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

Cell

Volumn 121, Issue 5, 2005, Pages 703-712

  Allen, Gregory S ^a   Zavialov, Andrey ^b   Gursky, Richard ^a   Ehrenberg, Måns ^b   Frank, Joachim ^a,c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UPPSALA UNIVERSITY   (Sweden)

^c STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE; INITIATION FACTOR 1; INITIATION FACTOR 2; INITIATION FACTOR 3; METHIONINE TRANSFER RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ESCHERICHIA COLI; MOLECULAR STABILITY; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RIBOSOME SUBUNIT; TRANSLATION INITIATION;

EID: 20444365142     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2005.03.023     Document Type: Article

References (64)

1. A. Antoun, M.Y. Pavlov, K. Andersson, T. Tenson, and M. Ehrenberg The roles of initiation factor 2 and guanosine triphosphate in initiation of protein synthesis EMBO J. 22 2003 5593 5601
2. A. Antoun, M.Y. Pavlov, T. Tenson, and M.M. Ehrenberg Ribosome formation from subunits studied by stopped-flow and Rayleigh light scattering Biol. Proced. Online 6 2004 35 54
3. P. Beaudry, G. Sander, M. Grunberg-Manago, and P. Douzou Cation-induced regulatory mechanism of GTPase activity dependent on polypeptide initiation factor 2 Biochemistry 18 1979 202 207
4. S.C. Blanchard, R.L. Gonzalez, H.D. Kim, S. Chu, and J.D. Puglisi tRNA selection and kinetic proofreading in translation Nat. Struct. Mol. Biol. 11 2004 1008 1014
5. E.V. Bocharov, A.G. Sobol, K.V. Pavlov, D.M. Korzhnev, V.A. Jaravine, A.T. Gudkov, and A.S. Arseniev From structure and dynamics of protein L7/L12 to molecular switching in ribosome J. Biol. Chem. 279 2004 17697 17706
6. N. Brooijmans, K.A. Sharp, and I.D. Kuntz Stability of macromolecular complexes Proteins 48 2002 645 653
7. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, and N.S. Pannu Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
8. M.A. Canonaco, R.A. Calogero, and C.O. Gualerzi Mechanism of translational initiation in prokaryotes. Evidence for a direct effect of IF2 on the activity of the 30 S ribosomal subunit FEBS Lett. 207 1986 198 204
9. M. Carson Ribbons Methods Enzymol. 277 1997 493 505
10. A.P. Carter, W.M. Clemons Jr., D.E. Brodersen, R.J. Morgan-Warren, T. Hartsch, B.T. Wimberly, and V. Ramakrishnan Crystal structure of an initiation factor bound to the 30S ribosomal subunit Science 291 2001 498 501
11. J.Z. Chen, J. Furst, M.S. Chapman, and N. Grigorieff Low-resolution structure refinement in electron microscopy J. Struct. Biol. 144 2003 144 151
12. A. Dallas, and H.F. Noller Interaction of translation initiation factor 3 with the 30S ribosomal subunit Mol. Cell 8 2001 855 864
13. D. Dey, D.E. Bochkariov, G.G. Jokhadze, and R.R. Traut Cross-linking of selected residues in the N- and C-terminal domains of Escherichia coli protein L7/L12 to other ribosomal proteins and the effect of elongation factor Tu J. Biol. Chem. 273 1998 1670 1676
14. J. Frank, and R.K. Agrawal A ratchet-like inter-subunit reorganization of the ribosome during translocation Nature 406 2000 318 322
15. J. Frank, M. Radermacher, P. Penczek, J. Zhu, Y. Li, M. Ladjadj, and A. Leith SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116 1996 190 199
