Methyltransferases do not work by compression, cratic, or desolvation effects, but by electrostatic preorganization

Proteins: Structure, Function and Bioinformatics

Volumn 83, Issue 2, 2015, Pages 318-330

  Lameira, Jeronimo ^a,b   Bora, Ram Prasad ^a   Chu, Zhen T ^a   Warshel, Arieh ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b FEDERAL UNIVERSITY OF PARÁ   (Brazil)

Author keywords

Compression; Electrostatic; Methyltransferase; NAC; Preorganization

Indexed keywords

CATECHOL; CATECHOL METHYLTRANSFERASE; DOPAMINE; WATER;

ARTICLE; CATALYSIS; CATALYTIC EFFICIENCY; COMPLEX FORMATION; COMPRESSION; CRYSTAL STRUCTURE; ENTROPY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; PRIORITY JOURNAL; SOLVATION; STATIC ELECTRICITY; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; HUMAN; KINETICS; METHYLATION; THERMODYNAMICS;

BIOCATALYSIS; CATALYTIC DOMAIN; CATECHOL O-METHYLTRANSFERASE; HUMANS; KINETICS; METHYLATION; MODELS, MOLECULAR; THERMODYNAMICS;

EID: 84937642270     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24717     Document Type: Article

References (52)

1. Copeland RA, Solomon ME, Richon VM. Protein methyltransferases as a target class for drug discovery. Nat Rev Drug Discov 2009;8:724-732.
2. O'Hagan D, Schmidberger JW. Enzymes that catalyse S(N)2 reaction mechanisms. Nat Prod Rep 2010;27:900-918.
3. Albert M, Helin K. Histone methyltransferases in cancer. Semin Cell Dev Biol 2010;21:209-220.
4. Wagner T, Jung M. New lysine methyltransferase drug targets in cancer. Nat Biotechnol 2012;30:622-623.
5. Espinoza S, Manago F, Leo D, Sotnikova TD, Gainetdinov RR. Role of catechol-O-methyltransferase (COMT)-dependent processes in Parkinson's disease and L-DOPA treatment. CNS Neurol Disord Drug Targets 2012;11:251-263.
6. Rutherford K, Le Trong I, Stenkamp RE, Person VW. Crystal structures of human 108V and 108M catechol O-methyltransferase. J Mol Biol 2008;380:120-130.
7. Axelrod J, Tomchick R. Enzymatic O-methylation of epinephtine and other catechols. J Biol Chem 1958;233:702-705.
8. Mihel IK, Coward JK, Schowen RL. Deuterium isotope effects and transition state structure in an intramolecular model system for methyl-transfer enzymes. J Am Chem Soc 1979;101:4349-4351.
9. Warshel A, Sharma PK, Kato M, Xiang Y, Liu H, Olsson MHM. Electrostatic basis for enzyme catalysis. Chem Rev 2006;106:3210-3235.
10. Olsson MHM, Warshel A. Solute solvent dynamics and energetics in enzyme catalysis: The S(N)2 reaction of dehalogenase as a general benchmark. J Am Chem Soc 2004;126:15167-15179.
11. Bruice TC. A view at the millennium: the efficiency of enzymatic catalysis. Acc Chem Res 2002;35:139-148.
12. Hegazi MF, Borchardt RT, Schowen RL. Alpha-Deuterium and C-13 isotope effects for methyl-transfer catalyzed by catechol O-methyltransferase -SN2-Like transition state. J Am Chem Soc 1979;101:4359-4365.
13. Zhang J, Klinman JP. Enzymatic methyl transfer: role of an active site residue in generating active site compaction that correlates with catalytic efficiency. J Am Chem Soc 2011;133:17134-17137.
14. Kollman PA, Kuhn B, Donini O, Perakyla M, Stanton R, Bakowies D. Elucidating the nature of enzyme catalysis utilizing a new twist on an old methodology: quantum mechanical - free energy calculations on chemical reactions in enzymes and in aqueous solution. Acc Chem Res 2001;34:72-79.
