The C domain of translation termination factor eRF1 is close to the stop codon in the A site of the 80S ribosome

Molecular Biology

Volumn 41, Issue 5, 2007, Pages 781-789

  Bulygin, K N ^a   Popugaeva, E A ^a   Repkova, M N ^a   Meschaninova, M I ^a   Ven'Yaminova, A G ^a   Graifer, D M ^a   Frolova, L Yu ^a,b   Karpova, G G ^a  

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

^b ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

Author keywords

Eukaryotes; Photocrosslinking; Ribosome; Stop codon recognition; Translation termination; Translation termination factor

Indexed keywords

EUKARYOTA;

EID: 35349005890     PISSN: 00268933     EISSN: 16083245     Source Type: Journal    
DOI: 10.1134/S0026893307050111     Document Type: Article

References (45)

1. Kisselev L.L., Ehrenberg M., Frolova L.Yu. 2003. Termination of translation: interplay of mRNA, rRNAs and release factors. EMBO J. 22, 175-182.
2. Nakamura Y., Ito K. 2003. Making sense of mimic in translation termination. Trends Biochem. Sci. 28, 99-105.
3. Poole E.S., Askarian-Amiri M.E., Major L.L., McCaughan K.K., Scarlett D.J., Wilson D.N., Tate W.P. 2003. Molecular mimicry in the decoding of translational stop signals. Prog. Nucl. Acid Res. Mol. Biol. 74, 83-121.
4. Buckingham R.H., Grentzmann G., Kisselev L. 1997. Polypeptide chain release factors. Mol. Microbiol. 24, 449-456.
5. Kisselev L.L. Buckingham R.H. 2000. Translation termination comes of age. Trends Biochem. Sci. 25, 561-566.
6. Zavialov A.V., Buckingham R.H., Ehrenberg M. 2001. A posttermination ribosomal complex is the guanine nucleotide exchange factor for peptide release factor RF3. Cell. 107, 115-124.
7. Alkalaeva E.Z., Pisarev A.V., Frolova L.Yu., Kisselev L.L., Pestova T.V. 2006. In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell. 125, 1125-1136.
8. Frolova L., Le Goff X., Rasmussen H.H., Cheperegin S., Drugeon G., Kress M., Arman I., Haenni A.-L., Celis J.E., Philippe M., Justesen J., Kisselev L. 1994. A highly conserved eukaryotic protein family possessing properties of polypeptide chain release factor. Nature. 372, 701-703.
9. Kisselev L.L., 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. 34, 427-442.
10. Song H., Mugnier P., Webb H.M., Evans D.R., Tuite M.F., Hemmings B.A., 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.
11. Vestergaard B., Van L.B., Andersen G.R., Nyborg J., Buckingham R.H., Kjeldgaard M. 2001. Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1. Mol. Cell. 8, 1375-1382.
12. Shin D.H., 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.
13. 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.
14. Eurwilaichitr L., Graves F.M., Stansfield I., Tuite M.F. 1999. The C-terminus of eRF1 defines a functionally important domain for translation termination in Saccharomyces cerevisiae. Mol. Microbiol. 32, 485-496.
15. Merkulova T.I., Frolova L.Y., Lazar M., Camonis J., Kisselev L.L. 1999. C-terminal domains of human translation termination factors eRF1 and eRF3 mediate their in vivo interaction. FEBS Lett. 443, 41-47.
16. Frolova L., Tsivkovskii R.Y., Sivolobova G.F., Oparina N.Y., Serpinsky O.I., Blinov V.M., Tatkov S.I., 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.
17. 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.
18. Mora L., Heurgue-Hamard V., Champ S., Ehrenberg M., Kisselev L.L., Buckingham R.H. 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.
19. Scarlett D.J., McCaughan K.K., Wilson D.N., Tate W.P. 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, 15,095-15,104.
20. Petry S., Brodersen D.E., Murphy IV F.V., Dunham C.M., Selme M., Tarry M.J., Kelley A.C., 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.
21. 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.
