Accommodating the bacterial decoding release factor as an alien protein among the RNAs at the active site of the ribosome

Cell Research

Volumn 17, Issue 7, 2007, Pages 591-607

  Poole, Elizabeth S ^a   Young, David J ^a   Askarian Amiri, Marjan E ^a   Scarlett, Debbie Jane G ^a   Tate, Warren P ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Functional mimicry; Molecular mimicry; Protein synthesis termination; Release factor; Ribosome; SELEX; tRNA

Indexed keywords

BACTERIAL PROTEIN; TRANSFER RNA; TRANSLATION TERMINATION FACTOR;

ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; GENETICS; METABOLISM; PROTEIN BINDING; PROTEIN CONFORMATION; RIBOSOME;

BACTERIAL PROTEINS; BINDING SITES; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PEPTIDE TERMINATION FACTORS; PROTEIN BINDING; PROTEIN CONFORMATION; RIBOSOMES; RNA, TRANSFER;

BACTERIA (MICROORGANISMS);

EID: 34547226652     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2007.56     Document Type: Article

References (77)

1. Ogle JM, Carter AP, Ramakrishnan V. Insights into the decoding mechanism from recent ribosome structures. Trends Biochem Sci 2003; 28:259-266.
2. Ogle JM, Ramakrishnan V. Structural insights into translational fidelity. Annu Rev Biochem 2005; 74:129-177.
3. Cech TR. The ribosome is a ribozyme. Science 2000; 289:878-879.
4. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. The complete atomic structure of the large ribosomal subunit at 2.4 Åresolution. Science 2000; 289:905-920.
5. Nissen P, Hansen J, Ban N, Moore PB, Steitz TA. The structural basis of ribosome activity in peptide bond synthesis. Science 2000; 289:920-930.
6. Wilson KS, Noller HF. Molecular movement inside the translational engine. Cell 1998; 92:337-349.
7. Maguire BA, Beniaminov AD, Ramu H, Mankin AS, Zimmer-mann RA. A protein component at the heart of an RNA machine: the importance of protein L27 for the function of the bacterial ribosome. Mol Cell 2005; 20:427-435.
8. Tate WP, Mannering SA. Three, four or more: the translational stop signal at length. Mol Microbiol 1996; 21:213-219.
9. Capecchi MR. Polypeptide chain termination in vitro: isolation of a release factor. Proc Natl Acad Sci USA 1967; 58:1144-1151.
10. Hampl H, Schulze H, Nierhaus KH. Ribosomal components fromEscherichia coli 50S subunits involved in the reconstitution of peptidyltransferase activity. J Biol Chem 1981; 256:2284-2288.
11. Moffat JG, Tate WP. A single proteolytic cleavage in release factor 2 stabilises ribosome binding and abolishes peptidyl-tRNA hydrolysis activity. J Biol Chem 1994; 269:18899-18903.
12. Nakamura Y, Ito K, Isaksson LA. Emerging understanding of translation termination. Cell 1996; 87:147-150.
13. Kisselev L, Ehrenberg M, Frolova L. Termination of translation: interplay of mRNA, rRNAs and release factors? EMBO J 2003; 22:175-182.
14. Song H, Mugnier P, Das AK, et al. The crystal structure of human eukaryotic release factor eRF1-mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 2000; 100:311-321.
15. Vestergaard B, Van LB, Andersen GR, Nyborg J, Buckingham RH, Kjeldgaard M. Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1. Mol Cell 2001; 8:1375-1382.
16. Shin DH, Brandsen J, Jancarik J, Yokota H, Kim R, Kim S-H. Structural analyses of peptide release factor 1 from Thermotoga maritima reveal domain flexibility required for its interaction with the ribosome. J Mol Biol 2004; 341:227-239.
17. Graille M, Heurgué-Hamard V, Champ S, et al. Molecular basis for bacterial class I release factor methylation by PrmC. Mol Cell 2005; 20:917-927.
