hinnebusch. 1991. Suppression of ribosomal reinitiation at upstream open reading frames in amino acid-starved cells forms the basis for GCN4 translational control. Mol. Cell. Biol. 11:486-496.
2. Ahlemann, M., R. Zeidler, S. Lang, B. Mack, M. Münz, and O. Gires. 2006. Carcinoma-associated eIF3i overexpression facilitates mTOR-dependent growth transformation. Mol. Carcinog. 45:957-967.
3. Asano, K., L. Phan, J. Anderson, and A. G. Hinnebusch. 1998. Complex formation by all five homologues of mammalian translation initiation factor 3 subunits from yeast Saccharomyces cerevisiae. J. Biol. Chem. 273:18573-18585.
4. Asano, K., H.-P. Vornlocher, N. J. Richter-Cook, W. C. Merrick, A. G. Hinnebusch, and J. W. B. Hershey. 1997. Structure of cDNAs encoding human eukaryotic initiation factor 3 subunits: possible roles in RNA binding and macromolecular assembly. J. Biol. Chem. 272:27042-27052.
5. Berthelot, K., M. Muldoon, L. Rajkowitsch, J. Hughes, and J. E. G. McCarthy. 2004. Dynamics and processivity of 40S ribosome scanning on mRNA in yeast. Mol. Microbiol. 51:987-1001.
6. Chiu, W. L., S. Wagner, A. Herrmannova, L. Burela, F. Zhang, A. K. Saini, L. Valasek, and A. G. Hinnebusch. 28 June 2010. The C-terminal region of eIF3a promotes mRNA recruitment, scanning and, together with eIF3j and the eIF3b RRM, selection of AUG start codons. Mol. Cell Biol. doi:10.1128/MCB.00280-10.
7. de la Cruz, J., I. Iost, D. Kressler, and P. Linder. 1997. The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 94:5201-5206.
8. Dever, T. E., L. Feng, R. C. Wek, A. M. Cigan, T. D. Donahue, and A. G. Hinnebusch. 1992. Phosphorylation of initiation factor 2α by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68:585-596.
9. ElAntak, L., S. Wagner, A. Herrmannova, M. Karáskova, E. Rutkai, P. J. Lukavsky, and L. Valášek. 2010. The indispensable N-terminal half of eIF3j co-operates with its structurally conserved binding partner eIF3b-RRM and eIF1A in stringent AUG selection. J. Mol. Biol. 396:1097-1116.
10. Fekete, C. A., S. F. Mitchell, V. A. Cherkasova, D. Applefield, M. A. Algire, D. Maag, A. K. Saini, J. R. Lorsch, and A. G. Hinnebusch. 2007. N- and C-terminal residues of eIF1A have opposing effects on the fidelity of start codon selection. EMBO J. 26:1602-1614.
11. Gietz, R. D., and A. Sugino. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:527-534.
12. Grant, C. M., and A. G. Hinnebusch. 1994. Effect of sequence context at stop codons on efficiency of reinitiation in GCN4 translational control. Mol. Cell. Biol. 14:606-618.
13. Grant, C. M., P. F. Miller, and A. G. Hinnebusch. 1994. Requirements for intercistronic distance and level of eIF-2 activity in reinitiation on GCN4 mRNA varies with the downstream cistron. Mol. Cell. Biol. 14:2616-2628.
14. Grant, C. M., P. F. Miller, and A. G. Hinnebusch. 1995. Sequences 5′ of the first upstream open reading frame in GCN4 mRNA are required for efficient translational reinitiation. Nucleic Acids Res. 23:3980-3988.
15. Hanachi, P., J. W. B. Hershey, and H. P. Vornlocher. 1999. Characterization of the p33 subunit of eukaryotic translation initiation factor-3 from Saccharomyces cerevisiae. J. Biol. Chem. 274:8546-8553.
16. Hannig, E. M., A. M. Cigan, B. A. Freeman, and T. G. Kinzy. 1992. GCD11, a negative regulator of GCN4 expression, encodes the γ subunit of eIF-2 in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:506-520.
17. Hinnebusch, A. G. 2006. eIF3: a versatile scaffold for translation initiation complexes. Trends Biochem. Sci. 31:553-562.
18. Hinnebusch, A. G. 2005. Translational regulation of GCN4 and the general amino acid control of yeast. Annu. Rev. Microbiol. 59:407-450.
19. Hinnebusch, A. G., K. Asano, D. S. Olsen, L. O. N. Phan, K. H. Nielsen, and L. Valasek. 2004. Study of translational control of eukaryotic gene expression using yeast. Ann. N. Y. Acad. Sci. 1038:60-74.
