Insights into the binding mode of sulphamates and sulphamides to hCA II: crystallographic studies and binding free energy calculations

References

• Alterio V, Di Fiore A, D’Ambrosio K, et al. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem Rev 2012;112:4421–68.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, Fisher GM, et al. Discovery of a new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum: the eta-carbonic anhydrases. Bioorg Med Chem Lett 2014;24:4389–96.
   PubMed Web of Science ®Google Scholar
• De Simone G, Di Fiore A, Capasso C, Supuran CT. The zinc coordination pattern in the eta-carbonic anhydrase from Plasmodium falciparum is different from all other carbonic anhydrase genetic families. Bioorg Med Chem Lett 2015;25:1385–9.
   PubMed Web of Science ®Google Scholar
• Kikutani S, Nakajima K, Nagasato C, et al. Thylakoid luminal theta-carbonic anhydrase critical for growth and photosynthesis in the marine diatom Phaeodactylum tricornutum. Proc Natl Acad Sci USA 2016;113:9828–33.
   PubMed Web of Science ®Google Scholar
• Xu Y, Feng L, Jeffrey PD, et al. Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 2008;452:56–61.
   PubMed Web of Science ®Google Scholar
• Smith KS, Jakubzick C, Whittam TS, Ferry JG. Carbonic anhydrase is an ancient enzyme widespread in prokaryotes. Proc Natl Acad Sci USA 1999;96:15184–9.
   PubMed Web of Science ®Google Scholar
• Alterio V, Monti SM, Simone G. Thermal-stable carbonic anhydrases: a structural overview. In: Frost SC, McKenna R, eds. Carbonic anhydrase: mechanism, regulation, links to disease, and industrial applications. Amsterdam, The Netherlands: Springer; 2014:387–404.
   Google Scholar
• Alterio V, Langella E, De Simone G, Monti SM. Cadmium-containing carbonic anhydrase CDCA1 in marine diatom Thalassiosira weissflogii. Mar Drugs 2015;13:1688–97.
   PubMed Web of Science ®Google Scholar
• Parkkila S. An overview of the distribution and function of carbonic anhydrase in mammals. EXS 2000;90:79–93.
   Google Scholar
• Supuran CT. Carbonic anhydrases – an overview. Curr Pharm Des 2008;14:603–14.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81.
   PubMed Web of Science ®Google Scholar
• Supuran CT, De Simone G, eds. Carbonic anhydrases as biocatalysts: from theory to medical and industrial applications. Amsterdam, The Netherlands: Elsevier; 2015.
   Google Scholar
• Supuran CT, Scozzafava A, Conway J, eds. Carbonic anhydrase: its inhibitors and activators. Boca Raton, FL: CRC Press; 2004.
   Google Scholar
• Winum JY, Scozzafava A, Montero JL, Supuran CT. Sulfamates and their therapeutic potential. Med Res Rev 2005;25:186–228.
   PubMed Web of Science ®Google Scholar
• Winum JY, Scozzafava A, Montero JL, Supuran CT. Therapeutic potential of sulfamides as enzyme inhibitors. Med Res Rev 2006;26:767–92.
   PubMed Web of Science ®Google Scholar
• De Monte C, Carradori S, Secci D, et al. Cyclic tertiary sulfamates: selective inhibition of the tumor-associated carbonic anhydrases IX and XII by N- and O-substituted acesulfame derivatives. Eur J Med Chem 2014;84:240–6.
   PubMed Web of Science ®Google Scholar
• Carradori S, Secci D, De Monte C, et al. A novel library of saccharin and acesulfame derivatives as potent and selective inhibitors of carbonic anhydrase IX and XII isoforms. Bioorg Med Chem 2016;24:1095–105.
   PubMed Web of Science ®Google Scholar
• Winum JY, Colinas PA, Supuran CT. Glycosidic carbonic anhydrase IX inhibitors: a sweet approach against cancer. Bioorg Med Chem 2013;21:1419–26.
   PubMed Web of Science ®Google Scholar
• Krishnamurthy VM, Kaufman GK, Urbach AR, et al. Carbonic anhydrase as a model for biophysical and physical-organic studies of proteins and protein-ligand binding. Chem Rev 2008;108:946–1051.
   PubMed Web of Science ®Google Scholar
• De Simone G, Supuran CT. Antiobesity carbonic anhydrase inhibitors. Curr Top Med Chem 2007;7:879–84.
