Three distinct peptides from the N domain of translation termination factor eRF1 surround stop codon in the ribosome

RNA

Volumn 16, Issue 10, 2010, Pages 1902-1914

  Bulygin, Konstantin N ^a   Khairulina, Yulia S ^a   Kolosov, Petr M ^b   Ven'yaminova, Aliya G ^a   Graifer, Dmitri M ^a   Vorobjev, Yuri N ^a   Frolova, Ludmila Yu ^b   Kisselev, Lev L ^b   Karpova, Galina G ^a  

^a INSTITUTE OF CHEMICAL BIOLOGY AND FUNDAMENTAL MEDICINE   (Russian Federation)

^b ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

Author keywords

Cross linking; Eukaryotes; Ribosome bound eRF1; Stop codon recognition; Translation termination

Indexed keywords

PEPTIDE DERIVATIVE; TRANSLATION TERMINATION FACTOR; TRANSLATION TERMINATION FACTOR ERF1; UNCLASSIFIED DRUG; CROSS LINKING REAGENT; ETF1 PROTEIN, HUMAN; MESSENGER RNA; PEPTIDE FRAGMENT; RECOMBINANT PROTEIN; STOP CODON; TRANSFER RNA;

ARTICLE; CROSS LINKING; HUMAN; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; RIBOSOME; STOP CODON; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; IN VITRO STUDY; METABOLISM; NUCLEOTIDE SEQUENCE; PEPTIDE MAPPING; PROTEIN TERTIARY STRUCTURE; RNA TRANSLATION; SITE DIRECTED MUTAGENESIS;

EUKARYOTA;

BASE SEQUENCE; CODON, TERMINATOR; CROSS-LINKING REAGENTS; HUMANS; IN VITRO TECHNIQUES; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PEPTIDE CHAIN TERMINATION, TRANSLATIONAL; PEPTIDE FRAGMENTS; PEPTIDE MAPPING; PEPTIDE TERMINATION FACTORS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RIBOSOMES; RNA, MESSENGER; RNA, TRANSFER;

EID: 77957312136     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2066910     Document Type: Article

References (62)

