Mechanism of ribosome rescue by ArfA and RF2

eLife

Volumn 6, Issue , 2017, Pages

  Demo, Gabriel ^a   Svidritskiy, Egor ^a   Madireddy, Rohini ^a,d   Diaz Avalos, Ruben ^b   Grant, Timothy ^b   Grigorieff, Nikolaus ^b   Sousa, Duncan ^c   Korostelev, Andrei A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c FLORIDA STATE UNIVERSITY   (United States)

^d Medicago USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE RIBOSOME RESCUE FACTOR A; DIPEPTIDYL PEPTIDASE I; PEPTIDE; PROTEINASE; RECRUITING RELEASE FACTOR 2; TRANSFER RNA; UNCLASSIFIED DRUG; ARFA PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; PRFB PROTEIN, E COLI; PROTEIN BINDING; RNA BINDING PROTEIN; TRANSLATION TERMINATION FACTOR;

AMINO TERMINAL SEQUENCE; ARTICLE; CRYOELECTRON MICROSCOPY; DNA SEQUENCE; ENZYME ACTIVITY; GENE EXPRESSION; GENE REARRANGEMENT; ION EXCHANGE CHROMATOGRAPHY; NONHUMAN; PROTEIN PURIFICATION; PROTEIN STRUCTURE; RIBOSOME; SEQUENCE ANALYSIS; SIZE EXCLUSION CHROMATOGRAPHY; STOP CODON; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; METABOLISM; ULTRASTRUCTURE;

CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI PROTEINS; PEPTIDE TERMINATION FACTORS; PROTEIN BINDING; RIBOSOMES; RNA-BINDING PROTEINS;

EID: 85017125753     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.23687     Document Type: Article

References (69)

