Ensemble cryo-EM elucidates the mechanism of translation fidelity

Nature

Volumn 546, Issue 7656, 2017, Pages 113-117

  Loveland, Anna B ^a   Demo, Gabriel ^a   Grigorieff, Nikolaus ^b   Korostelev, Andrei A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOACYL TRANSFER RNA; ELONGATION FACTOR TU; NUCLEOTIDE; ANTICODON; CODON; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; RNA 16S;

CYTOGENETICS; GENE EXPRESSION; GENOME; PHYSIOLOGY; RNA;

ANTICODON; ARTICLE; BINDING SITE; CONFORMATION; CRYOELECTRON MICROSCOPY; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; RIBOSOME; RNA TRANSLATION; CHEMISTRY; CODON; ESCHERICHIA COLI; GENETICS; METABOLISM; MOLECULAR MODEL; PROTEIN DOMAIN; PROTEIN SYNTHESIS; RIBOSOME SUBUNIT; ULTRASTRUCTURE;

ANTICODON; CODON; CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; GTP PHOSPHOHYDROLASES; GUANOSINE TRIPHOSPHATE; HYDROLYSIS; MODELS, MOLECULAR; PEPTIDE ELONGATION FACTOR TU; PROTEIN BIOSYNTHESIS; PROTEIN DOMAINS; RIBOSOME SUBUNITS; RIBOSOMES; RNA, RIBOSOMAL, 16S; RNA, TRANSFER, AMINO ACYL;

EID: 85020224321     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature22397     Document Type: Article

References (77)