18. Poole ES, Brown CM, Tate WP. The identity of the base following the stop codon determines the efficiency of in vivo translation termination in Escherichia coli. EMBO J 1995; 14:151-158.
19. Scarlett D-JG, McCaughan KK, Wilson DN, Tate WP. Mapping functionally important motifs SPF and GGQ of the decoding release factor RF2 to the Escherichia coli ribosome by hydroxyl radical footprinting. Implications for macromolecular mimicry and structural changes in RF2. J Biol Chem 2003; 278:15095-15104.
20. Tate W, Greuer B, Brimacombe R. Codon recognition in polypeptide chain termination: site directed crosslinking of termination codon to Escherichia coli release factor 2. Nucleic Acids Res 1990; 25:6537-6544.
21. Brown CM,Tate WP. Direct recognition of mRNA stop signals by Escherichia coli polypeptide chain release factor two. J Biol Chem 1994; 269:33164-33170.
22. Czworkowski J, Wang J, Steitz TA, Moore PB. The crystal structure of elongation factor G complexed with GDP, at 2.7 Å resolution. EMBO J 1994; 13:3661-3668.
23. AEvarsson A, Brazhnikov E, Garber M, et al. Three-dimensional structure of the ribosomal translocase: elongation factor G from Thermus thermophilus. EMBO J 1994; 13:3669-3677.
24. Nissen P, Kjeldgaard M, Thirup S, et al. Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science 1995; 270:1464-1472.
25. Nissen P, Kjeldgaard M, Nyborg J. Macromolecular mimicry. EMBO J 2000; 19:489-495.
26. Klaholz BP, Myasnikov AG, van Heel M. Visualization of release actor 3 on the ribosome during termination of protein synthesis. Nature 2004; 427:862-865.
27. Wilson DN, Dalphin ME, Pel HJ, Major LL, Mansell JB, Tate WP. Factor-mediated termination of protein synthesis: a welcome return to the mainstream of translation. In: Garrett RA, Douthwaite SR, Liljas A, Matheson AT, Moore PB, Noller HF, eds. The ribosome: structure, function, antibiotics, and cellular interactions. Washington, DC: ASM Press, 2000; 495-508.
28. Ito K, Uno M, Nakamura Y. A tripeptide 'anticodon' deciphers stop codons in messenger RNA. Nature 2000; 403:680-684.
29. Frolova LY, Tsivkovskii RY, Sivolobova GF, et al. Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRFl to trigger peptidyl-tRNA hydrolysis. RNA 1999; 5:1014-1020.
30. Rawat UBS, Zavialov AV, Sengupta J, et al. A cryo-electron microscopic study of ribosome-bound termination factor RF2. Nature 2003; 421:87-90.
31. Klaholz BP, Pape T, Zavialov AV, et al. Structure of the Escherichia coli ribosomal termination complex with release factor 2. Nature 2003; 421:90-94.
32. Petry S, Brodersen DE, Murphy IV FV, et al. Crystal structures of the ribosome in complex with release factors RFl and RF2 bound to a cognate stop codon. Cell 2005; 123:1255-1266.
33. Rawat U, Gao H, Zavialov A, Gursky R, Ehrenberg M, Frank J. Interactions of the release factor RFl with the ribosome as revealed by cryo-EM. J Mol Biol 2006; 357:1144-1153.
34. Ito K, Uno M, Nakamura Y. Single amino acid substitution in prokaryote polypeptide release factor 2 permits it to terminate translation at all three stop codons. Proc Natl Acad Sci USA 1998; 95:8165-8169.
35. Uno M, Ito K, Nakamura Y. Polypeptide release at sense and noncognate stop codons by localized charge-exchange alterations in translational release factors. Proc Natl Acad Sci USA 2002; 99:1819-1824.
36. Ogle JM, Brodersen DE, demons WM, Tarry MJ, Carter AP, Ramakrishnan V. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 2000; 292:897-902.
37. Konecki DS, Aune KC, Tate W, Caskey CT. Characterization of reticulocyte release factor. J Biol Chem 1977; 252:4514-4520.
38. Brown CM, Stockwell PA, Trotinan CN, Tate WP. The signal for the termination of protein synthesis in prokaryotes. Nucleic Acids Res 1990; 18:2079-2086.