1. Abeyrathne PD, Koh CS, Grant T, Grigorieff N, Korostelev AA. 2016. Ensemble cryo-EM uncovers inchworm-like translocation of a viral IRES through the ribosome. eLife 5:e14874. doi: 10.7554/eLife.14874 PMID: 27159452
2. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse- Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica Section D Biological Crystallography 66:213–221. doi: 10.1107/S0907444909052925 PMID: 20124702
3. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI- BLAST: a new generation of protein database search programs. Nucleic Acids Research 25:3389–3402. doi: 10.1093/nar/25.17.3389 PMID: 9254694
4. Arenz S, Abdelshahid M, Sohmen D, Payoe R, Starosta AL, Berninghausen O, Hauryliuk V, Beckmann R, Wilson DN. 2016. The stringent factor RelA adopts an open conformation on the ribosome to stimulate ppGpp synthesis. Nucleic Acids Research 44:6471–6481. doi: 10.1093/nar/gkw470 PMID: 27226493
5. Bairoch A, Boeckmann B, Ferro S, Gasteiger E. 2004. Swiss-Prot: juggling between evolution and stability. Briefings in Bioinformatics 5:39–55. doi: 10.1093/bib/5.1.39 PMID: 15153305
6. Brown A, Fernández IS, Gordiyenko Y, Ramakrishnan V. 2016. Ribosome-dependent activation of stringent control. Nature 534:277–280. doi: 10.1038/nature17675 PMID: 27279228
7. Brunger AT. 2007. Version 1.2 of the crystallography and NMR system. Nature Protocols 2:2728–2733. doi: 10. 1038/nprot.2007.406 PMID: 18007608
8. Chadani Y, Ono K, Ozawa S, Takahashi Y, Takai K, Nanamiya H, Tozawa Y, Kutsukake K, Abo T. 2010. Ribosome rescue by Escherichia coli ArfA (YhdL) in the absence of trans-translation system. Molecular Microbiology 78: 796–808. doi: 10.1111/j.1365-2958.2010.07375.x PMID: 21062370
9. Chadani Y, Matsumoto E, Aso H, Wada T, Kutsukake K, Sutou S, Abo T. 2011. trans-translation-mediated tight regulation of the expression of the alternative ribosome-rescue factor ArfA in Escherichia coli. Genes & Genetic Systems 86:151–163. doi: 10.1266/ggs.86.151 PMID: 21952205
10. Chadani Y, Ito K, Kutsukake K, Abo T. 2012. ArfA recruits release factor 2 to rescue stalled ribosomes by peptidyl-tRNA hydrolysis in Escherichia coli. Molecular Microbiology 86:37–50. doi: 10.1111/j.1365-2958.2012. 08190.x PMID: 22857598
11. Chapman MS. 1995. Restrained real-space macromolecular atomic refinement using a new resolution-dependent electron-density function. Acta Crystallographica Section a Foundations of Crystallography 51:69–80. doi: 10.1107/S0108767394007130
12. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallographica Section D Biological Crystallography 66:12–21. doi: 10.1107/S0907444909042073 PMID: 20057044
13. Craigen WJ, Caskey CT. 1987. The function, structure and regulation of E. coli peptide chain release factors. Biochimie 69:1031–1041. doi: 10.1016/0300-9084(87)90003-4 PMID: 3126822
14. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Research 14:1188–1190. doi: 10.1101/gr.849004 PMID: 15173120
15. DeLano WL. 2002. The PyMOL molecular graphics system. In: The PyMOL Molecular Graphics System. Palo Alto, CA, USA: DeLano Scientific.
16. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32:1792–1797. doi: 10.1093/nar/gkh340 PMID: 15034147
17. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallographica Section D Biological Crystallography 60:2126–2132. doi: 10.1107/S0907444904019158 PMID: 15572765
18. Freistroffer DV, Kwiatkowski M, Buckingham RH, Ehrenberg M. 2000. The accuracy of codon recognition by polypeptide release factors. PNAS 97:2046–2051. doi: 10.1073/pnas.030541097 PMID: 10681447
19. Gagnon MG, Seetharaman SV, Bulkley D, Steitz TA. 2012. Structural basis for the rescue of stalled ribosomes: structure of YaeJ bound to the ribosome. Science 335:1370–1372. doi: 10.1126/science.1217443 PMID: 22422986
20. Garza-Sánchez F, Schaub RE, Janssen BD, Hayes CS. 2011. tmRNA regulates synthesis of the ArfA ribosome rescue factor. Molecular Microbiology 80:1204–1219. doi: 10.1111/j.1365-2958.2011.07638.x PMID: 21435036
21. Gonen T, Cheng Y, Sliz P, Hiroaki Y, Fujiyoshi Y, Harrison SC, Walz T. 2005. Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438:633–638. doi: 10.1038/nature04321 PMID: 16319884
22. Grigorieff N. 2016. Frealign: an exploratory tool for Single-Particle Cryo-EM. Methods in Enzymology 579:191–226. doi: 10.1016/bs.mie.2016.04.013 PMID: 27572728
23. Handa Y, Inaho N, Nameki N. 2011. YaeJ is a novel ribosome-associated protein in Escherichia coli that can hydrolyze peptidyl-tRNA on stalled ribosomes. Nucleic Acids Research 39:1739–1748. doi: 10.1093/nar/gkq1097 PMID: 21051357
24. Hayes CS, Keiler KC. 2010. Beyond ribosome rescue: tmrna and co-translational processes. FEBS Letters 584: 413–419. doi: 10.1016/j.febslet.2009.11.023 PMID: 19914241
25. He SL, Green R. 2010. Visualization of codon-dependent conformational rearrangements during translation termination. Nature Structural & Molecular Biology 17:465–470. doi: 10.1038/nsmb.1766 PMID: 20208546
