A Model for How Ribosomal Release Factors Induce Peptidyl-tRNA Cleavage in Termination of Protein Synthesis

Molecular Cell

Volumn 27, Issue 5, 2007, Pages 758-766

  Trobro, Stefan ^a   Åqvist, Johan ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

RNA

Indexed keywords

PEPTIDYLTRANSFERASE; PROTEIN SUBUNIT; RIBOSOME RECYCLING FACTOR; TRANSFER RNA;

AMINO ACID SEQUENCE; ARTICLE; COMPUTER SIMULATION; CRYSTAL STRUCTURE; HYDROGEN BOND; MOLECULAR DYNAMICS; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN HYDROLYSIS; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS REGULATION; STOP CODON;

AMINO ACID MOTIFS; BINDING SITES; COMPUTER SIMULATION; HYDROLYSIS; MODELS, GENETIC; MODELS, MOLECULAR; MUTATION; PEPTIDE CHAIN TERMINATION, TRANSLATIONAL; PEPTIDE TERMINATION FACTORS; RNA, TRANSFER, AMINO ACYL;

BACTERIA (MICROORGANISMS);

EID: 34548227759     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.06.032     Document Type: Article

References (47)

1. Almlöf M., Åqvist J., Smalås A.O., and Brandsdal B.O. Probing the effects of point mutations at protein-protein interfaces with free energy calculations. Biophys. J. 90 (2006) 433-442
2. Almlöf M., Andér M., and Åqvist J. Energetics of codon-anticodon recognition on the small ribosomal subunit. Biochemistry 46 (2007) 200-209
3. Åqvist J., and Warshel A. Simulation of enzyme reactions using valence bond force fields and other hybrid quantum/classical approaches. Chem. Rev. 93 (1993) 2523-2544
4. Ban N., Nissen P., Hansen J., Moore P.B., and Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289 (2000) 905-920
5. Bieling P., Beringer M., Adio S., and Rodnina M.V. Peptide bond formation does not involve acid-base catalysis by ribosomal residues. Nat. Struct. Mol. Biol. 13 (2006) 423-428
6. Brunelle J.L., Youngman E.M., Sharma D., and Green R. The interaction between C75 of tRNA and the A loop of the ribosome stimulates peptidyl transferase activity. RNA 12 (2006) 33-39
7. Capecchi M.R. Polypeptide chain termination in vitro: isolation of a release factor. Proc. Natl. Acad. Sci. U.S.A. 58 (1967) 1144-1151
8. Caskey C.T., Beaudet A.L., Scolnick E.M., and Rosman M. Hydrolysis of fMet-tRNA by peptidyl transferase. Proc. Natl. Acad. Sci. USA 68 (1971) 3163-3167
9. Dincbas-Renqvist V., Engström A., Mora L., Heurgué-Hamard V., Buckingham R., and Ehrenberg M. A post-translational modification in the GGQ motif of RF2 from Escherichia coli stimulates termination of translation. EMBO J. 19 (2000) 6900-6907
10. Dorner S., Panuschka C., Schmid W., and Barta A. Mononucleotide derivatives as ribosomal P-site substrates reveal an important contribution of the 2′-OH to activity. Nucleic Acids Res. 31 (2003) 6536-6542
11. Erlacher M.D., Lang K., Shankaran N., Wotzel B., Hüttenhofer A., Micura R., Mankin A.S., and Polacek N. Chemical engineering of the peptidyl transferase center reveals an important role of the 2′-hydroxyl group of A2451. Nucleic Acids Res. 33 (2005) 1618-1627
12. Fersht A. Enzyme structure and mechanism (1977), W.H. Freeman & Co., San Francisco
13. Frolova L.Y., Tsivkovskii R.Y., Sivolobova G.F., Oparina N.Y., Serpinsky O.I., Blinov V.M., Tatkov S.I., and Kissilev L.L. 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 (1999) 1014-1020
14. Guthrie J.P. Hydration of carboxylic acids and esters. Evaluation of the free energy change for addition of water to acetic and formic acids and their methyl esters. J. Am. Chem. Soc. 95 (1973) 6999-7003
15. Gutiérrez-de-Terán H., Nervall M., Dunn B.M., Clemente J.C., and Åqvist J. Computational analysis of plasmepsin IV bound to an allophenylnorstatine inhibitor. FEBS Lett. 580 (2006) 5910-5916
16. Harms J., Schluenzen F., Zarivach R., Bashan A., Gat S., Agmon I., Bartels H., Franceschi F., and Yonath A. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107 (2001) 679-688
17. Heurgué-Hamard V., Champ S., Engström A., Ehrenberg M., and Buckingham R.H. The hemK gene in Escherichia coli encodes the N5-glutamine methyltransferase that modifies peptide release factors. EMBO J. 21 (2002) 769-778
18. Ito K., Uno M., and Nakamura Y. A tripeptide 'anticodon' deciphers stop codons in messager RNA. Nature 403 (2000) 680-684
19. Jones G., Willett P., Glen R.C., Leach A.R., and Taylor R. Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 267 (1997) 727-748
20. Kellenberger E., Rodrigo J., Muller P., and Rognan D. Comparative evaluation of eight docking tools for docking and virtual screening accuracy. Proteins 57 (2004) 225-242
21. Klaholz B.P., Pape T., Zavialov A.V., Myasnikov A.G., Orlova E.V., Vestergaard B., Ehrenberg M., and van Heel M. Structure of the Escherichia coli ribosomal termination complex with release factor 2. Nature 421 (2003) 90-94