16. H. Gao, J. Sengupta, M. Valle, A. Korostelev, N. Eswar, S.M. Stagg, P. Van Roey, R.K. Agrawal, S.C. Harvey, and A. Sali Study of the structural dynamics of the E coli 70S ribosome using real-space refinement Cell 113 2003 789 801
17. H. Gao, M. Valle, M. Ehrenberg, and J. Frank Dynamics of EF-G interaction with the ribosome explored by classification of a heterogeneous cryo-EM dataset J. Struct. Biol. 147 2004 283 290
18. D.J. Goss, L.J. Parkhurst, and A.J. Wahba Kinetic studies on the interaction of chain initiation factor 3 with 70 S Escherichia coli ribosomes and subunits J. Biol. Chem. 257 1982 10119 10127
19. C. Grigoriadou, S. Marzi, H.S. Seo, P. Dongli, S. Kirillov, C.O. Gualerzi, and B.S. Cooperman IF2, IF3 and thiostrepton interaction during initiation complex formation A. Hinnebusch T. Pestova J. Richter Translational Control 2004 Cold Spring Harbor Laboratory Press Cold Spring Harbor, New York 407
20. Y. Groner, and M. Revel Escherichia coli initiation factors: isolation of an IF2-fMet-transfer RNA complex J. Mol. Biol. 74 1973 407 410
21. M. Grunberg-Manago, J. Dondon, and M. Graffe Inhibition by thiostrepton of the IF-2-dependent ribosomal GTPase FEBS Lett. 22 1972 217 221
22. M. Grunberg-Manago, P. Dessen, D. Pantaloni, T. Godefroy-Colburn, A.D. Wolfe, and J. Dondon Light-scattering studies showing the effect of initiation factors on the reversible dissociation of Escherichia coli ribosomes J. Mol. Biol. 94 1975 461 478
23. C. Gualerzi, C.L. Pon, and A. Kaji Initiation factor dependent release of aminoacyl-tRNAs from complexes of 30S ribosomal subunits, synthetic polynucleotide and aminoacyl tRNA Biochem. Biophys. Res. Commun. 45 1971 1312 1319
24. C.O. Gualerzi, and C.L. Pon Initiation of mRNA translation in prokaryotes Biochemistry 29 1990 5881 5889
25. M. Guenneugues, E. Caserta, L. Brandi, R. Spurio, S. Meunier, C.L. Pon, R. Boelens, and C.O. Gualerzi Mapping the fMet-tRNA(f)(Met) binding site of initiation factor IF2 EMBO J. 19 2000 5233 5240
26. D. Hartz, D.S. McPheeters, and L. Gold Selection of the initiator tRNA by Escherichia coli initiation factors Genes Dev. 3 1989 1899 1912
27. D. Hartz, J. Binkley, T. Hollingsworth, and L. Gold Domains of initiator tRNA and initiation codon crucial for initiator tRNA selection by Escherichia coli IF3 Genes Dev. 4 1990 1790 1800
28. R.L. Heimark, J.W. Hersehy, and R.R. Traut Cross-linking of initiation factor IF2 to proteins L7/L12 in 70 S ribosomes of Escherichia coli J. Biol. Chem. 251 1976 779 784
29. H.K. Huang, H. Yoon, E.M. Hannig, and T.F. Donahue GTP hydrolysis controls stringent selection of the AUG start codon during translation initiation in Saccharomyces cerevisiae Genes Dev. 11 1997 2396 2413
30. T.A. Jones, J.Y. Zou, and S.W. Cowan Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallogr. A 47 1991 110 119
31. R. Karimi, M.Y. Pavlov, R.H. Buckingham, and M. Ehrenberg Novel roles for classical factors at the interface between translation termination and initiation Mol. Cell 3 1999 601 609
32. A.C. Kay, and M. Grunberg-Manago The mechanism of action of initiation factor IF1: non-analogy with elongation factor EFTs Biochim. Biophys. Acta 277 1972 225 230
33. J.H. Lee, S.K. Choi, A. Roll-Mecak, S.K. Burley, and T.E. Dever Universal conservation in translation initiation revealed by human and archaeal homologs of bacterial translation initiation factor IF2 Proc. Natl. Acad. Sci. USA 96 1999 4342 4347
