The cryo-EM structure of a complete 30S translation initiation complex from Escherichia coli

PLoS Biology

Volumn 9, Issue 7, 2011, Pages

  Julián, Patricia ^a   Milon, Pohl ^b   Agirrezabala, Xabier ^a   Lasso, Gorka ^a   Gil, David ^a   Rodnina, Marina V ^b   Valle, Mikel ^a,c  

^a CIC BIOGUNE   (Spain)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

30S TRANSLATION INITIATION COMPLEX; BACTERIAL PROTEIN; GUANOSINE TRIPHOSPHATE; INITIATION FACTOR 1; INITIATION FACTOR 2; INITIATION FACTOR 3; MESSENGER RNA; TRANSFER RNA; UNCLASSIFIED DRUG; FMET TRNA(FMET); FMET-TRNA(FMET); INITIATION FACTOR; METHIONINE TRANSFER RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYO ELECTRON MICROSCOPY; ELECTRON MICROSCOPY; ESCHERICHIA COLI; HYDROLYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; TRANSLATION INITIATION; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; CRYOELECTRON MICROSCOPY; GENETICS; METABOLISM; SMALL RIBOSOMAL SUBUNIT; ULTRASTRUCTURE;

ESCHERICHIA COLI;

CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PEPTIDE INITIATION FACTORS; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RNA, MESSENGER; RNA, TRANSFER, MET;

EID: 79960917084     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001095     Document Type: Article

References (72)

