Kinetic isotope effect analysis of the ribosomal peptidyl transferase reaction

Biochemistry

Volumn 44, Issue 10, 2005, Pages 4018-4027

  Seila, Amy C ^a,b   Okuda, Kensuke ^a,c   Núñez, Sara ^a,d   Seila, Andrew F ^a,e   Strobel, Scott A ^a  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c OKAYAMA UNIVERSITY   (Japan)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOLYSIS REACTION; NUCLEOPHILES; PEPTIDE BONDS; RIBOSOMES;

ASSAYS; CATALYSTS; CELLS; ISOTOPES; PH EFFECTS; PROTEINS; REACTION KINETICS; SUBSTITUTION REACTIONS;

ENZYMES;

ISOTOPE; PEPTIDYLTRANSFERASE; PUROMYCIN;

ARTICLE; CHEMICAL STRUCTURE; ISOTOPE ANALYSIS; KINETICS; PH; PRIORITY JOURNAL; RIBOSOME;

BIOTIN; DEUTERIUM EXCHANGE MEASUREMENT; DINUCLEOSIDE PHOSPHATES; ESCHERICHIA COLI PROTEINS; KINETICS; MODELS, CHEMICAL; NITROGEN ISOTOPES; PEPTIDYL TRANSFERASES; PROTEIN SUBUNITS; PROTONS; PUROMYCIN; RIBOSOMAL PROTEINS; RNA, TRANSFER, AMINO ACYL; SUBSTRATE SPECIFICITY;

EID: 14844352639     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047742f     Document Type: Article

References (57)

