Combined density functional theory (DFT) and continuum calculations of p K a in carbonic anhydrase

Biochemistry

Volumn 51, Issue 30, 2012, Pages 5979-5989

  Jiao, Dian ^a   Rempe, Susan B ^a  

^a SANDIA NATIONAL LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ACTIVE SITE STRUCTURE; CARBONIC ANHYDRASE II; CONTINUUM MODEL; DENSITY FUNCTIONAL THEORIES (DFT); ELECTRONIC ENVIRONMENTS; LOCAL POLARIZATION; QUANTUM CHEMISTRY CALCULATIONS; RATE-LIMITING STEPS; SURROUNDING ENVIRONMENT; WATER-SOLUBLE FORM; ZINC IONS;

CARBON DIOXIDE; CARBONIC ANHYDRASE; CONTINUUM MECHANICS; DENSITY FUNCTIONAL THEORY; QUANTUM CHEMISTRY;

ZINC;

CARBON DIOXIDE; CARBONATE DEHYDRATASE; WATER; ZINC ION;

ARTICLE; CALCULATION; CONFORMATION; CRYSTAL STRUCTURE; DENSITY FUNCTIONAL THEORY; DEPROTONATION; DIPOLE; DISSOCIATION; POLARIZATION; PRIORITY JOURNAL; PROTON TRANSPORT; QUANTUM CHEMISTRY; QUANTUM MECHANICS;

CARBONIC ANHYDRASES; CATALYTIC DOMAIN; COMPUTATIONAL BIOLOGY; CRYSTALLOGRAPHY, X-RAY; HUMANS; HYDROGEN-ION CONCENTRATION; MUTAGENESIS, SITE-DIRECTED; WATER; ZINC;

EID: 84864455063     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201771q     Document Type: Article

References (98)