15. Lau EY, Bruice TC. Importance of correlated motions in forming highly reactive near attack conformations in catechol O-methyltransferase. J Am Chem Soc 1998;120:12387-12394.
16. Strajbl M, Shurki A, Kato M, Warshel A. Apparent NAC effect in chorismate mutase reflects electrostatic transition state stabilization. J Am Chem Soc 2003;125:10228-10237.
17. Rodgers J, Femec DA, Schowen RL. Isotopic mapping of transition-state strucutural features associated with enzymatic catalysis of methyl tranfer. J Am Chem Soc 1982;104:3263-3268.
18. Gray CH, Coward JK, Schowen KB, Schowen RL. alpha.-Deuterium and carbon-13 isotope effects for a simple, intermolecular sulfur-to-oxygen methyl-transfer reaction. Transition-state structures and isotope effects in transmethylation and transalkylation. J Am Chem Soc 1979;101:4351-4358.
19. Kanaan N, Pernia JJR, Williams IH. QM/MM simulations for methyl transfer in solution and catalysed by COMT: ensemble-averaging of kinetic isotope effects. Chem Commun 2008:6114-6116.
20. Soriano A, Castillo R, Christov C, Andres J, Moliner V, Tunon I. Catalysis in glycine N-methyltransferase: testing the electrostatic stabilization and compression hypothesis. Biochemistry 2006;45:14917-14925.
21. Roca M, Marti S, Andres J, Moliner V, Tunon I, Bertran J, Williams IH. Theoretical modeling of enzyme catalytic power: analysis of "cratic" and electrostatic factors in catechol O-methyltransferase. J Am Chem Soc 2003;125:7726-7737.
22. García-Meseguer R, Zinovjev K, Roca M, Ruiz-Pernía JJ, Tuñón I. Linking electrostatic effects and protein motions in enzymatic catalysis. a theoretical analysis of catechol O-methyltransferase. J Phys Chemi B, in press.
23. Warshel A, Weiss RM. An empirical valence bond approach for comparing reactions in solutions and in enzymes. J Am Chem Soc 1980;102:6218-6226.
24. Warshel A. Computer modeling of chemical reactions in enzymes and solutions. In: Sons JW, editor. John Wiley & Sons, INC, New York; 1991.
25. Lee FS, Chu ZT, Bolger MB, Warshel A. Calculations of antibody antigen interactions - microscopic and semimicroscopic evaluation of the free-energies of binding of phosphorylcholine analogs to Mcpc603. Protein Eng 1992;5:215-228.
26. Florian J, Goodman MF, Warshel A. Theoretical investigation of the binding free energies and key substrate-recognition components of the replication fidelity of human DNA polymerase beta. J Phys Chem B 2002;106:5739-5753.
27. Swain CG, Taylor LJ. Catalysis by secondary valence forces. J Am Chem Soc 1962;84:2456.
28. Warshel A, Parson WW. Dynamics of biochemical and biophysical reactions: insight from computer simulations. Quart Rev Biophys 2001;34:563-679.
29. Strajbl M, Shurki A, Warshel A. Converting conformational changes to electrostatic energy in molecular motors: the energetics of ATP synthase. Proc Natl Acad Sci USA 2003;100:14834-14839.
30. Schultz E, Nissinen E. Inhibition of rat-liver and duodenum soluble catechol-ortho-methyltransferase by a tight-binding OR-462. Biochem Pharmacol 1989;38:3953-3956.
31. Lohman DC, Edwards DR, Wolfenden R. Catalysis by desolvation: the catalytic prowess of SAM-dependent halide-alkylating enzymes. J Am Chem Soc 2013;135:14473-14475.
32. Kahn K, Bruice TC. Transition-state and ground-state structures and their interaction with the active-site residues in catechol O-methyltransferase. J Am Chem Soc 1999;122:46-51.