1. Gualerzi C. O, Pon C. L, (1990) Initiation of mRNA translation in prokaryotes. Biochemistry 29: 5881-5889.
2. Laursen B. S, Sorensen H. P, Mortensen K. K, Sperling-Petersen H. U, (2005) Initiation of protein synthesis in bacteria. Microbiol Mol Biol Rev 69: 101-123.
3. Studer S. M, Joseph S, (2006) Unfolding of mRNA secondary structure by the bacterial translation initiation complex. Mol Cell 22: 105-115.
4. Korostelev A, Trakhanov S, Asahara H, Laurberg M, Lancaster L, et al. (2007) Interactions and dynamics of the Shine Dalgarno helix in the 70S ribosome. Proc Natl Acad Sci U S A 104: 16840-16843.
5. Yusupova G. Z, Yusupov M. M, Cate J. H, Noller H. F, (2001) The path of messenger RNA through the ribosome. Cell 106: 233-241.
6. Selmer M, Dunham C. M, Murphy F. V. t, Weixlbaumer A, Petry S, et al. (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313: 1935-1942.
7. Carter A. P, Clemons W. M Jr, Brodersen D. E, Morgan-Warren R. J, Hartsch T, et al. (2001) Crystal structure of an initiation factor bound to the 30S ribosomal subunit. Science 291: 498-501.
8. Caserta E, Tomsic J, Spurio R, La Teana A, Pon C. L, et al. (2006) Translation initiation factor IF2 interacts with the 30 S ribosomal subunit via two separate binding sites. J Mol Biol 362: 787-799.
9. Moreno J. M, Drskjotersen L, Kristensen J. E, Mortensen K. K, Sperling-Petersen H. U, (1999) Characterization of the domains of E. coli initiation factor IF2 responsible for recognition of the ribosome. FEBS Lett 455: 130-134.
10. Milon P, Carotti M, Konevega A. L, Wintermeyer W, Rodnina M. V, et al. (2010) The ribosome-bound initiation factor 2 recruits initiator tRNA to the 30S initiation complex. EMBO Rep 11: 312-316.
11. Simonetti A, Marzi S, Myasnikov A. G, Fabbretti A, Yusupov M, et al. (2008) Structure of the 30S translation initiation complex. Nature 455: 416-420.
12. Allen G. S, Zavialov A, Gursky R, Ehrenberg M, Frank J, (2005) The cryo-EM structure of a translation initiation complex from Escherichia coli. Cell 121: 703-712.
13. Myasnikov A. G, Marzi S, Simonetti A, Giuliodori A. M, Gualerzi C. O, et al. (2005) Conformational transition of initiation factor 2 from the GTP- to GDP-bound state visualized on the ribosome. Nat Struct Mol Biol 12: 1145-1149.
14. Milon P, Konevega A. L, Gualerzi C. O, Rodnina M. V, (2008) Kinetic checkpoint at a late step in translation initiation. Mol Cell 30: 712-720.
15. McCutcheon J. P, Agrawal R. K, Philips S. M, Grassucci R. A, Gerchman S. E, et al. (1999) Location of translational initiation factor IF3 on the small ribosomal subunit. Proc Natl Acad Sci U S A 96: 4301-4306.
16. Fabbretti A, Pon C. L, Hennelly S. P, Hill W. E, Lodmell J. S, et al. (2007) The real-time path of translation factor IF3 onto and off the ribosome. Mol Cell 25: 285-296.
17. Dallas A, Noller H. F, (2001) Interaction of translation initiation factor 3 with the 30S ribosomal subunit. Mol Cell 8: 855-864.
18. Lomakin I. B, Kolupaeva V. G, Marintchev A, Wagner G, Pestova T. V, (2003) Position of eukaryotic initiation factor eIF1 on the 40S ribosomal subunit determined by directed hydroxyl radical probing. Genes Dev 17: 2786-2797.
19. Grunberg-Manago M, Dessen P, Pantaloni D, Godefroy-Colburn T, Wolfe A. D, et al. (1975) Light-scattering studies showing the effect of initiation factors on the reversible dissociation of Escherichia coli ribosomes. J Mol Biol 94: 461-478.
20. Gualerzi C, Risuleo G, Pon C. L, (1977) Initial rate kinetic analysis of the mechanism of initiation complex formation and the role of initiation factor IF-3. Biochemistry 16: 1684-1689.
21. Wintermeyer W, Gualerzi C, (1983) Effect of Escherichia coli initiation factors on the kinetics of N-Acphe-tRNAPhe binding to the 30S ribosomal subunits. Biochemistry 22: 690-694.
22. Hartz D, Binkley J, Hollingsworth T, Gold L, (1990) Domains of initiator tRNA and initiation codon crucial for initiator tRNA selection by Escherichia coli IF3. Genes Dev 4: 1790-1800.
23. Hartz D, McPheeters D. S, Gold L, (1989) Selection of the initiator tRNA by Escherichia coli initiation factors. Genes Dev 3: 1899-1912.
24. Lomakin I. B, Shirokikh N. E, Yusupov M. M, Hellen C. U, Pestova T. V, (2006) The fidelity of translation initiation: reciprocal activities of eIF1, IF3 and YciH. Embo J 25: 196-210.
