The Crystal Structure of a hCA VII Variant Provides Insights into the Molecular Determinants Responsible for Its Catalytic Behavior(304 views) Buonanno M, Di Fiore A, Langella E, D’ambrosio K, Supuran CT, Monti SM, De Simone G
Keywords: Carbonic Anhydrases, Catalytic Efficiency, Pka, Proton Shuttle, Proton Transfer, Water Network, Carbonate Dehydratase, Carbonic Anhydrase Vii, Histidine, Unclassified Drug, Zinc, Protein Binding, Article, Crystal Structure, Crystallization, Enzyme Activity, Gene Mutation, Human, Hydrogen Bond, Protein Conformation, Protein Data Bank, Protein Expression, Protein Interaction, Protein Purification, Protein Stability, Proton Transport, X Ray Crystallography, Amino Acid Substitution, Chemistry, Enzyme Active Site, Genetics, Metabolism, Molecular Dynamics, Catalytic Domain, X-Ray, Molecular Dynamics Simulation,
Affiliations: *** IBB - CNR ***
Istituto di Biostrutture e Bioimmagini, CNR, Via Mezzocannone 16, Napoli, 80134, Italy
Dipartimento Neurofarba, Sezione di Scienze Farmaceutiche e Nutraceutiche, Università degli Studi di Firenze, Via U. Schiff 6, Florence, 50019, Italy
References: Alterio, V., Di Fiore, A., D’Ambrosio, K., Supuran, C.T., de Simone, G., Multiple binding modes of inhibitors to carbonic anhydrases: How to design specific drugs targeting 15 different isoforms? (2012) Chem. Rev., 112, pp. 4421-446
Del Prete, S., Vullo, D., Fisher, G.M., Andrews, K.T., Poulsen, S.A., Capasso, C., Supuran, C.T., Discovery of a new family of carbonic anhydrases in the malaria pathogen plasmodium falciparum—The eta-carbonic anhydrases (2014) Bioorg. Med. Chem. Lett., 24, pp. 4389-4396
Kikutani, S., Nakajima, K., Nagasato, C., Tsuji, Y., Miyatake, A., Matsuda, Y., Thylakoid luminal theta-carbonic anhydrase critical for growth and photosynthesis in the marine diatom phaeodactylum tricornutum (2016) Proc. Natl. Acad. Sci. USA, 113, pp. 9828-9833
Xu, Y., Feng, L., Jeffrey, P.D., Shi, Y., Morel, F.M., Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms (2008) Nature, 452, pp. 56-61
Smith, K.S., Jakubzick, C., Whittam, T.S., Ferry, J.G., Carbonic anhydrase is an ancient enzyme widespread in prokaryotes (1999) Proc. Natl. Acad. Sci. USA, 96, pp. 15184-15189
Alterio, V., Monti, S.M., de Simone, G., (2014) Thermal-Stable Carbonic Anhydrases: A Structural Overview, 75, pp. 387-404. , Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications
Frost, S.C., McKenna, R., Eds.
Springer: Dordrecht, The Netherlands
Alterio, V., Langella, E., de Simone, G., Monti, S.M., Cadmium-containing carbonic anhydrase CDCA1 in marine diatom Thalassiosira weissflogii (2015) Mar. Drugs, 13, pp. 1688-1697
de Simone, G., Di Fiore, A., Capasso, C., Supuran, C.T., The zinc coordination pattern in the eta-carbonic anhydrase from plasmodium falciparum is different from all other carbonic anhydrase genetic families (2015) Bioorg. Med. Chem. Lett., 25, pp. 1385-1389
Supuran, C.T., Carbonic anhydrases: Novel therapeutic applications for inhibitors and activators (2008) Nat. Rev. Drug Discov., 7, pp. 168-181
Silverman, D.N., McKenna, R., Solvent-mediated proton transfer in catalysis by carbonic anhydrase (2007) Acc. Chem. Res., 40, pp. 669-675
Aggarwal, M., Boone, C.D., Kondeti, B., McKenna, R., Structural annotation of human carbonic anhydrases (2013) J. Enzym. Inhib. Med. Chem., 28, pp. 267-277
Boone, C.D., Pinard, M., McKenna, R., Silverman, D., Catalytic mechanism of alpha-class carbonic anhydrases: CO2 hydration and proton transfer (2014) Subcell. Biochem., 75, pp. 31-52
Mikulski, R.L., Silverman, D.N., Proton transfer in catalysis and the role of proton shuttles in carbonic anhydrase (2010) Biochim. Biophys. Acta, 1804, pp. 422-426
Aggarwal, M., Kondeti, B., Tu, C., Maupin, C.M., Silverman, D.N., McKenna, R., Structural insight into activity enhancement and inhibition of H64A carbonic anhydrase II by imidazoles (2014) Iucrj, 1, pp. 129-135
Tu, C.K., Silverman, D.N., Forsman, C., Jonsson, B.H., Lindskog, S., Role of histidine 64 in the catalytic mechanism of human carbonic anhydrase II studied with a site-specific mutant (1989) Biochemistry, 28, pp. 7913-7918
