Conformational changes in the P site and mRNA entry channel evoked by AUG recognition in yeast translation preinitiation complexes

Nucleic Acids Research

Volumn 43, Issue 4, 2015, Pages 2293-2312

  Zhang, Fan ^a   Saini, Adesh K ^a,b   Shin, Byung Sik ^a   Nanda, Jagpreet ^a   Hinnebusch, Alan G ^a  

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

^b SHOOLINI UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

1-(4-BROMOACETAMIDOBENZYL)EDTA; CYSTEINE; EDETIC ACID; EUKARYOTIC PEPTIDE INITIATION FACTOR-1A; INITIATION FACTOR 1; MESSENGER RNA; METHIONINE TRANSFER RNA; RNA 18S; START CODON;

AMINO ACID SUBSTITUTION; ANALOGS AND DERIVATIVES; CHEMISTRY; GENETICS; METABOLISM; RNA TRANSLATION; SMALL RIBOSOMAL SUBUNIT; START CODON; YEAST;

AMINO ACID SUBSTITUTION; CODON, INITIATOR; CYSTEINE; EDETIC ACID; EUKARYOTIC INITIATION FACTOR-1; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RNA, MESSENGER; RNA, RIBOSOMAL, 18S; RNA, TRANSFER, MET; YEASTS;

EID: 84941027177     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv028     Document Type: Article

References (36)