   PubMed Web of Science ®Google Scholar
• van Passel L, Arif H, Hirsch LJ. Topiramate for the treatment of epilepsy and other nervous system disorders. Expert Rev Neurother 2006;6:19–31.
   PubMedGoogle Scholar
• Maryanoff BE, McComsey DF, Costanzo MJ, et al. Comparison of sulfamate and sulfamide groups for the inhibition of carbonic anhydrase-II by using topiramate as a structural platform. J Med Chem 2005;48:1941–7.
   PubMed Web of Science ®Google Scholar
• Gavernet L, Gonzalez Funes JL, Palestro PH, et al. Inhibition pattern of sulfamide-related compounds in binding to carbonic anhydrase isoforms I, II, VII, XII and XIV. Bioorg Med Chem 2013;21:1410–8.
   PubMed Web of Science ®Google Scholar
• Parker MH, Smith-Swintosky VL, McComsey DF, et al. Novel, broad-spectrum anticonvulsants containing a sulfamide group: advancement of N-((benzo[b]thien-3-yl)methyl)sulfamide (JNJ-26990990) into human clinical studies. J Med Chem 2009;52:7528–36.
   PubMed Web of Science ®Google Scholar
• Di Fiore A, De Simone G, Alterio V, et al. The anticonvulsant sulfamide JNJ-26990990 and its S,S-dioxide analog strongly inhibit carbonic anhydrases: solution and X-ray crystallographic studies. Org Biomol Chem 2016;14:4853–8.
   PubMed Web of Science ®Google Scholar
• Rami M, Dubois L, Parvathaneni NK, et al. Hypoxia-targeting carbonic anhydrase IX inhibitors by a new series of nitroimidazole-sulfonamides/sulfamides/sulfamates. J Med Chem 2013;56:8512–20.
   PubMed Web of Science ®Google Scholar
• Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 1997;276:307–26.
   PubMed Web of Science ®Google Scholar
• Eriksson AE, Jones TA, Liljas A. Refined structure of human carbonic anhydrase II at 2.0 A resolution. Proteins 1988;4:274–82.
   PubMed Web of Science ®Google Scholar
• Brünger AT, Adams PD, Clore GM, et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 1998;54:905–21.
   PubMed Web of Science ®Google Scholar
• Brünger AT. Version 1.2 of the crystallography and NMR system. Nat Protoc 2007;2:2728–33.
   PubMed Web of Science ®Google Scholar
• Jones TA, Zou JY, Cowan SW, Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst A 1991;47:110–19.
   PubMed Web of Science ®Google Scholar
• Allen FH. The Cambridge Structural Database: a quarter of a million crystal structures and rising. Acta Crystallogr B 2002;58:380–8.
   PubMed Web of Science ®Google Scholar
• Frisch MJ, Trucks GW, Schlegel HB, et al. Gaussian 09, Revision A.1. 2009.
   Google Scholar
• Vanquelef E, Simon S, Marquant G, et al. R.E.D. Server: a web service for deriving RESP and ESP charges and building force field libraries for new molecules and molecular fragments. Nucleic Acids Res 2011;39:W511–17.
   PubMed Web of Science ®Google Scholar
• Wang F, Becker J-P, Cieplak P, Dupradeau F-Y. R.E.D. Python: Object oriented programming for Amber force fields, Université de Picardie-Jules Verne, Sanford Burnham Prebys Medical Discovery Institute, 2013.
   Google Scholar
• King RW, Burgen AS. Sulphonamide complexes of human carbonic anhydrases. Ultraviolet difference spectroscopy. Biochim Biophys Acta 1970;207:278–85.
   PubMed Web of Science ®Google Scholar
• Taylor PW, King RW, Burgen AS. Influence of pH on the kinetics of complex formation between aromatic sulfonamides and human carbonic anhydrase. Biochemistry 1970;9:3894–902.
   PubMed Web of Science ®Google Scholar
• Wang J, Wolf RM, Caldwell JW, et al. Development and testing of a general amber force field. J Comput Chem 2004;25:1157–74.
   PubMed Web of Science ®Google Scholar
• Maier JA, Martinez C, Kasavajhala K, et al. ff14SB: improving the accuracy of protein side chain and backbone parameters from ff99SB. J Chem Theory Comput 2015;11:3696–713.