Jewell, D.A., Tu, C.K., Paranawithana, S.R., Tanhauser, S.M., Lograsso, P.V., Laipis, P.J., Silverman, D.N., Enhancement of the catalytic properties of human carbonic anhydrase III by site-directed mutagenesis (1991) Biochemistry, 30, pp. 1484-1490
Duda, D., Tu, C., Qian, M., Laipis, P., Agbandje-Mckenna, M., Silverman, D.N., McKenna, R., Structural and kinetic analysis of the chemical rescue of the proton transfer function of carbonic anhydrase II (2001) Biochemistry, 40, pp. 1741-1748
Nair, S.K., Christianson, D.W., Structural properties of human carbonic anhydrase II at pH 9.5 (1991) Biochem. Biophys. Res. Commun., 181, pp. 579-584
Fisher, Z., Hernandez Prada, J.A., Tu, C., Duda, D., Yoshioka, C., An, H., Govindasamy, L., McKenna, R., Structural and kinetic characterization of active-site histidine as a proton shuttle in catalysis by human carbonic anhydrase II (2005) Biochemistry, 44, pp. 1097-1105
Krebs, J.F., Fierke, C.A., Alexander, R.S., Christianson, D.W., Conformational mobility of His-64 in the Thr-200→Ser mutant of human carbonic anhydrase II (1991) Biochemistry, 30, pp. 9153-9160
Taraphder, S., Maupin, C.M., Swanson, J.M., Voth, G.A., Coupling protein dynamics with proton transport in human carbonic anhydrase II (2016) J. Phys. Chem. B, 120, pp. 8389-8404
Maupin, C.M., Voth, G.A., Proton transport in carbonic anhydrase: Insights from molecular simulation (2010) Biochim. Biophys. Acta, 1804, pp. 332-341
Maupin, C.M., McKenna, R., Silverman, D.N., Voth, G.A., Elucidation of the proton transport mechanism in human carbonic anhydrase II (2009) JACS, 131, pp. 7598-7608
Kim, C.U., Song, H., Avvaru, B.S., Gruner, S.M., Park, S., McKenna, R., Tracking solvent and protein movement during CO2 release in carbonic anhydrase II crystals (2016) Proc. Natl. Acad. Sci. USA, 113, pp. 5257-5262
Fisher, S.Z., Tu, C., Bhatt, D., Govindasamy, L., Agbandje-Mckenna, M., McKenna, R., Silverman, D.N., Speeding up proton transfer in a fast enzyme: Kinetic and crystallographic studies on the effect of hydrophobic amino acid substitutions in the active site of human carbonic anhydrase II (2007) Biochemistry, 46, pp. 3803-3813
Domsic, J.F., Williams, W., Fisher, S.Z., Tu, C., Agbandje-Mckenna, M., Silverman, D.N., McKenna, R., Structural and kinetic study of the extended active site for proton transfer in human carbonic anhydrase II (2010) Biochemistry, 49, pp. 6394-6399
Huang, S., Sjoblom, B., Sauer-Eriksson, A.E., Jonsson, B.H., Organization of an efficient carbonic anhydrase: Implications for the mechanism based on structure-function studies of a T199P/C206S mutant (2002) Biochemistry, 41, pp. 7628-7635
Zheng, J., Avvaru, B.S., Tu, C., McKenna, R., Silverman, D.N., Role of hydrophilic residues in proton transfer during catalysis by human carbonic anhydrase II (2008) Biochemistry, 47, pp. 12028-12036
Montgomery, J.C., Venta, P.J., Eddy, R.L., Fukushima, Y.S., Shows, T.B., Tashian, R.E., Characterization of the human gene for a newly discovered carbonic anhydrase, CA VII, and its localization to chromosome 16 (1991) Genomics, 11, pp. 835-848
Earnhardt, J.N., Qian, M., Tu, C., Lakkis, M.M., Bergenhem, N.C., Laipis, P.J., Tashian, R.E., Silverman, D.N., The catalytic properties of murine carbonic anhydrase VII (1998) Biochemistry, 37, pp. 10837-10845
Di Fiore, A., Truppo, E., Supuran, C.T., Alterio, V., Dathan, N., Bootorabi, F., Parkkila, S., de Simone, G., Crystal structure of the C183S/C217S mutant of human CA VII in complex with acetazolamide (2010) Bioorg. Med. Chem. Lett, 20, pp. 5023-5026
Del Giudice, R., Monti, D.M., Truppo, E., Arciello, A., Supuran, C.T., de Simone, G., Monti, S.M., Human carbonic anhydrase VII protects cells from oxidative damage (2013) Biol. Chem., 394, pp. 1343-1348
Monti, D.M., de Simone, G., Langella, E., Supuran, C.T., Di Fiore, A., Monti, S.M., Insights into the role of reactive sulfhydryl groups of carbonic anhydrase III and VII during oxidative damage (2017) J. Enzym. Inhib. Med. Chem., 32, pp. 5-12
Ruusuvuori, E., Li, H., Huttu, K., Palva, J.M., Smirnov, S., Rivera, C., Kaila, K., Voipio, J., Carbonic anhydrase isoform VII acts as a molecular switch in the development of synchronous gamma-frequency firing of hippocampal CA1 pyramidal cells (2004) J. Neurosci., 24, pp. 2699-2707