1. Hinnebusch, A. G. (2011) Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiol. Mol. Biol. Rev., 75, 434-467.
2. Hinnebusch, A. G. (2014) The scanning mechanism of eukaryotic translation initiation. Annu. Rev. Biochem., 83, 779-812.
3. Maag, D., Fekete, C. A., Gryczynski, Z. And Lorsch, J. R. (2005) A conformational change in the eukaryotic translation preinitiation complex and release of eIF1 signal recognition of the start codon. Mol. Cell, 17, 265-275.
4. Nanda, J. S., Saini, A. K., Munoz, A. M., Hinnebusch, A. G. And Lorsch, J. R. (2013) Coordinated movements of eukaryotic translation initiation factors eIF1, eIF1A, and eIF5 trigger phosphate release from eIF2 in response to start codon recognition by the ribosomal preinitiation complex. J. Biol. Chem., 288, 5316-5329.
5. Algire, M. A., Maag, D. And Lorsch, J. R. (2005) Pi release from eIF2, not GTP hydrolysis, is the step controlled by start-site selection during eukaryotic translation initiation. Mol. Cell, 20, 251-262.
6. Passmore, L. A., Schmeing, T. M., Maag, D., Applefield, D. J., Acker, M. G., Algire, M. A., Lorsch, J. R. And Ramakrishnan, V. (2007) The eukaryotic translation initiation factors eIF1 and eIF1A induce an open conformation of the 40S ribosome. Mol. Cell, 26, 41-50.
7. Pestova, T. V., Lorsch, J. R. And Hellen, C. U. T. (2007) The Mechanism of Translation Initiation in Eukaryotes. In: Mathews, M., Sonenberg, N. And Hershey, J. W. B. (eds), Translational Control in Biology and Medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp. 87-128.
8. Fekete, C. A., Mitchell, S. F., Cherkasova, V. A., Applefield, D., Algire, M. A., Maag, D., Saini, A., Lorsch, J. R. And Hinnebusch, A. G. (2007) N-and C-terminal residues of eIF1A have opposing effects on the fidelity of start codon selection. EMBO 26, 1602-1614.
9. Cheung, Y. N., Maag, D., Mitchell, S. F., Fekete, C. A., Algire, M. A., Takacs, J. E., Shirokikh, N., Pestova, T., Lorsch, J. R. And Hinnebusch, A. G. (2007) Dissociation of eIF1 from the 40S ribosomal subunit is a key step in start codon selection in vivo. Genes Dev., 21, 1217-1230.
10. Saini, A. K., Nanda, J. S., Lorsch, J. R. And Hinnebusch, A. G. (2010) Regulatory elements in eIF1A control the fidelity of start codon selection by modulating tRNA(i)(Met) binding to the ribosome. Genes Dev., 24, 97-110.
11. Rabl, J., Leibundgut, M., Ataide, S. F., Haag, A. And Ban, N. (2011) Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science, 331, 730-736.
12. Weisser, M., Voigts-Hoffmann, F., Rabl, J., Leibundgut, M. And Ban, N. (2013) The crystal structure of the eukaryotic 40S ribosomal subunit in complex with eIF1 and eIF1A. Nat. Struct. Mol. Biol., 20, 1015-1017.
13. Lomakin, I. B. And Steitz, T. A. (2013) The initiation of mammalian protein synthesis and mRNA scanning mechanism. Nature, 500, 307-311.
14. Hussain, T., Llácer, J. L., Fernández, I. S., Munoz, A., Martin-Marcos, P., Savva, C. G., Lorsch, J. R., Hinnebusch, A. G. And Ramakrishnan, V. (2014) Structure of a eukaryotic translational initiation complex reveals key interactions in recognition of the start codon. Cell, 159, 597-607.
15. Yu, Y., Marintchev, A., Kolupaeva, V. G., Unbehaun, A., Veryasova, T., Lai, S. C., Hong, P., Wagner, G., Hellen, C. U. And Pestova, T. V. (2009) Position of eukaryotic translation initiation factor eIF1A on the 40S ribosomal subunit mapped by directed hydroxyl radical probing. Nucleic Acids Res., 37, 5167-5182.
16. Yoon, H. J. And Donahue, T. F. (1992) The sui1 suppressor locus in Saccharomyces cerevisiae encodes a translation factor that functions during tRNAi Met recognition of the start codon. Mol. Cell. Biol., 12, 248-260.
17. Donahue, T. (2000) In: Sonenberg, N., Hershey, J. W. B. And Mathews, M. B. (eds), Translational Control of Gene Expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp. 487-502.
18. Olsen, D. S., S, E. M., Mathew, A., Zhang, F., Krishnamoorthy, T., Phan, L. And Hinnebusch, A. G. (2003) Domains of eIF1A that mediate binding to eIF2, eIF3 and eIF5B and promote ternary complex recruitment in vivo. EMBO J., 22, 193-204.
19. Acker, M. G., Shin, B. S., Nanda, J. S., Saini, A. K., Dever, T. E. And Lorsch, J. R. (2009) Kinetic analysis of late steps of eukaryotic translation initiation. J. Mol. Biol., 385, 491-506.
20. Gietz, R. D. And Sugino, A. (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene, 74, 527-534.
21. Fekete, C. A., Applefield, D. J., Blakely, S. A., Shirokikh, N., Pestova, T., Lorsch, J. R. And Hinnebusch, A. G. (2005) The eIF1A C-terminal domain promotes initiation complex assembly, scanning and AUG selection in vivo. EMBO J., 24, 3588-3601.
22. Acker, M. G., Kolitz, S. E., Mitchell, S. F., Nanda, J. S. And Lorsch, J. R. (2007) Reconstitution of yeast translation initiation. Methods Enzymol., 430, 111-145.
23. Shin, B. S., Kim, J. R., Walker, S. E., Dong, J., Lorsch, J. R. And Dever, T. E. (2011) Initiation factor eIF2 promotes eIF2-GTP-Met-tRNA(i)(Met) ternary complex binding to the 40S ribosome. Nat. Struct. Mol. Biol., 18, 1227-1234.
24. Algire, M. A., Maag, D., Savio, P., Acker, M. G., Tarun, S. Z. Jr, Sachs, A. B., Asano, K., Nielsen, K. H., Olsen, D. S., Phan, L. et al. (2002) Development and characterization of a reconstituted yeast translation initiation system. RNA, 8, 382-397.
25. Walker, S. E., Zhou, F., Mitchell, S. F., Larson, V. S., Valasek, L., Hinnebusch, A. G. And Lorsch, J. R. (2013) Yeast eIF4B binds to the head of the 40S ribosomal subunit and promotes mRNA recruitment through its N-terminal and internal repeat domains. RNA, 19, 191-207.
26. Boeke, J. D., Trueheart, J., Natsoulis, G. And Fink, G. R. (1987) 5-fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol., 154, 164-175.
27. Kapp, L. D., Kolitz, S. E. And Lorsch, J. R. (2006) Yeast initiator tRNA identity elements cooperate to influence multiple steps of translation initiation. RNA, 12, 751-764.
28. Kolitz, S. E., Takacs, J. E. And Lorsch, J. R. (2009) Kinetic and thermodynamic analysis of the role of start codon/anticodon base pairing during eukaryotic translation initiation. RNA, 15, 138-152.
29. Dong, J., Munoz, A., Kolitz, S. E., Saini, A. K., Chiu, W. L., Rahman, H., Lorsch, J. R. And Hinnebusch, A. G. (2014) Conserved residues in yeast initiator tRNA calibrate initiation accuracy by regulating preinitiation complex stability at the start codon. Genes Dev., 28, 502-520.
30. Dong, J., Nanda, J. S., Rahman, H., Pruitt, M. R., Shin, B. S., Wong, C. M., Lorsch, J. R. And Hinnebusch, A. G. (2008) Genetic identification of yeast 18S rRNA residues required for efficient recruitment of initiator tRNA(Met) and AUG selection. Genes Dev., 22, 2242-2255.
31. Dong, J., Qiu, H., Garcia-Barrio, M., Anderson, J. And Hinnebusch, A. G. (2000) Uncharged tRNA activates GCN2 by displacing the protein kinase moiety from a bipartite tRNA-binding domain. Mol. Cell, 6, 269-279.
32. Hashem, Y., des Georges, A., Dhote, V., Langlois, R., Liao, H. Y., Grassucci, R. A., Hellen, C. U., Pestova, T. V. And Frank, J. (2013) Structure of the Mammalian Ribosomal 43S Preinitiation Complex Bound to the Scanning Factor DHX29. Cell, 153, 1108-1119.
33. Hinnebusch, A. G. And Lorsch, J. R. (2012) The mechanism of eukaryotic translation initiation: new insights and challenges. Cold Spring Harb. Perspect. Biol., 4, 1-25.
34. Battiste, J. B., Pestova, T. V., Hellen, C. U. T. And Wagner, G. (2000) The eIF1A solution structure reveals a large RNA-binding surface important for scanning function. Mol. Cell, 5, 109-119.
35. DeLano, W. L. (2002) PyMol Molecular Graphics System User's Manual. In: PyMol User's Manual. DeLano Scientific, Palo Alto, CA.
36. Taylor, D. J., Devkota, B., Huang, A. D., Topf, M., Narayanan, E., Sali, A., Harvey, S. C. And Frank, J. (2009) Comprehensive molecular structure of the eukaryotic ribosome. Structure, 17, 1591-1604.