1. Pauling, L. (1946) Chem. Eng. News, 1375.
2. Melander, L., and Saunders, W. H., Jr. (1980) Reaction Rates of Isotopic Molecules, Wiley, New York.
3. (1978) Transition States for Biochemical Processes, Plenum Press, New York.
4. (1970) Isotope Effects in Chemical Reactions, Van Nostrand Reinhold, New York.
5. (1977) Isotope Effects on Enzyme Catalyzed Reactions, University Park Press, Baltimore, MD.
6. Schramm, V. L. (1999) Enzymatic transition-state analysis and transition-state analogs, Methods Enzymol. 308, 301-355.
7. Cleland, W. W. (1982) The use of isotope effects to determine transition-state structure for enzymatic reactions Methods Enzymol. 87, 625-641.
8. Cleland, W. W. (1982) Use of isotope effects to elucidate enzyme mechanisms, CRC Crit Rev. Biochem. 13, 385-428.
9. Cleland, W. W. (1995) Isotope effects: Determination of enzyme transition state structure, Methods Enzymol. 249, 341-373.
10. Schramm, V. L. (1998) Enzymatic transition states and transition state analog design, Annu. Rev. Biochem. 67, 693-720.
11. Schramm, V. L. (2001) Transition state variation in enzymatic reactions, Curr. Opin. Chem. Biol. 5, 556-563.
12. O'Leary, M. H. (1980) Determination of heavy-atom isotope effects on enzyme-catalyzed reactions, Methods Enzymol. 64, 83-104.
13. Pape, T., Wintermeyer, W., and Rodnina, M. V. (1998) Complete kinetic mechanism of elongation factor Tu-dependent binding of aminoacyl-tRNA to the A site of the E. coli ribosome, EMBO J. 17, 7490-7497.
14. Katunin, V., Muth, G., Strobel, S., Wintermeyer, W., and Rodnina, M. (2002) Important contribution to catalysis of peptide bond formation by a single ionizing group within the ribosome, Mol. Cell 10, 339-346.
15. + hydrolysis by cholera toxin catalytic subunit, J. Am. Chem. Soc. 119, 27-37.
16. Kline, P. C., and Schramm, V. L. (1993) Purine nucleoside phosphorylase. Catalytic mechanism and transition-state analysis of the arenolysis reaction, Biochemistry 32, 13212-13219.
17. Birck, M. R., and Schramm, V. L. (2004) Nucleophilic participation in the transition state for human thymidine phosphorylase, J. Am. Chem. Soc. 126, 2447-2453.
18. + catalyzed by diphtheria toxin, J. Am. Chem. Soc. 119, 12079-12088.
19. Bahnson, B. J., and Anderson, V. E. (1991) Crotonase-catalyzed beta-elimination is concerted: A double isotope effect study, Biochemistry 30, 5894-5906.
20. Monro, R. E., and Marcker, K. A. (1967) Ribosome-catalysed reaction of puromycin with a formylmethionine-containing oligonucleotide, J. Mol. Biol. 25, 347-350.
21. Schmeing, T. M., Seila, A. C., Hansen, J. L., Freeborn, B., Soukup, J. K., Scaringe, S. A., Strobel, S. A., Moore, P. B., and Steitz, T. A. (2002) A pre-translocational intermediate in protein synthesis observed in crystals of enzymatically active 50S subunits, Nat. Struct. Biol. 9, 225-230.
22. Jencks, W. P., and Gilchrist, M. (1968) Nonlinear structure - reactivity correlations. The reactivity of nucleophilic reagents toward esters, J. Am. Chem. Soc. 90, 2622-2637.
23. Okuda, K., Seila, A. C., and Strobel, S. (2004) Synthesis of isotopically labeled puromycin derivatives for kinetic isotope effect analysis of ribosome catalyzed peptide bond formation, Tetrahedron 60, 12101-12112.
24. Lodmell, J. S., Tapprich, W. E., and Hill, W. E. (1993) Evidence for a conformational change in the exit site of the Escherichia coli ribosome upon tRNA binding, Biochemistry 32, 4067-4072.
25. Rodnina, M. V., and Wintermeyer, W. (1995) GTP consumption of elongation factor Tu during translation of heteropolymeric mRNAs, Proc. Natl. Acad. Sci. U.S.A. 92, 1945-1949.
26. Segal, I. H. (1993) Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Systems, John Wiley and Sons, Inc., New York.
27. Oleary, M. H., and Marlier, J. F. (1979) Heavy-atom isotope effects on the alkaline-hydrolysis and hydrazinolysis of methyl benzoate, J. Am. Chem. Soc. 101, 3300-3306.
28. Bigeleisen, J., and Wolfsberg, M. (1958) Theoretical and experimantal aspects of isotope effects in chemical kinetics, Adv. Biochem, Phys. 1, 15-76.
29. Singleton, D. A., and Thomas, A. A. (1995) High-precision simultaneous determination of multiple small kinetic isotope effects at natural-abundance, J. Am. Chem. Soc. 117, 9357-9358.
30. Fishman, G. S. (1996) Monte Carlo: Concepts, Algorithms, and Applications, Springer-Verlag, New York.
31. van Kempen, G. M. P., and van Vliet, L. J. (2000) Mean and variance of ratio estimators used in fluorescence ratio imaging, Cytometry 39, 300-305.
32. Bigeleisen, J. (1955) Statistical mechanics of isotopic systems with small quantum corrections. 1. General considerations and the rule of the geometric mean, J. Chem. Phys. 23, 2264-2267.
