On the pH dependence of class-1 RF-dependent termination of mRNA translation

Journal of Molecular Biology

Volumn 427, Issue 9, 2015, Pages 1848-1860

  Indrisiunaite, Gabriele ^a   Pavlov, Michael Y ^a   Heurgué Hamard, Valérie ^b   Ehrenberg, Måns ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

Author keywords

conformational change; fast kinetics; nucleophile; release factor; ribosome

Indexed keywords

AMINOACYL TRANSFER RNA; BACTERIAL PROTEIN; MESSENGER RNA; PEPTIDE FRAGMENT; STOP CODON; TRANSFER RNA; TRANSLATION TERMINATION FACTOR;

CHEMICAL STRUCTURE; GENETICS; METABOLISM; PH; PHYSIOLOGY; PROTEIN SYNTHESIS; RIBOSOME; STOP CODON;

BACTERIAL PROTEINS; CODON, TERMINATOR; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PEPTIDE TERMINATION FACTORS; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA, TRANSFER; RNA, TRANSFER, AMINO ACYL;

EID: 84932126313     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.01.007     Document Type: Article

References (53)

1. E. Scolnick, R. Tompkins, T. Caskey, and M. Nirenberg Release factors differing in specificity for terminator codons Proc Natl Acad Sci U S A 61 1968 768 774
2. D.V. Freistroffer, M.Y. Pavlov, J. MacDougall, R.H. Buckingham, and M. Ehrenberg Release factor RF3 in E. coli accelerates the dissociation of release factors RF1 and RF2 from the ribosome in a GTP-dependent manner EMBO J 16 1997 4126 4133
3. 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
4. A.V. Zavialov, L. Mora, R.H. Buckingham, and M. Ehrenberg Release of peptide promoted by the GGQ motif of class 1 release factors regulates the GTPase activity of RF3 Mol Cell 10 2002 789 798
5. 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
6. L. Kisselev, M. Ehrenberg, and L. Frolova Termination of translation: interplay of mRNA, rRNAs and release factors? EMBO J 22 2003 175 182
7. E.M. Youngman, M.E. McDonald, and R. Green Peptide release on the ribosome: mechanism and implications for translational control Annu Rev Microbiol 62 2008 353 373
8. D.S. Konecki, K.C. Aune, W. Tate, and C.T. Caskey Characterization of reticulocyte release factor J Biol Chem 252 1977 4514 4520
9. J. Salas-Marco, and D.M. Bedwell GTP hydrolysis by eRF3 facilitates stop codon decoding during eukaryotic translation termination Mol Cell Biol 24 2004 7769 7778
10. E.Z. Alkalaeva, A.V. Pisarev, L.Y. Frolova, L.L. Kisselev, and T.V. Pestova In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3 Cell 125 2006 1125 1136
11. D.E. Eyler, K.A. Wehner, and R. Green Eukaryotic release factor 3 is required for multiple turnovers of peptide release catalysis by eukaryotic release factor 1 J Biol Chem 288 2013 29530 29538
12. L. Mora, A. Zavialov, M. Ehrenberg, and R.H. Buckingham Stop codon recognition and interactions with peptide release factor RF3 of truncated and chimeric RF1 and RF2 from Escherichia coli Mol Microbiol 50 2003 1467 1476
13. L.Y. Frolova, R.Y. Tsivkovskii, G.F. Sivolobova, N.Y. Oparina, O.I. Serpinsky, and V.M. Blinov Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis RNA 5 1999 1014 1020
14. A. Korostelev, H. Asahara, L. Lancaster, M. Laurberg, A. Hirschi, and J. Zhu Crystal structure of a translation termination complex formed with release factor RF2 Proc Natl Acad Sci U S A 105 2008 19684 19689
15. M. Laurberg, H. Asahara, A. Korostelev, J. Zhu, S. Trakhanov, and H.F. Noller Structural basis for translation termination on the 70S ribosome Nature 454 2008 852 857
