Crystal Structure of 70S Ribosome with Both Cognate tRNAs in the E and P Sites Representing an Authentic Elongation Complex

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Feng, Shu ^a   Chen, Yun ^a   Gao, Yong Gui ^a,b,c  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR G; MESSENGER RNA; NUCLEAR PROTEIN; RIBOSOMAL PROTEIN L6; RIBOSOME RNA; TRANSFER RNA; UNCLASSIFIED DRUG;

70S RIBOSOME; ANTICODON; ARTICLE; BASE PAIRING; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CODON; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; NONHUMAN; PROTEIN INTERACTION; RIBOSOME; RNA BINDING; RNA CONFORMATION; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

CODON; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; NUCLEIC ACID CONFORMATION; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PEPTIDE ELONGATION FACTORS; PROTEIN BINDING; PROTEIN CONFORMATION; RIBOSOME SUBUNITS; RNA, MESSENGER; RNA, TRANSFER;

EID: 84875116452     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058829     Document Type: Article

References (49)

1. Schmeing TM, Ramakrishnan V, (2009) What recent ribosome structures have revealed about the mechanism of translation. Nature 461: 1234-1242.
2. Frank J, Agrawal RK, (2000) A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406: 319-322.
3. Moazed D, Noller HF, (1989) Intermediate states in the movement of transfer RNA in the ribosome. Nature 342: 142-148.
4. Rodnina MV, Savelsbergh A, Katunin VI, Wintermeyer W, (1997) Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385: 37-41.
5. Bodley JW, Zieve FJ, Lin L, Zieve ST, (1970) Studies on translocation. 3. Conditions necessary for the formation and detection of a stable ribosome-G factor-guanosine diphosphate complex in the presence of fusidic acid. J Biol Chem 245: 5656-5661.
6. Rheinberger HJ, Sternbach H, Nierhaus KH, (1981) Three tRNA binding sites on Escherichia coli ribosomes. Proc Natl Acad Sci 78: 5310-5314.
7. Agrawal RK, Penczek P, Grassucci RA, Burkhardt N, Nierhaus KH, et al. (1999) Effect of buffer conditions on the position of tRNA on the 70 S ribosome as visualized by cryoelectron microscopy. J Biol Chem 274: 8723-8729.
8. Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, et al. (2001) Crystal structure of the ribosome at 5.5 A resolution. Science 292: 883-896.
9. Lill R, Robertson JM, Wintermeyer W, (1989) Binding of the 3′ terminus of tRNA to 23S rRNA in the ribosomal exit site actively promotes translocation. Embo J 8: 3933-3938.
10. Walker SE, Shoji S, Pan D, Cooperman BS, Fredrick K, (2008) Role of hybrid tRNA-binding states in ribosomal translocation. Proc Natl Acad Sci U S A 105: 9192-9197.
11. Nierhaus KH, (2006) Decoding errors and the involvement of the E-site. Biochimie 88: 1013-1019.
12. Marquez V, Wilson DN, Tate WP, Triana-Alonso F, Nierhaus KH, (2004) Maintaining the ribosomal reading frame: the influence of the E site during translational regulation of release factor 2. Cell 118: 45-55.
13. Petropoulos AD, Green R, (2012) Further in vitro exploration fails to support the allosteric three-site model. J Biol Chem 287: 11642-11648.
14. Nierhaus KH, Pech M, (2012) Problems with the Analyses of the Ribosomal Allosteric Three-site Model. J Biol Chem 287: 27049.
15. Jenner LB, Demeshkina N, Yusupova G, Yusupov M, (2010) Structural aspects of messenger RNA reading frame maintenance by the ribosome. Nat Struct Mol Biol 17: 555-560.
16. Jenner L, Rees B, Yusupov M, Yusupova G, (2007) Messenger RNA conformations in the ribosomal E site revealed by X-ray crystallography. EMBO Rep 8: 846-850.
17. Gao YG, Selmer M, Dunham CM, Weixlbaumer A, Kelley AC, et al. (2009) The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326: 694-699.
18. Selmer M, Gao YG, Weixlbaumer A, Ramakrishnan V, (2012) Ribosome engineering to promote new crystal forms. Acta Crystallogr D Biol Crystallogr 68: 578-583.
19. Selmer M, Dunham CM, Murphy FVt, Weixlbaumer A, Petry S, et al. (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313: 1935-1942.
20. Kabsch W, (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Cryst 26: 795-200.
21. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921.
22. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
23. Collaborative Computational Project Number 4 (1994) The CCP4 suite: Programs for protein crystallography. Acta Cryst D50: 760-763.
