Selectivity of stop codon recognition in translation termination is modulated by multiple conformations of GTS loop in eRF1

Nucleic Acids Research

Volumn 40, Issue 12, 2012, Pages 5751-5765

  Wong, Leo E ^a   Li, Yan ^a   Pillay, Shubhadra ^a   Frolova, Ludmila ^b   Pervushin, Konstantin ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTIC CLASS I RELEASE FACTOR; RELEASING FACTOR; RNA 18S; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GTS LOOP; HUMAN; MOLECULAR INTERACTION; MUTANT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RIBOSOME; RNA STRUCTURE; STOP CODON; STRUCTURE ANALYSIS; TRANSLATION REGULATION; WILD TYPE;

BINDING SITES; CODON, TERMINATOR; HUMANS; MODELS, MOLECULAR; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE CHAIN TERMINATION, TRANSLATIONAL; PEPTIDE TERMINATION FACTORS; PROTEIN STRUCTURE, TERTIARY; RNA;

EUKARYOTA;

EID: 84863226738     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks192     Document Type: Article

References (74)

1. Capecchi,M.R. (1967) Polypeptide chain termination in vitro: isolation of a release factor. Proc. Natl Acad. Sci. USA, 58, 1144-1151.
2. Kisselev,L., Ehrenberg,M. and Frolova,L. (2003) Termination of translation: interplay of mRNA, rRNAs and release factors? EMBO J., 22, 175-182. (Pubitemid 36119423)
3. Ito,K., Uno,M. and Nakamura,Y. (2000) A tripeptide 'anticodon' deciphers stop codons in messenger RNA. Nature, 403, 680-684. (Pubitemid 30104012)
4. Nakamura,Y. and Ito,K. (2002) A tripeptide discriminator for stop codon recognition. FEBS Lett., 514, 30-33. (Pubitemid 34251237)
5. Laurberg,M., Asahara,H., Korostelev,A., Zhu,J., Trakhanov,S. and Noller,H.F. (2008) Structural basis for translation termination on the 70S ribosome. Nature, 454, 852-857.
6. Korostelev,A., Zhu,J., Asahara,H. and Noller,H.F. (2010) Recognition of the amber UAG stop codon by release factor RF1. EMBO J., 29, 2577-2585.
7. Korostelev,A., Asahara,H., Lancaster,L., Laurberg,M., Hirschi,A., Zhu,J., Trakhanov,S., Scott,W.G. and Noller,H.F. (2008) Crystal structure of a translation termination complex formed with release factor RF2. Proc. Natl Acad. Sci. USA, 105, 19684-19689.
8. Weixlbaumer,A., Jin,H., Neubauer,C., Voorhees,R.M., Petry,S., Kelley,A.C. and Ramakrishnan,V. (2008) Insights into translational termination from the structure of RF2 bound to the ribosome. Science, 322, 953-956.
9. Sund,J., Ander,M. and Aqvist,J. (2010) Principles of stop-codon reading on the ribosome. Nature, 465, 947-950.
10. Song,H., Mugnier,P., Das,A.K., Webb,H.M., Evans,D.R., Tuite,M.F., Hemmings,B.A. and 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. (Pubitemid 30353087)
11. Frolova,L.Y., Merkulova,T.I. and Kisselev,L.L. (2000) Translation termination in eukaryotes: Polypeptide release factor eRF1 is composed of functionally and structurally distinct domains. RNA, 6, 381-390. (Pubitemid 30161282)
12. Ito,K., Ebihara,K. and Nakamura,Y. (1998) The stretch of C-terminal acidic amino acids of translational release factor eRF1 is a primary binding site for eRF3 of fission yeast. RNA, 4, 958-972. (Pubitemid 28359766)
13. Ito,K., Frolova,L., Seit-Nebi,A., Karamyshev,A., Kisselev,L. and Nakamura,Y. (2002) Omnipotent decoding potential resides in eukaryotic translation termination factor eRF1 of variant-code organisms and is modulated by the interactions of amino acid sequences within domain 1. Proc. Natl Acad. Sci. USA, 99, 8494-8499. (Pubitemid 34693590)
14. Frolova,L., Seit-Nebi,A. and Kisselev,L. (2002) Highly conserved NIKS tetrapeptide is functionally essential in eukaryotic translation termination factor eRF1. RNA, 8, 129-136. (Pubitemid 34288901)
15. Seit-Nebi,A., Frolova,L. and Kisselev,L. (2002) Conversion of omnipotent translation termination factor eRF1 into ciliate-like UGA-only unipotent eRF1. EMBO Rep., 3, 881-886. (Pubitemid 35154115)
