Preferred orientations of His64 in human carbonic anhydrase II

Biochemistry

Volumn 46, Issue 11, 2007, Pages 2938-2947

  Maupin, C Mark ^a   Voth, Gregory A ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; DEHYDRATION; HYDRATION; MOLECULAR DYNAMICS; PROTONS; SOLVATION;

BIOCHEMICAL EFFECTS; HISTIDINE; HUMAN CARBONIC ANHYDRASE II (HCA II); PROTON DONORS;

ENZYME KINETICS;

CARBONATE DEHYDRATASE II; HISTIDINE; IMIDAZOLE; NITROGEN; PROTON; WATER; ZINC;

AMINO ACID SEQUENCE; ARTICLE; CALCULATION; CATALYSIS; CATALYST; ENERGY; ENZYME STRUCTURE; HUMAN; HYDRATION; MATHEMATICAL ANALYSIS; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTON TRANSPORT; ROTATION; SEQUENCE ANALYSIS; SIMULATION; SOLVATION; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BINDING SITES; CARBONIC ANHYDRASE II; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; HISTIDINE; HUMANS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; THERMODYNAMICS;

EID: 33947367836     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi062170f     Document Type: Article

References (56)

1. Lindskog, S., Behravean, G., Engstrand, C., Forsman, C., Jonsson, B., Liang, Z., Ren, X., and Xue, Y. (1991) in Carbonic Anhydrase-From Biochemistry and Genetics to Physiology and Clinical Medicine (Botre, F., Gros, G., Storey, B. T., Ed.) pp 1-13, VCH, Weinheim, Germany.
2. 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. 117, 9455-9458.
3. Christianson, D. W. (1991) The structural biology of zinc, Adv. Protein Chem. 42, 281-355.
4. Lesburg, C. A., and Christianson, D. W. (1995) X-ray crystallographic studies of engineered hydrogen bond networks in protein zinc binding site, J. Am. Chem. Soc. 117, 6838-6844.
5. Eriksson, A. E., Jones, A. T., and Liljas, A. (1988) Refined structure of human carbonic anhydrase II at 2.0 Å resolution, Proteins 4, 274-282.
6. Liljas, A., Kannan, K. K., Bergsten, P. C., and Waara, I. (1972) Crystal structure of human carbonic anhydrase C, Nature 235, 131-137.
7. Kannan, K. K., Ramanadham, M., and Jones, T. A. (1984) Structure, refinement, and function of carbonic anhydrase I, Ann. N.Y. Acad. Sci. 429, 49-60.
8. 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.
9. Duda, D., Tu, C., Qian, M., Laipis, P., Agvandje-McKenna, A., 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.
10. Duda, D., Govindasamy, L., Agbandje-McKenna, Tu, C., 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. Fersnt, A. (1985) Enzyme Structure and Mechanism, W. H. Freeman, New York.
12. 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.
13. Maren, T. H. (1967) Carbonic anhydrase: chemistry, physiology, and inhibition, Physiol. Rev. 47, 595-781.
14. Tashian, R. E. (1989) The carbonic anhydrase: widening perspectives on their evolution, expression and function, BioEssays 10, 186-192.
15. Henderson, L. E., Hendriksson, D., and Nyman, P. O. (1976) Primary structure of human carbonic anhydrase, J. Biol. Chem. 251, 5457-5463.
16. Lindskog, S., and Coleman, J. E. (1973) The catalytic mechanism of carbonic anhydrase, Proc. Natl. Acad. Sci. U.S.A. 70, 2505-2508.
17. Lindskog, S. (1983) In Zinc Enzymes (Spiro, I. G., Eds.) pp 78-121, John Wiley & Sons, New York.
18. Silverman, D. N., and Vincent, S. H. (1983) Proton transfer in the catalytic mechanism of carbonic anhydrase, CRC Crit. Rev. Biochem. 14, 207-255.
19. Toba, S., Colombo, G., and Merz, K. M., Jr. (1999) Solvent dynamics and mechanism of proton transfer in human carbonic anhydrase II, J. Am. Chem. Soc. 121, 2290-2302.
20. Lu, D., and Voth, G. A. (1998) Molecular dynamics simulations of human carbonic anhydrase II: insights into experimental results and the role of solvation, Proteins: Struct., Funct., Genet. 33, 119-134.
