Atomic crystal and molecular dynamics simulation structures of human carbonic anhydrase II: Insights into the proton transfer mechanism

Biochemistry

Volumn 46, Issue 11, 2007, Pages 2930-2937

  Fisher, S Zoë ^a   Maupin, C Mark ^b   Budayova Spano, Monika ^c   Govindasamy, Lakshmanan ^a   Tu, Chingkuang ^a   Agbandje McKenna, Mavis ^a   Silverman, David N ^a   Voth, Gregory A ^b   McKenna, Robert ^a  

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

^b UNIVERSITY OF UTAH   (United States)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER CONCENTRATION; CONFORMATIONS; CRYSTAL STRUCTURE; MOLECULAR DYNAMICS; PROTON TRANSFER;

ROOT-MEAN-SQUARE FLUCTUATION; THERMAL PARAMETERS; ZINC-METALLOENZYME;

ENZYME KINETICS;

BICARBONATE; CARBON DIOXIDE; CARBONATE DEHYDRATASE II; HISTIDINE; HYDROXYL GROUP; PROTON; SOLVENT; WATER; ZINC;

ANISOTROPY; ARTICLE; CALCULATION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME STRUCTURE; HUMAN; MOLECULAR DYNAMICS; MOTION; PRIORITY JOURNAL; PROTON TRANSPORT; SIMULATION; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; CARBONIC ANHYDRASE II; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; HISTIDINE; HUMANS; MODELS, MOLECULAR; PROTONS;

EID: 33947414441     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi062066y     Document Type: Article

References (31)

1. The Carbonic Anhydrases: New Horizons (Chegwidden, W. R., Carter, N. D., and Edwards, Y. H., Eds.) Birkhäuser Verlag, Basel, Switzerland.
2. Duda, D. M., and McKenna, R. (2004) Handbook of Metalloproteins (A. Messerschmidt, A., Ed.) pp 249-263, John Wiley & Sons, New York.
3. Khalifah, R. G. (1971) The carbon dioxide hydration activity of carbonic anhydrase, J. Biol. Chem. 246, 2561-2573.
4. 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.
5. 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.
6. Lindskog, S. (1997) Structure and mechanism of carbonic anhydrase, Pharmacol. Ther. 74, 1-20.
7. 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.
8. Nair, S. K., and Christianson, D. W. (1991) Unexpected pH-dependent conformation of His64, the proton shuttle of carbonic anhydrase II, J. Am. Chem. Soc. 113, 9455-9458.
9. Fisher, Z., Hernandez Prada, J. A., Tu, C. K., 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.
10. Duda, D. M., 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., Sect. D 59, 93-104.
11. Jude, K. M., Banerjee, A. L., Haldar, M. K., Manokaran, S., Roy, B., Mallik, S, Srivastava, D. K., and Christianson, D. W. (2006) Ultrahigh resolution crystal structures of human carbonic anhydrase I and II complexed with "two-prong" inhibitors, J. Am. Chem. Soc. 128, 3011-3018.
12. 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, Biochemistry 16, 2241-2247.
13. Tanhauser, S. M., Jewell, D. A., Tu, C. K., Silverman, D. N., and Laipis, P. J. (1992) T7 expression vector optimized for site-directed mutagenesis using oligodeoxyribonucleotide cassettes, Gene 117, 113-117.
14. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
15. 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 & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr., Sect. B 54, 905-921.
16. Budayova-Spano, M., Fisher, S. Z., Dauvergne, M. T., Agbandje-McKenna, M., Silverman, D. N., Myles, D. A. A., and McKenna, R. (2006) Production and X-ray crystallographic analysis of fully deuterated human carbonic anhydrase II, Acta Crystallogr., Sect. F 62, 6-9.
17. Sheldrick, G. M., and Schneider, T. R. (1997) SHELXL: high-resolution refinement, Methods Enzymol. 277, 319-343.
18. Engh, R. A., and Huber, R. (1991) Accurate bond and angle parameters for X-ray protein structure refinement, Acta Crystallogr., Sect. A 47, 392-400.
19. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics, Acta Crystallogr., Sect. D 60, 2126-2132.
20. 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.
21. Kleywegt, G. J. (1992) Moleman, unpublished program, Uppsala University, Uppsala, Sweden.
22. Maupin C. M., and Voth G. A. (2007) Preferred orientations of His-64 in human carbonic anhydrase II, Biochemistry 46, 2938-2947.
23. 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.
24. Coates, L., Erskine, P. T., Wood, S. P., Myles, D. A. A., and Cooper, J. B. (2001) A neutron Laue diffraction study of endothiapepsin: Implications for the aspartic proteinase mechanism, Biochemistry 40, 13149-13157.
25. Post, C. B., Brooks, B. R., Karplus, M., Dobson, C., Artymiuk, P. J., Cheetham, J. C., and Phillips, D. C. (1986) Molecular dynamics simulations of native and substrate-bound lysozyme, J. Mol. Biol. 190, 455-479.
26. 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.
27. Amiss, J. C., and Gurman, S. J. (1999) Biological EXAFS at room temperature, J. Synchrotron Radiat. 6, 387-388.
28. Bergquist, C., Fillebeen, T., Morlok, M. M., and Parkin, G. J. (2003) Protonation and reactivity towards carbon dioxide of the mononuclear tetrahedral zinc and cobalt hydroxide complexes, [Tp(Bu)t(,Me)]ZnOH and [Tp(Bu)t(,Me)]CoOH: comparison of the reactivity of the metal hydroxide function in synthetic analogues of carbonic anhydrase, J. Am. Chem. Soc. 125, 6189-6199.
29. Cui, Q., and Karplus, M. (2003) Is a "proton wire" concerted or stepwise? A model study of proton transfer in carbonic anhydrase, J. Phys. Chem. B 107, 1071-1078.
30. Esnouf, R. M. (1997) An extensively modified version of MolScript that includes greatly enhanced coloring capabilities, J. Mol. Graphics Modell. 15, 132-134.
31. Merritt, E. A., and Bacon, D. J. (1997) Raster3D: photorealistic molecular graphics, Methods Enzymol. 277, 505-524.