16. Chavatte,L., Seit-Nebi,A., Dubovaya,V. and Favre,A. (2002) The invariant uridine of stop codons contacts the conserved NIKSR loop of human eRF1 in the ribosome. EMBO J., 21, 5302-5311.
17. Bulygin,K.N., Khairulina,Y.S., Kolosov,P.M., Ven'yaminova,A.G., Graifer,D.M., Vorobjev,Y.N., Frolova,L.Y., Kisselev,L.L. and Karpova,G.G. (2010) Three distinct peptides from the N domain of translation termination factor eRF1 surround stop codon in the ribosome. RNA, 16, 1902-1914.
18. Bertram,G., Bell,H.A., Ritchie,D.W., Fullerton,G. and Stansfield,I. (2000) Terminating eukaryote translation: domain 1 of release factor eRF1 functions in stop codon recognition. RNA, 6, 1236-1247.
19. Inagaki,Y., Blouin,C., Doolittle,W.F. and Roger,A.J. (2002) Convergence and constraint in eukaryotic release factor 1 (eRF1) domain 1: the evolution of stop codon specificity. Nucleic Acids Res., 30, 532-544. (Pubitemid 34679615)
20. Inagaki,Y. and Doolittle,W.F. (2001) Class I release factors in ciliates with variant genetic codes. Nucleic Acids Res., 29, 921-927. (Pubitemid 32162260)
21. Lozupone,C.A., Knight,R.D. and Landweber,L.F. (2001) The molecular basis of nuclear genetic code change in ciliates. Curr. Biol., 11, 65-74. (Pubitemid 32116838)
22. Salas-Marco,J., Fan-Minogue,H., Kallmeyer,A.K., Klobutcher,L.A., Farabaugh,P.J. and Bedwell,D.M. (2006) Distinct paths to stop codon reassignment by the variant-code organisms Tetrahymena and Euplotes. Mol. Cell Biol., 26, 438-447. (Pubitemid 43089758)
23. Lekomtsev,S., Kolosov,P., Bidou,L., Frolova,L., Rousset,J.P. and Kisselev,L. (2007) Different modes of stop codon restriction by the Stylonychia and Paramecium eRF1 translation termination factors. Proc. Natl Acad. Sci. USA, 104, 10824-10829. (Pubitemid 47175185)
24. Eliseev,B., Kryuchkova,P., Alkalaeva,E. and Frolova,L. (2010) A single amino acid change of translation termination factor eRF1 switches between bipotent and omnipotent stop-codon specificity. Nucleic Acids Res., 39, 599-608.
25. Velichutina,I.V., Hong,J.Y., Mesecar,A.D., Chernoff,Y.O. and Liebman,S.W. (2001) Genetic interaction between yeast Saccharomyces cerevisiae release factors and the decoding region of 18 S rRNA. J. Mol. Biol., 305, 715-727. (Pubitemid 33030021)
26. Fourmy,D., Recht,M.I., Blanchard,S.C. and Puglisi,J.D. (1996) Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic. Science, 274, 1367-1371. (Pubitemid 26391459)
27. Lynch,S.R. and Puglisi,J.D. (2001) Structure of a eukaryotic decoding region A-site RNA. J. Mol. Biol., 306, 1023-1035. (Pubitemid 33030003)
28. Lynch,S.R., Gonzalez,R.L. and Puglisi,J.D. (2003) Comparison of X-ray crystal structure of the 30S subunit-antibiotic complex with NMR structure of decoding site oligonucleotide-paromomycin complex. Structure, 11, 43-53. (Pubitemid 36071495)
29. Kondo,J., Urzhumtsev,A. and Westhof,E. (2006) Two conformational states in the crystal structure of the Homo sapiens cytoplasmic ribosomal decoding A site. Nucleic Acids Res., 34, 676-685. (Pubitemid 43240254)
30. Dubovaya,V.I., Kolosov,P.M., Alkalaeva,E.Z., Frolova,L.Y. and Kisselev,L.L. (2006) Influence of individual domains of the translation termination factor eRF1 on induction of the GTPase activity of the translation termination factor eRF3. Mol. Biol., 40, 310-316.
31. Kononenko,A.V., Mitkevich,V.A., Dubovaya,V.I., Kolosov,P.M., Makarov,A.A. and Kisselev,L.L. (2008) Role of the individual domains of translation termination factor eRF1 in GTP binding to eRF3. Proteins, 70, 388-393.
32. Caskey,C.T., Beaudet,A.L. and Tate,W.P. (1974) Mammalian release factor: in vitro assay and purification. Methods Enzymol., 30, 293-303.
33. Oda,Y., Muramatsu,T., Yumoto,F., Ito,M. and Tanokura,M. (2004) Backbone (1)H, (13)C and (15)N resonance assignment of the N-terminal domain of human eRF1. J. Biomol. NMR, 30, 109-110.