24. Ogle JM, Brodersen DE, Clemons WM Jr, Tarry MJ, Carter AP, et al. (2001) Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292: 897-902.
25. Zaher HS, Green R, (2009) Quality control by the ribosome following peptide bond formation. Nature 457: 161-166.
26. Jorgensen F, Kurland CG, (1990) Processivity errors of gene expression in Escherichia coli. J Mol Biol 215: 511-521.
27. Trabuco LG, Schreiner E, Eargle J, Cornish P, Ha T, et al. (2010) The role of L1 stalk-tRNA interaction in the ribosome elongation cycle. J Mol Biol 402: 741-760.
28. Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A, et al. (2005) Structures of the bacterial ribosome at 3.5 A resolution. Science 310: 827-834.
29. Fukai S, Nureki O, Sekine S, Shimada A, Vassylyev DG, et al. (2003) Mechanism of molecular interactions for tRNA(Val) recognition by valyl-tRNA synthetase. RNA 9: 100-111.
30. Du X, Wang ED, (2003) Tertiary structure base pairs between D- and TpsiC-loops of Escherichia coli tRNA(Leu) play important roles in both aminoacylation and editing. Nucleic Acids Res 31: 2865-2872.
31. Pan D, Kirillov S, Zhang CM, Hou YM, Cooperman BS, (2006) Rapid ribosomal translocation depends on the conserved 18-55 base pair in P-site transfer RNA. Nat Struct Mol Biol 13: 354-359.
32. Nissen P, Kjeldgaard M, Thirup S, Polekhina G, Reshetnikova L, et al. (1995) Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science 270: 1464-1472.
33. Schmeing TM, Voorhees RM, Kelley AC, Gao YG, Murphy FVt, et al. (2009) The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326: 688-694.
34. Cukras AR, Southworth DR, Brunelle JL, Culver GM, Green R, (2003) Ribosomal proteins S12 and S13 function as control elements for translocation of the mRNA:tRNA complex. Mol Cell 12: 321-328.
35. Cukras AR, Green R, (2005) Multiple effects of S13 in modulating the strength of intersubunit interactions in the ribosome during translation. J Mol Biol 349: 47-59.
36. Davies C, Bussiere DE, Golden BL, Porter SJ, Ramakrishnan V, et al. (1998) Ribosomal proteins S5 and L6: high-resolution crystal structures and roles in protein synthesis and antibiotic resistance. J Mol Biol 279: 873-888.
37. Rodnina MV, Stark H, Savelsbergh A, Wieden HJ, Mohr D, et al. (2000) GTPases mechanisms and functions of translation factors on the ribosome. Biol Chem 381: 377-387.
38. Nechifor R, Wilson KS, (2007) Crosslinking of translation factor EF-G to proteins of the bacterial ribosome before and after translocation. J Mol Biol 368: 1412-1425.
39. Norstrom T, Lannergard J, Hughes D, (2007) Genetic and phenotypic identification of fusidic acid-resistant mutants with the small-colony-variant phenotype in Staphylococcus aureus. Antimicrob Agents Chemother 51: 4438-4446.
40. Kuhberger R, Piepersberg W, Petzet A, Buckel P, Bock A, (1979) Alteration of ribosomal protein L6 in gentamicin-resistant strains of Escherichia coli. Effects on fidelity of protein synthesis. Biochemistry 18: 187-193.
41. Devaraj A, Shoji S, Holbrook ED, Fredrick K, (2009) A role for the 30S subunit E site in maintenance of the translational reading frame. RNA 15: 255-265.
42. Sanders CL, Curran JF, (2007) Genetic analysis of the E site during RF2 programmed frameshifting. RNA 13: 1483-1491.
43. Blaha G, Nierhaus KH, (2001) Features and functions of the ribosomal E site. Cold Spring Harb Symp Quant Biol 66: 135-146.
44. Cornish PV, Ermolenko DN, Staple DW, Hoang L, Hickerson RP, et al. (2009) Following movement of the L1 stalk between three functional states in single ribosomes. Proc Natl Acad Sci U S A 106: 2571-2576.
45. Blaha G, Stanley RE, Steitz TA, (2009) Formation of the first peptide bond: the structure of EF-P bound to the 70S ribosome. Science 325: 966-970.
46. Dunkle JA, Wang L, Feldman MB, Pulk A, Chen VB, et al. (2011) Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science 332: 981-984.
47. Zhou J, Lancaster L, Trakhanov S, Noller HF, (2012) Crystal structure of release factor RF3 trapped in the GTP state on a rotated conformation of the ribosome. RNA 18: 230-240.
48. Jin H, Kelley AC, Ramakrishnan V, (2011) Crystal structure of the hybrid state of ribosome in complex with the guanosine triphosphatase release factor 3. Proc Natl Acad Sci U S A 108: 15798-15803.
49. Fei J, Bronson JE, Hofman JM, Srinivas RL, Wiggins CH, et al. (2009) Allosteric collaboration between elongation factor G and the ribosomal L1 stalk directs tRNA movements during translation. Proc Natl Acad Sci U S A 106: 15702-15707.