25. Betney R, de Silva E, Krishnan J, Stansfield I, Autoregulatory systems controlling translation factor expression: thermostat-like control of translational accuracy. Rna 16: 655-663.
26. Marshall R. A, Aitken C. E, Puglisi J. D, (2009) GTP hydrolysis by IF2 guides progression of the ribosome into elongation. Mol Cell 35: 37-47.
27. Brandi L, Fabbretti A, Milon P, Carotti M, Pon C. L, et al. (2007) Methods for identifying compounds that specifically target translation. Methods Enzymol 431: 229-267.
28. Antoun A, Pavlov M. Y, Lovmar M, Ehrenberg M, (2006) How initiation factors tune the rate of initiation of protein synthesis in bacteria. Embo J 25: 2539-2550.
29. Scheres S. H, Gao H, Valle M, Herman G. T, Eggermont P. P, et al. (2007) Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization. Nat Methods 4: 27-29.
30. Julian P, Konevega A. L, Scheres S. H, Lazaro M, Gil D, et al. (2008) Structure of ratcheted ribosomes with tRNAs in hybrid states. Proc Natl Acad Sci U S A 105: 16924-16927.
31. Schmitt E, Panvert M, Blanquet S, Mechulam Y, (1998) Crystal structure of methionyl-tRNAfMet transformylase complexed with the initiator formyl-methionyl-tRNAfMet. Embo J 17: 6819-6826.
32. Steffensen S. A, Poulsen A. B, Mortensen K. K, Sperling-Petersen H. U, (1997) E. coli translation initiation factor IF2-an extremely conserved protein. Comparative sequence analysis of the infB gene in clinical isolates of E. coli. FEBS Lett 419: 281-284.
33. Roll-Mecak A, Cao C, Dever T. E, Burley S. K, (2000) X-Ray structures of the universal translation initiation factor IF2/eIF5B: conformational changes on GDP and GTP binding. Cell 103: 781-792.
34. Moreno J. M, Kildsgaard J, Siwanowicz I, Mortensen K. K, Sperling-Petersen H. U, (1998) Binding of Escherichia coli initiation factor IF2 to 30S ribosomal subunits: a functional role for the N-terminus of the factor. Biochem Biophys Res Commun 252: 465-471.
35. Yusupov M. M, Yusupova G. Z, Baucom A, Lieberman K, Earnest T. N, et al. (2001) Crystal structure of the ribosome at 5.5 A resolution. Science 292: 883-896.
36. Biou V, Shu F, Ramakrishnan V, (1995) X-ray crystallography shows that translational initiation factor IF3 consists of two compact alpha/beta domains linked by an alpha-helix. Embo J 14: 4056-4064.
37. Garcia C, Fortier P. L, Blanquet S, Lallemand J. Y, Dardel F, (1995) Solution structure of the ribosome-binding domain of E. coli translation initiation factor IF3. Homology with the U1A protein of the eukaryotic spliceosome. J Mol Biol 254: 247-259.
38. Schmeing T. M, Voorhees R. M, Kelley A. C, Gao Y. G, Murphy F. Vt, et al. (2009) The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326: 688-694.
39. Tomsic J, Vitali L. A, Daviter T, Savelsbergh A, Spurio R, et al. (2000) Late events of translation initiation in bacteria: a kinetic analysis. Embo J 19: 2127-2136.
40. La Teana A, Gualerzi C. O, Brimacombe R, (1995) From stand-by to decoding site. Adjustment of the mRNA on the 30S ribosomal subunit under the influence of the initiation factors. Rna 1: 772-782.
41. Yusupova G, Jenner L, Rees B, Moras D, Yusupov M, (2006) Structural basis for messenger RNA movement on the ribosome. Nature 444: 391-394.
42. Gabashvili I. S, Agrawal R. K, Spahn C. M, Grassucci R. A, Svergun D. I, et al. (2000) Solution structure of the E. coli 70S ribosome at 11.5 A resolution. Cell 100: 537-549.
43. Agirrezabala X, Lei J, Brunelle J. L, Ortiz-Meoz R. F, Green R, et al. (2008) Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Mol Cell 32: 190-197.
44. Agrawal R. K, Sharma M. R, Kiel M. C, Hirokawa G, Booth T. M, et al. (2004) Visualization of ribosome-recycling factor on the Escherichia coli 70S ribosome: functional implications. Proc Natl Acad Sci U S A 101: 8900-8905.
45. Cornish P. V, Ermolenko D. N, Noller H. F, Ha T, (2008) Spontaneous intersubunit rotation in single ribosomes. Mol Cell 30: 578-588.
46. Ermolenko D. N, Majumdar Z. K, Hickerson R. P, Spiegel P. C, Clegg R. M, et al. (2007) Observation of intersubunit movement of the ribosome in solution using FRET. J Mol Biol 370: 530-540.
47. Frank J, Agrawal R. K, (2000) A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406: 318-322.
