Structure-based drug discovery of carbonic anhydrase inhibitors

References

• Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–181.
   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;96:15184–15189.
   PubMed Web of Science ®Google Scholar
• Xu Y, Feng L, Jeffrey PD, Shi Y, Morel FM. Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 2008;452:56–61.
   PubMed Web of Science ®Google Scholar
• Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–777.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibitors. Bioorg Med Chem Lett 2010;20:3467–3474.
   PubMed Web of Science ®Google Scholar
• Pastorekova S, Parkkila S, Pastorek J, Supuran CT. Carbonic anhydrases: current state of the art, therapeutic applications and future prospects. J Enzyme Inhib Med Chem 2004;19:199–229.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibitors and activators for novel therapeutic applications. Future Med Chem 2011;3:1165–1180.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Bacterial carbonic anhydrases as drug targets: toward novel antibiotics? Front Pharmacol 2011;2:34.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Scozzafava A, Casini A. Carbonic anhydrase inhibitors. Med Res Rev 2003;23:146–189.
   PubMed Web of Science ®Google Scholar
• Domsic JF, Avvaru BS, Kim CU, Gruner SM, Agbandje-McKenna M, Silverman DN et al. Entrapment of carbon dioxide in the active site of carbonic anhydrase II. J Biol Chem 2008;283:30766–30771.
   PubMed Web of Science ®Google Scholar
• De Simone G, Supuran CT. (In)organic anions as carbonic anhydrase inhibitors. J Inorg Biochem 2012.
   PubMedGoogle Scholar
• Suarez Covarrubias A, Larsson AM, Högbom M, Lindberg J, Bergfors T, Björkelid C et al. Structure and function of carbonic anhydrases from Mycobacterium tuberculosis. J Biol Chem 2005;280:18782–18789.
   PubMed Web of Science ®Google Scholar
• Covarrubias AS, Bergfors T, Jones TA, Högbom M. Structural mechanics of the pH-dependent activity of beta-carbonic anhydrase from Mycobacterium tuberculosis. J Biol Chem 2006;281:4993–4999.
   PubMed Web of Science ®Google Scholar
• Temperini C, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. X-ray crystal studies of the carbonic anhydrase II-trithiocarbonate adduct–an inhibitor mimicking the sulfonamide and urea binding to the enzyme. Bioorg Med Chem Lett 2010;20:474–478.
   PubMed Web of Science ®Google Scholar
• Briganti F, Mangani S, Orioli P, Scozzafava A, Vernaglione G, Supuran CT. Carbonic anhydrase activators: X-ray crystallographic and spectroscopic investigations for the interaction of isozymes I and II with histamine. Biochemistry 1997;36:10384–10392.
   PubMed Web of Science ®Google Scholar
• Temperini C, Scozzafava A, Vullo D, Supuran CT. Carbonic anhydrase activators. Activation of isozymes I, II, IV, VA, VII, and XIV with l- and d-histidine and crystallographic analysis of their adducts with isoform II: engineering proton-transfer processes within the active site of an enzyme. Chemistry 2006;12:7057–7066.
   PubMed Web of Science ®Google Scholar
• Maupin CM, Castillo N, Taraphder S, Tu C, McKenna R, Silverman DN et al. Chemical rescue of enzymes: proton transfer in mutants of human carbonic anhydrase II. J Am Chem Soc 2011;133:6223–6234.
   PubMed Web of Science ®Google Scholar
• Carta F, Temperini C, Innocenti A, Scozzafava A, Kaila K, Supuran CT. Polyamines inhibit carbonic anhydrases by anchoring to the zinc-coordinated water molecule. J Med Chem 2010;53:5511–5522.
   PubMed Web of Science ®Google Scholar
• Maresca A, Temperini C, Vu H, Pham NB, Poulsen SA, Scozzafava A et al. Non-zinc mediated inhibition of carbonic anhydrases: coumarins are a new class of suicide inhibitors. J Am Chem Soc 2009;131:3057–3062.
   PubMed Web of Science ®Google Scholar
• Maresca A, Temperini C, Pochet L, Masereel B, Scozzafava A, Supuran CT. Deciphering the mechanism of carbonic anhydrase inhibition with coumarins and thiocoumarins. J Med Chem 2010;53:335–344.