34. A.H. Lockwood, P.R. Chakraborty, and U. Maitra A complex between initiation factor IF2, guanosine triphosphate, and fMet-tRNA: an intermediate in initiation complex formation Proc. Natl. Acad. Sci. USA 68 1971 3122 3126
35. S. Luchin, H. Putzer, J.W. Hershey, Y. Cenatiempo, M. Grunberg-Manago, and S. Laalami In vitro study of two dominant inhibitory GTPase mutants of Escherichia coli translation initiation factor IF2. Direct evidence that GTP hydrolysis is necessary for factor recycling J. Biol. Chem. 274 1999 6074 6079
36. S. Marzi, W. Knight, L. Brandi, E. Caserta, N. Soboleva, W.E. Hill, C.O. Gualerzi, and J.S. Lodmell Ribosomal localization of translation initiation factor IF2 RNA 9 2003 958 969
37. C. Mayer, C. Kohrer, E. Kenny, C. Prusko, and U.L. RajBhandary Anticodon sequence mutants of Escherichia coli initiator tRNA: effects of overproduction of aminoacyl-tRNA synthetases, methionyl-tRNA formyltransferase, and initiation factor 2 on activity in initiation Biochemistry 42 2003 4787 4799
38. J.P. McCutcheon, R.K. Agrawal, S.M. Philips, R.A. Grassucci, S.E. Gerchman, W.M. Clemons Jr., V. Ramakrishnan, and J. Frank Location of translational initiation factor IF3 on the small ribosomal subunit Proc. Natl. Acad. Sci. USA 96 1999 4301 4306
39. D. Mohr, W. Wintermeyer, and M.V. Rodnina GTPase activation of elongation factors Tu and G on the ribosome Biochemistry 41 2002 12520 12528
40. L. Montesano-Roditis, D.G. Glitz, R.R. Traut, and P.L. Stewart Cryo-electron microscopic localization of protein L7/L12 within the Escherichia coli 70 S ribosome by difference mapping and Nanogold labeling J. Biol. Chem. 276 2001 14117 14123
41. J.M. Moreno, J. Kildsgaard, I. Siwanowicz, K.K. Mortensen, and H.U. Sperling-Petersen 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 1998 465 471
42. J.M. Moreno, L. Drskjotersen, J.E. Kristensen, K.K. Mortensen, and H.U. Sperling-Petersen Characterization of the domains of E. coli initiation factor IF2 responsible for recognition of the ribosome FEBS Lett. 455 1999 130 134
43. N.R. Nyengaard, K.K. Mortensen, S.F. Lassen, J.W. Hershey, and H.U. Sperling-Petersen Tandem translation of E. coli initiation factor IF2 beta: purification and characterization in vitro of two active forms Biochem. Biophys. Res. Commun. 181 1991 1572 1579
44. H.U. Petersen, T. Roll, M. Grunberg-Manago, and B.F. Clark Specific interaction of initiation factor IF2 of E. coli with formylmethionyl-tRNA f Met Biochem. Biophys. Res. Commun. 91 1979 1068 1074
45. H.U. Petersen, T.A. Kruse, H. Worm-Leonhard, G.E. Siboska, B.F. Clark, A.S. Boutorin, P. Remy, J.P. Ebel, J. Dondon, and M. Grunberg-Manago Study of the interaction of Escherichia coli initiation factor IF2 with formylmethionyl-tRNAMetf by partial digestion with cobra venom ribonuclease FEBS Lett. 128 1981 161 165
46. U. Pieper, N. Eswar, H. Braberg, M.S. Madhusudhan, F.P. Davis, A.C. Stuart, N. Mirkovic, A. Rossi, M.A. Marti-Renom, and A. Fiser MODBASE, a database of annotated comparative protein structure models, and associated resources Nucleic Acids Res. 32 Database issue 2004 D217 D222
47. M. Pioletti, F. Schlunzen, J. Harms, R. Zarivach, M. Gluhmann, H. Avila, A. Bashan, H. Bartels, T. Auerbach, and C. Jacobi Crystal structures of complexes of the small ribosomal subunit with tetracycline, edeine and IF3 EMBO J. 20 2001 1829 1839
