Human carbonic anhydrase III: Structural and kinetic study of catalysis and proton transfer

Biochemistry

Volumn 44, Issue 30, 2005, Pages 10046-10053

  Duda, David M ^a   Tu, Chingkuang ^a   Fisher, S Zoë ^a   An, Haiqain ^a   Yoshioka, Craig ^a   Govindasamy, Lakshmanan ^a   Laipis, Philip J ^a   Agbandje McKenna, Mavis ^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

CATALYSIS; CRYSTAL STRUCTURE; ENZYMES; PURIFICATION;

HUMAN CARBONIC ANHYDRASE III (HCA III); IMIDAZOLE; ISOZYMES; PROTON DONORS;

PROTONS;

CARBONATE DEHYDRATASE II; CARBONATE DEHYDRATASE III; HISTIDINE; IMIDAZOLE DERIVATIVE; LEUCINE; PHENYL GROUP; PHENYLALANINE; ZINC;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CRYSTALLIZATION; ENZYME ACTIVE SITE; ENZYME KINETICS; ENZYME PURIFICATION; HUMAN; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTON TRANSPORT; SITE DIRECTED MUTAGENESIS; STEREOCHEMISTRY; STRUCTURE ANALYSIS;

CARBONIC ANHYDRASE III; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; ENZYME ACTIVATION; HISTIDINE; HUMANS; IMIDAZOLES; KINETICS; LEUCINE; LYSINE; OLIGOPEPTIDES; PROTONS; STRUCTURE-ACTIVITY RELATIONSHIP; THREONINE; ZINC;

EID: 23044492686     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050610h     Document Type: Article

References (47)

