Peptide release promoted by methylated RF2 and ArfA in nonstop translation is achieved by an induced-fit mechanism

RNA

Volumn 22, Issue 1, 2016, Pages 49-60

  Zeng, Fuxing ^a   Jin, Hong ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Alternative rescuing factor A; Nonstop translation; Quality control; RF2; Ribosome; Translational termination

Indexed keywords

ALTERNATIVE RIBOSOME RESCUING FACTOR A; MESSENGER RNA; PAROMOMYCIN; PEPTIDE; RELEASE FACTOR 1; RELEASE FACTOR 2; UNCLASSIFIED DRUG; VIOMYCIN; ARFA PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; PRFB PROTEIN, E COLI; RNA BINDING PROTEIN; TRANSLATION TERMINATION FACTOR;

ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; ESCHERICHIA COLI; IN VITRO STUDY; ION EXCHANGE; KINETICS; NONHUMAN; PEPTIDE RELEASE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN SECRETION; QUALITY CONTROL; RATE CONSTANT; RIBOSOME; RIBOSOME SUBUNIT; RNA METHYLATION; RNA TRANSLATION; STOP CODON; SUCROSE GRADIENT; TRANSLATION INITIATION; WESTERN BLOTTING; BIOCATALYSIS; METABOLISM; METHYLATION; PROTEIN SYNTHESIS;

BIOCATALYSIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; METHYLATION; PAROMOMYCIN; PEPTIDE CHAIN TERMINATION, TRANSLATIONAL; PEPTIDE TERMINATION FACTORS; PEPTIDES; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA-BINDING PROTEINS; VIOMYCIN;

EID: 85009799718     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.053082.115     Document Type: Article

References (54)