34. Ivanova,E.V., Kolosov,P.M., Birdsall,B., Kisselev,L.L. and Polshakov,V.I. (2006) NMR Assignments of the Middle Domain of Human Polypeptide Release Factor eRF1. J. Biomol. NMR, 36(Suppl. 1), 8. (Pubitemid 46909565)
35. Mantsyzov,A.B., Ivanova,E.V., Birdsall,B., Kolosov,P.M., Kisselev,L.L. and Polshakov,V.I. (2007) NMR assignments of the C-terminal domain of human polypeptide release factor eRF1. Biomol. NMR Assign., 1, 183-185.
36. Kelly,M.J.S., Krieger,C., Ball,L.J., Yu,Y.H., Richter,G., Schmieder,P., Bacher,A. and Oschkinat,H. (1999) Application of amino acid type-specific H-1- and N-14-labeling in a H-2-, N-15-labeled background to a 47 kDa homodimer: Potential for NMR structure determination of large proteins. J. Biomol. NMR, 14, 79-83. (Pubitemid 29258289)
37. Kainosho,M. and Tsuji,T. (1982) Assignment of the three methionyl carbonyl carbon resonances in Streptomyces subtilisin inhibitor by a carbon-13 and nitrogen-15 double-labeling technique. A new strategy for structural studies of proteins in solution. Biochemistry, 21, 6273-6279. (Pubitemid 13141631)
38. Yabuki,T., Kigawa,T., Dohmae,N., Takio,K., Terada,T., Ito,Y., Laue,E.D., Cooper,J.A., Kainosho,M. and Yokoyama,S. (1998) Dual amino acid-selective and site-directed stable-isotope labeling of the human c-Ha-Ras protein by cell-free synthesis. J. Biomol. NMR, 11, 295-306. (Pubitemid 128511280)
39. Zweckstetter,M. (2008) NMR: prediction of molecular alignment from structure using the PALES software. Nat. Protoc., 3, 679-690.
40. Cornilescu,G., Delaglio,F. and Bax,A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR, 13, 289-302. (Pubitemid 29143535)
41. Guntert,P., Mumenthaler,C. and Wuthrich,K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol., 273, 283-298. (Pubitemid 27460230)
42. Herrmann,T., Guntert,P. and Wuthrich,K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol., 319, 209-227. (Pubitemid 34729497)
43. Koradi,R., Billeter,M. and Wuthrich,K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph., 14, 51-55. (Pubitemid 26152976)
44. Laskowski,R.A., Rullmannn,J.A., MacArthur,M.W., Kaptein,R. and Thornton,J.M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8, 477-486. (Pubitemid 126706801)
45. Roy,A., Kucukural,A. and Zhang,Y. (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc., 5, 725-738.
46. Zhang,Y. (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9, 40.
47. Zhang,Y. and Skolnick,J. (2005) TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res., 33, 2302-2309. (Pubitemid 41439897)
48. Schanda,P., Kupce,E. and Brutscher,B. (2005) SOFAST-HMQC experiments for recording two-dimensional heteronuclear correlation spectra of proteins within a few seconds. J. Biomol. NMR, 33, 199-211. (Pubitemid 43118574)
49. Fielding,L. (2003) NMR methods for the determination of protein-ligand dissociation constants. Curr. Top. Med. Chem., 3, 39-53.
50. Cheng,Z., Saito,K., Pisarev,A.V., Wada,M., Pisareva,V.P., Pestova,T.V., Gajda,M., Round,A., Kong,C., Lim,M. et al. (2009) Structural insights into eRF3 and stop codon recognition by eRF1. Genes Dev., 23, 1106-1118.
51. Ishima,R. and Torchia,D.A. (2000) Protein dynamics from NMR. Nat. Struct. Biol., 7, 740-743.
52. Jarymowycz,V.A. and Stone,M.J. (2006) Fast time scale dynamics of protein backbones: NMR relaxation methods, applications, and functional consequences. Chem. Rev., 106, 1624-1671. (Pubitemid 43792775)
53. Fan-Minogue,H. and Bedwell,D.M. (2008) Eukaryotic ribosomal RNA determinants of aminoglycoside resistance and their role in translational fidelity. RNA, 14, 148-157.
54. Phe: a 500MHz1H-n.m.r. study. Biochem. J., 221, 737-751.