   PubMed Web of Science ®Google Scholar
• Touisni N, Maresca A, McDonald PC, Lou Y, Scozzafava A, Dedhar S et al. Glycosyl Coumarin Carbonic Anhydrase IX and XII Inhibitors Strongly Attenuate the Growth of Primary Breast Tumors. J Med Chem 2011;54:8271–8277.
   PubMed Web of Science ®Google Scholar
• Woo LW, Ganeshapillai D, Thomas MP, Sutcliffe OB, Malini B, Mahon MF et al. Structure-activity relationship for the first-in-class clinical steroid sulfatase inhibitor Irosustat (STX64, BN83495). ChemMedChem 2011;6:2019–2034.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Scozzafava A. Carbonic anhydrases as targets for medicinal chemistry. Bioorg Med Chem 2007;15:4336–4350.
   PubMed Web of Science ®Google Scholar
• Baranauskiene L, Hilvo M, Matuliene J, Golovenko D, Manakova E, Dudutiene V et al. Inhibition and binding studies of carbonic anhydrase isozymes I, II and IX with benzimidazo[1,2-c][1,2,3]thiadiazole-7-sulphonamides. J Enzyme Inhib Med Chem 2010;25:863–870.
   PubMed Web of Science ®Google Scholar
• Zimmerman S, Innocenti A, Casini A, Ferry JG, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. Inhibition of the prokariotic beta and gamma-class enzymes from Archaea with sulfonamides. Bioorg Med Chem Lett 2004;14:6001–6006.
   PubMed Web of Science ®Google Scholar
• Schlicker C, Hall RA, Vullo D, Middelhaufe S, Gertz M, Supuran CT et al. Structure and inhibition of the CO2-sensing carbonic anhydrase Can2 from the pathogenic fungus Cryptococcus neoformans. J Mol Biol 2009;385:1207–1220.
   PubMed Web of Science ®Google Scholar
• Pacchiano F, Carta F, Vullo D, Scozzafava A, Supuran CT. Inhibition of ß-carbonic anhydrases with ureido-substituted benzenesulfonamides. Bioorg Med Chem Lett 2011;21:102–105.
   PubMed Web of Science ®Google Scholar
• Alterio V, Hilvo M, Di Fiore A, Supuran CT, Pan P, Parkkila S et al. Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX. Proc Natl Acad Sci USA 2009;106:16233–16238.
   PubMed Web of Science ®Google Scholar
• Weber A, Casini A, Heine A, Kuhn D, Supuran CT, Scozzafava A et al. Unexpected nanomolar inhibition of carbonic anhydrase by COX-2-selective celecoxib: new pharmacological opportunities due to related binding site recognition. J Med Chem 2004;47:550–557.
   PubMed Web of Science ®Google Scholar
• Di Fiore A, Pedone C, D’Ambrosio K, Scozzafava A, De Simone G, Supuran CT. Carbonic anhydrase inhibitors: Valdecoxib binds to a different active site region of the human isoform II as compared to the structurally related cyclooxygenase II “selective” inhibitor celecoxib. Bioorg Med Chem Lett 2006;16:437–442.
   PubMed Web of Science ®Google Scholar
• Köhler K, Hillebrecht A, Schulze Wischeler J, Innocenti A, Heine A, Supuran CT et al. Saccharin inhibits carbonic anhydrases: possible explanation for its unpleasant metallic aftertaste. Angew Chem Int Ed Engl 2007;46:7697–7699.
   PubMed Web of Science ®Google Scholar
• Hilvo M, Innocenti A, Monti SM, De Simone G, Supuran CT, Parkkila S. Recent advances in research on the most novel carbonic anhydrases, CA XIII and XV. Curr Pharm Des 2008;14:672–678.
   PubMed Web of Science ®Google Scholar
• Di Fiore A, Monti SM, Hilvo M, Parkkila S, Romano V, Scaloni A et al. Crystal structure of human carbonic anhydrase XIII and its complex with the inhibitor acetazolamide. Proteins 2009;74:164–175.
   PubMed Web of Science ®Google Scholar
• Di Fiore A, Truppo E, Supuran CT, Alterio V, Dathan N, Bootorabi F et al. Crystal structure of the C183S/C217S mutant of human CA VII in complex with acetazolamide. Bioorg Med Chem Lett 2010;20:5023–5026.
   PubMed Web of Science ®Google Scholar
• Whittington DA, Waheed A, Ulmasov B, Shah GN, Grubb JH, Sly WS et al. Crystal structure of the dimeric extracellular domain of human carbonic anhydrase XII, a bitopic membrane protein overexpressed in certain cancer tumor cells. Proc Natl Acad Sci USA 2001;98:9545–9550.
