Structural and kinetic characterization of active-site histidine as a proton shuttle in catalysis by human carbonic anhydrase II

Biochemistry

Volumn 44, Issue 4, 2005, Pages 1097-1105

  Fisher, Zoë ^a   Hernandez Prada, Jose A ^a   Tu, Chingkuang ^a   Duda, David ^a   Yoshioka, Craig ^a   An, Haiqian ^a   Govindasamy, Lakshmanan ^a   Silverman, David N ^a   McKenna, Robert ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTAL STRUCTURE; ENZYME KINETICS; ENZYMES; HYDRATION; HYDROGEN BONDS; MASS SPECTROMETRY; PH EFFECTS; PROTONS; STRUCTURAL ANALYSIS;

HISTIDINE; HUMAN CARBONIC ANHYDRASES; PROTON TRANSFER; WATER BRIDGE;

CATALYSIS;

BICARBONATE; CARBON DIOXIDE; CARBONATE DEHYDRATASE II; HISTIDINE; WATER; ZINC;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME KINETICS; ENZYME STRUCTURE; EVALUATION; HUMAN; HYDRATION; HYDROGEN BOND; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTON TRANSPORT;

ALANINE; AMINO ACID SUBSTITUTION; ASPARAGINE; BINDING SITES; CARBON DIOXIDE; CARBONIC ANHYDRASE II; CATALYSIS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; ENERGY TRANSFER; HISTIDINE; HUMANS; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; KINETICS; OXYGEN ISOTOPES; PROTONS; STRUCTURE-ACTIVITY RELATIONSHIP; WATER;

EID: 13444269025     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0480279     Document Type: Article

References (37)

