Catalysis by enzyme conformational change as illustrated by orotidine 5′-monophosphate decarboxylase

Current Opinion in Structural Biology

Volumn 13, Issue 2, 2003, Pages 184-192

  Gao, Jiali ^a  

^a University of Minnesota   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OROTIDINE 5' PHOSPHATE DECARBOXYLASE;

BINDING AFFINITY; CATALYSIS; CHEMICAL MODIFICATION; CHEMICAL REACTION; CONFORMATIONAL TRANSITION; ENZYME CONFORMATION; ENZYME SUBSTRATE; EXPERIMENTAL TEST; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN METABOLISM; RADIATION SCATTERING; REVIEW;

EID: 0037396515     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(03)00041-1     Document Type: Review

References (35)

1. Karplus M., McCammon J.A. Molecular dynamics simulations of biomolecules. Nat. Struct. Biol. 9:2002;646-652.
2. Colonna-Cesari F., Perahia D., Karplus M., Eklund H., Branden C.I., Tapia O. Interdomain motion in liver alcohol dehydrogenase. Structural and energetic analysis of the hinge bending mode. J. Biol. Chem. 261:1986;15273-15278.
3. Rozovsky S., Jogl G., Tong L., McDermott A.E. Solution-state NMR investigations of triosephosphate isomerase active site loop motion: ligand release in relation to active site loop dynamics. J. Mol. Biol. 310:2001;271-280.
4. Case D.A., Karplus M. Stereochemistry of carbon monoxide binding to myoglobin and hemoglobin. J. Mol. Biol. 123:1978;697-701.
5. Sawaya M.R., Kraut J. Loop and subdomain movements in the mechanism of Escherichia coli dihydrofolate reductase: crystallographic evidence. Biochemistry. 36:1997;586-603.
6. McMillan F.M., Cahoon M., White A., Hedstrom L., Petsko G.A., Ringe D. Crystal structure at 2.4 Å resolution of Borrelia burgdorferi inosine 5′-monophosphate dehydrogenase: evidence of a substrate-induced hinged-lid motion by loop 6. Biochemistry. 39:2000;4533-4542.
7. Wagner C.R., Huang Z., Singleton S.F., Benkovic S.J. Molecular basis for nonadditive mutational effects in Escherichia coli dihydrofolate reductase. Biochemistry. 34:1995;15671-15680.
8. Miller B.G., Snider M.J., Short S.A., Wolfenden R. Contribution of enzyme-phosphoribosyl contacts to catalysis by orotidine 5′-phosphate decarboxylase. Biochemistry. 39:2000;8113-8118 This paper reports the remarkable connectivity effects of the orotate unit and the phosphoribosyl group on the catalytic reaction rate, providing experimental evidence of enzyme-substrate cooperative interactions. Mutations of Tyr217Ala and Arg235Ala, two residues that form hydrogen bonds with the phosphate group, significantly reduce the enzyme rate enhancement, but have surprisingly small effects on substrate binding.
9. Jencks W.P. Binding energy, specificity, and enzymic catalysis: the Circe effect. Adv. Enzymol. Relat. Areas Mol. Biol. 43:1975;219-410.
10. Radzicka A., Wolfenden R. A proficient enzyme. Science. 267:1995;90-93.
11. Appleby T.C., Kinsland C., Begley T.P., Ealick S.E. The crystal structure and mechanism of orotidine 5-monophosphate decarboxylase. Proc. Natl. Acad. Sci. U.S.A. 97:2000;2005-2010 The X-ray structure of ODCase from B. subtilis complexed with UMP was determined. A concerted electrophilic substitution mechanism was suggested, along with reactant state destabilization by Asp60.
12. Wu N., Mo Y., Gao J., Pai E.F. Electrostatic stress in catalysis: structure and mechanism of the enzyme orotidine monophosphate decarboxylase. Proc. Natl. Acad. Sci. U.S.A. 97:2000;2017-2022 This paper describes the X-ray structure of unliganded and 6-azauridine-bound ODCase from M. thermoautotrophicum. A ground state destabilization mechanism due to protein-substrate repulsive interactions in part of the substrate was proposed based on combined QM/MM molecular dynamics simulations.
13. Miller B.G., Hassell A.M., Wolfenden R., Milburn M.V., Short S.A. Anatomy of a proficient enzyme: the structure of orotidine 5′-monophosphate decarboxylase in the presence and absence of a potential transition state analog. Proc. Natl. Acad. Sci. U.S.A. 97:2000;2011-2016.
14. Harris P., Poulsen J.-C.N., Jensen K.F., Larsen S. Structural basis for the catalytic mechanism of a proficient enzyme: orotidine 5′-monophosphate decarboxylase. Biochemistry. 39:2000;4217-4224.
