Release factors 2 from Escherichia coli and Thermus thermophilus: Structural, spectroscopic and microcalorimetric studies

Nucleic Acids Research

Volumn 35, Issue 4, 2007, Pages 1343-1353

  Zoldák, Gabriel ^a   Redecke, Lars ^b   Svergun, Dmitri I ^c,d   Konarev, Peter V ^c,d   Voertler, C Stefan ^e   Dobbek, Holger ^e   Sedlák, Erik ^e   Sprinzl, Mathias ^e  

^a P J AFÁRIK UNIVERSITY   (Slovakia)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d SHUBNIKOV INSTITUTE OF CRYSTALLOGRAPHY   (Russian Federation)

^e UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; MESSENGER RNA; PEPTIDYLTRANSFERASE; RELEASE FACTORS 2; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIFFERENTIAL SCANNING CALORIMETRY; ESCHERICHIA COLI; FLUORESCENCE SPECTROSCOPY; LOW TEMPERATURE; MELTING POINT; MICROCALORIMETRY; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS INHIBITION; RIBOSOME; SPECTROSCOPY; STOP CODON; TEMPERATURE DEPENDENCE; THERMODYNAMICS; THERMUS THERMOPHILUS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CALORIMETRY, DIFFERENTIAL SCANNING; CIRCULAR DICHROISM; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE TERMINATION FACTORS; PROTEIN DENATURATION; SCATTERING, SMALL ANGLE; THERMUS THERMOPHILUS; X-RAY DIFFRACTION;

ESCHERICHIA COLI; PROKARYOTA; THERMUS THERMOPHILUS;

EID: 34047120718     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl696     Document Type: Article

References (56)