16. S. Petry, D.E. Brodersen, F.V.t. Murphy, C.M. Dunham, M. Selmer, and M.J. Tarry Crystal structures of the ribosome in complex with release factors RF1 and RF2 bound to a cognate stop codon Cell 123 2005 1255 1266
17. H. Jin, A.C. Kelley, D. Loakes, and V. Ramakrishnan Structure of the 70S ribosome bound to release factor 2 and a substrate analog provides insights into catalysis of peptide release Proc Natl Acad Sci U S A 107 2010 8593 8598
18. B.P. Klaholz, T. Pape, A.V. Zavialov, A.G. Myasnikov, E.V. Orlova, and B. Vestergaard Structure of the Escherichia coli ribosomal termination complex with release factor 2 Nature 421 2003 90 94
19. U.B. Rawat, A.V. Zavialov, J. Sengupta, M. Valle, R.A. Grassucci, and J. Linde A cryo-electron microscopic study of ribosome-bound termination factor RF2 Nature 421 2003 87 90
20. H. Song, P. Mugnier, A.K. Das, H.M. Webb, D.R. Evans, and M.F. Tuite The crystal structure of human eukaryotic release factor eRF1-mechanism of stop codon recognition and peptidyl-tRNA hydrolysis Cell 100 2000 311 321
21. L. Mora, V. Heurgue-Hamard, S. Champ, M. Ehrenberg, L.L. Kisselev, and R.H. Buckingham The essential role of the invariant GGQ motif in the function and stability in vivo of bacterial release factors RF1 and RF2 Mol Microbiol 47 2003 267 275
22. J.J. Shaw, and R. Green Two distinct components of release factor function uncovered by nucleophile partitioning analysis Mol Cell 28 2007 458 467
23. S. Trobro, and J. Aqvist A model for how ribosomal release factors induce peptidyl-tRNA cleavage in termination of protein synthesis Mol Cell 27 2007 758 766
24. V. Dincbas-Renqvist, A. Engstrom, L. Mora, V. Heurgue-Hamard, R. Buckingham, and M. Ehrenberg A post-translational modification in the GGQ motif of RF2 from Escherichia coli stimulates termination of translation EMBO J 19 2000 6900 6907
25. V. Heurgue-Hamard, S. Champ, A. Engstrom, M. Ehrenberg, and R.H. Buckingham The hemK gene in Escherichia coli encodes the N(5)-glutamine methyltransferase that modifies peptide release factors EMBO J 21 2002 769 778
26. V. Heurgue-Hamard, S. Champ, L. Mora, T. Merkulova-Rainon, L.L. Kisselev, and R.H. Buckingham The glutamine residue of the conserved GGQ motif in Saccharomyces cerevisiae release factor eRF1 is methylated by the product of the YDR140w gene J Biol Chem 280 2005 2439 2445
27. P. Liu, S. Nie, B. Li, Z.Q. Yang, Z.M. Xu, and J. Fei Deficiency in a glutamine-specific methyltransferase for release factor causes mouse embryonic lethality Mol Cell Biol 30 2010 4245 4253
28. D. Liger, L. Mora, N. Lazar, S. Figaro, J. Henri, and N. Scrima Mechanism of activation of methyltransferases involved in translation by the Trm112 "hub" protein Nucleic Acids Res 39 2011 6249 6259
29. S. Kuhlenkoetter, W. Wintermeyer, and M.V. Rodnina Different substrate-dependent transition states in the active site of the ribosome Nature 476 2011 351 354
30. J.J. Shaw, S. Trobro, S.L. He, J. Aqvist, and R. Green A Role for the 2′ OH of peptidyl-tRNA substrate in peptide release on the ribosome revealed through RF-mediated rescue Chem Biol 19 2012 983 993
31. B. Vestergaard, L.B. Van, G.R. Andersen, J. Nyborg, R.H. Buckingham, and M. Kjeldgaard Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1 Mol Cell 8 2001 1375 1382
32. D.H. Shin, J. Brandsen, J. Jancarik, H. Yokota, R. Kim, and S.H. Kim Structural analyses of peptide release factor 1 from Thermotoga maritima reveal domain flexibility required for its interaction with the ribosome J Mol Biol 341 2004 227 239
