Thermodynamic analysis of catalysis by the dihydroorotases from hamster and Bacillus caldolyticus, as compared with the uncatalyzed reaction

Biochemistry

Volumn 45, Issue 27, 2006, Pages 8275-8283

  Huang, Danny T ^c   Kaplan, Jacob ^a   Menz, R Ian ^d   Katis, Vittorio L ^e   Wake, R Gerry ^a   Zhao, Feng ^b   Wolfenden, Richard ^b   Christopherson, Richard I ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d FLINDERS UNIVERSITY   (Australia)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; HYDROGEN BONDS; HYDROLYSIS; MONOMERS; PARAMETER ESTIMATION; THERMAL EFFECTS; THERMODYNAMICS;

DIHYDROOROTASES; L-DIHYDROOROTATE; THERMOPHILIC DHOASE; THERMOPHILIC ENZYME;

ENZYMES;

DIHYDROOROTASE; UREA;

ARTICLE; BACILLUS CALDOLYTICUS; CATALYSIS; CIRCULAR DICHROISM; COMPETITIVE INHIBITION; DISSOCIATION CONSTANT; ENTHALPY; ENTROPY; ENZYME DENATURATION; ENZYME MECHANISM; ENZYME PURIFICATION; ENZYME SUBSTRATE COMPLEX; GEL FILTRATION; HAMSTER; HYDROGEN BOND; HYDROLYSIS; MASS SPECTROMETRY; MICHAELIS MENTEN KINETICS; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; TEMPERATURE DEPENDENCE; THERMODYNAMICS; THERMOPHILIC BACTERIUM; THERMOSTABILITY;

AMINO ACID SEQUENCE; ANIMALS; BACILLUS; CATALYSIS; CRICETINAE; DIHYDROOROTASE; ENZYME ACTIVATION; HYDROLYSIS; MOLECULAR SEQUENCE DATA; OROTIC ACID; PROTEIN DENATURATION; SEQUENCE ALIGNMENT; TEMPERATURE; THERMODYNAMICS;

BACILLUS CALDOLYTICUS; CRICETINAE;

EID: 33745848832     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060595w     Document Type: Article

References (40)