1. IPCC (2001) The Carbon Cycle and Atmospheric Carbon Dioxide, in Climate Change 2001: The Scientific Basis, Cambridge University Press, U.K.
2. Lindskog, S. (1973) The catalytic mechanism of carbonic anhydrase Proc. Natl. Acad. Sci. U.S.A. 70, 4
3. Lindskog, S. (1997) Structure and mechanism of carbonic anhydrase Pharmacol. Therapeut. 74, 1-20
4. 2 solvation free energy using quasi-chemical theory J. Chem. Phys. 134, 224506-224514
5. Hakansson, 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
6. Woolley, P. (1975) Models for metal ion function in carbonic anhydrase Nature 258, 677-682
7. 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
8. Zhang, X., Hubbard, C. D., and van Eldik, R. (1996) Carbonic anhydrase catalysis: A volume profile analysis J. Phys. Chem. 100, 9161-9171
9. Kimura, E. (2000) Model studies for molecular recognition of carbonic anhydrase and carboxypeptidase Acc. Chem. Res. 34, 171-179
10. Lindskog, S. and Silverman, D. N. (2000) The Catalytic Mechanism of Mammalian Carbonic Anhydrases, Birkhauser Verlag, Basel, Switzerland.
11. Domsic, J. F., Avvaru, B. S., Kim, C. U., Gruner, S. M., Agbandje-McKenna, M., Silverman, D. N., and McKenna, R. (2008) Entrapment of carbon dioxide in the active site of carbonic anhydrase II J. Biol. Chem. 283, 30766-30771
12. Liang, J. Y. and Lipscomb, W. N. (1986) Theoretical study of the uncatalyzed hydration of carbon dioxide in the gas phase J. Am. Chem. Soc. 108, 5051-5058
13. Merz, K. M., Hoffmann, R., and Dewar, M. J. S. (1989) The mode of action of carbonic anhydrase J. Am. Chem. Soc. 111, 5636-5649
14. + hypersurfaces. On the role of zinc in the catalytic mechanism of carbonic anhydrase J. Am. Chem. Soc. 112, 8692-8705
15. Merz, K. M. (1991) Carbon dioxide binding to human carbonic anhydrase II J. Am. Chem. Soc. 113, 406-411
16. Aqvist, J. and Warshel, A. (1992) Computer simulation of the initial proton transfer step in human carbonic anhydrase I J. Mol. Biol. 224, 7-14
17. Aqvist, J., Fothergill, M., and Warshel, A. (1993) Computer simulation of the carbon dioxide/bicarbonate interconversion step in human carbonic anhydrase I J. Am. Chem. Soc. 115, 631-635
18. Hartsough, D. S. and Merz, K. M., Jr. (1995) Dynamic force field models: Molecular dynamics simulations of human carbonic anhydrase II using a quantum mechanical/molecular mechanical coupled potential J. Phys. Chem. 99, 11266-11275
19. Merz, K. M. and Banci, L. (1997) Binding of bicarbonate to human carbonic anhydrase II: A continuum of binding states J. Am. Chem. Soc. 119, 863-871
20. 2 J. Mol. Model. 4, 355-365
21. Schutz, C. N. and Warshel, A. (2004) Analyzing free energy relationships for proton translocations in enzymes: carbonic anhydrase revisited J. Phys. Chem. B 108, 2066-2075
22. Braun-Sand, S., Strajbl, M., and Warshel, A. (2004) Studies of proton translocations in biological systems: simulating proton transport in carbonic anhydrase by EVB-based models Biophys. J. 87, 2221-2239
23. Brauer, M., Perez-Lustres, J. L., Weston, J., and Anders, E. (2002) Quantitative reactivity model for the hydration of carbon dioxide by biomimetic zinc complexes Inorg. Chem. 41, 1454-1463
24. Mohammed, O. F., Pines, D., Dreyer, J., Pines, E., and Nibbering, E. T. J. (2005) Sequential proton transfer through water bridges in acid-base reactions Science 310, 83-86
25. Domsic, J. F., Williams, W., Fisher, S. Z., Tu, C., Agbandje-McKenna, M., Silverman, D. N., and McKenna, R. (2010) Structural and kinetic study of the extended active site for proton transfer in human carbonic anhydrase II Biochemistry 49, 6394-6399
26. Riccardi, D., Konig, P., Prat-Resina, X., Yu, H., Elstner, M., Frauenheim, T., and Cui, Q. (2006) "Proton holes" in long-range proton transfer reactions in solution and enzymes: a theoretical analysis J. Am. Chem. Soc. 128, 16302-16311