Rivera, C., Voipio, J., Kaila, K., Two developmental switches in GABAergic signalling: The K+–Cl− cotransporter KCC2 and carbonic anhydrase CA VII (2005) J. Physiol., 562, pp. 27-36
Bootorabi, F., Janis, J., Smith, E., Waheed, A., Kukkurainen, S., Hytonen, V., Valjakka, J., Sly, W.S., Analysis of a shortened form of human carbonic anhydrase VII expressed in vitro compared to the full-length enzyme (2010) Biochimie, 92, pp. 1072-1080
Asiedu, M., Ossipov, M.H., Kaila, K., Price, T.J., Acetazolamide and midazolam act synergistically to inhibit neuropathic pain (2010) Pain, 148, pp. 302-308
Avvaru, B.S., Kim, C.U., Sippel, K.H., Gruner, S.M., Agbandje-Mckenna, M., Silverman, D.N., McKenna, R., A short, strong hydrogen bond in the active site of human carbonic anhydrase II (2010) Biochemistry, 49, pp. 249-251
Fisher, S.Z., Maupin, C.M., Budayova-Spano, M., Govindasamy, L., Tu, C., Agbandje-Mckenna, M., Silverman, D.N., McKenna, R., Atomic crystal and molecular dynamics simulation structures of human carbonic anhydrase II: Insights into the proton transfer mechanism (2007) Biochemistry, 46, pp. 2930-2937
Hakansson, K., Carlsson, M., Svensson, L.A., Liljas, A., Structure of native and apo carbonic anhydrase II and structure of some of its anion-ligand complexes (1992) J. Mol. Biol., 227, pp. 1192-1204
Li, H., Robertson, A.D., Jensen, J.H., Very fast empirical prediction and rationalization of protein pKa values (2005) Proteins, 61, pp. 704-721
Olsson, M.H., Sondergaard, C.R., Rostkowski, M., Jensen, J.H., PROPKA3: Consistent treatment of internal and surface residues in empirical pKa predictions (2011) J. Chem. Theory Comput., 7, pp. 525-537
Olsson, M.H., Protein electrostatics and pKa blind predictions
contribution from empirical predictions of internal ionizable residues (2011) Proteins, 79, pp. 3333-3345
Mikulski, R., Domsic, J.F., Ling, G., Tu, C., Robbins, A.H., Silverman, D.N., McKenna, R., Structure and catalysis by carbonic anhydrase II: Role of active-site tryptophan 5 (2011) Arch. Biochem. Biophys., 516, pp. 97-102
Mikulski, R., West, D., Sippel, K.H., Avvaru, B.S., Aggarwal, M., Tu, C., McKenna, R., Silverman, D.N., Water networks in fast proton transfer during catalysis by human carbonic anhydrase II (2013) Biochemistry, 52, pp. 125-131
Riccardi, D., Konig, P., Guo, H., Cui, Q., Proton transfer in carbonic anhydrase is controlled by electrostatics rather than the orientation of the acceptor (2008) Biochemistry, 47, pp. 2369-2378
Cudney, R., Patel, S., Weisgraber, K., Newhouse, Y., McPherson, A., Screening and optimization strategies for macromolecular crystal growth (1994) Acta Crystallogr. D Biol. Crystallogr., 50, pp. 414-423
Jancarik, J., Kim, S.-H., Sparse matrix sampling: A screening method for crystallization of proteins (1991) J. Appl. Crystallogr., 24, pp. 409-411
Otwinowski, Z., Minor, W., Processing of X-ray diffraction data collected in oscillation mode (1997) Methods Enzymol, 276, pp. 307-326
Navaza, J., Amore: An automated package for molecular replacement (1994) Acta Crystallogr. Sect. a Found. Crystallogr., 50, pp. 157-163
Brunger, A.T., Adams, P.D., Clore, G.M., Delano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Pannu, N.S., Crystallography & NMR system: A new software suite for macromolecular structure determination (1998) Acta Crystallogr. D Biol. Crystallogr., 54, pp. 905-921
Brunger, A.T., Version 1.2 of the crystallography and NMR system (2007) Nat. Protoc., 2, pp. 2728-2733
Jones, T.A., Zou, J.Y., Cowan, S.W., Kjeldgaard, M., Improved methods for building protein models in electron density maps and the location of errors in these models (1991) Acta Crystallogr. Sect. a Found. Crystallogr., 47 (2), pp. 110-119
Hooft, R.W., Vriend, G., Sander, C., Abola, E.E., Errors in protein structures (1996) Nature, 381, p. 272
Laskowski, R.A., Macarthur, M.W., Moss, D.S., Thornton, J.M., Procheck: A program to check the stereochemical quality of protein structures (1993) J. Appl. Crystallogr., 26, pp. 283-291
The Crystal Structure of a hCA VII Variant Provides Insights into the Molecular Determinants Responsible for Its Catalytic Behavior