   PubMed Web of Science ®Google Scholar
• Li P, Merz KM Jr. Taking into account the ion-induced dipole interaction in the nonbonded model of ions. J Chem Theory Comput 2014;10:289–97.
   PubMed Web of Science ®Google Scholar
• Tsui V, Case DA. Theory and applications of the generalized Born solvation model in macromolecular simulations. Biopolymers 2000;56:275–91.
   PubMed Web of Science ®Google Scholar
• Kollman PA, Massova I, Reyes C, et al. Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc Chem Res 2000;33:889–97.
   PubMed Web of Science ®Google Scholar
• Case DA, Cerutti DS, Cheatham I, et al. AMBER 14. San Francisco: University of California; 2014.
   Google Scholar
• Wang J, Morin P, Wang W, Kollman PA. Use of MM-PBSA in reproducing the binding free energies to HIV-1 RT of TIBO derivatives and predicting the binding mode to HIV-1 RT of efavirenz by docking and MM-PBSA. J Am Chem Soc 2001;123:5221–30.
   PubMed Web of Science ®Google Scholar
• Langella E, D’Ambrosio K, D’Ascenzio M, et al. A combined crystallographic and theoretical study explains the capability of carboxylic acids to adopt multiple binding modes in the active site of carbonic anhydrases. Chemistry 2016;22:97–100.
   PubMed Web of Science ®Google Scholar
• Homeyer N, Gohlke H. Free energy calculations by the molecular mechanics Poisson–Boltzmann surface area method. Mol Inform 2012;31:114–22.
   PubMed Web of Science ®Google Scholar
• Onufriev A, Bashford D, Case DA. Exploring protein native states and large-scale conformational changes with a modified generalized born model. Proteins 2004;55:383–94.
   PubMed Web of Science ®Google Scholar
• Weiser J, Shenkin PS, Still WC. Approximate atomic surfaces from linear combinations of pairwise overlaps (LCPO). J Comp Chem 1999;20:217–30.
   Web of Science ®Google Scholar
• Recacha R, Costanzo MJ, Maryanoff BE, Chattopadhyay D. Crystal structure of human carbonic anhydrase II complexed with an anti-convulsant sugar sulphamate. Biochem J 2002;361:437–41.
   PubMed Web of Science ®Google Scholar
• Lopez M, Paul B, Hofmann A, et al. S-glycosyl primary sulfonamides – a new structural class for selective inhibition of cancer-associated carbonic anhydrases. J Med Chem 2009;52:6421–32.
   PubMed Web of Science ®Google Scholar
• Lopez M, Vu H, Wang CK, et al. Promiscuity of carbonic anhydrase II. Unexpected ester hydrolysis of carbohydrate-based sulfamate inhibitors. J Am Chem Soc 2011;133:18452–62.
   PubMed Web of Science ®Google Scholar
• Mahon BP, Lomelino CL, Ladwig J, et al. Mapping selective inhibition of the cancer-related carbonic anhydrase IX using structure–activity relationships of glucosyl-based sulfamates. J Med Chem 2015;58:6630–8.
   PubMed Web of Science ®Google Scholar
• Vitale RM, Alterio V, Innocenti A, et al. Carbonic anhydrase inhibitors. Comparison of aliphatic sulfamate/bis-sulfamate adducts with isozymes II and IX as a platform for designing tight-binding, more isoform-selective inhibitors. J Med Chem 2009;52:5990–8.
   PubMed Web of Science ®Google Scholar
• Lloyd MD, Pederick RL, Natesh R, et al. Crystal structure of human carbonic anhydrase II at 1.95 A resolution in complex with 667-coumate, a novel anti-cancer agent. Biochem J 2005;385:715–20.
   PubMed Web of Science ®Google Scholar
• Lloyd MD, Thiyagarajan N, Ho YT, et al. First crystal structures of human carbonic anhydrase II in complex with dual aromatase-steroid sulfatase inhibitors. Biochemistry 2005;44:6858–66.
   PubMed Web of Science ®Google Scholar
• Leese MP, Leblond B, Smith A, et al. 2-substituted estradiol bis-sulfamates, multitargeted antitumor agents: synthesis, in vitro SAR, protein crystallography, and in vivo activity. J Med Chem 2006;49:7683–96.