27. Swanson, J. M. J., Maupin, C. M., Chen, H., Petersen, M. K., Xu, J., Wu, Y., and Voth, G. A. (2007) Proton solvation and transport in aqueous and biomolecular systems: insights from computer simulations J. Phys. Chem. B 111, 4300-4314
28. 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
29. Kiefer, L. L. and Fierke, C. A. (1994) Functional characterization of human carbonic anhydrase II variants with altered zinc binding sites Biochemistry 33, 15233-15240
30. March, J. (1985) Advanced Organic Chemistry, 3 rd ed., John Wiley & Sons Inc, Hoboken, NJ.
31. a calculations with continuum dielectric methods J. Phys. Chem. 95, 5610-5620
32. Chipot, C. and Pohorille, A. (2007) Free Energy Calculations. Theory and Applications in Chemistry and Biology, Springer, New York, NY.
33. Warshel, A., Sussman, F., and King, G. (1986) Free energy of charges in solvated proteins: microscopic calculations using a reversible charging process Biochemistry 25, 8368-8372
34. Warshel, A. and Weiss, R. M. (1980) An empirical valence bond approach for comparing reactions in solutions and in enzymes J. Am. Chem. Soc. 102, 6218-6226
35. a's of ionizable residues in proteins: semi-microscopic and microscopic approaches J. Phys. Chem. B 101, 4458-4472
36. a calculations along a bacteriorhodopsin molecular dynamics trajectory Biophys. Chem. 65, 189-204
37. a calculations Protein Sci. 12, 14
38. a shifts in proteins using a combination of molecular mechanical and continuum solvent calculations J. Comput. Chem. 25, 1865-1872
39. a calculations with explicit and implicit solvent models J. Am. Chem. Soc. 126, 4167-4180
40. a's of ionizable groups in proteins: atomic detail from a continuum electrostatic model Biochemistry 29, 10219-10225
41. a values of protonated benzimidazoles (Part 2) J. Phys. Chem. B 110, 20546-20554
42. as of phosphoric (V) acid in the polarisable continuum and cluster-continuum models J. Mol. Struct. 924-926, 170-174
43. Leung, K., Nielsen, I. M. B., and Criscenti, L. J. (2009) Elucidating the bimodal acid-base behavior of the water-silica interface from first principles J. Am. Chem. Soc. 131, 18358-18365
44. a calculations with QM/MM free energy perturbations J. Phys. Chem. B 107, 14521-14528
45. a calculations in solution and proteins with QM/MM free energy perturbation simulations: A quantitative test of QM/MM protocols J. Phys. Chem. B 109, 17715-17733
46. a analysis for the zinc-bound water in human carbonic anhydrase II: Benchmark for "multiscale" QM/MM simulations and mechanistic implications J. Phys. Chem. A 111, 5703-5711
47. a of residue 66 in Staphylococcal nuclease. I. Insights from QM/MM simulations with conventional sampling J. Phys. Chem. B 112, 8387-8397
48. a analysis of Glu286 in cytochrome c oxidase (Rhodobacter sphaeroides): Toward a calibrated molecular model Biochemistry 48, 2468-2485
49. a and infrared spectra J. Am. Chem. Soc. 133, 14981-14997
50. a, redox reactions and solvation free energies J. Phys. Chem. B 113, 1253-1272
51. Bottoni, A., Lanza, C. Z., Miscione, G. P., and Spinelli, D. (2004) New model for a theoretical density functional theory investigation of the mechanism of the carbonic anhydrase: How does the internal bicarbonate rearrangement occur? J. Am. Chem. Soc. 126, 1542-1550
52. Miscione, G., Stenta, M., Spinelli, D., Anders, E., and Bottoni, A. (2007) New computational evidence for the catalytic mechanism of carbonic anhydrase Theoretical Chem. Acc.: Theory, Computat. Modeling (Theoretica Chim. Acta) 118, 193-201
53. Pratt, L. R. and Rempe, S. B. (1999) Quasi-chemical theory and implicit solvent models for simulations Simulation and Theory of Electrostatic Interactions in Solution. AIP Conference Proceedings 492, 30