1. Alkalaeva EZ, Pisarev AV, Frolova LYu, Kisselev LL, Pestova TV. 2006. In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell 125: 1125-1136.
2. Baker D, Sali A. 2001. Protein structure prediction and structural genomics. Science 294: 93-96. (Pubitemid 32952955)
3. Bertram G, Bell HA, Ritchie DW, Fullerton G, Stansfield I. 2000. Terminating eukaryote translation: domain 1 of release factor eRF1 functions in stop codon recognition. RNA 6: 1236-1247.
4. Buckingham RH, Grentzmann G, Kisselev L. 1997. Polypeptide chain release factors. Mol Microbiol 24: 449-456.
5. Bulygin KN, Repkova MN, Ven'yaminova AG, Graifer DM, Karpova GG, Frolova LY, Kisselev LL. 2002. Positioning of the mRNA stop signal with respect to polypeptide chain release factors and ribosomal proteins in 80S ribosomes. FEBS Lett 514: 96-101.
6. Bulygin K, Chavatte L, Frolova L, Karpova G, Favre A. 2005. The first position of a codon placed in the A site of the human 80S ribosome contacts nucleotide C1696 of the 18S rRNA as well as proteins S2, S3, S3a, S30 and S15. Biochemistry 44: 2153-2162. (Pubitemid 40223643)
7. Caskey C, Beaudet AL, Tate WP. 1974. Mammalian release factor: In vitro assay and purification. Methods Enzymol 30: 293-303.
8. Chandramouli P, Topf M, Menetret J-F, Eswar N, Cannone JJ, Gutell RR, Sali A, Akey CW. 2008. Structure of the mammalian 80S ribosome at 8.7 Å resolution. Structure 16: 535-548. (Pubitemid 351467748)
9. Changchien LM, Craven GR. 1986. The use of hydroxylamine cleavage to produce a fragment of ribosomal protein S4 which retains the capacity to specifically bind 16S ribosomal RNA. Nucleic Acids Res 14: 1957-1966.
10. 4UGA stop codon located in the A-site of eukaryotic ribosomes. Eur J Biochem 268: 2896-2904.
11. Chavatte L, Seit-Nebi A, Dubovaya V, 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.
12. Chavatte L, Frolova L, Laugâa P, Kisselev L, Favre A. 2003. Stop codons and UGG promote efficient binding of the human polypeptide release factor eRF1 to the eukaryotic ribosomal A-site. J Mol Biol 331: 745-758.
13. Cheng Z, Saito K, Pisarev AV, Wada M, Pisareva VP, Pestova TV, 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.
14. Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM, Ferguson DM, Spellmeyer DC, Fox T, Caldwell JW, Kollman PA. 1995. A second generation force field for simulation of proteins, nucleic acids and organic molecules. J Am Chem Soc 117: 5179-5197.
15. Demeshkina NA, Styazhkina VA, Bulygin KN, Repkova MN, Ven'yaminova AG, Karpova GG. 2005. Arrangement of mRNA on the human ribosome: Environment of mRNA nucleotide 3′ of the A-site-bound codon. Bioorg. Khem. (Mosk.) 31: 295-302.
16. Ebihara K, Nakamura Y. 1999. C-terminal interaction of translational release factors eRF1 and eRF3 of fission yeast: G-domain uncoupled binding and the role of conserved amino acids. RNA 5: 739-750.
17. Eurwilaichitr L, Graves FM, Stansfield I, Tuite MF. 1999. The C-terminus of eRF1 defines a functionally important domain for translation termination in Saccharomyces cerevisiae. Mol Microbiol 32: 485-496.
18. Fan-Minogue H, Du M, Pisarev AV, Kallmeyer AK, Salas-Marco J, Keeling K, Thompson SR, Pestova T, Bedwell DM. 2008. Distinct eRF3 requirements suggest alternate eRF1 conformations mediate peptide release during eukaryotic translation termination. Mol Cell 30: 599-609. (Pubitemid 351755058)
19. Frolova L, Le Goff X, Rasmussen HH, Cheperegin S, Drugeon G, Kress M, Arman I, Haenni A-L, Celis JE, Philippe M, et al. 1994. A highly conserved eukaryotic protein family possessing properties of polypeptide chain release factor. Nature 372: 701-703.
20. Frolova L, Tsivkovskii RY, Sivolobova GF, Oparina NY, Serpinsky OI, Blinov VM, Tatkov SI, Kisselev L. 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. (Pubitemid 29365331)
21. Frolova LY, Merkulova TI, Kisselev LL. 2000. Translation termination in eukaryotes: Polypeptide release factor eRF1 is composed of functionally and structurally distinct domains. RNA 6: 381-390.
22. Frolova L, Seit-Nebi A, Kisselev L. 2002. Highly conserved NIKS tetrapeptide is functionally essential in eukaryotic translation termination factor eRF1. RNA 8: 129-136.
23. Gallicchio E, Levy RM. 2004. AGBNP: An analytic implicit solvent model suitable for molecular dynamics simulations and high-resolution modeling. J Comput Chem 25: 479-499.
24. Graifer D, Molotkov M, Styazhkina V, Demeshkina N, Bulygin K, Eremina A, Ivanov A, Laletina E, Ven'yaminova A, Karpova G. 2004. Variable and conserved elements of human ribosomes surrounding the mRNA at the decoding and upstream sites. Nucleic Acids Res 32: 3282-3293.
25. Inagaki Y, Blouin C, Doolittle WF, Roger AJ. 2002. Convergence and constraint in eukaryotic release factor (eRF1) domain 1: The evolution of stop codon specificity. Nucleic Acids Res 32: 532-544.
26. Ito K, Uno M, Nakamura Y. 2000. A tripeptide 'anticodon' deciphers stop codons in messenger RNA. Nature 403: 680-684.
27. Ito K, Frolova L, Seit-Nebi A, Karamyshev A, Kisselev L, 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 the domain 1. Proc Natl Acad Sci 99: 8494-8499.
28. Kisselev LL, Buckingham RH. 2000. Translation termination comes of age. Trends Biochem Sci 25: 561-566.
29. Kisselev LL, Oparina N Yu, Frolova L Yu. 2000. Class-1 polypeptide chain release factors are structurally and functionally similar to suppressor tRNAs and comprise different structural-functional families of prokaryotic/ mitochondrial and eukaryotic/archaebacterial factors. Mol Biol (Mosk) 34: 427-442.