33. B. Vestergaard, S. Sanyal, M. Roessle, L. Mora, R.H. Buckingham, and J.S. Kastrup The SAXS solution structure of RF1 differs from its crystal structure and is similar to its ribosome bound cryo-EM structure Mol Cell 20 2005 929 938
34. G. Zoldak, L. Redecke, D.I. Svergun, P.V. Konarev, C.S. Voertler, and H. Dobbek Release factors 2 from Escherichia coli and Thermus thermophilus: structural, spectroscopic and microcalorimetric studies Nucleic Acids Res 35 2007 1343 1353
35. M. Graille, V. Heurgue-Hamard, S. Champ, L. Mora, N. Scrima, and N. Ulryck Molecular basis for bacterial class I release factor methylation by PrmC Mol Cell 20 2005 917 927
36. M. Johansson, K.W. Ieong, S. Trobro, P. Strazewski, J. Aqvist, and M.Y. Pavlov pH-sensitivity of the ribosomal peptidyl transfer reaction dependent on the identity of the A-site aminoacyl-tRNA Proc Natl Acad Sci U S A 108 2011 79 84
37. R.A. Alberty, and V. Massey On the interpretation of the pH variation of the maximum initial velocity of an enzyme-catalyzed reaction Biochim Biophys Acta 13 1954 347 353
38. P.C. Jelenc, and C.G. Kurland Nucleoside triphosphate regeneration decreases the frequency of translation errors Proc Natl Acad Sci U S A 76 1979 3174 3178
39. J.A. da Silva, J. Felcman, C.C. Lopes, R.S.C. Lopes, and J.D.F. Villar Study of the protonation/deprotonation sequence of two polyamines: bis-[(2S)-2-pyrrolidinylmethyl] ethylenediamine and spermidine by H-1 and C-13 nuclear magnetic resonance Spectrosc Lett 35 2002 643 661
40. S. Trobro, and J. Aqvist Mechanism of the translation termination reaction on the ribosome Biochemistry 48 2009 11296 11303
41. D.V. Freistroffer, M. Kwiatkowski, R.H. Buckingham, and M. Ehrenberg The accuracy of codon recognition by polypeptide release factors Proc Natl Acad Sci U S A 97 2000 2046 2051
42. A. Fersht Enzyme structure and mechanism 1977 W. H. Freeman, Reading [Eng.] San Francisco
43. B. Hetrick, K. Lee, and S. Joseph Kinetics of stop codon recognition by release factor 1 Biochemistry 48 2009 11178 11184
44. E.M. Youngman, S.L. He, L.J. Nikstad, and R. Green Stop codon recognition by release factors induces structural rearrangement of the ribosomal decoding center that is productive for peptide release Mol Cell 28 2007 533 543
45. S.L. He, and R. Green Visualization of codon-dependent conformational rearrangements during translation termination Nat Struct Mol Biol 17 2010 465 470
46. U. Rawat, H. Gao, A. Zavialov, R. Gursky, M. Ehrenberg, and J. Frank Interactions of the release factor RF1 with the ribosome as revealed by cryo-EM J Mol Biol 357 2006 1144 1153
47. T. Pape, W. Wintermeyer, and M. Rodnina Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome EMBO J 18 1999 3800 3807
48. N. Santos, J. Zhu, J.P. Donohue, A.A. Korostelev, and H.F. Noller Crystal structure of the 70S ribosome bound with the Q253P mutant form of release factor RF2 Structure 21 2013 1258 1263
49. M. Johansson, E. Bouakaz, M. Lovmar, and M. Ehrenberg The kinetics of ribosomal peptidyl transfer revisited Mol Cell 30 2008 589 598
50. 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
51. A. Soffientini, R. Lorenzetti, L. Gastaldo, J.H. Parlett, R. Spurio, and A. La Teana Purification procedure for bacterial translational initiation factors IF2 and IF3 Protein Expr Purif 5 1994 118 124
52. 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
53. M. Ehrenberg, N. Bilgin, and C. Kurland Design and use of a fast and accurate in vitro translation system in ribosomes and protein synthesis: a practical approach G. Spedding, 1990 IRL Press at Oxford University Press Oxford, UK 101 129