1. Ogle, J. M., Murphy, F. V., IV, Tarry, M. J. & Ramakrishnan, V. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111, 721-732 (2002).
2. Rodnina, M. V., Pape, T., Fricke, R., Kuhn, L. & Wintermeyer, W. Initial binding of the elongation factor Tu.GTP.aminoacyl-tRNA complex preceding codon recognition on the ribosome. J. Biol. Chem. 271, 646-652 (1996).
3. Pape, T., Wintermeyer, W. & Rodnina, M. V. Conformational switch in the decoding region of 16S rRNA during aminoacyl-tRNA selection on the ribosome. Nat. Struct. Mol. Biol. 7, 104-107 (2000).
4. Pape, T., Wintermeyer, W. & Rodnina, M. Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome. EMBO J. 18, 3800-3807 (1999).
5. Gromadski, K. B. & Rodnina, M. V. Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Mol. Cell 13, 191-200 (2004).
6. Gromadski, K. B., Daviter, T. & Rodnina, M. V. A uniform response to mismatches in codon-Anticodon complexes ensures ribosomal fidelity. Mol. Cell 21, 369-377 (2006).
7. Zhang, J., Ieong, K.-W., Johansson, M. & Ehrenberg, M. Accuracy of initial codon selection by aminoacyl-tRNAs on the mRNA-programmed bacterial ribosome. Proc. Natl Acad. Sci. USA 112, 9602-9607 (2015).
8. Blanchard, S. C., Gonzalez, R. L., Kim, H. D., Chu, S. & Puglisi, J. D. tRNA selection and kinetic proofreading in translation. Nat. Struct. Mol. Biol. 11, 1008-1014 (2004).
9. Ieong, K.-W., Uzun, U., Selmer, M. & Ehrenberg, M. Two proofreading steps amplify the accuracy of genetic code translation. Proc. Natl Acad. Sci. USA 113, 13744-13749 (2016).
10. Voorhees, R. M. & Ramakrishnan, V. Structural basis of the translational elongation cycle. Annu. Rev. Biochem. 82, 203-236 (2013).
11. Maracci, C. & Rodnina, M. V. Review: translational GTPases. Biopolymers 105, 463-475 (2016).
12. Pape, T., Wintermeyer, W. & Rodnina, M. V. Complete kinetic mechanism of elongation factor Tu-dependent binding of aminoacyl-tRNA to the A site of the E. coli ribosome. EMBO J. 17, 7490-7497 (1998).
13. Rodnina, M. V., Fricke, R., Kuhn, L. & Wintermeyer, W. Codon-dependent conformational change of elongation factor Tu preceding GTP hydrolysis on the ribosome. EMBO J. 14, 2613-2619 (1995).
14. Schmeing, T. M. et al. The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326, 688-694 (2009).
15. Voorhees, R. M., Schmeing, T. M., Kelley, A. C. & Ramakrishnan, V. The mechanism for activation of GTP hydrolysis on the ribosome. Science 330, 835-838 (2010).
16. Hausner, T. P., Atmadja, J. & Nierhaus, K. H. Evidence that the G2661 region of 23S rRNA is located at the ribosomal binding sites of both elongation factors. Biochimie 69, 911-923 (1987).
17. Bilgin, N. & Ehrenberg, M. Mutations in 23 S ribosomal RNA perturb transfer RNA selection and can lead to streptomycin dependence. J. Mol. Biol. 235, 813-824 (1994).
18. Daviter, T., Wieden, H.-J. & Rodnina, M. V. Essential role of histidine 84 in elongation factor Tu for the chemical step of GTP hydrolysis on the ribosome. J. Mol. Biol. 332, 689-699 (2003).
19. Moazed, D., Robertson, J. M. & Noller, H. F. Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23S RNA. Nature 334, 362-364 (1988).
20. Ogle, J. M. et al. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292, 897-902 (2001).
21. Jenner, L., Demeshkina, N., Yusupova, G. & Yusupov, M. Structural rearrangements of the ribosome at the tRNA proofreading step. Nat. Struct. Mol. Biol. 17, 1072-1078 (2010).
22. Selmer, M. et al. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313, 1935-1942 (2006).
23. Demeshkina, N., Jenner, L., Westhof, E., Yusupov, M. & Yusupova, G. A new understanding of the decoding principle on the ribosome. Nature 484, 256-259 (2012).
24. Zeng, X., Chugh, J., Casiano-Negroni, A., Al-Hashimi, H. M. & Brooks, C. L., III. Flipping of the ribosomal A-site adenines provides a basis for tRNA selection. J. Mol. Biol. 426, 3201-3213 (2014).
25. Schrode, P., Huter, P., Clementi, N. & Erlacher, M. Atomic mutagenesis at the ribosomal decoding site. RNA Biol. 14, 104-112 (2016).
26. Khade, P. K., Shi, X. & Joseph, S. Steric complementarity in the decoding center is important for tRNA selection by the ribosome. J. Mol. Biol. 425, 3778-3789 (2013).
27. Lyumkis, D., Brilot, A. F., Theobald, D. L. & Grigorieff, N. Likelihood-based classification of cryo-EM images using FREALIGN. J. Struct. Biol. 183, 377-388 (2013).
28. Grigorieff, N. Frealign: an exploratory tool for single-particle cryo-EM. Methods Enzymol. 579, 191-226 (2016).
29. Loveland, A. B. et al. Ribosome.RelA structures reveal the mechanism of stringent response activation. eLife 5, e17029 (2016).
30. Wimberly, B. T. et al. Structure of the 30S ribosomal subunit. Nature 407, 327-339 (2000).
31. Schuwirth, B. S. et al. Structures of the bacterial ribosome at 3.5 A resolution. Science 310, 827-834 (2005).
32. Nissen, P. et al. Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science 270, 1464-1472 (1995).
33. Fischer, N. et al. Structure of the E. coli ribosome-EF-Tu complex at 3 A resolution by Cs-corrected cryo-EM. Nature 520, 567-570 (2015
34. Valle, M. et al. Cryo-EM reveals an active role for aminoacyl-tRNA in the accommodation process. EMBO J. 21, 3557-3567 (2002).
35. Stark, H. et al. Visualization of elongation factor Tu on the Escherichia coli ribosome. Nature 389, 403-406 (1997).
36. Ledoux, S. & Uhlenbeck, O. C. Different aa-tRNAs are selected uniformly on the ribosome. Mol. Cell 31, 114-123 (2008).
37. Fahlman, R. P., Dale, T. & Uhlenbeck, O. C. Uniform binding of aminoacylated transfer RNAs to the ribosomal A and P sites. Mol. Cell 16, 799-805 (2004).