1. Ogle,J.M. and Ramakrishnan,V. (2005) Structural insights into translational fidelity. Annu. Rev. Biochem., 74, 129-177.
2. Schuwirth,B.S., Borovinskaya,M.A., Hau,C.W., Zhang,W., Vila-Sanjurjo,A., Holton,J.M. and Cate,J.H. (2005) Structures of the bacterial ribosome at 3.5 A resolution. Science, 310, 827-834.
3. Gao,H., Sengupta,J., Valle,M., Korostelev,A., Eswar,N., Stagg,S.M., Van Roey,P., Agrawal,R.K., Harvey,S.C., Sali,A. et al. (2003) Study of the structural dynamics of the Escherichia coli 70S ribosome using real-space refinement. Cell, 113, 789-801.
4. Frank,J., Sengupta,J., Gao,H., Li,W., Valle,M., Zavialov,A. and Ehrenberg,M. (2005) The role of tRNA as a molecular spring in decoding, accommodation, and peptidyl transfer. FEBS Lett., 579, 959-962.
5. Schmeing,T.M., Huang,K.S., Strobel,S.A. and Steitz,T.A. (2005) An induced-fit mechanism to promote peptide bond formation and exclude hydrolysis of peptidyl-tRNA. Nature, 438, 520-524.
6. Cochella,L. and Green,R. (2005) An active role for tRNA in decoding beyond codon: anticodon pairing. Science, 308, 1178-1180.
7. Diaconu,M., Kothe,U., Schlunzen,F., Fischer,N., Harms,J.M., Tonevitsky,A.G., Stark,H., Rodnina,M.V. and Wahl,M.C. (2005) Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation. Cell, 121, 991-1004.
8. Wilson,D.N. (2004) Termination and ribosome recycling. In Nierhaus,K.H. and Wilson,D.N. (eds), Protein Synthesis and Ribosome Structure. Wiley-VCH, Weinheim, Germany, pp. 367-395.
9. Kisselev,L., Ehrenberg,M. and Frolova,L. (2003) Termination of translation: Interplay of mRNA, rRNAs and release factors? EMBO J., 22, 175-182.
10. Zavialov,A.V., Mora,L., Buckingham,R.H. and 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.
11. Hirokawa,G., Kiel,M.C., Muto,A., Selmer,M., Raj,V.S., Liljas,A., Igarashi,K., Kaji,H. and Kaji,A. (2002) Post-termination complex disassembly by ribosome recycling factor, a functional tRNA mimic. EMBO J., 21, 2272-2281.
12. 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.
13. Brown,C.M. and Tate,W.P. (1994) Direct recognition of mRNA stop signals by Escherichia coli polypeptide chain release factor two. J. Biol. Chem., 269, 33164-33170.
14. Scarlett,D.J., McCaughan,K.K., Wilson,D.N. and 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. J. Biol. Chem., 278, 15095-15104.
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.
16. Salas-Marco,J. and Bedwell,D.M. (2004) GTP hydrolysis by eRF3 facilitates stop codon decoding during eukaryotic translation termination. Mol. Cell. Biol., 24, 7769-7778.
17. Vestergaard,B., Van,L.B., Andersen,G.R., Nyborg,J., Buckingham,R.H. and Kjeldgaard,M. (2001) Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1. Mol. Cell, 8, 1375-1382.
18. 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.
19. 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.
20. Ito,K., Uno,M. and Nakamura,Y. (2000) A tripeptide 'anticodon' deciphers stop codons in messenger RNA. Nature, 403, 680-684.
21. Mora,L., Heurgue-Hamard,V., Champ,S., Ehrenberg,M., Kisselev,L.L. and 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.
22. Petry,S., Brodersen,D.E., Murphy,F.V., Dunham,C.M., Selmer,M., Tarry,M.J., Kelley,A.C. and 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.
23. Seit-Nebi,A., Frolova,L., Justesen,J. and 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.
24. 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.
25. Shin,D.H., Brandsen,J., Jancarik,J., Yokota,H., Kim,R. and Kim,S.H. (2004) Structural analyses of peptide release factor 1 from Thermotoga maritima reveal domain flexibility required for its interaction with the ribosome. J. Mol. Biol., 341, 227-239.
26. Klaholz,B.P., Pape,T., Zavialov,A.V., Myasnikov,A.G., Orlova,E.V., Vestergaard,B., Ehrenberg,M. and van Heel,M. (2003) Structure of the Escherichia coli ribosomal termination complex with release factor 2. Nature, 421, 90-94.
27. Rawat,U.B., Zavialov,A.V., Sengupta,J., Valle,M., Grassucci,R.A., Linde,J., Vestergaard,B., Ehrenberg,M. and Frank,J. (2003) A cryo-electron microscopic study of ribosome-bound termination factor RF2. Nature, 421, 87-90.
28. Ma,B. and Nussinov,R. (2004) Release factors eRF1 and RF2: A universal mechanism controls the large conformational changes. J. Biol. Chem., 279, 53875-53885.
29. Vestergaard,B., Sanyal,S., Roessle,M., Mora,L., Buckingham,R.H., Kastrup,J.S., Gajhede,M., Svergun,D.I. and Ehrenberg,M. (2005) The SAXS solution structure of RF1 differs from its crystal structure and is similar to its ribosome bound cryo-EM structure. Mol. Cell, 20, 929-938.