1. Capecchi MR. 1967. Polypeptide chain termination in vitro: isolation of a release factor. Proc Natl Acad Sci 58:1144-1151.
2. Caskey CT, Tompkins R, Scolnick E, Caryk T, Nirenberg M. 1968. Sequential translation of trinucleotide codons for the initiation and termination of protein synthesis. Science 162:135-138.
3. 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. Mol Microbiol 78:796-808.
4. 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 Genet Syst 86:151-163.
5. 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. Mol Microbiol 86:37-50.
6. Dincbas-Renqvist V, Engström A, Mora L, Heurgué-Hamard V, Buckingham R, Ehrenberg M. 2000. A post-translational modification in the GGQ motif of RF2 from Escherichia coli stimulates termination of translation. EMBO J 19:6900-6907.
7. Fei J, Wang J, Sternberg SH, MacDougall DD, Elvekrog MM, Pulukkunat DK, Englander MT, Gonzalez RL Jr. 2010. A highly purified, fluorescently labeled in vitro translation system for singlemolecule studies of protein synthesis. Methods Enzymol 472:221-259.
8. Freistroffer DV, Kwiatkowski M, Buckingham RH, Ehrenberg M. 2000. The accuracy of codon recognition by polypeptide release factors. Proc Natl Acad Sci 97:2046-2051.
9. Frolova LY, Tsivkovskii RY, Sivolobova GF, Oparina NY, Serpinsky OI, Blinov VM, Tatkov SI, Kisselev LL. 1999. Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis. RNA 5:1014-1020.
10. 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.
11. Garza-Sanchez F, Schaub RE, Janssen BD, Hayes CS. 2011. tmRNA regulates synthesis of the ArfA ribosome rescue factor. Mol Microbiol 80:1204-1219.
12. Heurgué-Hamard V, Champ S, Mora L, Merkulova-Rainon T, Kisselev LL, Buckingham RH. 2005. 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 280:2439-2445.
13. Ito K, Uno M, Nakamura Y. 1998. Single amino acid substitution in prokaryote polypeptide release factor 2 permits it to terminate translation at all three stop codons. Proc Natl Acad Sci 95:8165-8169.
14. Ito K, Uno M, Nakamura Y. 2000. A tripeptide 'anticodon' deciphers stop codons in messenger RNA. Nature 403:680-684.
15. 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.
16. Ivanova N, Pavlov MY, Felden B, Ehrenberg M. 2004. Ribosome rescue by tmRNA requires truncated mRNAs. J Mol Biol 338:33-41.
17. Jin H, Kelley AC, Loakes D, Ramakrishnan V. 2010. 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 107:8593-8598.
18. 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 108:15798-15803.
19. Keiler KC, Feaga HA. 2014. Resolving nonstop translation complexes is a matter of life or death. J Bacteriol 196:2123-2130.
20. Klaholz BP, Pape T, Zavialov AV, Myasnikov AG, Orlova EV, Vestergaard B, Ehrenberg M, van Heel M. 2003. Structure of the Escherichia coli ribosomal termination complex with release factor 2. Nature 421:90-94.
21. 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. Proc Natl Acad Sci 105:19684-19689.
22. Korostelev A, Zhu J, Asahara H, Noller HF. 2010. Recognition of the amber UAG stop codon by release factor RF1. EMBO J 29:2577-2585.
23. Koutmou KS, McDonald ME, Brunelle JL, Green R. 2014. RF3:GTP promotes rapid dissociation of the class 1 termination factor. RNA 20:609-620.
24. Kuhlenkoetter S, Wintermeyer W, Rodnina MV. 2011. Different substrate-dependent transition states in the active site of the ribosome. Nature 476:351-354.
25. 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 Res 42:13339-13352.
26. 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.
27. Modolell J, Vázquez. 1977. The inhibition of ribosomal translocation by viomycin. Eur J Biochem 81:491-497.
28. Monteiro RA, Souza EM, Yates MG, Pedrosa FO, Chubatsu LS. 2000. Use of lactose to induce expression of soluble NifA protein domains of Herbaspirillum seropedicae in Escherichia coli. Can J Microbiol 46:1087-1090.
29. Mora L, Heurgué-Hamard V, Champ S, Ehrenberg M, Kisselev LL, Buckingham RH. 2003. The essential role of the invariant GGQ motif in the function and stability in vivo of bacterial release factors RF1 and RF2. Mol Microbiol 47:267-275.
30. 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.
31. Pape T, Wintermeyer W, Rodnina M. 1999. Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome. EMBO J 18:3800-3807.
32. Peske F, Kuhlenkoetter S, Rodnina MV, Wintermeyer W. 2014. Timing of GTP binding and hydrolysis by translation termination factor RF3. Nucleic Acids Res 42:1812-1820.
33. Petropoulos AD, McDonald ME, Green R, Zaher HS. 2014. Distinct roles for release factor 1 and release factor 2 in translational quality control. J Biol Chem 289:17589-17596.
34. Petry S, Brodersen DE, Murphy FVT IV, Dunham CM, Selmer M, Tarry MJ, Kelley AC, Ramakrishnan V. 2005. Crystal structures of the ribosome in complex with release factors RF1 and RF2 bound to a cognate stop codon. Cell 123:1255-1266.
35. Rawat UBS, 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.
36. 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.
37. Schaub RE, Poole SJ, Garza-Sánchez F, Benbow S, Hayes CS. 2012. Proteobacterial ArfA peptides are synthesized from non-stop messenger RNAs. J Biol Chem 287:29765-29775.
38. Schmitt E, Mechulam Y, Ruff M, Mitschler A, Moras D, Blanquet S. 1996. Crystallization and preliminary x-ray analysis of Escherichia coli methionyl-tRNA (fMet) formyltransferase. Proteins 25:139-141.
39. Scolnick E, Tompkins R, Caskey T, Nirenberg M. 1968. Release factors differing in specificity for terminator codons. Proc Natl Acad Sci 61:768-774.
40. Shaw JJ, Green R. 2007. Two distinct components of release factor function uncovered by nucleophile partitioning analysis. Mol Cell 28:458-467.
41. Shimizu Y. 2012. ArfA recruits RF2 into stalled ribosomes. J Mol Biol 423:624-631.
42. Song H, Mugnier P, Das AK, Webb HM, Evans DR, Tuite MF, Hemmings BA, Barford D. 2000. The crystal structure of human eukaryotic release factor eRF1-mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 100:311-321.
43. Stanley RE, Blaha G, Grodzicki RL, Strickler MD, Steitz TA. 2010. The structures of the anti-tuberculosis antibiotics viomycin and capreomycin bound to the 70S ribosome. Nat Struct Mol Biol 17:289-293.
44. Trobro S, Aqvist J. 2007. A model for how ribosomal release factors induce peptidyl-tRNA cleavage in termination of protein synthesis. Mol Cell 27:758-766.
45. Trobro S, Aqvist J. 2009. Mechanism of the translation termination reaction on the ribosome. Biochemistry 48:11296-11303.
46. Walker SE, Fredrick K. 2008. Preparation and evaluation of acylated tRNAs. Methods 44:81-86.
47. 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.
48. Wilson KS, Ito K, Noller HF, Nakamura Y. 2000. Functional sites of interaction between release factor RF1 and the ribosome. Nat Struct Biol 7:866-870.
49. Wolfrum A, Brock S, Mac T, Grillenbeck N. 2003. Expression in E. coli and purification of Thermus thermophilus translation initiation factors IF1 and IF3. Protein Expr Purif 29:15-23.
50. Yamada T, Mizugichi Y, Nierhaus KH, Wittmann HG. 1978. Resistance to viomycin conferred by RNA of either ribosomal subunit. Nature 275:460-461.
51. Youngman EM, He SL, Nikstad LJ, Green R. 2007. Stop codon recognition by release factors induces structural rearrangement of the ribosomal decoding center that is productive for peptide release. Mol Cell 28:533-543.
52. Zaher HS, Green R. 2009. Quality control by the ribosome following peptide bond formation. Nature 457:161-166.
53. Zavialov AV, Buckingham RH, Ehrenberg M. 2001. A posttermination ribosomal complex is the guanine nucleotide exchange factor for peptide release factor RF3. Cell 107:115-124.
54. Zavialov AV, Mora L, Buckingham RH, Ehrenberg M. 2002. Release of peptide promoted by the GGQ motif of class 1 release factors regulates the GTPase activity of RF3. Mol Cell 10:789-798.