   PubMed Web of Science ®Google Scholar
• Whittington DA, Grubb JH, Waheed A, Shah GN, Sly WS, Christianson DW. Expression, assay, and structure of the extracellular domain of murine carbonic anhydrase XIV: implications for selective inhibition of membrane-associated isozymes. J Biol Chem 2004;279:7223–7228.
   PubMed Web of Science ®Google Scholar
• Casini A, Scozzafava A, Mincione F, Menabuoni L, Ilies MA, Supuran CT. Carbonic anhydrase inhibitors: water-soluble 4-sulfamoylphenylthioureas as topical intraocular pressure-lowering agents with long-lasting effects. J Med Chem 2000;43:4884–4892.
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Menabuoni L, Mincione F, Supuran CT. Carbonic anhydrase inhibitors. A general approach for the preparation of water-soluble sulfonamides incorporating polyamino-polycarboxylate tails and of their metal complexes possessing long-lasting, topical intraocular pressure-lowering properties. J Med Chem 2002;45:1466–1476.
   PubMed Web of Science ®Google Scholar
• Fabrizi F, Mincione F, Somma T, Scozzafava G, Galassi F, Masini E et al. A new approach to antiglaucoma drugs: carbonic anhydrase inhibitors with or without NO donating moieties. Mechanism of action and preliminary pharmacology. J Enzyme Inhib Med Chem 2012;27:138–147.
   PubMed Web of Science ®Google Scholar
• Ebbesen P, Pettersen EO, Gorr TA, Jobst G, Williams K, Kieninger J et al. Taking advantage of tumor cell adaptations to hypoxia for developing new tumor markers and treatment strategies. J Enzyme Inhib Med Chem 2009;24 Suppl 1:1–39.
   PubMed Web of Science ®Google Scholar
• Svastová E, Hulíková A, Rafajová M, Zat’ovicová M, Gibadulinová A, Casini A et al. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett 2004;577:439–445.
   PubMed Web of Science ®Google Scholar
• Dubois L, Lieuwes NG, Maresca A, Thiry A, Supuran CT, Scozzafava A et al. Imaging of CA IX with fluorescent labelled sulfonamides distinguishes hypoxic and (re)-oxygenated cells in a xenograft tumour model. Radiother Oncol 2009;92:423–428.
   PubMed Web of Science ®Google Scholar
• Ahlskog JK, Dumelin CE, Trüssel S, Mårlind J, Neri D. In vivo targeting of tumor-associated carbonic anhydrases using acetazolamide derivatives. Bioorg Med Chem Lett 2009;19:4851–4856.
   PubMed Web of Science ®Google Scholar
• Lou Y, McDonald PC, Oloumi A, Chia S, Ostlund C, Ahmadi A et al. Targeting Tumor Hypoxia: Suppression of Breast Tumor Growth and Metastasis by Novel Carbonic Anhydrase IX Inhibitors. Cancer Res 2011;71:3364–3376.
   PubMed Web of Science ®Google Scholar
• Pacchiano F, Carta F, McDonald PC, Lou Y, Vullo D, Scozzafava A et al. Ureido-substituted benzenesulfonamides potently inhibit carbonic anhydrase IX and show antimetastatic activity in a model of breast cancer metastasis. J Med Chem 2011;54:1896–1902.
   PubMed Web of Science ®Google Scholar
• Mincione F, Scozzafava A, Supuran CT. The development of topically acting carbonic anhydrase inhibitors as anti-glaucoma agents. Curr Top Med Chem 2007;7:849–854.
   PubMed Web of Science ®Google Scholar
• Carta F, Supuran CT, Scozzafava A. Novel therapies for glaucoma: a patent review 2007 - 2011. Expert Opin Ther Pat 2012;22:79–88.
   PubMed Web of Science ®Google Scholar
• Steele RM, Benedini F, Biondi S, Borghi V, Carzaniga L, Impagnatiello F et al. Nitric oxide-donating carbonic anhydrase inhibitors for the treatment of open-angle glaucoma. Bioorg Med Chem Lett 2009;19:6565–6570.
   PubMed Web of Science ®Google Scholar
• Mincione F, Benedini F, Biondi S, Cecchi A, Temperini C, Formicola G et al. Synthesis and crystallographic analysis of new sulfonamides incorporating NO-donating moieties with potent antiglaucoma action. Bioorg Med Chem Lett 2011;21:3216–3221.