1. Williams, N. K., Simpson, R. J., Moritz, R. L., Peide, Y., Crofts, L., Minasian, E., Leach, S. J., Wake, R. G., and Christopherson, R. I. (1990) Location of the dihydroorotase domain within trifunctional hamster dihydroorotate synthetase, Gene 94, 283-288.
2. Jones, M. E. (1980) Pyrimidine nucleotide biosynthesis in animals: genes, enzymes, and regulation of UMP biosynthesis, Annu. Rev. Biochem. 49, 253-279.
3. Simmer, J. P., Kelly, R. E., Rinker, A. G., Jr., Zimmermann, B. H., Scully, J. L., Kim, H., and Evans, D. R. (1990) Mammalian dihydroorotase: nucleotide sequence, peptide sequences, and evolution of the dihydroorotase domain of the multifunctional protein CAD, Proc. Natl. Acad. Sci. U.S.A. 87, 174-178.
4. Fields, C., Brichta, D., Shepherdson, M., Farinha, M., and O'Donovan, G. (1999) Phylogenetic analysis and classification of dihydroorotases: a complex history for a complex enzyme, Paths Pyrimidines 7, 49-62.
5. Kelly, R. E., Mally, M. I., and Evans, D. R. (1986) The dihydroorotase domain of the multifunctional protein CAD. Subunit structure, zinc content, and kinetics, J. Biol. Chem. 261, 6073-6083.
6. Martin, P. D., Purcarea, C., Zhang, P., Vaishnav, A., Sadecki, S., Guy-Evans, H. I., Evans, D. R., and Edwards, B. F. P. (2005) The crystal structure of a novel, latent dihydroorotase from Aquifex aeolicus at 1.7Å resolution, J. Mol. Biol. 348, 535-547.
7. Taylor, W. H., Taylor, M. L., Balch, W. E., and Gilchrist, P. S. (1976) Purification and properties of dihydroorotase, a zinc-containing metalloenzyme in Clostridium oroticum, J. Bacteriol. 127, 863-873.
8. Thoden, J. B., Phillips, G. N. J., Neal, T. M., Raushel, F. M., and Holden, H. M. (2001) Molecular structure of dihydroorotase: a paradigm for catalysis through the use of a binuclear metal center, Biochemistry 40, 6989-6997.
9. Lee, M., Chan, C. W., Guss, J. M., Christopherson, R. I., and Maher, M. J. (2005) Dihydroorotase from Escherichia coli: loop movement and cooperativity between subunits, J. Mol. Biol. 348, 523-533.
10. Williams, N. K., Manthey, M. K., Hambley, T. W., O'Donoghue, S. I., Keegan, M., Chapman, B. E., and Christopherson, R. I. (1995) Catalysis by hamster dihydroorotase: zinc binding, site-directed mutagenesis, and interaction with inhibitors, Biochemistry 34, 11344-11352.
11. Christopherson, R. I., and Jones, M. E. (1980) The effects of pH and inhibitors upon the catalytic activity of the dihydroorotase of multienzymatic protein pyr1-3 from mouse Ehrlich ascites carcinoma, J. Biol. Chem. 255, 3358-3370.
12. Ghim, S. Y., Nielsen, P., and Neuhard, J. (1994) Molecular characterization of pyrimidine biosynthesis genes from the thermophile Bacillus caldolyticus, Microbiology 140, 479-491.
13. Hemmens, B., and Carrey, E. A. (1995) Mammalian dihydroorotase; secondary structure, and interactions with other proteolytic fragments from the multienzyme polypeptide CAD, Eur. J. Biochem. 231, 220-225.
14. Pace, C. N., and Scholtz, M. (1997) in Protein function: a practical approach (Creighton, T. E., Ed.) pp 299-321, Oxford University Press, Oxford, New York.
15. Christopherson, R. I., Schmalzl, K. J., Szabados, E., Goodridge, R. J., Harsanyi, M. C., Sant, M. E., Algar, E. M., Anderson, J. E., Armstrong, A., and Sharma, S. C. (1989) Mercaptan and dicarboxylate inhibitors of hamster dihydroorotase, Biochemistry 28, 463-470.
16. Washabaugh, M. W., and Collins, K. D. (1984) Dihydroorotase from Escherichia coli. Purification and characterization, J. Biol. Chem. 259, 3293-3298.
17. Pettigrew, D. W., Bidigare, R. R., Mehta, B. J., Williams, M. I., and Sander, E. G. (1985) Dihydro-orotase from Clostridium oroticum. Purification and reversible removal of essential zinc, Biochem. J. 230, 101-108.
18. Ogawa, J., and Shimizu, S. (1995) Purification and characterization of dihydroorotase from Pseudomonas putida, Arch. Microbiol. 164, 353-357.
19. Krungkrai, J., Cerami, A., and Henderson, G. B. (1990) Pyrimidine biosynthesis in parasitic protozoa: purification of a monofunctional dihydroorotase from Plasmodium berghei and Crithidia fasciculata, Biochemistry 29, 6270-6275.
20. Washabaugh, M. W., and Collins, K. D. (1986) Dihydroorotase from Escherichia coli. Sulfhydryl group-metal ion interactions, J. Biol. Chem. 261, 5920-5929.
21. Laidler, K. J., and Peterman, B. F. (1979) Temperature effects in enzyme kinetics, Methods Enzymol. 63, 234-257.
22. Fersht, A. (1977) Enzyme Structure and Mechanism, Freeman, New York.
23. Schramm, V. L. (1998) Enzymatic transition states and transition state analogue design, Annu. Rev. Biochem. 67, 693-720.
24. Cleland, W. W., and Northrop, D. B. (1999) Energetics of substrate binding, catalysis, and product release, Methods Enzymol. 308, 3-27.
25. Huang, D. T., Thomas, M. A., and Christopherson, R. I. (1999) Divalent metal derivatives of the hamster dihydroorotase domain, Biochemistry 38, 9964-9970.
26. Snider, M. J., Gaunitz, S., Ridgway, C., Short, S. A., and Wolfenden, R. (2000) Temperature effects on the catalytic efficiency, rate enhancement, and transition state affinity of cytidine deaminase, and the thermodynamic consequences for catalysis of removing a substrate "anchor", Biochemistry 39, 9746-9753.
27. 2, J. Biol. Chem. 261, 1164-1169.
28. Borgmann, U., Moon, T. W., and Laidler, K. J. (1974) Molecular kinetics of beef heart lactate dehydrogenase, Biochemistry 13, 5152-5158.
29. Eftink, M. R., and Biltonen, R. L. (1983) Energetics of ribonuclease A catalysis. 3. Temperature dependence of the hydrolysis of cytidine cyclic 2′,3′-phosphate, Biochemistry 22, 5140-5150.
30. Gaudin, C., Marty, B., Ragot, M., Sari, J. C., and Belaich, J. P. (1980) Thermodynamic studies of binding proteins: effects of temperature variations on substrate binding and conformation of the leucine-isoleucine-valine binding protein of Escherichia coli, Biochimie 62, 741-746.
31. Fabry, S., and Hensel, R. (1987) Purification and characterization of D-glyceraldehyde-3-phosphate dehydrogenase from the thermophilic archaebacterium Methanothermus fervidus, Eur. J. Biochem. 165, 147-155.
32. Wrba, A., Schweiger, A., Schultes, V., Jaenicke, R., and Zavodsky, P. (1990) Extremely thermostable D-glyceraldehyde-3-phosphate dehydrogenase from the eubacterium Thermotoga maritima, Biochemistry 29, 7584-7592.
33. Hensel, R., Laumann, S., Lang, J., Heumann, H., and Lottspeich, F. (1987) Characterization of two D-glyceraldehyde-3-phosphate dehydrogenases from the extremely thermophilic archaebacterium Thermoproteus tenax, Eur. J. Biochem. 170, 325-333.
34. Zavodszky, P., Kardos, J., Svingor, and Petsko, G. A. (1998) Adjustment of conformational flexibility is a key event in the thermal adaptation of proteins, Proc. Natl. Acad. Sci. U.S.A. 95, 7406-7411.
35. Jaenicke, R. (1991) Protein stability and molecular adaptation to extreme conditions, Eur. J. Biochem. 202, 715-728.
36. Callahan, B. P., Yuan, Y., and Wolfenden, R. (2005) The burden borne by urease, J. Am. Chem. Soc. 127, 10828-10829.
37. Wolfenden, R., Sinder, M., Ridgway, C., and Miller, B. (1999) The temperature dependence of enzyme rate enhancements, J. Am. Chem. Soc. 121, 7419-7420.
38. Williams, N. K., Peide, Y., Seymour, K. K., Ralston, G. B., and Christopherson, R. I. (1993) Expression of catalytically active hamster dihydroorotase domain in Escherichia coli: purification and characterization, Protein Eng. 6, 333-340.
39. Riddles, P. W., Blakeley, R. L., and Zerner, B. (1983) Reassessment of Ellman's reagent, Methods Enzymol. 91, 49-60.
40. Segal, I. H. (1975) Enzyme Kinetics: Behaviour and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems, Wiley, New York.