21. Lu, D., and Voth, G. A. (1998) Proton transfer in the enzyme carbonic anhydrase: an ab initio study, J. Am. Chem. Soc. 120, 4006-4014.
22. Cui, Q., and Karplus, K. (2003) Is a "proton wire" concerted or stepwise? A model study of proton transfer in carbonic anhydrase, J. Phys. Chem. B 107, 1071-1078.
23. Riccardi, D., Schaefer, P., Yang, Y., Yu, H., Ghosh, N., Prat-Resina, X., Konig, P., Li, G., Xu, D., Guo, H., Elstner, M., and Cui, Q. (2006) Development of effective quantum mechanical/ molecular mechanical (QM/MM) methods for complex biological processes, J. Phys. Chem. B 110, 6458-6469.
24. Tu, C., 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 stie-specific mutant, Biochemistry 28, 7913-7918.
25. Qian, M., Tu, C., Earnhardt, N., Laipis, P. J., and Silverman, D. N. (1997) Gultamate and aspartate as proton shuttles in mutants of carbonic anhydrase, Biochemistry 36, 15758-15764.
26. An, H., Tu, C., Duda, D., Montanez-Clemente, I., Math, K., Laipis, P. J., McKenna, R., and Silverman, D. N. (2002) Chemical rescue in catalysis by human carbonic anhydrase II, Biochemistry 41, 3235-3242.
27. Dapprich, S., Komaromi, I., Byun, K. S., Morokuma, K., and Frisch, M. J. (1999) A new ONIOM implementation in Gaussian98. Part I. The calculation of energies, gradients, vibrational frequencies and electric field derivatives. J. Mol. Struct. 462, 1-21.
28. -, J. Chem. Phys. 105, 1959-1967.
29. Kuno, M., Hannongbua, S., and Morokuma, K. (2003) Theoretical investigation on nevirapine and HIV-1 reverse transcriptase binding site interaction based on ONIOM method, Chem. Phys. Lett. 380, 456-463.
30. Maseras, F., and Morokuma, K. (1995) IMOMM: A new ab initio + molecular mechanics geometry optimization scheme of equilibrium structures and transition states, J. Comput. Chem. 16, 1170-1179.
31. Svensson, M., Humbel, S., Froese, R. D. J., Matsubara, T., Sieber, S., and Morkima, K. (1996) ONIOM: A multilayered integrated MO + MM method for geometry optimizations and single point energy predictions. A test for Diels-Alder reactions and Pt(P(t-Bu)3)2 + H2 oxidative addition, J. Phys. Chem. 100, 19357-19363.
32. Svensson, M., Humbel, S., and Morkuma, K. (1996) Energetics using the single point IMOMO (integrated molecular orbital + molecular orbital) calculations. Choices of computational levels and model system, J. Chem. Phys. 105, 3654-3661.
33. Vreven, T., and Morokuma, K. (2000) On the application of the IMOMO (integrated molecular orbital + molecular orbital) method, J. Comput. Chem. 21, 1419-1432.
34. Vreven, T., Mennucci, B., da Silva, C. O., Morokuma, K., and Tomasi, J. (2001) The ONIOM-PCM method: combining the hybrid molecular orbital method and the polarizable continuum model for solvation. Application to the geometry and properties of a merocyanine in solution, J. Chem. Phys. 115, 62-72.
35. Vreven, T., Morkuma, K., Farakas, O., Schlegel, H. B., and Frish, M. J. (2003) Geometry optimization with QM/MM, ONIOM, and other combined methods. I. Microiterations and constraints, J. Comput. Chem. 24, 760-769.
36. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J. A., Jr., Vreven, T., Kudin, K. N., Burant, J. C., Millam, J. M., Iyengar, S. S., Tomasi, J., Barone, V., Mennucci, B., Cossi, M., Scalmani, G., Rega, N., Petersson, G. A., Nakatsuji, H., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Klene, M., Li, X., Knox, J. E., Hratchian, H. P., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Ayala, P. Y., Morokuma, K., Voth, G. A., Salvador, P., Dannenberg, J. J., Zakrzewski, V. G., Dapprich, S., Daniels, A. D., Strain, M. C., Farkas, O., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Ortiz, J. V., Cui, Q., Baboul, A. G., Clifford, S., Cioslowski, J., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Gonzalez, C., and Pople, J. A. (2003) Gaussian 03, revision C.02; Gaussian, Inc., Wallingford, CT.