48. C.L. Pon, and C.O. Gualerzi Mechanism of protein biosynthesis in prokaryotic cells. Effect of initiation factor IF1 on the initial rate of 30 S initiation complex formation FEBS Lett. 175 1984 203 207
49. C.L. Pon, and C.O. Gualerzi Mechanism of translational initiation in prokaryotes. IF3 is released from ribosomes during and not before 70 S initiation complex formation FEBS Lett. 195 1986 215 219
50. B.K. Rath, R. Hegerl, A. Leith, T.R. Shaikh, T. Wagenknecht, and J. Frank Fast 3D motif search of EM density maps using a locally normalized cross-correlation function J. Struct. Biol. 144 2003 95 103
51. A. Roll-Mecak, C. Cao, T.E. Dever, and S.K. Burley X-Ray structures of the universal translation initiation factor IF2/eIF5B: conformational changes on GDP and GTP binding Cell 103 2000 781 792
52. H. Shi, and P.B. Moore The crystal structure of yeast phenylalanine tRNA at 1.93 A resolution: a classic structure revisited RNA 6 2000 1091 1105
53. B.S. Shin, D. Maag, A. Roll-Mecak, M.S. Arefin, S.K. Burley, J.R. Lorsch, and T.E. Dever Uncoupling of initiation factor eIF5B/IF2 GTPase and translational activities by mutations that lower ribosome affinity Cell 111 2002 1015 1025
54. J. Shine, and L. Dalgarno The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites Proc. Natl. Acad. Sci. USA 71 1974 1342 1346
55. M. Valle, A. Zavialov, W. Li, S.M. Stagg, J. Sengupta, R.C. Nielsen, P. Nissen, S.C. Harvey, M. Ehrenberg, and J. Frank Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy Nat. Struct. Biol. 10 2003 899 906
56. M. Valle, A. Zavialov, J. Sengupta, U. Rawat, M. Ehrenberg, and J. Frank Locking and unlocking of ribosomal motions Cell 114 2003 123 134
57. I.R. Vetter, and A. Wittinghofer The guanine nucleotide-binding switch in three dimensions Science 294 2001 1299 1304
58. H. Wakao, P. Romby, E. Westhof, S. Laalami, M. Grunberg-Manago, J.P. Ebel, C. Ehresmann, and B. Ehresmann The solution structure of the Escherichia coli initiator tRNA and its interactions with initiation factor 2 and the ribosomal 30 S subunit J. Biol. Chem. 264 1989 20363 20371
59. H. Wakao, P. Romby, S. Laalami, J.P. Ebel, C. Ehresmann, and B. Ehresmann Binding of initiation factor 2 and initiator tRNA to the Escherichia coli 30S ribosomal subunit induces allosteric transitions in 16S rRNA Biochemistry 29 1990 8144 8151
60. J. Weiel, and J.W. Hershey The binding of fluorescein-labeled protein synthesis initiation factor 2 to Escherichia coli 30 S ribosomal subunits determined by fluorescence polarization J. Biol. Chem. 257 1982 1215 1220
61. W. Wintermeyer, and C. Gualerzi Effect of Escherichia coli initiation factors on the kinetics of N-Acphe-tRNAPhe binding to 30S ribosomal subunits. A fluorescence stopped-flow study Biochemistry 22 1983 690 694
62. A.V. Zavialov, and M. Ehrenberg Peptidyl-tRNA regulates the GTPase activity of translation factors Cell 114 2003 113 122
63. A.V. Zavialov, R.H. Buckingham, and M. Ehrenberg A posttermination ribosomal complex is the guanine nucleotide exchange factor for peptide release factor RF3 Cell 107 2001 115 124
64. F.H. Zucker, and J.W. Hershey Binding of Escherichia coli protein synthesis initiation factor IF1 to 30S ribosomal subunits measured by fluorescence polarization Biochemistry 25 1986 3682 3690