20. Hinnebusch, A. G., T. E. Dever, and K. A. Asano. 2007. Mechanism of translation initiation in the yeast Saccharomyces cerevisiae, p. 225-268. In N. Sonenberg, M. Mathews, and J. W. B. Hershey (ed.), Translational control in biology and medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
21. Humphrey, T., and T. Enoch. 1998. Sum1, a highly conserved WD-repeat protein, suppresses S-M checkpoint mutants and inhibits the osmotic stress cell cycle response in fission yeast. Genetics 148:1731-1742. (Pubitemid 28180700)
22. Kozak, M. 2005. Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 361:13-37. (Pubitemid 41506931)
23. Lee, J. H., T. V. Pestova, B. S. Shin, C. Cao, S. K. Choi, and T. E. Dever. 2002. Initiation factor eIF5B catalyzes second GTP-dependent step in eukaryotic translation initiation. Proc. Natl. Acad. Sci. U. S. A. 99:16689-16694.
24. Maris, C., C. Dominguez, and F. H.-T. Allain. 2005. The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J. 272:2118-2131.
25. Masutani, M., N. Sonenberg, S. Yokoyama, and I. H. 2007. Reconstitution reveals the functional core of mammalian eIF3. EMBO J. 26:3373-3383. (Pubitemid 47123530)
26. Miller, P. F., and A. G. Hinnebusch. 1989. Sequences that surround the stop codons of upstream open reading frames in GCN4 mRNA determine their distinct functions in translational control. Genes Dev. 3:1217-1225.
27. Mitchell, S. F., and J. R. Lorsch. 2008. Should I stay or should I go? Eukaryotic translation initiation factors 1 and 1a control start codon recognition. J. Biol. Chem. 283:27345-27349.
28. Mueller, P. P., S. Harashima, and A. G. Hinnebusch. 1987. A segment of GCN4 mRNA containing the upstream AUG codons confers translational control upon a heterologous yeast transcript. Proc. Natl. Acad. Sci. U. S. A. 84:2863-2867.
29. Mueller, P. P., and A. G. Hinnebusch. 1986. Multiple upstream AUG codons mediate translational control of GCN4. Cell 45:201-207.
30. Naranda, T., M. Kainuma, S. E. McMillan, and J. W. B. Hershey. 1997. The 39-kilodalton subunit of eukaryotic translation initiation factor 3 is essential for the complex's integrity and for cell viability in Saccharomyces cerevisiae. Mol. Cell. Biol. 17:145-153.
31. Nielsen, K. H., B. Szamecz, L. J. Valasek, A., B. S. Shin, and A. G. Hinnebusch. 2004. Functions of eIF3 downstream of 48S assembly impact AUG recognition and GCN4 translational control. EMBO J. 23:1166-1177.
32. Nielsen, K. H., and L. Valášek. 2007. In vivo deletion analysis of the architecture of a multi-protein complex of translation initiation factors. Methods Enzymol. 431:15-32.
33. Nielsen, K. H., L. Valášek, C. Sykes, A. Jivotovskaya, and A. G. Hinnebusch. 2006. Interaction of the RNP1 motif in PRT1 with HCR1 promotes 40S binding of eukaryotic initiation factor 3 in yeast. Mol. Cell. Biol. 26:2984-2998.
34. Olsen, D. S., E. M. Savner, A. Mathew, F. Zhang, T. Krishnamoorthy, L. Phan, and A. G. Hinnebusch. 2003. Domains of eIF1A that mediate binding to eIF2, eIF3 and eIF5B and promote ternary complex recruitment in vivo. EMBO J. 22:193-204.
35. Park, H. S., A. Himmelbach, K. S. Browning, T. Hohn, and L. A. Ryabova. 2001. A plant viral "reinitiation" factor interacts with the host translational machinery. Cell 106:723-733.
36. Passmore, L. A., T. M. Schmeing, D. Maag, D. J. Applefield, M. G. Acker, M. A. Algire, J. R. Lorsch, and V. Ramakrishnan. 2007. The eukaryotic translation initiation factors eIF1 and eIF1A induce an open conformation of the 40S ribosome. Mol. Cell 26:41-50.
37. Pestova, T. V., S. I. Borukhov, and C. U. T. Hellen. 1998. Eukaryotic ribosomes require initiation factors 1 and 1A to locate initiation codons. Nature 394:854-859.
38. Pestova, T. V., and V. G. Kolupaeva. 2002. The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev. 16:2906-2922.
39. Pestova, T. V., J. R. Lorsch, and C. U. T. Hellen. 2007. The mechanism of translation initiation in eukaryotes, p. 87-128. In N. Sonenberg, M. Mathews, and J. W. B. Hershey (ed.), Translational control in biology and medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Met. EMBO J. 20:2954-2965.
41. Pisarev, A. V., C. U. T. Hellen, and T. V. Pestova. 2007. Recycling of eukaryotic posttermination ribosomal complexes. Cell 131:286-299.
42. Pöyry, T. A., A. Kaminski, E. J. Connell, C. S. Fraser, and R. J. Jackson. 2007. The mechanism of an exceptional case of reinitiation after translation of a long ORF reveals why such events do not generally occur in mammalian mRNA translation. Genes Dev. 21:3149-3162.
43. Pöyry, T. A., A. Kaminski, and R. J. Jackson. 2004. What determines whether mammalian ribosomes resume scanning after translation of a short upstream open reading frame? Genes Dev. 18:62-75.