33. Gawlita, E., Paneth, P., and Anderson, V. E. (1995) Equilibrium isotope effect on ternary complex formation of [1-18O]oxamate with NADH and lactate dehydrogenase, Biochemistry 34, 6050-6058.
34. Becke, A. D. (1993) Density-functional thermochemistry. III. The role of exact exchange, J. Chem. Phys. 98, 5648-5652.
35. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Zakrzewski, V. G., Montgomery, J. A., Stratmann, R. E., Burant, J. C., Dapprich, S., Millam, J. M., Daniels, A. D., Kudin, K. N., Strain, M. C., Farkas, O., Tomasi, J., Barone, V., Cossi, M., Cammi, R., Mennucci, B., Pomelli, C., Adamo, C., Clifford, S., Ochterski, J., Petersson, G. A., Ayala, P. Y., Cui, Q., Morokuma, K., Salvador, P., Dannenberg, J. J., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Cioslowski, J., Ortiz, J. V., Baboul, A. G., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Gomperts, R., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Andres, J. L., Gonzalez, C., Head-Gordon, M., Replogle, E. S., and Pople, J. A. (1998) Gaussian 98, Pittsburgh, PA.
36. Anisimov, V., and Paneth, P. (1999) Isoeff98. A program for studies of isotope effects using Hessian modifications, J. Math. Chem. 26, 75-86.
37. Northrop, D. B. (1981) The expression of isotope effects on enzyme-catalyzed reactions, Annu. Rev. Biochem. 50, 103-131.
38. 15N isotope effects as a probe of the chemical mechanism of Escherichia coli aspartate transcarbamylase, Biochemistry 31, 6570-6576.
39. Stoker, P. W., O'Leary, M. H., Boehlein, S. K., Schuster, S. M., and Richards, N. G. (1996) Probing the mechanism of nitrogen transfer in Escherichia coli asparagine synthetase by using heavy atom isotope effects, Biochemistry 35, 3024-3030.
40. Narula, S. S., and Dhingra, M. M. (1986) Determination of ionization sites and pK values in puromycin and puromycin aminonucleoside by C-13 and H-1 magnetic-resonance, Indian J. Biochem. Biophys. 23, 306-315.
41. a of the ribosomal peptidyl transferase reaction utilizing a fluorinated puromycin derivative, manuscript submitted.
42. Hermes, J. D., Weiss, P. M., and Cleland, W. W. (1985) Use of N-15 and deuterium-isotope effects to determine the chemical mechanism of phenylalanine ammonia-lyase, Biochemistry 24, 2959-2967.
43. Blackburn, G. M., and Jencks, W. P. (1968) Mechanism of aminolysis of methyl formate, J. Am. Chem. Soc. 90, 2638-2645.
44. Satterthwait, A. C., and Jencks, W. P. (1974) Mechanism of aminolysis of acetate esters, J. Am. Chem. Soc. 96, 7018-7031.
45. Yang, C. C., and Jencks, W. P. (1988) The aminolysis of methyl formate with aniline - Evidence for catalysis by a trapping mechanism, J. Am. Chem. Soc. 110, 2972-2973.
46. Cox, M. M., and Jencks, W. P. (1981) Catalysis of the methoxyaminolysis of phenyl acetate by a preassociation mechanism with a solvent isotope effect maximum, J. Am. Chem. Soc. 103, 572-580.
47. Cox, M. M., and Jencks, W. P. (1981) Concerted bifunctional proton-transfer and general-base catalysis in the methoxyaminolysis of phenyl acetate, J. Am. Chem. Soc. 103, 580-587.
48. Kaminski, Z. J., Paneth, P., and Oleary, M. H. (1991) Nitrogen kinetic isotope effects on the acylation of aniline, J. Org. Chem. 56, 5716-5718.
49. Marlier, J. F., Haptonstall, B. A., Johnson, A. J., and Sacksteder, K. A. (1997) Heavy-atom isotope effects on the hydrazinolysis of methyl formate, J. Am. Chem. Soc. 119, 8838-8842.
50. Singleton, D. A., and Merrigan, S. R. (2000) Resolution of conflicting mechanistic observations in ester aminolysis. A warning on the qualitative prediction of isotope effects for reactive intermediates, J. Am. Chem. Soc. 122, 11035-11036.
51. Parnell, K. M., and Strobel, S. A. (2003) HIS and HERS, magic magnesium and the ballet of protein synthesis, Curr. Opin. Chem. Biol. 7, 528-533.
52. Green, R., and Lorsch, J. R. (2002) The path to perdition is paved with protons, Cell 110, 665-668.
53. Rodnina, M. V., and Wintermeyer, W. (2003) Peptide bond formation on the ribosome: Structure and mechanism, Curr. Opin. Struct. Biol. 13, 334-340.
54. Sievers, A., Beringer, M., Rodnina, M. V., and Wolfenden, R. (2004) The ribosome as an entropy trap, Proc. Natl. Acad. Sci. U.S.A. 101, 7897-7901.
55. Youngman, E. M., Brunelle, J. L., Kochaniak, A. B., and Green, R. (2004) 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, 589-599.
56. Weinger, J. S., Kitchen, D., Scaringe, S. A., Strobel, S. A., and Muth, G. W. (2004) Solid-phase synthesis and binding affinity of peptidyl transferase transition state mimics containing 2′-OH at P-site position A76, Nucleic Acids Res. 32, 1502-1511.
57. Dorner, S., Polacek, N., Schulmeister, U., Panuschka, C., and Barta, A. (2002) Molecular aspects of the ribosomal peptidyl transferase, Biochem. Soc. Trans. 30, 1131-1136.