26. Huter P, Müller C, Beckert B, Arenz S, Berninghausen O, Beckmann R, Wilson DN. 2017. Structural basis for ArfA-RF2-mediated translation termination on mRNAs lacking stop codons. Nature 541:546–549. doi: 10.1038/nature20821 PMID: 27906161
27. Ito K, Chadani Y, Nakamori K, Chiba S, Akiyama Y, Abo T. 2011. Nascentome analysis uncovers futile protein synthesis in Escherichia coli. PLoS One 6:e28413. doi: 10.1371/journal.pone.0028413 PMID: 22162769
28. Ivanova N, Pavlov MY, Felden B, Ehrenberg M. 2004. Ribosome rescue by tmRNA requires truncated mRNAs. Journal of Molecular Biology 338:33–41. doi: 10.1016/j.jmb.2004.02.043 PMID: 15050821
29. James NR, Brown A, Gordiyenko Y, Ramakrishnan V. 2016. Translational termination without a stop codon. Science 354:1437–1440. doi: 10.1126/science.aai9127 PMID: 27934701
30. Keiler KC. 2015. Mechanisms of ribosome rescue in bacteria. Nature Reviews Microbiology 13:285–297. doi: 10.1038/nrmicro3438 PMID: 25874843
31. Kim DE, Chivian D, Baker D. 2004. Protein structure prediction and analysis using the robetta server. Nucleic Acids Research 32:W526–W531. doi: 10.1093/nar/gkh468 PMID: 15215442
32. Koh CS, Brilot AF, Grigorieff N, Korostelev AA. 2014. Taura syndrome virus IRES initiates translation by binding its tRNA-mRNA-like structural element in the ribosomal decoding center. PNAS 111:9139–9144. doi: 10.1073/pnas.1406335111 PMID: 24927574
33. Korostelev A, Bertram R, Chapman MS. 2002. Simulated-annealing real-space refinement as a tool in model building. Acta Crystallographica Section D Biological Crystallography 58:761–767. doi: 10.1107/S0907444902003402 PMID: 11976486
34. Korostelev A, Trakhanov S, Laurberg M, Noller HF. 2006. Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 126:1065–1077. doi: 10.1016/j.cell.2006.08.032 PMID: 16962654
35. Korostelev A, Asahara H, Lancaster L, Laurberg M, Hirschi A, Zhu J, Trakhanov S, Scott WG, Noller HF. 2008. Crystal structure of a translation termination complex formed with release factor RF2. PNAS 105:19684–19689. doi: 10.1073/pnas.0810953105 PMID: 19064930
36. Korostelev A, Zhu J, Asahara H, Noller HF. 2010. Recognition of the amber UAG stop codon by release factor RF1. The EMBO Journal 29:2577–2585. doi: 10.1038/emboj.2010.139 PMID: 20588254
37. Korostelev AA. 2011. Structural aspects of translation termination on the ribosome. Rna 17:1409–1421. doi: 10. 1261/rna.2733411 PMID: 21700725
38. Kurita D, Chadani Y, Muto A, Abo T, Himeno H. 2014. ArfA recognizes the lack of mRNA in the mRNA channel after RF2 binding for ribosome rescue. Nucleic Acids Research 42:13339–13352. doi: 10.1093/nar/gku1069 PMID: 25355516
39. Laurberg M, Asahara H, Korostelev A, Zhu J, Trakhanov S, Noller HF. 2008. Structural basis for translation termination on the 70S ribosome. Nature 454:852–857. doi: 10.1038/nature07115 PMID: 18596689
40. Loveland AB, Bah E, Madireddy R, Zhang Y, Brilot AF, Grigorieff N, Korostelev AA . 2016. Ribosome.RelA structures reveal the mechanism of stringent response activation. eLife 5:e17029. doi: 10.7554/eLife.17029 PMID: 27434674
41. Ma C, Kurita D, Li N, Chen Y, Himeno H, Gao N. 2017. Mechanistic insights into the alternative translation termination by ArfA and RF2. Nature 541:550–553. doi: 10.1038/nature20822 PMID: 27906160
42. Moazed D, Noller HF. 1986. Transfer RNA shields specific nucleotides in 16S ribosomal RNA from attack by chemical probes. Cell 47:985–994. doi: 10.1016/0092-8674(86)90813-5 PMID: 2430725
43. Moazed D, Noller HF. 1989. Interaction of tRNA with 23S rRNA in the ribosomal A, P, and E sites. Cell 57:585–597. doi: 10.1016/0092-8674(89)90128-1 PMID: 2470511
44. Neubauer C, Gillet R, Kelley AC, Ramakrishnan V. 2012. Decoding in the absence of a codon by tmRNA and SmpB in the ribosome. Science 335:1366–1369. doi: 10.1126/science.1217039 PMID: 22422985
45. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF chimera–a visualization system for exploratory research and analysis. Journal of Computational Chemistry 25:1605–1612. doi: 10.1002/jcc.20084 PMID: 15264254
46. Ramrath DJ, Yamamoto H, Rother K, Wittek D, Pech M, Mielke T, Loerke J, Scheerer P, Ivanov P, Teraoka Y, Shpanchenko O, Nierhaus KH, Spahn CM. 2012. The complex of tmRNA-SmpB and EF-G on translocating ribosomes. Nature 485:526–529. doi: 10.1038/nature11006 PMID: 22622583
47. Rawat UB, Zavialov AV, Sengupta J, Valle M, Grassucci RA, Linde J, Vestergaard B, Ehrenberg M, Frank J. 2003. A cryo-electron microscopic study of ribosome-bound termination factor RF2. Nature 421:87–90. doi: 10.1038/nature01224 PMID: 12511960
48. Rohou A, Grigorieff N. 2015. CTFFIND4: fast and accurate defocus estimation from electron micrographs. Journal of Structural Biology 192:216–221. doi: 10.1016/j.jsb.2015.08.008 PMID: 26278980