15. Traut T.W., Temple B.R.S. The chemistry of the reaction determines the invariant amino acids during the evolution and divergence of orotidine 5′-monophosphate decarboxylase. J. Biol. Chem. 275:2000;28675-28681.
16. Miller B.G., Snider M.J., Wolfenden R., Short S.A. Dissecting a charged network at the active site of orotidine-5′-phosphate decarboxylase. J. Biol. Chem. 276:2001;15174-15176.
17. Feng W.Y., Austin T.J., Chew F., Gronert S., Wu W. The mechanism of orotidine 5′-monophosphate decarboxylase: catalysis by destabilization of the substrate. Biochemistry. 39:2000;1778-1783.
18. Lee J.K., Houk K.N. A proficient enzyme revisited: the predicted mechanism for orotidine monophosphate decarboxylase. Science. 276:1997;942-945.
19. Silverman R.B., Groziak M.P. Model chemistry for a covalent mechanism of action of orotidine 5′-phosphate decarboxylase. J. Am. Chem. Soc. 104:1982;6434-6439.
20. Lee T.-S., Chong L.T., Chodera J.D., Kollman P.A. An alternative explanation for the catalytic proficiency of orotidine 5′-phosphate decarboxylase. J. Am. Chem. Soc. 123:2001;12837-12848.
21. Hur S., Bruice T.C. Molecular dynamic study of orotidine-5′-monophosphate decarboxylase in ground state and in intermediate state: a role of the 203-218 loop dynamics. Proc. Nat. Acad. Sci. U.S.A. 99:2002;9668-9673 Molecular dynamics simulations of OMP in water and in ODCase were performed. When compared with the structures of the reactant state and TS simulations, the authors found significant conformational motions in a loop encapsulating the active site. The authors propose that protein loop motion contributes to catalysis.
22. Schowen RL: Catalytic power and transition-state stabilization. Transition States Biochem Processes 1978:77-114.
23. Yu E.W., Koshland D.E. Jr. Propagating conformational changes over long (and short) distances in proteins. Proc. Natl. Acad. Sci. U.S.A. 98:2001;9517-9520 A concise picture is presented of the mechanism and energetics associated with substrate-binding-induced protein conformational change. The idea is illustrated by aspartate receptor signal transduction through a 1 Å protein conformational change over long distance.
24. Aaqvist J., Warshel A. Simulation of enzyme reactions using valence bond force fields and other hybrid quantum/classical approaches. Chem. Rev. 93:1993;2523-2544.
25. Koshland D.E. Jr. The active site and enzyme action. Adv. Enzymol. 22:1960;45-97.
26. Warshel A., Levitt M. Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. J. Mol. Biol. 103:1976;227-249.
27. Gao J., Xia X. A prior evaluation of aqueous polarization effects through Monte Carlo QM-MM simulations. Science. 258:1992;631-635.
28. Truhlar D.G., Gao J., Alhambra C., Garcia-Viloca M., Corchado J., Sanchez M.L., Villa J. The incorporation of quantum effects in enzyme kinetics modeling. Acc. Chem. Res. 35:2002;341-349.
29. Miller B.G., Wolfenden R. Catalytic proficiency: the unusual case of OMP decarboxylase. Annu. Rev. Biochem. 71:2002;847-885.
30. Dewar M.J.S., Zoebisch E.G., Healy E.F., Stewart J.J.P. Development and use of quantum mechanical molecular models. 76. AM1: a new general purpose quantum mechanical molecular model. J. Am. Chem. Soc. 107:1985;3902-3909.
31. 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. Biochem. 39:2000;14728-14738 This paper describes an EVB study of the ODCase reaction. A novel reference state was designed by including Lys72 as a counterion, placed 6 Å from the carboxylate carbon of orotic acid. It was proposed that Lys72 neutralizes the charge of the substrate carboxylate group, producing a small dipole moment in the reactant state, whereas the dipole moment is increased in the TS, leading to TS stabilization.
32. Sievers A., Wolfenden R. Equilibrium of formation of the 6-carbanion of UMP, a potential intermediate in the action of OMP decarboxylase. J. Am. Chem. Soc. 124:2002;13986-13987.
33. Kollman P. Free energy calculations: applications to chemical and biochemical phenomena. Chem. Rev. 93:1993;2395-2417.
34. Alhambra C., Wu L., Zhang Z.-Y., Gao J. Walden-inversion-enforced transition-state stabilization in a protein tyrosine phosphatase. J. Am. Chem. Soc. 120:1998;3858-3866.
35. M, an observation that cannot be explained by TS stabilization.