37. Lee, C. T., Yang, W. T., and Parr, R. G. (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density, Phys. Rev. B 37, 785-789.
38. Becke, A. D. (1993) Density-functional thermochemistry. 3. The role of exact exchange, J. Chem. Phys. 98, 5648-5652.
39. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M. Jr., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules, J. Am. Chem. Soc. 117, 5179-5197.
40. Hoops, S. C., Anderson, K. W., and Merz, K. M., Jr. (1991) Force field design for metalloproteins. J. Am. Chem. Soc. 113, 8262-8270.
41. Cieplak, P., Cornell, W. D., Bayly, C., and Kollman, P. A. (1995) Application of the multimolecule and multiconformational RESP methodology to biopolymers: charge derivation for DNA, RNA, and proteins, J. Comput. Chem. 16, 1357-1376.
42. Case, D. A., Pearlman, D. A., Caldwell, J. W., Cheatham, T. E., III, Wang, J., Ross, W. S., Simmerling, C. L., Darden, T. A., Merz, K. M., Stanton, R.V., Cheng, A. L., Vincent, J. J., Crow-ley, M., Tsui, V., Gohlke, H., Radmer, R. J., Duan, Y., Pitera, J., Massova, I., Seibel, G. L., Singh, U. C., Weiner, P. K., and Kollman, K. A. (2002) AMBER, University of California, San Francisco, CA.
43. Day, T. J., Soudackov, A. V., Cuma, M., Schmitt, U. W., and Voth, G. A. (2002) A second generation multistate empirical valence bond model for proton transport in aqueous systems, J. Chem. Phys. 117, 5839-5849.
44. Wang, J., Cieplak, P., and Kollman, P. A. (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 21, 1049.
45. Kast, S. M., Nicklas, K. Bär, H.-J., and Brickmann, J. (1994) Constant temperature molecular dynamics simulations by means of a stochastic collision model. I. Noninteracting particles, J. Chem. Phys. 100, 566-576.
46. Hummer, G., Pratt, L. R., and Garcia, A. E. (1996) Free energy of ionic hydration, J. Phys. Chem. 100, 1206-1215.
47. Kumar, S., Bouzida, D., Swendsen, R. H., Kollman, P. A., and Rosenberg, J. M. (1992) The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method, J. Comput. Chem. 13, 1011-1021.
48. Roux, B. (1995) The calculation of the potential of mean force using computer simulations, Comput. Phys. Commun. 91, 275-282.
49. 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.
50. Tu, C., Qian, M., Earnhardt, J. N., Laipis, P. J., and Silverman, D. N. (1998) Properties of intramolecular proton transport in carbonic anhydrase III, Biophys. J. 74, 3182-3189.
51. Fisher, Z. S., Maupin, C. M., Govindasamy, L., Budayova-Spano, M., Tu, C., Agbandje-McKenna, M., Silverman, D. N., Voth, G. A., and McKenna, R. (2006) Atomic crystal and molecular dynamics simulation structures of human carbonic anhydrase II: insights into the proton transfer mechanism, Biochemistry 46, 2930-2937.
52. Allen, T. W., Andersen, O. S., and Roux, B. (2004) Energetics of ion conduction through the gramacidin channel, Proc. Natl. Acad. Sci. U.S.A. 101, 117-122.
53. Gall, C. M., Cross, T. A., DiVerdi, J. A., and Opella, S. J. (1982) Protein dynamics by solid state NMR: the aromatic rings of the coat protein in fd, Proc. Natl. Acad. Sci. U.S.A. 79, 101-105.
54. Voth, G. A. (2006) Computer simulations of proton solvation and transport in aqueous and biomolecular systems, Acc. Chem. Res. 39, 143-150.
55. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics, J. Mol. Graphics 14, 33-38.
56. Merrit, E. A., and Murphy, M. E. P. (1994) Raster3D version 2.0: A program for photorealistic molecular graphics, Acta Crystallogr., Sect. D 50, 869-873.