Determinants of the rate of mRNA translocation in bacterial protein synthesis

Journal of Molecular Biology

Volumn 427, Issue 9, 2015, Pages 1835-1847

  Borg, Anneli ^a,b   Ehrenberg, Måns ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b 3H Biomedical AB Uppsala Science Park   (Sweden)

Author keywords

accuracy monitoring bases; fitness maximization; magnesium ions; mRNA translocation; speed accuracy trade off

Indexed keywords

BACTERIAL PROTEIN; BUFFER; ELONGATION FACTOR G; GUANOSINE TRIPHOSPHATE; MAGNESIUM ION; MESSENGER RNA; RNA 16S; TRANSFER RNA; START CODON;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ARTICLE; CELL FREE SYSTEM; CODON; CONCENTRATION (PARAMETERS); NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; RIBOSOME; RNA TRANSLATION; RNA TRANSPORT; ESCHERICHIA COLI; GENETICS; METABOLISM; PHYSIOLOGY; START CODON;

BACTERIA (MICROORGANISMS);

BACTERIAL PROTEINS; CODON, INITIATOR; ESCHERICHIA COLI; OPEN READING FRAMES; PEPTIDE ELONGATION FACTOR G; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA, RIBOSOMAL, 16S; RNA, TRANSFER;

EID: 84927635725     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.10.027     Document Type: Article

References (55)