39. Cridge AG, Major LL, Mahagaonkar AA, Poole ES, Isaksson LA, Tate WP. Comparison of characteristics and function of translation termination signals between and within prokaryotic and eukaryotic organisms. Nucleic Acids Res 2006; 34:1959-1973.
40. Freistroffer DV, Kwiatkowski M, Buckingham RH, Ehrenberg M. The accuracy of codon recognition by polypeptide release factors. Proc Natl Acad Sci USA 2000; 97:2046-2051.
41. Major LL. Is the prokaryotic termination signal a simple triplet codon or an extended sequence element? PhD thesis, University of Otago, 2001.
42. Poole ES, Major LL, Mannering SA, Tate WP. Translational termination in Escherichia coli: three bases following the stop codon crosslink to release factor 2 and affect the decoding efficiency of UGA-containing signals. Nucleic Acids Res 1998; 26:954-960.
43. Boycheva S, Chkodrov G, Ivanov I. Codon pairs in the genome f Escherichia coli. Bioinformatics 2003; 19:987-998.
44. Mottagui-Tabar S, Isaksson LA. Only the last amino acids in the nascent peptide influence translation termination in Escherichia coli genes. FEBS Lett 1997; 414:165-170.
45. Mottagui-Tabar S, Bjornsson A, Isaksson LA. The second to last amino acid in the nascent chain as a codon context determinant. EMBO J 1994; 13:249-257.
46. Marquez V, Wilson DN, Tate WP, Triana-Alonso F, Nierhaus KH. Maintaining the ribosomal reading frame: the influence of the E site during translational regulation of release factor 2. Cell 2004; 118:45-55.
47. Vestergaard B, Sanyal S, Roessle M, et al. The SAXS solution structure of RFl differs from its crystal structure and is similar to its ribosome bound cryo-EM structure. Mol Cell 2005; 20:929-938.
48. Stelzl U, Nierhaus KH. SERF: In vitro selection of random RNA fragments to identify protein binding sites within large RNAs. Methods (Duluth) 2001; 25:351-357.
49. Stelzl U, Spahn CMT, Nierhaus KH. Selecting rRNA binding sites for the ribosomal proteins L4 and L6 from randomly fragmented rRNA: Application of a method called SERF. Proc Natl Acad Sci USA 2000; 97:4597-4602.
50. Stelzl U, Nierhaus KH. A short fragment of 23S rRNA containing the binding sites for two ribosomal proteins, L24 and L4 is a key element for rRNA folding during early assembly. RNA 2001; 7:598-609.
51. Tate WP, Brown CM, Kastner B. Codon recognition by the polypeptide release factor. In: Hill WE, Dahlberg AE, Garrett RA, Moore PB, Schlessinger D, Warner JR, eds. The ribosome: structure, function, and evolution. Washington, DC: ASM Press, 1990; 393-401.
52. Harms J, Schluenzen F, Zarivach R, et al. High resolution structure of the large ribosomal subunit from a mesophilic Eubacterium. Cell 2001; 107:679-688.
53. Wilson KS, Ito K, Noller HF, Nakamura Y. Functional sites of interaction between release factor RF1 and the ribosome. Natl Struct Biol 2000; 7:866-870.
54. Wilson KS, Noller HF. Mapping the position of translational elongation factor EF-G in the ribosome by directed hydroxyl radical probing. Cell 1998; 92:131-139.
55. Chan YL, Sitikov AS, Wool IG. The phenotype of mutations of the base-pair C2658.G2663 that closes the tetraloop in the sarcin/ricin domain of Escherichia coli 23 S ribosomal RNA. J Mol Biol 2000; 298:795-805.
56. Szewczak AA, Moore PB. The sarcin/ricin loop, a modular RNA. J Mol Biol 1995;247:81-98.
57. Xu WB, Pagel FT, Murgola EJ. Mutations in the GTPase center of Escherichia coli 23S rRNA indicate release factor 2-interactive sites. J Bacteriol 2002; 184:1200-1203.
58. Arkov AL, Mankin A, Murgola EJ. An rRNA fragment and its antisense can alter decoding of genetic information. J Bacteriol 1998;180:2744-2748.