30. Kisselev LL, Ehrenberg M, Frolova LYu. 2003. Termination of translation: Interplay of mRNA, rRNAs and release factors. EMBO J 22: 175-182. (Pubitemid 36119423)
31. 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. (Pubitemid 36077091)
32. Kolosov P, Frolova L, Seit-Nebi A, Dubovaya V, Kononenko A, Oparina N, Justesen J, Efimov A, Kisselev L. 2005. Invariant amino acids essential for decoding function of polypeptide release factor eRF1. Nucleic Acids Res 33: 6418-6425. (Pubitemid 41742578)
33. Kononenko AV, Dembo KA, Kisselev LL, Volkov VV. 2004. Molecular morphology of eukaryotic class I translation termination factor eRF1 in solution. Mol Biol (Mosk) 38: 303-311. (Pubitemid 44245340)
34. 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.
35. 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.
36. Liang H, Wong JY, Bao Q, Cavalcanti ARO, Landweber LF. 2005. Decoding region: Analysis of eukaryotic release factor (eRF1) stop codon binding residues. J Mol Evol 60: 337-344.
37. Ma B, Nussinov R. 2004. Release factors eRF1 and RF2: A universal mechanism controls the large conformational changes. J Biol Chem 279: 53875-53885.
38. Matasova NB, Myltseva SV, Zenkova MA, Graifer DM, Vladimirov SN, Karpova GG. 1991. Isolation of ribosomal subunits containing intact rRNA from human placenta. Estimation of functional activity of 80S ribosomes. Anal Biochem 198: 219-223.
39. Megli FM, Van Loon D, Barbuti AA, Quagliarello E, Wirtz KW. 1985. Chemical modification of methionine residues of the phosphatidylcholine transfer protein from bovine liver. A spin-label study. Eur J Biochem 149: 585-590.
40. Merkulova TI, Frolova LY, Lazar M, Camonis J, Kisselev LL. 1999. C-terminal domains of human translation termination factors eRF1 and eRF3 mediate their in vivo interaction. FEBS Lett 443: 41-47.
41. Molotkov MV, Graifer DM, Popugaeva EA, Bulygin KN, Meschaninova MI, Ven'yaminova AG, Karpova GG. 2006. mRNA 39 of the A site-bound codon is located close to protein S3 on the human 80S ribosome. RNA Biol 3: 122-129.
42. Mora L, Heurgue-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. (Pubitemid 36051340)
43. Nakamura Y, Ito K. 2003. Making sense of mimic in translation termination. Trends Biochem Sci 28: 99-105. (Pubitemid 36165139)
44. Nakamura Y, Ito K, Ehrenberg M. 2000. Mimicry grasps reality in translation termination. Cell 101: 349-352.
45. Petry S, Brodersen DE, Murphy FV 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.
46. Poole ES, Tate W. 2000. Release factors and their role as decoding proteins: Specificity and fidelity for termination of protein synthesis. Biochim Biophys Acta 1493: 1-11.
47. Poole ES, Askarian-Amiri ME, Major LL, McCaughan KK, Scarlett DJ, Wilson DN, Tate WP. 2003. Molecular mimicry in the decoding of translational stop signals. Prog Nucleic Acid Res Mol Biol 74: 83-121.
48. 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. (Pubitemid 36077090)
49. Saenger W. 1984. Principles of nucleic acid structure (ed. CR Cantor), Chap. 18. Springer-Verlag, New York.
50. Scarlett DJ, McCaughan KK, Wilson DN, Tate WP. 2003. 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 278: 15095-15104.
51. Seit-Nebi A, Frolova L, Justesen J, Kisselev L. 2001. Class-1 translation termination factors: Invariant GGQ minidomain is essential for release activity and ribosome binding but not for stop codon recognition. Nucleic Acids Res 29: 3982-3987.
52. Seit-Nebi A, Frolova L, Kisselev L. 2002. Conversion of omnipotent translation termination factor eRF1 into ciliate-like UGA-only unipotent eRF1. EMBO Rep 3: 881-886.
53. Shin DH, Brandsen J, Jancarik J, Yokota H, Kim R, Kim S-H. 2004. Structural analyses of peptide release factor 1 from Thermogota maririma reveal domain flexibility required for its interaction with the ribosomes. J Mol Biol 341: 227-239.
54. Siridechadilok B, Fraser CS, Hall RJ, Doudna JA, Nogales E. 2005. Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310: 1513-1515. (Pubitemid 41746350)
55. Song H, Mugnier P, Webb HM, Evans DR, Tuite MF, Hemmings BA, Barford D. 2000. The crystal structure of human eukaryotic release factors eRF1 - mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 100: 311-321. (Pubitemid 30353087)
56. Spahn CMT, Beckmann R, Eswar N, Penczek PA, Sali A, Blobel G, Frank J. 2001. Structure of the 80S ribosome from Saccaromyces serevisiae - tRNA-ribosome and subunit-subunit interactions. Cell 107: 373-386. (Pubitemid 33049980)
57. Styazhkina VA, Molotkov MV, Demeshkina NA, Bulygin KN, Graifer DM, Meshchaninova MI, Repkova MN, Ven'yaminova AG, Karpova GG. 2003. Arrangement of the sense and stop codons of the template in the A site of the human ribosome as inferred from crosslinking with oligonucleotide derivatives. Mol Biol (Mosk) 37: 866-872.
58. Vestergaard B, Van LB, Andersen GR, Nyborg J, Buckingham RH, Kjeldgaard M. 2001. Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1. Mol Cell 8: 1375-1382.
59. Phe by computer modeling. Mol Biol (Mosk) 39: 777-784.
60. 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.
61. Yusupova G, Jenner L, Rees B, Moras D, Yusupov M. 2006. Structural basis for messenger RNA movement on the ribosome. Nature 444: 391-394.
62. Zavialov AV, Buckingham RH, Ehrenberg M. 2001. A post-termination ribosomal complex is the guanine nucleotide exchange factor for peptide release factor RF3. Cell 107: 115-124.