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. 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.
5. 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.
6. 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.
7. Parkkila, S. (2000) An overview of the distribution and function of carbonic anhydrase in mammals, in The Carbonic Anhydrases New Horizons (Chegwidden, W. R., Carter, N. D., and Edwards, Y. H., Eds.) pp 79-93, Birkhäuser Verlag, Basel.
8. Sly, W. S., and Hu, P. Y. (1995) Human carbonic anhydrases and carbonic anhydrase deficiencies, Annu. Rev. Biochem. 64, 375-401.
9. Chegwidden, W. R., and Carter, N. D. (2000) Introduction to the carbonic anhydrases, in The Carbonic Anhydrases New Horizons (Chegwidden, W. R., Carter, N. D., and Edwards, Y. H., Eds.) pp 13-28, Birkhäuser Verlag, Basel.
10. Kim, G., Lee, T. H., Wetzel, P., Geers, C., Robinson, M. A., Myers, T. G., Owens, J. W., Wehr, N. B., Eckhaus, M. W., Gros, G., Wynshaw-Boris, A., and Levine, R. L. (2004) Carbonic anhydrase III is not required in the mouse for normal growth, development, and life span, Mol. Cell. Biol. 24, 9942-9947.
11. Sanyal, G. S., Swenson, E. R., Pessah, N. I., and Maren, T. H. (1982) The carbon dioxide hydration activity of skeletal muscle carbonic anhydrase. Inhibition by sulfonamides and anions, Mol. Pharmacol. 22, 211-220.
12. Jewell, D. A., Tu, C. K., Paranawithana, S. R., Tanhauser, S. M., LoGrasso, P. V., Laipis, P. J., and Silverman, D. N. (1991) Enhancement of the catalytic properties of human carbonic anhydrase III by site-directed mutagenesis, Biochemistry 30, 1484-1490.
13. Eriksson, A. E., and Liljas, A. (1993) Refined structure of bovine carbonic anhydrase III at 2.0 Å resolution, Proteins: Struct., Funct., Genet. 16, 29-42.
14. Mallis, R. J., Poland, B. W., Chatterjee, T. K., Fisher, R. A., Darmawan, S., Honztko, R. B., and Thomas, J. (2000) Crystal structure of S-glutathiolated carbonic anhydrase III, FEBS Lett. 482, 237-241.
15. Ren, X., Jonsson, B.-H., and Lindskog, S. (1991) Some properties of site-specific mutants of human carbonic anhydrase II having active-site residues characterizing carbonic anhydrase III, Eur. J. Biochem. 201, 417-420.
16. LoGrasso, P. V., Tu, C. K., Jewell, D. A., Wynns, G. C., Laipis, P. J., and Silverman, D. N. (1991) Catalytic enhancement of human carbonic anhydrase III by replacement of phenylalanine-198 with leucine, Biochemistry 30, 8463-8470.
17. Chen, X., Tu, C. K., LoGrasso, P. V., Laipis, P. J., and Silverman, D. N. (1993) Interaction and influence of phenylalanine-198 and threonine-199 on catalysis by human carbonic anhydrase III, Biochemistry 32, 7861-7865.
18. Duda, D., 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.
19. An, H., Tu, C. K., Duda, D., Montanez-Clemente, I., Math, K., Laipis, P. J., McKenna, R., and Silverman, D. N. (2002) Chemical rescue in catalysis by human carbonic anhydrases II and III, Biochemistry 41, 3235-3242.
20. Silverman, D. N., Tu, C. K., 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.
21. Duda, D., Govindasamy, L., Agbandje-McKenna, M., Tu, C. K., Silverman, D. N., and McKenna, R. (2003) The refined atomic structure of carbonic anhydrase II at 1.05 Å resolution: implications of chemical rescue of proton transfer, Acta Crystallogr. D59, 93-104.
22. Briganti, F., Mangani, S., Orioli, P., Scozzafava, A., Vernaglione, G., and Supuran, C. T. (1997) Carbonic anhydrase activators: X-ray crystallographic and spectroscopic investigations for the interaction of isozymes I and II with histamine, Biochemistry 36, 10384-10392.
23. Duda, D., Yoshioka, C., Govindasamy, L., An, H., Tu, C. K., Silverman, D. N., and McKenna R. (2002) Crystallization and preliminary X-ray analysis of human carbonic anhydrase III, Acta Crystallogr. D58, 849-852.
24. Studier, F. W., Rosenberg, A. H., Dunn, J. J., and Dubendorff, S. J. W. (1990) Use of T7 RNA polymerase to direct expression of cloned genes, Methods Enzymol. 185, 60-89.
25. Engberg, P., Millqvist, E., Pohl, G., and Lindskog, S. (1985) A comparison of the kinetic properties of native bovine muscle carbonic anhydrase and an activated derivative with modified thiol groups, Arch. Biochem. Biophys. 241, 628-638.
26. McPherson, A. (1982) Preparation and Analysis of Protein Crystals, Wiley and Sons, New York.
27. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
28. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, 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 and NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
29. 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.
30. Silverman, D. N. (1982) Carbonic anhydrase: oxygen-18 exchange catalyzed by an enzyme with rate-contributing proton-transfer steps, Methods Enzymol. 87, 732-752.
31. 13C nuclear-magnetic-resonance study of CO2-HC03-exchange catalyzed by human carbonic anhydrase C at chemical equilibrium, Eur. J. Biochem. 93, 409-417.
32. 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.
33. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK-a program to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291.
34. Luzzati, V. (1952) Traitement statistique de erreurs dans la determination des structures cristallines, Acta Crystallogr. 5, 802-810.
35. Fisher, Z., Hernandez Prada, J. A., Tu, C., Duda, D., Yoshioka, C., An, H., Govindasamy, L., Silverman, D. N., and McKenna, R. (2005) Structural and kinetic characterization of active-site histidine as a proton shuttle in catalysis by human carbonic anhydrase II, Biochemistry 44, 1097-1105.
36. 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.
37. Kannan, K. K., Petef, M., Fridborg, K., Cid-Dresdner, H., and Lovgren, S. (1977) Structure and function of carbonic anhydrases. Imidazole binding to human carbonic anhydrase B and the mechanism of action of carbonic anhydrases, FEBS Lett. 73, 115-119.
38. Elder, I., Tu, C. K., Ming, L. J., McKenna, R., and Silverman, D. N. (2005) Proton transfer from exogenous donors in catalysis by human carbonic anhydrase II, Arch. Biochem. Biophys. 437, 106-114.
39. Krebs, J. F., Fierke, C. A., Aleander, 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.
40. Tu, C. K., Chen, X., Ren, X., LoGrasso, P. V., Jewell, D. A., Laipis, P. J., and Silverman, D. N. (1994) Interactions of active-site residues and catalytic activity of human carbonic anhydrase III, J. Biol. Chem. 269, 23002-32006.
41. Lograsso, P. V., Tu, C. K., Chen, X., Taoka, S., Laipis, P. J., and Silverman, D. N. (1993) Influence of amino acid replacement at position 198 on catalytic properties of zinc-bound water in human carbonic anhydrase III, Biochemistry 32, 5786-5791.
42. Martin, R. B. (1976) Nucleophilicities of metal-ion bound hydroxide, J. Inorg. Nucl. Chem. 38, 511-513.
43. Jeffry, G. A. (1997) An introduction to Hydrogen Bonding, Chapter 2, pp 11-32, Oxford University Press, Oxford.
44. Briganti, F., Scozzafava, A., and Supuran, C. T. (1999) Novel carbonic anhydrase isozymes I, II and IV activators incorporating sulfonyl-histamino moieties, Bioorg. Med. Chem. Lett. 9, 2043-2048.
45. Kresge, A. J., and Silverman, D. N. (1999) Application of Marcus rate theory to proton transfer in enzyme-catalyzed reactions, Methods Enzymol. 308, 276-297.
46. Merrit, E. A., and Bacon, D. J. (1997) Raster3D: Photorealistic Molecular Graphics, Methods Enzymol. 277, 505-524.
47. Esnouf, R. M. (1999) Further additions to MolScript version 1.4, including reading and contouring of electron-density maps, Acta Crystallogr. D55, 938-940.