48. Gao H, Zhou Z, Rawat U, Huang C, Bouakaz L, et al. (2007) RF3 induces ribosomal conformational changes responsible for dissociation of class I release factors. Cell 129: 929-941.
49. Gao N, Zavialov A. V, Li W, Sengupta J, Valle M, et al. (2005) Mechanism for the disassembly of the posttermination complex inferred from cryo-EM studies. Mol Cell 18: 663-674.
50. Klaholz B. P, Myasnikov A. G, Van Heel M, (2004) Visualization of release factor 3 on the ribosome during termination of protein synthesis. Nature 427: 862-865.
51. Stark H, Rodnina M. V, Wieden H. J, van Heel M, Wintermeyer W, (2000) Large-scale movement of elongation factor G and extensive conformational change of the ribosome during translocation. Cell 100: 301-309.
52. Valle M, Zavialov A, Sengupta J, Rawat U, Ehrenberg M, et al. (2003) Locking and unlocking of ribosomal motions. Cell 114: 123-134.
53. Guenneugues M, Caserta E, Brandi L, Spurio R, Meunier S, et al. (2000) Mapping the fMet-tRNA(f)(Met) binding site of initiation factor IF2. Embo J 19: 5233-5240.
54. Kapralou S, Fabbretti A, Garulli C, Spurio R, Gualerzi C. O, et al. (2008) Translation initiation factor IF1 of Bacillus stearothermophilus and Thermus thermophilus substitute for Escherichia coli IF1 in vivo and in vitro without a direct IF1-IF2 interaction. Mol Microbiol 70: 1368-1377.
55. Tapprich W. E, Goss D. J, Dahlberg A. E, (1989) Mutation at position 791 in Escherichia coli 16S ribosomal RNA affects processes involved in the initiation of protein synthesis. Proc Natl Acad Sci U S A 86: 4927-4931.
56. McCarthy J. E, Brimacombe R, (1994) Prokaryotic translation: the interactive pathway leading to initiation. Trends Genet 10: 402-407.
57. Chen H, Bjerknes M, Kumar R, Jay E, (1994) Determination of the optimal aligned spacing between the Shine-Dalgarno sequence and the translation initiation codon of Escherichia coli mRNAs. Nucleic Acids Res 22: 4953-4957.
58. Ringquist S, Shinedling S, Barrick D, Green L, Binkley J, et al. (1992) Translation initiation in Escherichia coli: sequences within the ribosome-binding site. Mol Microbiol 6: 1219-1229.
59. Antoun A, Pavlov M. Y, Lovmar M, Ehrenberg M, (2006) How initiation factors maximize the accuracy of tRNA selection in initiation of bacterial protein synthesis. Mol Cell 23: 183-193.
60. Baxter W. T, Leith A, Frank J, (2007) SPIRE: the SPIDER reconstruction engine. J Struct Biol 157: 56-63.
61. Scheres S. H, Nunez-Ramirez R, Sorzano C. O, Carazo J. M, Marabini R, (2008) Image processing for electron microscopy single-particle analysis using XMIPP. Nat Protoc 3: 977-990.
62. Pettersen E. F, Goddard T. D, Huang C. C, Couch G. S, Greenblatt D. M, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
63. Arnold K, Bordoli L, Kopp J, Schwede T, (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
64. Altschul S. F, Madden T. L, Schaffer A. A, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
65. Laursen B. S, Mortensen K. K, Sperling-Petersen H. U, Hoffman D. W, (2003) A conserved structural motif at the N terminus of bacterial translation initiation factor IF2. J Biol Chem 278: 16320-16328.
66. Low H. H, Lowe J, (2006) A bacterial dynamin-like protein. Nature 444: 766-769.
67. Stolboushkina E, Nikonov S, Nikulin A, Blasi U, Manstein D. J, et al. (2008) Crystal structure of the intact archaeal translation initiation factor 2 demonstrates very high conformational flexibility in the alpha- and beta-subunits. J Mol Biol 382: 680-691.
68. Wienk H, Tomaselli S, Bernard C, Spurio R, Picone D, et al. (2005) Solution structure of the C1-subdomain of Bacillus stearothermophilus translation initiation factor IF2. Protein Sci 14: 2461-2468.
69. Meunier S, Spurio R, Czisch M, Wechselberger R, Guenneugues M, et al. (2000) Structure of the fMet-tRNA(fMet)-binding domain of B. stearothermophilus initiation factor IF2. Embo J 19: 1918-1926.
70. Guex N, Peitsch M. C, (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
71. Topf M, Lasker K, Webb B, Wolfson H, Chiu W, et al. (2008) Protein structure fitting and refinement guided by cryo-EM density. Structure 16: 295-307.
72. Notredame C, Higgins D. G, Heringa J, (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205-217.