54. Beck, T. L., Paulaitis, M. E., and Pratt, L. R. (2006) The Potential Distribution Theorem and Models of Molecular Solutions, Cambridge University Press, Cambridge.
55. Varma, S. and Rempe, S. B. (2007) Tuning ion coordination architectures to enable selective partitioning Biophys. J. 93, 1093-1099
56. + selectivity in K channels and valinomycin: Over-coordination versus cavity-size constraints J. Mol. Biol. 376, 13-22
57. Varma, S. and Rempe, S. B. (2008) Structural transitions in ion coordination driven by changes in competition for ligand binding J. Am. Chem. Soc. 130, 15405-15419
58. Rogers, D. M. and Rempe, S. B. (2011) Probing the thermodynamics of competitive ion binding using minimum energy structures J. Phys. Chem. B 115, 14
59. Asthagiri, D., Dixit, P. D., Merchant, S., Paulaitis, M. E., Pratt, L. R., Rempe, S. B., and Varma, S. (2010) Ion selectivity from local configurations of ligands in solutions and ion channels Chem. Phys. Lett. 485, 1-7
60. Leung, K., Rempe, S. B., and von Lilienfeld, O. A. (2009) Ab initio molecular dynamics calculations of ion hydration free energies J. Chem. Phys. 130, 204507-204511
61. + in liquid water J. Am. Chem. Soc. 122, 966-967
62. + in liquid water Fluid Phase Equilib. 183-184, 121-132
63. Asthagiri, D., Pratt, L. R., and Ashbaugh, H. S. (2003) Absolute hydration free energies of ions, ion - water clusters, and quasichemical theory J. Chem. Phys. 119, 2702-2708
64. +(aq) on the basis of quasi-chemical theory and ab initio molecular dynamics Phys. Chem. Chem. Phys. 6, 1966-1969
65. Hummer, G., Pratt, L. R., and García, A. E. (1996) Free energy of ionic hydration J. Phys. Chem. 100, 1206-1215
66. 2+ and first transition row metals J. Am. Chem. Soc. 126, 1285-1289
67. Jiao, D., Leung, K., Rempe, S. B., and Nenoff, T. M. (2010) First principles calculations of atomic nickel redox potentials and dimerization free energies: A study of metal nanoparticle growth J. Chem. Theory Comput. 7, 485-495
68. LaViolette, R. A., Copeland, K. L., and Pratt, L. R. (2003) Cages of water coordinating Kr in aqueous solution J. Phys. Chem. A 107, 11267-11270
69. Ashbaugh, H. S., Asthagiri, D., Pratt, L. R., and Rempe, S. B. (2003) Hydration of krypton and consideration of clathrate models of hydrophobic effects from the perspective of quasi-chemical theory Biophys. Chem. 105, 323-338
70. Sabo, D., Rempe, S. B., Greathouse, J. A., and Martin, M. G. (2006) Molecular studies of the structural properties of hydrogen gas in bulk water Mol. Simul. 32, 269-278
71. Sabo, D., Varma, S., Martin, M. G., and Rempe, S. B. (2007) Studies of the thermodynamic properties of hydrogen gas in bulk water J. Phys. Chem. B 112, 867-876
72. Asthagiri, D., Merchant, S., and Pratt, L. R. (2008) Role of attractive methane-water interactions in the potential of mean force between methane molecules in water J. Chem. Phys. 128, 244512-244517
73. + selectivity in membrane transport J. Gen. Physiol. 137, 479-488
74. a, proton transfer reactions, and general acid catalysis reactions in enzymes Biochemistry 20, 3167-3177
75. Rogers, D. M., Jiao, D., Pratt, L. R., and Rempe, S. B. (2012) Structural models and molecular thermodynamics of hydration of ions and small molecules Annu. Rep. Computat. Chem. (In print) 7-14
76. +(aq) J. Phys. Chem. A 106, 9145-9148
77. DeLano, W. L. (2011) The PyMOL Molecular Graphics System, 1.3 ed., Schrodinger LLC, San Carlos, CA.