55. Popenda,M., Biala,E., Milecki,J. and Adamiak,R.W. (1997) Solution structure of RNA duplexes containing alternating CG base pairs: NMR study of r(CGCGCG)2 and 2′-O-Me(CGCGCG)2 under low salt conditions. Nucleic Acids Res., 25, 4589-4598. (Pubitemid 27500772)
56. Heus,H.A. and Pardi,A. (1991) Novel proton NMR assignment procedure for RNA duplexes. J. Am. Chem. Soc., 113, 4360-4361.
57. Popenda,L., Adamiak,R.W. and Gdaniec,Z. (2008) Bulged adenosine influence on the RNA duplex conformation in solution. Biochemistry, 47, 5059-5067. (Pubitemid 351620744)
58. Moazed,D. and Noller,H.F. (1987) Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature, 327, 389-394. (Pubitemid 17075811)
59. Recht,M.I., Douthwaite,S. and Puglisi,J.D. (1999) Basis for prokaryotic specificity of action of aminoglycoside antibiotics. EMBO J., 18, 3133-3138. (Pubitemid 29255621)
60. Morozova,N., Allers,J., Myers,J. and Shamoo,Y. (2006) Protein-RNA interactions: exploring binding patterns with a three-dimensional superposition analysis of high resolution structures. Bioinformatics, 22, 2746-2752. (Pubitemid 44742394)
61. Allers,J. and Shamoo,Y. (2001) Structure-based analysis of protein-RNA interactions using the program ENTANGLE. J. Mol. Biol., 311, 75-86. (Pubitemid 32735315)
62. Wang,Y., Chai,B., Wang,W. and Liang,A. (2010) Functional characterization of polypeptide release factor 1b in the ciliate Euplotes. Biosci. Rep., 30, 425-431.
63. Bulygin,K.N., Khairulina,Y.S., Kolosov,P.M., Ven'yaminova,A.G., Graifer,D.M., Vorobjev,Y.N., Frolova,L.Y. and Karpova,G.G. (2011) Adenine and guanine recognition of stop codon is mediated by different N domain conformations of translation termination factor eRF1. Nucleic Acids Res., 39, 7134-7146.
64. Liang,H., Wong,J.Y., Bao,Q., Cavalcanti,A.R. and Landweber,L.F. (2005) Decoding the decoding region: analysis of eukaryotic release factor (eRF1) stop codon-binding residues. J. Mol. Evol., 60, 337-344. (Pubitemid 40685126)
65. Kolosov,P., Frolova,L., Seit-Nebi,A., Dubovaya,V., Kononenko,A., Oparina,N., Justesen,J., Efimov,A. and Kisselev,L. (2005) Invariant amino acids essential for decoding function of polypeptide release factor eRF1. Nucleic Acids Res., 33, 6418-6425. (Pubitemid 41742578)
66. Rospert,S., Rakwalska,M. and Dubaquie,Y. (2005) Polypeptide chain termination and stop codon readthrough on eukaryotic ribosomes. Rev. Physiol. Biochem. Pharmacol., 155, 1-30.
67. Palmer,E., Wilhelm,J.M. and Sherman,F. (1979) Phenotypic suppression of nonsense mutants in yeast by aminoglycoside antibiotics. Nature, 277, 148-150. (Pubitemid 9093811)
68. Singh,A., Ursic,D. and Davies,J. (1979) Phenotypic suppression and misreading Saccharomyces cerevisiae. Nature, 277, 146-148. (Pubitemid 9093810)
69. Rowe,S.M. and Clancy,J.P. (2009) Pharmaceuticals targeting nonsense mutations in genetic diseases: progress in development. BioDrugs, 23, 165-174.
70. Salas-Marco,J. and Bedwell,D.M. (2005) Discrimination between defects in elongation fidelity and termination efficiency provides mechanistic insights into translational readthrough. J. Mol. Biol., 348, 801-815. (Pubitemid 40544383)
71. Alkalaeva,E.Z., Pisarev,A.V., Frolova,L.Y., Kisselev,L.L. and Pestova,T.V. (2006) In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell, 125, 1125-1136. (Pubitemid 43866201)
72. Hatin,I., Fabret,C., Rousset,J.P. and Namy,O. (2009) Molecular dissection of translation termination mechanism identifies two new critical regions in eRF1. Nucleic Acids Res., 37, 1789-1798.
73. Mantsyzov,A.B., Ivanova,E.V., Birdsall,B., Alkalaeva,E.Z., Kryuchkova,P.N., Kelly,G., Frolova,L.Y. and Polshakov,V.I. (2010) NMR solution structure and function of the C-terminal domain of eukaryotic class 1 polypeptide chain release factor. FEBS J., 277, 2611-2627.
74. Legault,P. and Pardi,A. (1994) 31P chemical shift as a probe of structural motifs in RNA. J. Magn. Reson. B, 103, 82-86.