33. Hur S, Bruice TC. The mechanism of catalysis of the chorismate to prephenate reaction by the Escherichia coli mutase enzyme. Proc Natl Acad Sci USA 2002;99:1176-1181.
34. Shurki A, Štrajbl M, Villa J, Warshel A. How much do enzymes really gain by restraining their reacting fragments? J Am Chem Soc 2002;124:4097-4107.
35. Hur S, Bruice TC. Enzymes do what is expected (chalcone isomerase versus chorismate mutase). J Am Chem Soc 2003;125:1472-1473.
36. Ruggiero GD, Williams IH, Roca M, Moliner V, Tunon I. QM/MM determination of kinetic isotope effects for COMT-catalyzed methyl transfer does not support compression hypothesis. J Am Chem Soc 2004;126:8634-8635.
37. Shurki A, Strajbl M, Villa J, Warshel A. How much do enzymes really gain by restraining their reacting fragments? J Am Chem Soc 2002;124:4097-4107.
38. Villa J, Strajbl M, Glennon TM, Sham YY, Chu ZT, Warshel A. How important are entropic contributions to enzyme catalysis? Proc Natl Acad Sci USA 2000;97:11899-11904.
39. Gurney RW. Ionic processes in solution; McGraw-Hill Book Company, Inc., New York, 1953.
40. Kauzmann W. Some factors in the interpretation of protein denaturation. Adv Protein Chem 1959;14:1-63.
41. Singh N, Warshel A. Toward accurate microscopic calculation of solvation entropies: extending the restraint release approach to studies of solvation effects. J Phys Chem B 2009;113:7372-7382.
42. Kuhn B, Kollman PA. QM-FE and molecular dynamics calculations on catechol O-methyltransferase: free energy of activation in the enzyme and in aqueous solution and regioselectivity of the enzyme-catalyzed reaction. J Am Chem Soc 2000;122:2586-2596.
43. Page MI, Jencks WP. Entropic contributions to rate accelerations in enzymic and intramolecular reactions and the chelate effect. Proc Natl Acad Sci USA 1971;68:1678-1683.
44. Stanton RV, Perakyla M, Bakowies D, Kollman PA. Combined ab initio and free energy calculations to study reactions in enzymes and solution: amide hydrolysis in trypsin and aqueous solution. J Am Chem Soc 1998;120:3448-3457.
45. Donini O, Darden T, Kollman PA. QM-FE calculations of aliphatic hydrogen abstraction in citrate synthase and in solution: reproduction of the effect of enzyme catalysis and demonstration that an enolate rather than an enol is formed. J Am Chem Soc 2000;122:12270-12280.
46. Strajbl M, Sham YY, Villa J, Chu ZT, Warshel A. Calculations of activation entropies of chemical reactions in solution. J Phys Chem B 2000;104:4578-4584.
47. Warshel A. Energetics of enzyme catalysis. Proc Natl Acad Sci USA 1978;75:5250-5254.
48. Singh N, Warshel A. A comprehensive examination of the contributions to the binding entropy of protein-ligand complexes. Proteins 2010;78:1724-1735.
49. Liu H, Warshel A. Origin of the temperature dependence of isotope effects in enzymatic reactions: the case of dihydrofolate reductase. J Phys Chem B 2007;111:7852-7861.
50. Kamerlin SCL, Warshel A. At the dawn of the 21st century: is dynamics the missing link for understanding enzyme catalysis? Proteins 2010;78:1339-1375.
51. Warshel A, Aqvist J, Creighton S. Enzyme work by solvation ratther than by desolvation. Proc Natl Acad Sci USA 1989;86:5820-5824.
52. Warshel A, Strajbl M, Villa J, Florian J. Remarkable rate enhancement of orotidine 5 '-monophosphate decarboxylase is due to transition-state stabilization rather than to ground-state destabilization. Biochemistry 2000;39:14728-14738.