44. Ruiz-Echevarria, M. J., and S. W. Peltz. 2000. The RNA binding protein Pub1 modulates the stability of transcripts containing upstream open reading frames. Cell 101:741-751.
45. Siridechadilok, B., C. S. Fraser, R. J. Hall, J. A. Doudna, and E. Nogales. 2005. Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310:1513-1515. (Pubitemid 41746350)
46. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31-40.
47. Spahn, C. M., R. Beckmann, N. Eswar, P. A. Penczek, A. Sali, G. Blobel, and J. Frank. 2001. Structure of the 80S ribosome from Saccharomyces cerevisiae-tRNA ribosome and subunit-subunit interactions. Cell 107:373-386.
48. Srivastava, S., A. Verschoor, and J. Frank. 1992. Eukaryotic initiation factor 3 does not prevent association through physical blockage of the ribosomal subunit-subunit interface. J. Mol. Biol. 220:301-304.
49. Szamecz, B., E. Rutkai, L. Cuchalova, V. Munzarova, A. Herrmannova, K. H. Nielsen, L. Burela, A. G. Hinnebusch, and L. Valášek. 2008. eIF3a cooperates with sequences 5′ of uORF1 to promote resumption of scanning by post-termination ribosomes for reinitiation on GCN4 mRNA. Genes Dev. 22:2414-2425.
50. Taylor, D. J., B. Devkota, A. D. Huang, M. Topf, E. Narayanan, A. Sali, S. C. Harvey, and J. Frank. 2009. Comprehensive molecular structure of the eukaryotic ribosome. Structure 17:1591-1604.
51. Valášek, L., A. Mathew, B. S. Shin, K. H. Nielsen, B. Szamecz, and A. G. Hinnebusch. 2003. The yeast eIF3 subunits TIF32/a and NIP1/c and eIF5 make critical connections with the 40S ribosome in vivo. Genes Dev. 17:786-799.
52. Valášek, L., K. H. Nielsen, and A. G. Hinnebusch. 2002. Direct eIF2-eIF3 contact in the multifactor complex is important for translation initiation in vivo. EMBO J. 21:5886-5898.
53. Valášek, L., K. H. Nielsen, F. Zhang, C. A. Fekete, and A. G. Hinnebusch. 2004. Interactions of eukaryotic translation initiation factor 3 (eIF3) subunit NIP1/c with eIF1 and eIF5 promote preinitiation complex assembly and regulate start codon selection. Mol. Cell. Biol. 24:9437-9455.
54. Valášek, L., L. Phan, L. W. Schoenfeld, V. Valášková, and A. G. Hinnebusch. 2001. Related eIF3 subunits TIF32 and HCR1 interact with an RNA recoginition motif in PRT1 required for eIF3 integrity and ribosome binding. EMBO J. 20:891-904.
55. Valášek, L., B. Szamecz, A. G. Hinnebusch, and K. H. Nielsen. 2007. In vivo stabilization of preinitiation complexes by formaldehyde cross-linking. Methods Enzymol. 429:163-183.
56. van der Velden, A. W., and A. A. M. Thomas. 1999. The role of the 5′ untranslated region of an mRNA in translation regulation during development. Int. J. Biochem. Cell Biol. 31:87-106.
57. Verlhac, M.-H., R.-H. Chen, P. Hanachi, J. W. B. Hershey, and R. Derynck. 1997. Identification of partners of TIF34, a component of the yeast eIF3 complex, required for cell proliferation and translation initiation. EMBO J. 16:6812-6822.
58. Vornlocher, H. P., P. Hanachi, S. Ribeiro, and J. W. B. Hershey. 1999. A 110-kilodalton subunit of translation initiation factor eIF3 and an associated 135-kilodalton protein are encoded by the Saccharomyces cerevisiae TIF32 and TIF31 genes. J. Biol. Chem. 274:16802-16812.
59. Wells, S. E., P. E. Hillner, R. D. Vale, and A. B. Sachs. 1998. Circularization of mRNA by eukaryotic translation initiation factors. Mol. Cell 2:135-140.
60. Williams, N. P., A. G. Hinnebusch, and T. F. Donahue. 1989. Mutations in the structural genes for eukaryotic initiation factors 2α and 2β of Saccharomyces cerevisiae disrupt translational control of GCN4 mRNA. Proc. Natl. Acad. Sci. U. S. A. 86:7515-7519.
61. Yamamoto, Y., C. R. Singh, A. Marintchev, N. S. Hall, E. M. Hannig, G. Wagner, and K. Asano. 2005. The eukaryotic initiation factor (eIF) 5 HEAT domain mediates multifactor assembly and scanning with distinct interfaces to eIF1, eIF2, eIF3, and eIF4G. Proc. Natl. Acad. Sci. U. S. A. 102:16164-16169.
62. Zhou, M., A. M. Sandercock, C. S. Fraser, G. Ridlova, E. Stephens, M. R. Schenauer, T. Yokoi-Fong, D. Barsky, J. A. Leary, J. W. Hershey, J. A. Doudna, and C. V. Robinson. 2008. Mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. Proc. Natl. Acad. Sci. U. S. A. 105:18139-18144.