1. R. Young, and H. Bremer Polypeptide-chain-elongation rate in Escherichia coli B/r as a function of growth rate Biochem J 160 1976 185 194
2. S. Proshkin, A.R. Rahmouni, A. Mironov, and E. Nudler Cooperation between translating ribosomes and RNA polymerase in transcription elongation Science 328 2010 504 508
3. S.T. Liang, Y.C. Xu, P. Dennis, and H. Bremer mRNA composition and control of bacterial gene expression J Bacteriol 182 2000 3037 3044
4. T.M. Schmeing, and V. Ramakrishnan What recent ribosome structures have revealed about the mechanism of translation Nature 461 2009 1234 1242
5. H. Bremer, and P. Dennis Modulation of chemical composition and other parameters of the cell by growth rate F.C. Neidhardt, Escherichia coli and Salmonella: Cellular and Molecular Biology 2 1996 ASM Press Washington, DC 1553 1569
6. H. Brunschede, and H. Bremer Synthesis and breakdown of proteins in Escherichia coli during amino-acid starvation J Mol Biol 57 1971 35 57
7. A.L. Goldberg, and J.F. Dice Intracellular protein degradation in mammalian and bacterial cells Annu Rev Biochem 43 1974 835 869
8. A.L. Goldberg, and A.C. St John Intracellular protein degradation in mammalian and bacterial cells: part 2 Annu Rev Biochem 45 1976 747 803
9. M.V. Rodnina, A. Savelsbergh, V.I. Katunin, and W. Wintermeyer Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome Nature 385 1997 37 41
10. M. Valle, A. Zavialov, J. Sengupta, U. Rawat, M. Ehrenberg, and J. Frank Locking and unlocking of ribosomal motions Cell 114 2003 123 134
11. S.M. Studer, J.S. Feinberg, and S. Joseph Rapid kinetic analysis of EF-G-dependent mRNA translocation in the ribosome J Mol Biol 327 2003 369 381
12. D.N. Ermolenko, Z.K. Majumdar, R.P. Hickerson, P.C. Spiegel, R.M. Clegg, and H.F. Noller Observation of intersubunit movement of the ribosome in solution using FRET J Mol Biol 370 2007 530 540
13. D. Pan, S.V. Kirillov, and B.S. Cooperman Kinetically competent intermediates in the translocation step of protein synthesis Mol Cell 25 2007 519 529
14. J. Chen, A. Petrov, A. Tsai, S.E. O'Leary, and J.D. Puglisi Coordinated conformational and compositional dynamics drive ribosome translocation Nat Struct Mol Biol 20 2013 718 727
15. M. Brune, J.L. Hunter, J.E. Corrie, and M.R. Webb Direct, real-time measurement of rapid inorganic phosphate release using a novel fluorescent probe and its application to actomyosin subfragment 1 ATPase Biochemistry 33 1994 8262 8271
16. M.V. Rodnina, A. Savelsbergh, N.B. Matassova, V.I. Katunin, Y.P. Semenkov, and W. Wintermeyer Thiostrepton inhibits the turnover but not the GTPase of elongation factor G on the ribosome Proc Natl Acad Sci USA 96 1999 9586 9590
17. P.V. Cornish, D.N. Ermolenko, H.F. Noller, and T. Ha Spontaneous intersubunit rotation in single ribosomes Mol Cell 30 2008 578 588
18. M. Johansson, J. Zhang, and M. Ehrenberg Genetic code translation displays a linear trade-off between efficiency and accuracy of tRNA selection Proc Natl Acad Sci USA 109 2012 131 136
19. C.G. Kurland, and M. Ehrenberg Optimization of translation accuracy Prog Nucleic Acid Res Mol Biol 31 1984 191 219
20. M.B. Feldman, D.S. Terry, R.B. Altman, and S.C. Blanchard Aminoglycoside activity observed on single pre-translocation ribosome complexes Nat Chem Biol 6 2010 244
21. O.G. Berg, and C.G. Kurland Growth rate-optimised tRNA abundance and codon usage J Mol Biol 270 1997 544 550
22. G. Zhang, M. Hubalewska, and Z. Ignatova Transient ribosomal attenuation coordinates protein synthesis and co-translational folding Nat Struct Mol Biol 16 2009 274 280
23. M. Stadler, and A. Fire Wobble base-pairing slows in vivo translation elongation in metazoans RNA 17 2011 2063 2073
24. N.T. Ingolia, L.F. Lareau, and J.S. Weissman Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes Cell 147 2011 789 802
25. B. Zinshteyn, and W.V. Gilbert Loss of a conserved tRNA anticodon modification perturbs cellular signaling PLoS Genet 9 2013 e1003675
26. G.W. Li, E. Oh, and J.S. Weissman The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria Nature 484 2012 538 541
27. J. Chen, A. Petrov, M. Johansson, A. Tsai, S.E. O'Leary, and J.D. Puglisi Dynamic pathways of - 1 translational frameshifting Nature 512 2014 328 332
28. W. Holtkamp, C.E. Cunha, F. Peske, A.L. Konevega, W. Wintermeyer, and M.V. Rodnina GTP hydrolysis by EF-G synchronizes tRNA movement on small and large ribosomal subunits EMBO J 33 2014 1073 1085