30. Kononenko,A.V., Dembo,K.A., Kiselev,L.L. and Volkov,V.V. (2004) Molecular morphology of eukaryotic class I translation termination factor eRF1 in solution. Mol. Biol. (Mosk), 38, 303-311.
31. Dincbas-Renqvist,V., Engstrom,A., Mora,L., Heurgue-Hamard,V., Buckingham,R. and 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.
32. Blank,J., Grillenbeck,N.W., Kreutzer,R. and Sprinzl,M. (1995) Overexpression and purification of Thermus thermophilus elongation factors G, Tu, and Ts from Escherichia coli. Protein Expr. Purif., 6, 637-645.
33. Kabsch,W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr., 26, 795-800.
34. Navaza,J. (1994) Amore - an automated package for molecular replacement. Acta Crystallogr. A, 50, 157-163.
35. Turk,D. (1992) Weiterentwicklung eines Programms fuer Molekuelgraphik und Elektrondichte-Manipulation und seine Anwendung auf verschiedene Protein-Strukturaufklaerungen. Technische Universität München.
36. Brunger,A.T., Adams,P.D., Clore,G.M., Delano,W.L., Gros,P., Grosse-Kunstleve,R.W., Jiang,J.S., Kuszewski,J., Nilges,M., Pannu,N.S. et al. (1998) Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr., 54, 905-921.
37. Freire,E. (1995) Thermal denaturation methods in the study of protein folding. Methods Enzymol., 259, 144-168.
38. Lopez,M.M. and Makhatadze,G.I. (2002) Differential scanning calorimetry. Methods Mol. Biol., 173, 113-119.
39. Pace,C.N., Vajdos,F., Fee,L., Grimsley,G. and Gray,T. (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci., 4, 2411-2423.
40. Konarev,P.V., Volkov,V.V., Sokolova,A.V., Koch,M.H.J. and Svergun,D.I. (2003) PRIMUS: A windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr., 36, 1277-1282.
41. Svergun,D.I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr., 25, 495-503.
42. Svergun,D., Barberato,C. and Koch,M.H.J. (1995) CRYSOL - a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallography, 28, 768-773.
43. Holm,L. and Sander,C. (1993) Protein-structure comparison by alignment of distance matrices. J. Mol. Biol., 233, 123-138.
44. Whitmore,L. and Wallace,B.A. (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res., 32, W668-W673.
45. Manavalan,P. and Johnson,W.C., Jr (1987) Variable selection method improves the prediction of protein secondary structure from circular dichroism spectra. Anal. Biochem., 167, 76-85.
46. Myers,J.K., Pace,C.N. and Scholtz,J.M. (1995) Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding. Protein Sci., 4, 2138-2148.
47. Tsodikov,O.V., Record,M.T., Jr and Sergeev,Y.V. (2002) Novel computer program for fast exact calculation of accessible and molecular surface areas and average surface curvature. J. Comput. Chem., 23, 600-609.
48. Brandts,J.F., Hu,C.Q., Lin,L.N. and Mos,M.T. (1989) A simple model for proteins with interacting domains. Applications to scanning calorimetry data. Biochemistry, 28, 8588-8596.
49. Privalov,P.L. (1982) Stability of proteins. Proteins which do not present a single cooperative system. Adv. Protein Chem., 35, 1-104.
50. Wilson,K.S., Ito,K., Noller,H.F. and Nakamura,Y. (2000) Functional sites of interaction between release factor RF1 and the ribosome. Nature Struct. Biol., 7, 866-870.
51. Mitkevich,V.A., Kononenko,A.V., Oparina,N.Y., Kolosov,P.M., Makarov,A.A. and Kisselev,L.L. (2006) Thermal denaturation of eukaryotic class-1 translation termination factor eRF1. Relationship between stability of the eRF1 molecule and alteration of functional activity of its mutants. Mol. Biol., 40, 100-110.
52. Graille,M., Heurgue-Hamard,V., Champ,S., Mora,L., Scrima,N., Ulryck,N., van,T.H. and Buckingham,R.H. (2005) Molecular basis for bacterial class I release factor methylation by PrmC. Mol. Cell, 20, 917-927.
53. Kumar,S., Tsai,C.J. and Nussinov,R. (2000) Factors enhancing protein thermostability. Protein Eng., 13, 179-191.
54. Petsko,G.A. (2001) Structural basis of thermostability in hyperthermophilic proteins, or 'there's more than one way to skin a cat'. Methods Enzymol., 334, 469-478.
55. Makhatadze,G.I. and Privalov,P.L. (1995) Energetics of protein structure. Adv. Protein Chem., 47, 307-425.
56. Chavatte,L., Frolova,L., Laugaa,P., Kisselev,L. and Favre,A. (2003) Stop codons and UGG promote efficient binding of the polypeptide release factor eRF1 to the ribosomal A site. J. Mol. Biol., 331, 745-758.