38. Zhang, J., Ieong, K.-W., Mellenius, H. & Ehrenberg, M. Proofreading neutralizes potential error hotspots in genetic code translation by transfer RNAs. RNA 22, 896-904 (2016).
39. Powers, T. & Noller, H. F. Evidence for functional interaction between elongation factor Tu and 16S ribosomal RNA. Proc. Natl Acad. Sci. USA 90, 1364-1368 (1993).
40. Cochella, L., Brunelle, J. L. & Green, R. Mutational analysis reveals two independent molecular requirements during transfer RNA selection on the ribosome. Nat. Struct. Mol. Biol. 14, 30-36 (2007).
41. Abdi, N. M. & Fredrick, K. Contribution of 16S rRNA nucleotides forming the 30S subunit A and P sites to translation in Escherichia coli. RNA 11, 1624-1632 (2005).
42. Santer, M. et al. Functional effects of a G to U base change at position 530 in a highly conserved loop of Escherichia coli 16S RNA. Biochemistry 32, 5539-5547 (1993).
43. Taliaferro, D. L. & Farabaugh, P. J. Testing constraints on rRNA bases that make nonsequence-specific contacts with the codon-Anticodon complex in the ribosomal A site. RNA 13, 1279-1286 (2007).
44. Westhof, E. Isostericity and tautomerism of base pairs in nucleic acids. FEBS Lett. 588, 2464-2469 (2014).
45. Fischer, N. et al. The pathway to GTPase activation of elongation factor SelB on the ribosome. Nature 540, 80-85 (2016).
46. Budkevich, T. V. et al. Regulation of the mammalian elongation cycle by subunit rolling: a eukaryotic-specific ribosome rearrangement. Cell 158, 121-131 (2014).
47. Brilot, A. F., Korostelev, A. A., Ermolenko, D. N. & Grigorieff, N. Structure of the ribosome with elongation factor G trapped in the pretranslocation state. Proc. Natl Acad. Sci. USA 110, 20994-20999 (2013).
48. Moazed, D. & Noller, H. F. Interaction of tRNA with 23S rRNA in the ribosomal A, P, and E sites. Cell 57, 585-597 (1989).
49. Moazed, D. & Noller, H. F. Transfer RNA shields specific nucleotides in 16S ribosomal RNA from attack by chemical probes. Cell 47, 985-994 (1986).
50. Traub, P., Mizushima, S., Lowry, C. V. & Nomura, M. in Nucleic Acids and Protein Synthesis, Part C (eds Kaplan, N. & Colowick, N.) Vol. 20, 391-407 (Academic Press, 1971).
51. Walker, S. E. & Fredrick, K. Preparation and evaluation of acylated tRNAs. Methods 44, 81-86 (2008).
52. Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36-51 (2005).
53. Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76 (1996).
54. Grant, T. & Grigorieff, N. Measuring the optimal exposure for single particle cryo-EM using a 2.6 A reconstruction of rotavirus VP6. eLife 4, e06980 (2015).
55. Grant, T. & Grigorieff, N. Automatic estimation and correction of anisotropic magnification distortion in electron microscopes. J. Struct. Biol. 192, 204-208 (2015).
56. Mindell, J. A. & Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
57. Chen, J. Z. & Grigorieff, N. SIGNATURE: a single-particle selection system for molecular electron microscopy. J. Struct. Biol. 157, 168-173 (2007).
58. Gabashvili, I. S. et al. Solution structure of the E. coli 70S ribosome at 11.5 A resolution. Cell 100, 537-549 (2000).
59. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
60. Cardone, G., Heymann, J. B. & Steven, A. C. One number does not fit all: mapping local variations in resolution in cryo-EM reconstructions. J. Struct. Biol. 184, 226-236 (2013).
61. Korostelev, A. et al. Crystal structure of a translation termination complex formed with release factor RF2. Proc. Natl Acad. Sci. USA 105, 19684-19689 (2008).
62. Rozov, A., Westhof, E., Yusupov, M. & Yusupova, G. The ribosome prohibits the G.U wobble geometry at the first position of the codon-Anticodon helix. Nucleic Acids Res. 44, 6434-6441 (2016).
63. Bairoch, A., Boeckmann, B., Ferro, S. & Gasteiger, E. Swiss-Prot: juggling between evolution and stability. Brief. Bioinform. 5, 39-55 (2004).
64. Tishchenko, S. et al. High-resolution crystal structure of the isolated ribosomal L1 stalk. Acta Crystallogr. D 68, 1051-1057 (2012).
65. Pettersen, E. F. et al. UCSF Chimera-A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
66. Korostelev, A., Bertram, R. & Chapman, M. S. Simulated-Annealing real-space refinement as a tool in model building. Acta Crystallogr. D 58, 761-767 (2002).
67. Chapman, M. S. Restrained real-space macromolecular atomic refinement using a new resolution-dependent electron-density function. Acta Crystallogr. A 51, 69-80 (1995).
68. Gonen, T. et al. Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438, 633-638 (2005).
69. Zhou, G., Wang, J., Blanc, E. & Chapman, M. S. Determination of the relative precision of atoms in a macromolecular structure. Acta Crystallogr. D 54, 391-399 (1998).
70. Laurberg, M. et al. Structural basis for translation termination on the 70S ribosome. Nature 454, 852-857 (2008).
71. Adams, P. D. et al. The Phenix software for automated determination of macromolecular structures. Methods 55, 94-106 (2011).
72. Brunger, A. T. Version 1.2 of the crystallography and NMR system. Nat. Protocols 2, 2728-2733 (2007).
73. Chen, V. B. et al. MolProbity: all-Atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12-21 (2010).
74. DeLano, W. L. The PyMOL Molecular Graphics System (DeLano Scientific, 2002).
75. Tinoco, I. Jr & Gonzalez, R. L. Jr. Biological mechanisms, one molecule at a time. Genes Dev. 25, 1205-1231 (2011).
76. Gonzalez, R. L. Jr, Chu, S. & Puglisi, J. D. Thiostrepton inhibition of tRNA delivery to the ribosome. RNA 13, 2091-2097 (2007).
77. Engh, R. A. & Huber, R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Cryst A 47, 392-400 (1991).