29. M. Johansson, E. Bouakaz, M. Lovmar, and M. Ehrenberg The kinetics of ribosomal peptidyl transfer revisited Mol Cell 30 2008 589 598
30. P.C. Jelenc, and C.G. Kurland Nucleoside triphosphate regeneration decreases the frequency of translation errors Proc Natl Acad Sci USA 76 1979 3174 3178
31. D.N. Ermolenko, and H.F. Noller mRNA translocation occurs during the second step of ribosomal intersubunit rotation Nat Struct Mol Biol 18 2011 457 462
32. S. Dorner, J.L. Brunelle, D. Sharma, and R. Green The hybrid state of tRNA binding is an authentic translation elongation intermediate Nat Struct Mol Biol 13 2006 234 241
33. C.E. Cunha, R. Belardinelli, F. Peske, W. Holtkamp, W. Wintermeyer, and M.V. Rodnina Dual use of GTP hydrolysis by elongation factor G on the ribosome Translation 1 2013 10.4161/trla.24315
34. Y. Semenkov, T. Shapkina, V. Makhno, and S. Kirillov Puromycin reaction for the A site-bound peptidyl-tRNA FEBS Lett 296 1992 207 210
35. A. Savelsbergh, V.I. Katunin, D. Mohr, F. Peske, M.V. Rodnina, and W. Wintermeyer An elongation factor G-induced ribosome rearrangement precedes tRNA-mRNA translocation Mol Cell 11 2003 1517 1523
36. T. Alatossava, H. Jutte, A. Kuhn, and E. Kellenberger Manipulation of intracellular magnesium content in polymyxin B nonapeptide-sensitized Escherichia coli by ionophore A23187 J Bacteriol 162 1985 413 419
37. V.I. Katunin, A. Savelsbergh, M.V. Rodnina, and W. Wintermeyer Coupling of GTP hydrolysis by elongation factor G to translocation and factor recycling on the ribosome Biochemistry 41 2002 12806 12812
38. Y.G. Gao, M. Selmer, C.M. Dunham, A. Weixlbaumer, A.C. Kelley, and V. Ramakrishnan The structure of the ribosome with elongation factor G trapped in the posttranslocational state Science 326 2009 694 699
39. J.M. Ogle, D.E. Brodersen, W.M. Clemons, M.J. Tarry, A.P. Carter, and V. Ramakrishnan Recognition of cognate transfer RNA by the 30S ribosomal subunit Science 292 2001 897 902
40. F. Peske, A. Savelsbergh, V.I. Katunin, M.V. Rodnina, and W. Wintermeyer Conformational changes of the small ribosomal subunit during elongation factor G-dependent tRNA-mRNA translocation J Mol Biol 343 2004 1183 1194
41. P. Satpati, J. Sund, and J. Aqvist Structure-based energetics of mRNA decoding on the ribosome Biochemistry 53 2014 1714 1722
42. N. Demeshkina, L. Jenner, E. Westhof, M. Yusupov, and G. Yusupova A new understanding of the decoding principle on the ribosome Nature 484 2012 256 259
43. K.B. Gromadski, T. Daviter, and M.V. Rodnina A uniform response to mismatches in codon-anticodon complexes ensures ribosomal fidelity Mol Cell 21 2006 369 377
44. T. Pape, W. Wintermeyer, and M.V. Rodnina Conformational switch in the decoding region of 16S rRNA during aminoacyl-tRNA selection on the ribosome Nat Struct Biol 7 2000 104 107
45. E.G. Wagner, P.C. Jelenc, M. Ehrenberg, and C.G. Kurland Rate of elongation of polyphenylalanine in vitro Eur J Biochem 122 1982 193 197
46. M. Ehrenberg, and C.G. Kurland Costs of accuracy determined by a maximal growth rate constraint Q Rev Biophys 17 1984 45 82
47. M.Y. Pavlov, and M. Ehrenberg Optimal control of gene expression for fast proteome adaptation to environmental change Proc Natl Acad Sci USA 110 2013 20527 20532
48. A. Zorzet, M.Y. Pavlov, A.I. Nilsson, M. Ehrenberg, and D.I. Andersson Error-prone initiation factor 2 mutations reduce the fitness cost of antibiotic resistance Mol Microbiol 75 2010 1299 1313
49. M.Y. Pavlov, A. Zorzet, D.I. Andersson, and M. Ehrenberg Activation of initiation factor 2 by ligands and mutations for rapid docking of ribosomal subunits EMBO J 30 2011 289 301
50. M. Lovmar, and M. Ehrenberg Rate, accuracy and cost of ribosomes in bacterial cells Biochimie 88 2006 951 961
51. S. Yoshizawa, D. Fourmy, and J.D. Puglisi Recognition of the codon-anticodon helix by ribosomal RNA Science 285 1999 1722 1725
52. K.B. Gromadski, and M.V. Rodnina Kinetic determinants of high-fidelity tRNA discrimination on the ribosome Mol Cell 13 2004 191 200
53. A. Antoun, M.Y. Pavlov, T. Tenson, and M.M. Ehrenberg Ribosome formation from subunits studied by stopped-flow and Rayleigh light scattering Biol Proceed Online 6 2004 35 54
54. A.D. Kelmers, C.W. Hancher, E.F. Phares, and G. David Novelli Large-scale fermentation of Escherichia coli and recovery of transfer ribonucleic acids Methods Enzymol 20 1971 3 9
55. M.Y. Pavlov, and M. Ehrenberg Rate of translation of natural mRNAs in an optimized in vitro system Arch Biochem Biophys 328 1996 9 16