78. Frisch, M. J. T., G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Scalmani, G., Barone, V., Mennucci, B., Petersson, G. A., Nakatsuji, H., Caricato, M., Li, X., Hratchian, H. P., Izmaylov, A. F., Bloino, J., Zheng, G., Sonnenberg, J. L., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Vreven, T., Montgomery, Jr., J. A., Peralta, J. E., Ogliaro, F., Bearpark, M., Heyd, J. J., Brothers, E., Kudin, K. N., Staroverov, V. N., Kobayashi, R., Normand, J., Raghavachari, K., Rendell, A., Burant, J. C., Iyengar, S. S., Tomasi, J., Cossi, M., Rega, N., Millam, N. J., Klene, M., Knox, J. E., 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., Martin, R. L., Morokuma, K., Zakrzewski, V. G., Voth, G. A., Salvador, P., Dannenberg, J. J., Dapprich, S., Daniels, A. D., Farkas, Ö., Foresman, J. B., Ortiz, J. V., Cioslowski, J., and Fox, D. J. (2009) Gaussian 09, Revision A.1, Gaussian, Inc., Wallingford, CT.
79. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome Proc. Natl. Acad. Sci. 98, 10037-10041
80. Warshel, A., Naray-Szabo, G., Sussman, F., and Hwang, J. K. (1989) How do serine proteases really work? Biochemistry 28, 3629-3637
81. Breneman, C. M. and Wiberg, K. B. (1990) Determining atom-centered monopoles from molecular electrostatic potentials. The need for high sampling density in formamide conformational analysis J. Comput. Chem. 11, 361-373
82. Ohtaki, H. and Radnai, T. (1993) Structure and dynamics of hydrated ions Chem. Rev. 93, 1157-1204
83. Cossi, M., Barone, V., Cammi, R., and Tomasi, J. (1996) Ab initio study of solvated molecules: a new implementation of the polarizable continuum model Chem. Phys. Lett. 255, 327-335
84. Marenich, A. V., Cramer, C. J., and Truhlar, D. G. (2009) Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions J. Phys. Chem. B 113, 6378-6396
85. Rappe, A. K., Casewit, C. J., Colwell, K. S., Goddard, W. A., and Skiff, W. M. (1992) UFF, a full periodic table force field for molecular mechanics and molecular dynamics simulations J. Am. Chem. Soc. 114, 10024-10035
86. Keith, T. A. (2011) AIMALL, TK Gristmill Software, Overland Park, KS.
87. Bader, R. F. W. (1991) A quantum theory of molecular structure and its applications Chem. Rev. 91, 893-928
88. Nelson, R. D. J., Lide, D. R. J., and Maryott, A. A. (1967) Selected values of electric dipole moments for molecules in the gas phase, National Bureau of Standards, Washington, DC.
89. Rao, L., Cui, Q., and Xu, X. (2010) Electronic properties and desolvation penalties of metal ions plus protein electrostatics dictate the metal binding affinity and selectivity in the copper efflux regulator J. Am. Chem. Soc. 132, 18092-18102
90. Gutten, O., Besseova, I., and Rulisek, L. (2011) Interaction of metal ions with biomolecular ligands: how accurate are calculated free energies associated with metal ion complexation? J. Phys. Chem. A 115, 11394-11402
91. Schaftenaar, G. and Noordik, J. H. (2000) Molden: a pre- and post-processing program for molecular and electronic structures J. Comput.-Aided Mol. Des. 14, 12
92. Ryde, U. (1996) The coordination of the catalytic zinc ion in alcohol dehydrogenase studied by combined quantum-chemical and molecular mechanics calculations J. Comput.-Aided Mol. Des. 10, 153-164
93. Boiwe, T. and Branden, C.-I. (1977) X-ray investigation of the binding of 1,10-phenanthroline and imidazole to horse-liver alcohol dehydrogenase Eur. J. Biochem. 77, 173-179
94. Sartorius, C., Dunn, M. F., and Zeppezauer, M. (1988) The binding of 1,10-phenanthroline to specifically active-site cobalt(II)-substituted horse-liver alcohol dehydrogenase Eur. J. Biochem. 177, 493-499
95. Berg, J. M., Tymoczko, J. L., and Stryer, L. (2002) Biochemistry, 5 th ed., W H Freeman, New York, NY.
96. Christianson, D. W. and Fierke, C. A. (1996) ChemInform Abstract: Carbonic anhydrase: evolution of the zinc binding site by nature and by design, ChemInform 27.
97. a of zinc-bound water and nucleophilicity of hydroxo-containing species. Ab initio calculations on models for zinc enzymes Inorg. Chem. 29, 1460-1463
98. Dokmanic, I., Sikic, M., and Tomic, S. (2008) Metals in proteins: correlation between the metal-ion type, coordination number and the amino-acid residues involved in the coordination Acta. Cryst. D64, 257-263