22. 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. USA. 99, 8494-8499.
23. 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.
24. 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. Nucl. Acids Res. 33, 6418-6425.
25. 4UGA stop codon located in the A-site of eukaryotic ribosomes. Eur. J. Biochem. 268, 2896-2904.
26. 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.
27. Spahn C.M.T., Beckmann R., Eswar N., Penczek P.A., 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.
28. Morgan D.G., Menetret J.-F., Neuhof A., Rapoport T.A., Akey C.W. 2002. Structure of the mammalian ribosome-channel complex at 17 Å resolution. J. Mol. Biol. 324, 871-886.
29. Chavatte L., Frolova L., Laugaa 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.
30. Bulygin K.N., Repkova M.N., Ven'yaminova A.G., Graifer D.M., Karpova G.G., Frolova L.Y., Kisselev L.L. 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.
31. Bulygin K.N., Demeshkina N.A., Frolova L.Yu., Graifer D.M., Ven'yaminova A.G., Kisselev L.L., Karpova G.G. 2003. The ribosomal A-site-bound sense and stop codons are similarly positioned towards the A1823-A1824 dinucleotide of the 18S ribosomal RNA. FEBS Lett. 548, 97-102.
32. Frolova L.Y., Merkulova T.I., Kisselev L.L. 2000. Translation termination in eukaryotes, polypeptide release factor eRF1 is composed of functionally and structurally distinct domains. RNA. 6, 381-390.
33. Frolova L.Y., Simonsen J.L., Merkulova T.I., Litvino D.Y., Martensen P.M., Rechinsky V.O., Camonis J.H., Kisselev L.L., Justesen J. 1998. Functional expression of eukaryotic polypeptide chain release factors 1 and 3 by means of baculovirus/insect cells and complex formation between the factors. Eur. J. Biochem. 256, 36-44.
34. Matasova N.B., Myltseva S.V., Zenkova M.A., Graifer D.M., Vladimirov S.N., Karpova G.G. 1991. Isolation of ribosomal subunits containing intact rRNA from human placenta. Estimation of functional activity of 80S ribosomes. Anal. Biochem. 198, 219-223.
35. Styazhkina V.A., Molotkov M.V., Demeshkina N.A., Bulygin K.N., Graifer D.M., Meshchaninova M.I., Repkova M.N., Ven'yaminova A.G., and Karpova G.G. 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. 37, 1019-1026.
36. 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.
37. Demeshkina N.A., Styazhkina V.A., Bulygin K.N., Repkova M.N., Ven'yaminova A.G., Karpova G.G. 2005. Template location on the human ribosome: Environment of the mRNA nucleotide adjoining the codon from the 3' side in the A site. Bioorg. Khim. 31, 295-302.
38. Molotkov M.V., Graifer D.M., Popugaeva E.A., Bulygin K.N., Meshchaninova M.I., Ven'yaminova A.G., Karpova G.G. 2007. Protein S3 in the human 80S ribosome adjoins mRNA 3' of the A-site codon. Bioorg. Khim. 33. In press.
39. 3. Mol. Biol. 31, 144-151.
40. Bertram G., Bell H.A., Ritchie D.W., Fullerton G., Stansfield I. 2000. Terminating eukaryote translation, domain 1 of release factor eRF1 functions in stop codon recognition. RNA. 6, 1236-1247.
41. Kononenko A.V., Dembo K.A., Kisselev L.L., Volkov V.V. 2004. Molecular morphology of eukaryotic class-1 translation termination factor eRF1 in solution. Mol. Biol. 38, 303-311.
42. Molotkov M., Graifer D., Demeshkina N., Repkova M., Ven'yaminova A., Karpova G. 2005. Arrangement of mRNA 3' of the A-site codon on the human 80S ribosome. RNA Biol. 2, 63-69.
43. Vorobjev Yu.N., Kisselev L.L. 2007. Model of the structure of the eukaryotic ribosomal translation termination complex. Mol. Biol. 41, 103-111.
44. Ivanov V., Mears J. 2004. Using crosslinks to study ribosomal dynamics. J. Biomol. Struct. Dynam. 21, 691-698.
45. Gabashvili I., Whirl-Carrillo M., Bada M., Rey Banatao D., Altman R.B. 2003. Ribosomal dynamics inferred from variations in experimental measurements. RNA. 9, 1301-1307.