Molecular architecture of a eukaryotic translational initiation complex

Science

Volumn 342, Issue 6160, 2013, Pages

  Fernández, Israel S ^a   Bai, Xiao Chen ^a   Hussain, Tanweer ^a   Kelley, Ann C ^a   Lorsch, Jon R ^b,c   Ramakrishnan, V ^a   Scheres, Sjors H W ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Eunice Kennedy Shriver Institute of Child Health and Human Development   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EIF5B PROTEIN; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE DERIVATIVE; INITIATION FACTOR; INITIATION FACTOR 1; INITIATION FACTOR 2; INITIATION FACTOR 5; MESSENGER RNA; PEPTIDYLTRANSFERASE; RIBOSOMAL PROTEIN L9; RIBOSOME PROTEIN; RNA 28S; TRANSFER RNA; UNCLASSIFIED DRUG; EUKARYOTIC INITIATION FACTOR 5B; EUKARYOTIC INITIATION FACTOR-5B; METHIONINE TRANSFER RNA;

EUKARYOTE; GENE EXPRESSION; MOLECULAR ANALYSIS; RNA;

ARTICLE; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; ELECTRON; FEEDBACK SYSTEM; IMAGE ANALYSIS; IN VITRO STUDY; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOLECULAR RECOGNITION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RIBOSOME SUBUNIT; SACCHAROMYCES CEREVISIAE; START CODON; TRANSCRIPTION INITIATION SITE; TRANSLATION INITIATION; ANALYSIS; CHEMISTRY; HUMAN; METHODOLOGY; PROTEIN CONFORMATION; RIBOSOME; RNA TRANSLATION; PROCEDURES;

EUKARYOTA;

ANALYTIC SAMPLE PREPARATION METHODS; CRYOELECTRON MICROSCOPY; EUKARYOTIC INITIATION FACTORS; HUMANS; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PROTEIN CONFORMATION; RIBOSOMES; RNA, TRANSFER, MET; SACCHAROMYCES CEREVISIAE;

EID: 84887101681     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.1240585     Document Type: Article

References (39)