59. Stoffler G, Cundliffe E, Stoffler-Meilicke M, Dabbs ER. Mutants of Escherichia coli lacking ribosomal protein-L11. J Biol Chem 1980;255:10517-10522.
60. 2-terminal domain of Escherichia coli ribosomal protein L11: its three dimensional location and its role in the binding of release factors 1 and 2. J Biol Chem 1984; 259:7317-7324.
61. Tate WP, McCaughan KK, Ward CD, et al. The ribosomal binding domain of the Escherichia coli release factors: modification of tyrosine in the N terminal domain of ribosomal protein L11 affects release factors 1 and 2 differentially. J Biol Chem 1986; 261:2289-2293.
62. Yusupova MM, Yusupova GZ, Baucom A, et al. Crystal structure of the ribosome at 5.5 angstrom resolution. Science 2001; 292:883-896.
63. Osswald M, Brimacombe R. The environment of 5S rRNA in the ribosome: cross-links to 23S rRNA from sites within helices II and III of the 5S molecule. Nucleic Acids Res 1999; 27:2283-2290.
64. Herr W, Noller HF. Protection of specific sites in 23S and 5S RNA from chemical modification by association of 30S and 50S ribosomes. J Mol Biol 1979; 130:421-432.
65. Ko J, Lee Y, Park I, Cho B. Identification of a structural motif of 23S rRNA interacting with 5S rRNA. FEBS Lett 2001; 508:300-304.
66. Ammons D, Rampersad J. An E. coli 5S rRNA deletion mutant useful for the study of 5S rRNA structure/function relationships. Curr Microbiol 2001; 43:89-92.
67. Ammons D, Rampersad J, Fox GE. 5S rRNA gene deletions cause an unexpectedly high fitness loss in Escherichia coli. Nucleic Acids Res 1999; 27:637-642.
68. Kohrer C, Mayer C, Neumair O, Grobner P, Piendl W. Interaction of ribosomal L1 proteins from mesophilic and thermophilic Archaea and bacteria with specific L1-binding sites on 23S rRNA and mRNA. Eur J Biochem 1998; 256:97-105.
69. Yoshimura K, Ito K, Nakamura Y. Amber (UAG) suppressors affected in UGA/UAA-specific polypeptide release factor 2 of acteria: genetic prediction of initial binding to ribosome preceding stop codon recognition. Genes Cells 1999; 4:253-266.
70. Poole ES, Tate WP. Release factors and their role as decoding proteins: specificity and fidelity for termination of protein synthesis. Biochim Biophys Acta 2000; 1493:1-11.
71. Polacek N, Gomez MJ, Ito K, Xiong L, Nakamura Y, Mankin A. The critical role of the universally conserved A2602 of 23S ribosomal RNA in the release of the nascent peptide during translation termination. Mol Cell 2003; 11:103-112.
72. Youngman EM, Brunelle JL, Kochaniak AB, Green R. The active site of the ribosome is composed of two layers of conserved nucleotides with distinct roles in peptide bond formation and peptide release. Cell 2004; 117:589-599.
73. Dinçbas-Renqvist V, Engström A, Mora L, Heurgué-Hamard V, Buckingham R, Ehrenberg M. Apost-translational modification in the GGQ motif of RF2 from Escherichia coli stimulates termination of translation. EMBO J 2000; 19:6900-6907.
74. Wilson DN, Guévremont D, Tate WP. The ribosomal binding and peptidyl-tRNA hydrolysis functions of Escherichia coli release factor 2 are linked through residue 246. RNA 2000; 6:1704-1713.
75. Schmeing TM, Huang KS, Kitchen DE, Strobel SA, Steitz TA. Structural insights into the roles of water and the 20 hydroxyl of the P site tRNA in the peptidyl transferase reaction. Mol Cell 2005; 20:437-448.
76. Gao H, Zhou Z, Rawat U, et al. RF3 induces ribosomal conformational changes responsible for dissociation of class I release factors. Cell 2007; 129:929-941.
77. Beringer M, Rodnina MV. The ribosomal peptidyl transferase. Mol Cell 2007; 26:311-321.