49. Santos N, Zhu J, Donohue JP, Korostelev AA, Noller HF. 2013. Crystal structure of the 70S ribosome bound with the Q253P mutant form of release factor RF2. Structure 21:1258–1263. doi: 10.1016/j.str.2013.04.028 PMID: 23769667
50. Sato H, Ito K, Nakamura Y. 2006. Ribosomal protein L11 mutations in two functional domains equally affect release factors 1 and 2 activity. Molecular Microbiology 60:108–120. doi: 10.1111/j.1365-2958.2006.05094.x PMID: 16556224
51. Schaub RE, Poole SJ, Garza-Sánchez F, Benbow S, Hayes CS. 2012. Proteobacterial ArfA peptides are synthesized from non-stop messenger RNAs. Journal of Biological Chemistry 287:29765–29775. doi: 10.1074/jbc.M112.374074 PMID: 22791716
52. Selmer M, Dunham CM, Murphy FV, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V. 2006. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313:1935–1942. doi: 10.1126/science.1131127 PMID: 16959973
53. Shimizu Y. 2012. ArfA recruits RF2 into stalled ribosomes. Journal of Molecular Biology 423:624–631. doi: 10.1016/j.jmb.2012.08.007 PMID: 22922063
54. Shin DH, Brandsen J, Jancarik J, Yokota H, Kim R, Kim SH. 2004. Structural analyses of peptide release factor 1 from thermotoga maritima reveal domain flexibility required for its interaction with the ribosome. Journal of Molecular Biology 341:227–239. doi: 10.1016/j.jmb.2004.05.055 PMID: 15312775
55. Suloway C, Pulokas J, Fellmann D, Cheng A, Guerra F, Quispe J, Stagg S, Potter CS, Carragher B. 2005. Automated molecular microscopy: the new leginon system. Journal of Structural Biology 151:41–60. doi: 10.1016/j.jsb.2005.03.010 PMID: 15890530
56. Svidritskiy E, Ling C, Ermolenko DN, Korostelev AA. 2013. Blasticidin S inhibits translation by trapping deformed tRNA on the ribosome. PNAS 110:12283–12288. doi: 10.1073/pnas.1304922110 PMID: 23824292
57. Svidritskiy E, Brilot AF, Koh CS, Grigorieff N, Korostelev AA. 2014. Structures of yeast 80S ribosome-tRNA complexes in the rotated and nonrotated conformations. Structure 22:1210–1218. doi: 10.1016/j.str.2014.06.003 PMID: 25043550
58. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I, Ludtke SJ. 2007. EMAN2: an extensible image processing suite for electron microscopy. Journal of Structural Biology 157:38–46. doi: 10.1016/j.jsb.2006.05.009 PMID: 16859925
59. Trappl K, Joseph S. 2016. Ribosome induces a closed to open conformational change in release factor 1. Journal of Molecular Biology 428:1333–1344. doi: 10.1016/j.jmb.2016.01.021 PMID: 26827724
60. Vestergaard B, Van LB, Andersen GR, Nyborg J, Buckingham RH, Kjeldgaard M. 2001. Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1. Molecular Cell 8:1375–1382. doi: 10.1016/S1097-2765(01)00415-4 PMID: 11779511
61. Vestergaard B, Sanyal S, Roessle M, Mora L, Buckingham RH, Kastrup JS, Gajhede M, Svergun DI, Ehrenberg M. 2005. The SAXS solution structure of RF1 differs from its crystal structure and is similar to its ribosome bound cryo-EM structure. Molecular Cell 20:929–938. doi: 10.1016/j.molcel.2005.11.022 PMID: 16364917
62. Vila-Sanjurjo A, Ridgeway WK, Seymaner V, Zhang W, Santoso S, Yu K, Cate JH. 2003. X-ray crystal structures of the WT and a hyper-accurate ribosome from Escherichia coli. PNAS 100:8682–8687. doi: 10.1073/pnas.1133380100 PMID: 12853578
63. Weixlbaumer A, Jin H, Neubauer C, Voorhees RM, Petry S, Kelley AC, Ramakrishnan V. 2008. Insights into translational termination from the structure of RF2 bound to the ribosome. Science 322:953–956. doi: 10.1126/science.1164840 PMID: 18988853
64. Xu W, Pagel FT, Murgola EJ. 2002. Mutations in the GTPase center of Escherichia coli 23S rRNA indicate release factor 2-interactive sites. Journal of Bacteriology 184:1200–1203. doi: 10.1128/jb.184.4.1200-1203.2002 PMID: 11807083
65. Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y. 2015. The I-TASSER suite: protein structure and function prediction. Nature Methods 12:7–8. doi: 10.1038/nmeth.3213 PMID: 25549265
66. Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, Noller HF. 2001. Crystal structure of the ribosome at 5.5 A resolution. Science 292:883–896. doi: 10.1126/science.1060089 PMID: 11283358
67. Zeng F, Jin H. 2016. Peptide release promoted by methylated RF2 and ArfA in nonstop translation is achieved by an induced-fit mechanism. Rna 22:49–60. doi: 10.1261/rna.053082.115 PMID: 26554029
68. Zeng F, Chen Y, Remis J, Shekhar M, Phillips JC, Tajkhorshid E, Jin H. 2017. Structural basis of co-translational quality control by ArfA and RF2 bound to ribosome. Nature 541:554–557. doi: 10.1038/nature21053 PMID: 28077875
69. Zoldák G, Redecke L, Svergun DI, Konarev PV, Voertler CS, Dobbek H, Sedlák E, Sprinzl M. 2007. Release factors 2 from Escherichia coli and thermus thermophilus: structural, spectroscopic and microcalorimetric studies. Nucleic Acids Research 35:1343–1353. doi: 10.1093/nar/gkl696 PMID: 17272297