22. Lee F.S., and Warshel A. A local reaction field method for fast evaluation of long-range electrostatic interactions in molecular simulations. J. Chem. Phys. 97 (1997) 3100-3107
23. MacKerell A.D., Wiórkiewicz-Kuczera J., and Karplus M. An all-atom empirical energy function for the simulation of nucleic acids. J. Am. Chem. Soc. 117 (1995) 11946-11975
24. Marelius J., Kolmodin K., Freierberg I., and Åqvist J. A molecular dynamics program for free energy calculations and empirical valence bond simulations in biomolecular systems. J. Mol. Graph. 16 (1998) 213-225
25. Mora L., Heurgué-Hamard V., Champ S., Ehrenberg M., Kisselev L.L., and Buckingham R.H. 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 (2003) 267-275
26. Ogle J.M., and Ramakrishnan V. Structural insights into translational fidelity. Annu. Rev. Biochem. 74 (2005) 129-177
27. Petry S., Brodersen D.E., Murphy F.V., Dunham C.M., Selmer M., Tarry M.J., Kelley A.C., and Ramakrishnan V. Crystal structures of the ribosome in complex with release factors RF1 and RF2 bound to a cognate stop codon. Cell 123 (2005) 1255-1266
28. Polacek N., Gomez M.J., Ito K., Xiong L., Nakamura Y., and 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 11 (2003) 103-112
29. Rawat U.B.S., Zavialov A.V., Sengupta J., Valle M., Grassucci R.A., Linde J., Vestergaard B., Ehrenberg M., and Frank J. A cryo-electron microscopic study of ribosome-bound termination factor RF2. Nature 421 (2003) 87-90
30. Schmeing T.M., Huang K.S., Kitchen D.E., Strobel S.A., and Steitz T.A. Structural insights into the roles of water and the 2′ hydroxyl of the P site tRNA in the peptidyl transferase reaction. Mol. Cell 20 (2005) 437-448
31. Schmeing T.M., Huang K.S., Strobel S.A., and Steitz T.A. An induced-fit mechanism to promote peptide bond formation and exclude hydrolysis of peptidyl-tRNA. Nature 438 (2005) 520-524
32. Schroeder G.K., and Wolfenden R. The rate enhancement produced by the ribosome: an improved model. Biochemistry 46 (2007) 4037-4044
33. Selmer M., Dunham C.M., Murphy F.V., Weixlbaumer A., Petry S., Kelley A.C., Weir J.R., and Ramakrishnan V. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313 (2006) 1935-1942
34. Sharma P.K., Xiang Y., Kato M., and Warshel A. What are the roles of substrate-assisted catalysis and proximity effects in peptide bond formation by the ribosome?. Biochemistry 44 (2005) 11307-11314
35. Sievers A., Beringer M., Rodnina M.V., and Wolfenden R. The ribosome as an entropy trap. Proc. Natl. Acad. Sci. USA 101 (2004) 7897-7901
36. Song H., Mugnier P., Das A.K., Webb H.M., Evans D.R., Tuite M.F., Hemmings B.A., and Barford D. The crystal structure of human eukaryotic release factor eRF1-mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 100 (2000) 311-321
37. Stefanidis D., and Jencks W.P. General base catalysis of ester hydrolysis. J. Am. Chem. Soc. 115 (1993) 6045-6050
38. Štrajbl M., Florián J., and Warshel A. Ab initio evaluation of the potential surface for general base-catalyzed methanolysis of formamide: a reference solution reaction for studies of serine proteases. J. Am. Chem. Soc. 122 (2000) 5354-5366
39. Trobro S., and Åqvist J. Mechanism of peptide bond synthesis on the ribosome. Proc. Natl. Acad. Sci. USA 102 (2005) 12395-12400
40. Trobro S., and Åqvist J. Analysis of predictions for the catalytic mechanism of ribosomal peptidyl transfer. Biochemistry 45 (2006) 7049-7056
41. Verdonk M.L., Cole J.C., Hartshorn M.J., Murray C.W., and Taylor R.D. Improved protein-ligand docking using GOLD. Proteins 52 (2003) 609-623
42. Vestergaard B., Sanyal S., Roessle M., Mora L., Buckingham R.H., Kastrup J.S., Gajhede M., Svergun D.I., and Ehrenberg M. The SAXS solution structure of RF1 differs from its crystal structure and is similar to its ribosome bound cryo-EM structure. Mol. Cell 20 (2005) 929-938
43. Warshel A. Computer modeling of chemical reactions in enzymes and solutions (1991), John Wiley & Sons, New York
44. Weinger J.S., Parnell K.M., Dorner S., Green R., and Strobel S.A. Substrate-assisted catalysis of peptide bond formation by the ribosome. Nat. Struct. Mol. Biol. 11 (2004) 1101-1106
45. Wimberly B.T., Brodersen D.E., Clemons Jr. W.M., Morgan-Warren R.J., Carter A.P., Vonrhein C., Hartsch T., and Ramakrishnan V. Structure of the 30S ribosomal subunit. Nature 407 (2000) 327-339
46. Youngman E.M., Brunelle J.L., Kochaniak A.B., and 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 117 (2004) 589-599
47. Zavialov A.V., Mora L., Buckinghan R.H., and Ehrenberg M. Release of peptide promoted by the GGQ motif of class 1 release factors regulates the GTPase activity of RF3. Mol. Cell 10 (2002) 789-798