1. Lindskog, S. (1997) Structure and mechanism of carbonic anhydrase, Pharmacol. Ther. 74, 1-20.
2. Christianson, D. W., and Fierke, C. A. (1996) Carbonic Anhydrase: Evolution of the Zinc Binding Site by Nature and by Design, Acc. Chem. Res. 29, 331-339.
3. Silverman, D. N., and Lindskog, S. (1988) The catalytic mechanism of carbonic anhydrase: Implications of a rate-limiting protolysis of water, Acc. Chem. Res. 21, 30-36.
4. Tu, C. K., Silverman, D. N., Forsman, C., Jonsson, B.-H., and Lindskog, S. (1989) Role of histidine 64 in the catalytic mechanism of human carbonic anhydrase II studied with a site-specific mutant, Biochemistry 28, 7913-7918.
5. Venkatasubban, K. S., and Silverman, D. N. (1980) Carbon dioxide hydration activity of carbonic anhydrase in mixtures of water and deuterium oxide, Biochemistry 19, 4984-4989.
6. Smedarchina, Z., Siebrand, W., Fernandez-Ramos, A., and Cui, Q. (2003) Kinetic isotope effects for concerted multiple proton transfer: A direct dynamics study of an active-site model of carbonic anhydrase II, J. Am. Chem. Soc. 125, 243-251.
7. Cui, Q., and Karplus, M. (2002) Quantum mechanics/molecular mechanics studies of triosephosphate isomerase-catalyzed reactions: Effect of geometry and tunneling on proton-transfer rate constants, J. Am. Chem. Soc. 124, 3093-3124.
8. Silverman, D. N., Tu, C., Chen, X., Tanhauser, S. M., Kresge, A. J., and Laipis, P. J. (1993) Rate-equilibria relationships in intramolecular proton transfer in human carbonic anhydrase III, Biochemistry 32, 10757-10762.
9. Nair, S. K., and Christianson, D. W. (1991) Unexpected pH-dependent conformation of His-64, the proton shuttle of carbonic anhydrase II, J. Am. Chem. Soc. 113, 9455-9458.
10. Tripp, B. C., and Ferry, J. G. (2000) A structure-function study of a proton transport pathway in the γ-class carbonic anhydrase from Methanosarcina thermophila, Biochemistry 39, 9232-9240.
11. Iverson, T. M., Alber, B. E., Kisker, C., Ferry, J. G., and Rees, D. C. (2000) A closer look at the active site of γ-class carbonic anhydrases: High-resolution crystallographic studies of the carbonic anhydrase from Methanosarcina thermophila, Biochemistry 39, 9222-9231.
12. Jude, K. M., Wright, S. K., Tu, C. K., Silverman, D. N., Viola, R. E., and Christianson, D. W. (2002) Crystal structure of F65A/Y131C-methylimidazole carbonic anhydrase V reveals architectural features of an engineered proton shuttle, Biochemistry 41, 2485-2491.
13. Khalifah, R. G. (1971) The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C, J. Biol. Chem. 246, 2561-2573.
14. Steiner, H., Jonsson, B.-H., and Lindskog, S. (1975) The catalytic mechanism of carbonic anhydrase. Hydrogen-isotope effects on the kinetic parameters of the human C isoenzyme, Eur. J. Biochem. 59, 253-259.
15. Campbell, I. D., Lindskog, S., and White, A. L. (1975) A study of the histidine residues of human carbonic anhydrase C using 270 MHz proton magnetic resonance, J. Mol. Biol. 98, 597-614.
16. Krebs, J. F., Fierke, C. A., Alexander, R. S., and Christianson, D. W. (1991) Conformational mobility of His-64 in the Thr-200 → Ser mutant of human carbonic anhydrase II, Biochemistry 30, 9153-9160.
17. Liang, Z., Jonsson, B.-H., and Lindskog, S. (1993) Proton transfer in the catalytic mechanism of carbonic anhydrase. Effects of placing histidine residues at various positions in the active site of human isoenzyme II, Biochim. Biophys. Acta 1203, 142-146.
18. An, H., Tu, C. K., Ren, K., Laipis, P. J., and Silverman, D. N. (2002) Proton transfer within the active-site cavity of carbonic anhydrase III, Biochim. Biophys. Acta 1599, 21-27.
19. Khalifah, R. G., Strader, D. J., Bryant, S. H., and Gibson, S. M. (1977) Carbon-13 nuclear magnetic resonance probe of active-site ionizations in human carbonic anhydrase B, Biochemistry 16, 2241-2247.
20. McPherson, A. (1982) Preparation and Analysis of Protein Crystals, Wiley, New York.
21. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode, Methods Enzymol. 276, 307-326.
22. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr. A47, 110-119.
23. Brünger, A. T., Adams, P. D., Clore, G. M., DeLaiio, W. L., Gros, P., Grosse-Kuntsleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M.. Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
24. Håkansson, K., Carlsson, M., Svensson, L. A., and Liljas, A. (1992) Structure of native and apo carbonic anhydrase II and structure of some of its anion-ligand complexes, J. Mol. Biol. 227, 1192-1204.
25. Silverman, D. N. (1982) Carbonic anhydrase:oxygen-18 exchange catalyzed by an enzyme with rate-contributing proton-transfer steps, Methods Enzymol. 87, 732-752.
26. Krebs, J. F., Ippolito, J. A., Christianson, D. W., and Fierke, C. A. (1993) Structural and functional importance of a conserved hydrogen bond network in human carbonic anhydrase II, J. Biol. Chem. 268, 27458-27466.
27. Simonsson, I., and Lindskog, S. (1982) The interaction of sulfate with carbonic anhydrase, Eur. J. Biochem. 123, 29-36.
28. Liljas, A., Håkansson, K., Jonsson, B.-H., and Xue, Y. (1994) Inhibition and catalysis of carbonic anhydrase. Recent crystallographic analyses, Eur. J. Biochem. 219, 1-10.
29. Xue, Y., Liljas, A., Jonsson, B.-H., and Lindskog, S. (1993) Structural analysis of the zinc hydroxide-Thr-199-Glu-106 hydrogen-bond network in human carbonic anhydrase II, Proteins 17, 93-106.
30. Eriksson, A. E., Jones, T. A., and Liljas, A. (1988) Refined structure of human carbonic anhydrase II at 2.0 Å resolution, Proteins 4, 274-282.
31. Earnhardt, J. N., Wright, S. K., Qian, M., Tu, C. K., Laipis, P. J., Viola, R. E., and Silverman, D. N. (1999) Introduction of histidine analogs leads to enhanced proton transfer in carbonic anhydrase V, Arch. Biochem. Biophys. 361, 264-270.
32. ButMe]CoOH: Comparison of the reactivity of the metal hydroxide function in synthetic analogues of carbonic anhydrase, J. Am. Chem. Soc. 125, 6189-6199.
33. Amiss, J. C., and Gurman, S. J. (1999) Biological EXAFS at room temperature, J. Synchrotron Radiat. 6, 387-388.
34. Merrit, E. A., and Bacon, D. J. (1997) Raster3D: Photorealistic Molecular Graphics, Methods Enzymol. 277, 505-524.
35. Esnouf, R. M. (1999) Further additions to MolScript version 1.4, including reading and contouring of electron-density maps, Acta Crystallogr. D55, 938-940.
36. Lindskog, S., and Silverman, D. N. (2000) The catalytic mechanism of mammalian carbonic anhydrases, in The Carbonic Anhydrases: New Horizons (Chegwidden, W. R., Carter, N. D., and Edwards, Y. H., Eds.) pp 175-195, Birkhäuser Verlag, Basel, Switzerland.
37. Duda, D. M., Tu, C. K., Qian, M., Laipis, P. J., Agbandje-McKenna, M., Silverman, D. N., and McKenna, R. (2001) Structural and kinetic analysis of the chemical rescue of the proton transfer function of carbonic anhydrase II, Biochemistry 40, 1741-1748.