   PubMed Web of Science ®Google Scholar
• Woo LW, Jackson T, Putey A, et al. Highly potent first examples of dual aromatase-steroid sulfatase inhibitors based on a biphenyl template. J Med Chem 2010;53:2155–70.
   PubMed Web of Science ®Google Scholar
• Cozier GE, Leese MP, Lloyd MD, et al. Structures of human carbonic anhydrase II/inhibitor complexes reveal a second binding site for steroidal and nonsteroidal inhibitors. Biochemistry 2010;49:3464–76.
   PubMed Web of Science ®Google Scholar
• Woo LW, Fischer DS, Sharland CM, et al. Anticancer steroid sulfatase inhibitors: synthesis of a potent fluorinated second-generation agent, in vitro and in vivo activities, molecular modeling, and protein crystallography. Mol Cancer Ther 2008;7:2435–44.
   PubMed Web of Science ®Google Scholar
• Temperini C, Innocenti A, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. Interaction of the antitumor sulfamate EMD 486019 with twelve mammalian carbonic anhydrase isoforms: kinetic and X-ray crystallographic studies. Bioorg Med Chem Lett 2008;18:4282–6.
   PubMed Web of Science ®Google Scholar
• Sippel K, Stander A, Tu C, et al. Characterization of carbonic anhydrase isozyme specific inhibition by sulfamated 2-ethylestra compounds. Lett Drug Design Discov 2008;8:678–84.
   Google Scholar
• Moeker J, Mahon BP, Bornaghi LF, et al. Structural insights into carbonic anhydrase IX isoform specificity of carbohydrate-based sulfamates. J Med Chem 2014;57:8635–45.
   PubMed Web of Science ®Google Scholar
• Mahon BP, Lomelino CL, Salguero AL, et al. Observed surface lysine acetylation of human carbonic anhydrase II expressed in Escherichia coli. Protein Sci 2015;24:1800–7.
   PubMed Web of Science ®Google Scholar
• Leese MP, Jourdan F, Kimberley MR, et al. Chimeric microtubule disruptors. Chem Commun (Camb) 2010;46:2907–9.
   PubMed Web of Science ®Google Scholar
• Leese MP, Jourdan FL, Gaukroger K, et al. Structure-activity relationships of C-17 cyano-substituted estratrienes as anticancer agents. J Med Chem 2008;51:1295–308.
   PubMed Web of Science ®Google Scholar
• De Simone G, Alterio V, Supuran CT. Exploiting the hydrophobic and hydrophilic binding sites for designing carbonic anhydrase inhibitors. Expert Opin Drug Discov 2013;8:793–810.
   PubMed Web of Science ®Google Scholar
• De Simone G, Pizika G, Monti SM, et al. Hydrophobic substituents of the phenylmethylsulfamide moiety can be used for the development of new selective carbonic anhydrase inhibitors. Biomed Res Int 2014;2014:523210.
   PubMed Web of Science ®Google Scholar
• Brynda J, Mader P, Šicha V, et al. Carborane-based carbonic anhydrase inhibitors. Angew Chem Int Ed Engl 2013;52:13760–3.
   PubMed Web of Science ®Google Scholar
• Winum JY, Temperini C, El Cheikh K, et al. Carbonic anhydrase inhibitors: clash with Ala65 as a means for designing inhibitors with low affinity for the ubiquitous isozyme II, exemplified by the crystal structure of the topiramate sulfamide analogue. J Med Chem 2006;49:7024–31.
   PubMed Web of Science ®Google Scholar
• Di Fiore A, Monti SM, Innocenti A, et al. Carbonic anhydrase inhibitors: crystallographic and solution binding studies for the interaction of a boron-containing aromatic sulfamide with mammalian isoforms I-XV. Bioorg Med Chem Lett 2010;20:3601–5.
   PubMed Web of Science ®Google Scholar
• Mader P, Pecina A, Cigler P, et al. Carborane-based carbonic anhydrase inhibitors: insight into CAII/CAIX specificity from a high-resolution crystal structure, modeling, and quantum chemical calculations. Biomed Res Int 2014;2014:389869.
   PubMed Web of Science ®Google Scholar
• Michalczyk R, Unkefer CJ, Bacik JP, et al. Joint neutron crystallographic and NMR solution studies of Tyr residue ionization and hydrogen bonding: implications for enzyme-mediated proton transfer. Proc Natl Acad Sci USA 2015;112:5673–8.
   PubMed Web of Science ®Google Scholar