1. A. Marintchev, G. Wagner, Translation initiation: Structures, mechanisms and evolution. Q. Rev. Biophys. 37, 197-284 (2004). doi: 10.1017/ S0033583505004026; pmid: 16194295
2. N. Sonenberg, A. G. Hinnebusch, Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell 136, 731-745 (2009). doi: 10.1016/j.cell.2009.01.042; pmid: 19239892
3. R. J. Jackson, C. U. Hellen, T. V. Pestova, The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 11, 113-127 (2010). doi: 10.1038/nrm2838; pmid: 20094052
4. C. E. Aitken, J. R. Lorsch, A mechanistic overview of translation initiation in eukaryotes. Nat. Struct. Mol. Biol. 19, 568-576 (2012). doi: 10.1038/nsmb.2303; pmid: 22664984
5. A. Roll-Mecak, B. S. Shin, T. E. Dever, S. K. Burley, Engaging the ribosome: Universal IFs of translation. Trends Biochem. Sci. 26, 705- 709 (2001). doi: 10.1016/S0968-0004(01)02024-2; pmid: 11738593
6. A. G. Hinnebusch, J. R. Lorsch, The mechanism of eukaryotic translation initiation: New insights and challenges. Cold Spring Harb. Perspect. Biol. 4, a011544 (2012). doi: 10.1101/cshperspect.a011544; pmid: 22815232
7. B. S. Strunk, M. N. Novak, C. L. Young, K. Karbstein, A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 150, 111-121 (2012). doi: 10.1016/j.cell.2012.04.044; pmid: 22770215
8. S. Lebaron et al., Proofreading of pre-40S ribosome maturation by a translation initiation factor and 60S subunits. Nat. Struct. Mol. Biol. 19, 744-753 (2012). doi: 10.1038/nsmb.2308; pmid: 22751017
9. A. Ben-Shem et al ., The structure of the eukaryotic ribosome at 3.0 Å resolution. Science 334, 1524-1529 (2011). doi: 10.1126/science.1212642; pmid: 22096102
10. J. Rabl, M. Leibundgut, S. F. Ataide, A. Haag, N. Ban, Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science 331, 730-736 (2011). doi: 10.1126/science.1198308; pmid: 21205638
11. S. Klinge, F. Voigts-Hoffmann, M. Leibundgut, S. Arpagaus, N. Ban, Crystal structure of the eukaryotic ribosomal subunit in complex with initiation factor 6. Science 334, 941-948 (2011). doi: 10.1126/science.1211204; pmid: 22052974
12. S. H. Scheres, A Bayesian view on cryo-EM structure determination. J. Mol. Biol. 415, 406-418 (2012). doi: 10.1016/j.jmb.2011.11.010; pmid: 22100448
13. X. C. Bai, I. S. Fernandez, G. McMullan, S. H. Scheres, Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. Elife 2, e00461 (2013). doi: 10.7554/eLife.00461; pmid: 23427024
14. M. G. Acker, S. E. Kolitz, S. F. Mitchell, J. S. Nanda, J. R. Lorsch, Reconstitution of yeast translation initiation. Methods Enzymol. 430, 111-145 (2007). doi: 10.1016/S0076-6879(07)30006-2; pmid: 17913637
15. B. S. Shin et al., Uncoupling of initiation factor eIF5B/IF2 GTPase and translational activities by mutations that lower ribosome affinity. Cell 111, 1015-1025 (2002). doi: 10.1016/S0092-8674(02)01171-6; pmid: 12507428
16. B. S. Shin et al., rRNA suppressor of a eukaryotic translation initiation factor 5B/initiation factor 2 mutant reveals a binding site for translational GTPases on the small ribosomal subunit. Mol. Cell. Biol. 29, 808-821 (2009). doi: 10.1128/MCB.00896-08; pmid: 19029250
17. R. M. Voorhees, A. Weixlbaumer, D. Loakes, A. C. Kelley, V. Ramakrishnan, Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome. Nat. Struct. Mol. Biol. 16, 528-533 (2009). doi: 10.1038/nsmb.1577; pmid: 19363482
18. L. G. Trabuco et al., Applications of the molecular dynamics flexible fitting method. J. Struct. Biol. 173, 420-427 (2011). doi: 10.1016/j.jsb.2010. 09.024; pmid: 20932910
19. A. Roll-Mecak, C. Cao, T. E. Dever, S. K. Burley, X-Ray structures of the universal translation initiation factor IF2/eIF5B: Conformational changes on GDP and GTP binding. Cell 103, 781-792 (2000). doi: 10.1016/S0092-8674(00)00181- 1; pmid: 11114334
20. G. S. Allen, A. Zavialov, R. Gursky, M. Ehrenberg, J. Frank, The cryo-EM structure of a translation initiation complex from Escherichia coli. Cell 121, 703-712 (2005). doi: 10.1016/j.cell.2005.03.023; pmid: 15935757
21. R. M. Voorhees, T. M. Schmeing, A. C. Kelley, V. Ramakrishnan, The mechanism for activation of GTP hydrolysis on the ribosome. Science 330, 835-838 (2010). doi: 10.1126/science.1194460; pmid: 21051640
22. T. Lacombe et al., Linear ubiquitin fusion to Rps31 and its subsequent cleavage are required for the efficient production and functional integrity of 40S ribosomal subunits. Mol. Microbiol. 72, 69-84 (2009). doi: 10.1111/j.1365-2958.2009.06622.x; pmid: 19210616
23. J. P. Ballesta, M. Remacha, The large ribosomal subunit stalk as a regulatory element of the eukaryotic translational machinery. Prog. Nucleic Acid Res. Mol. Biol. 55, 157-193 (1996). doi: 10.1016/S0079-6603(08)60193-2; pmid: 8787610
24. L. D. Kapp, J. R. Lorsch, GTP-dependent recognition of the methionine moiety on initiator tRNA by translation factor eIF2. J. Mol. Biol. 335, 923-936 (2004). doi: 10.1016/j.jmb.2003.11.025; pmid: 14698289
25. D. S. Tourigny, I. S. Fernández, A. C. Kelley, V. Ramakrishnan, Elongation factor G bound to the ribosome in an intermediate state of translocation. Science 340, 1235490 (2013). doi: 10.1126/science.1235490; pmid: 23812720
26. T. V. Pestova et al., The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature 403, 332-335 (2000). doi: 10.1038/35002118; pmid: 10659855
27. M. G. Acker et al., Kinetic analysis of late steps of eukaryotic translation initiation. J. Mol. Biol. 385, 491-506 (2009). doi: 10.1016/j.jmb.2008.10.029; pmid: 18976658
28. T. Pape, W. Wintermeyer, M. Rodnina, Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome. EMBO J. 18, 3800-3807 (1999). doi: 10.1093/emboj/18.13.3800; pmid: 10393195
29. M. A. Algire et al., Development and characterization of a reconstituted yeast translation initiation system. RNA 8, 382-397 (2002). doi: 10.1017/S1355838202029527; pmid: 12008673
30. L. D. Kapp, J. R. Lorsch, The molecular mechanics of eukaryotic translation. Annu. Rev. Biochem. 73, 657-704 (2004). doi: 10.1146/annurev. biochem.73.030403.080419; pmid: 15189156
31. M. G. Acker, B. S. Shin, T. E. Dever, J. R. Lorsch, Interaction between eukaryotic initiation factors 1A and is required for efficient ribosomal subunit joining. J. Biol. Chem. 281, 8469-8475 (2006). doi: 10.1074/jbc.M600210200; pmid: 16461768
32. G. Tang et al., EMAN2: An extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007). doi: 10.1016/j.jsb.2006.05.009; pmid: 16859925
33. J. A. Mindell, N. Grigorieff, Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334- 347 (2003). doi: 10.1016/S1047-8477(03)00069-8; pmid: 12781660
34. S. H. Scheres, RELION: Implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012). doi: 10.1016/j.jsb.2012.09.006; pmid: 23000701
35. S. H. Scheres, S. Chen, Prevention of overfitting in cryo-EM structure determination. Nat. Methods 9, 853-854 (2012). doi: 10.1038/nmeth.2115; pmid: 22842542
36. P. B. Rosenthal, R. Henderson, Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 333, 721-745 (2003). doi: 10.1016/j.jmb.2003.07. 013; pmid: 14568533
37. E. F. Pettersen et al., UCSF Chimera - A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004). doi: 10.1002/jcc.20084; pmid: 15264254
38. P. Emsley, B. Lohkamp, W. G. Scott, K. Cowtan, Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010). doi: 10.1107/S0907444910007493; pmid: 20383002
39. J. P. Armache et al., Cryo-EM structure and rRNA model of a translating eukaryotic 80S ribosome at 5.5-A resolution. Proc. Natl. Acad. Sci. U.S.A. 107, 19748-19753 (2010). doi: 10.1073/pnas.1009999107; pmid: 20980660