   PubMed Web of Science ®Google Scholar
• Alterio V, Di Fiore A, D’Ambrosio K, Supuran CT, De Simone G. X-Ray crystallography of CA inhibitors and its importance in drug design. In Drug Design of Zinc-Enzyme Inhibitors: Functional, Structural, and Disease Applications, Supuran CT, Winum JY., Eds., Wiley, Hoboken, 2009, pp. 73–138.
   Google Scholar
• Alterio V, Vitale RM, Monti SM, Pedone C, Scozzafava A, Cecchi A et al. Carbonic anhydrase inhibitors: X-ray and molecular modeling study for the interaction of a fluorescent antitumor sulfonamide with isozyme II and IX. J Am Chem Soc 2006;128:8329–8335.
   PubMed Web of Science ®Google Scholar
• Alterio V, De Simone G, Monti SM, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors: inhibition of human, bacterial, and archaeal isozymes with benzene-1,3-disulfonamides–solution and crystallographic studies. Bioorg Med Chem Lett 2007;17:4201–4207.
   PubMed Web of Science ®Google Scholar
• Wagner J, Avvaru BS, Robbins AH, Scozzafava A, Supuran CT, McKenna R. Coumarinyl-substituted sulfonamides strongly inhibit several human carbonic anhydrase isoforms: solution and crystallographic investigations. Bioorg Med Chem 2010;18:4873–4878.
   PubMed Web of Science ®Google Scholar
• Biswas S, Aggarwal M, Güzel Ö, Scozzafava A, McKenna R, Supuran CT. Conformational variability of different sulfonamide inhibitors with thienyl-acetamido moieties attributes to differential binding in the active site of cytosolic human carbonic anhydrase isoforms. Bioorg Med Chem 2011;19:3732–3738.
   PubMed Web of Science ®Google Scholar
• Pacchiano F, Aggarwal M, Avvaru BS, Robbins AH, Scozzafava A, McKenna R et al. Selective hydrophobic pocket binding observed within the carbonic anhydrase II active site accommodate different 4-substituted-ureido-benzenesulfonamides and correlate to inhibitor potency. Chem Commun (Camb) 2010;46:8371–8373.
   PubMed Web of Science ®Google Scholar
• Carta F, Garaj V, Maresca A, Wagner J, Avvaru BS, Robbins AH et al. Sulfonamides incorporating 1,3,5-triazine moieties selectively and potently inhibit carbonic anhydrase transmembrane isoforms IX, XII and XIV over cytosolic isoforms I and II: Solution and X-ray crystallographic studies. Bioorg Med Chem 2011;19:3105–3119.
   PubMed Web of Science ®Google Scholar
• Hen N, Bialer M, Yagen B, Maresca A, Aggarwal M, Robbins AH et al. Anticonvulsant 4-aminobenzenesulfonamide derivatives with branched-alkylamide moieties: X-ray crystallography and inhibition studies of human carbonic anhydrase isoforms I, II, VII, and XIV. J Med Chem 2011;54:3977–3981.
   PubMed Web of Science ®Google Scholar
• Kolayli S, Karahalil F, Sahin H, Dincer B, Supuran CT. Characterization and inhibition studies of an ?-carbonic anhydrase from the endangered sturgeon species Acipenser gueldenstaedti. J Enzyme Inhib Med Chem 2011;26:895–900.
   PubMed Web of Science ®Google Scholar
• Carta F, Aggarwal M, Maresca A, Scozzafava A, McKenna R, Supuran CT. Dithiocarbamates: a new class of carbonic anhydrase inhibitors. Crystallographic and kinetic investigations. Chem Commun (Camb) 2012;48:1868–1870.
   PubMed Web of Science ®Google Scholar
• Güzel O, Innocenti A, Scozzafava A, Salman A, Supuran CT. Carbonic anhydrase inhibitors. Phenacetyl-, pyridylacetyl- and thienylacetyl-substituted aromatic sulfonamides act as potent and selective isoform VII inhibitors. Bioorg Med Chem Lett 2009;19:3170–3173.
   PubMed Web of Science ®Google Scholar
• Güzel O, Innocenti A, Scozzafava A, Salman A, Supuran CT. Carbonic anhydrase inhibitors. Aromatic/heterocyclic sulfonamides incorporating phenacetyl, pyridylacetyl and thienylacetyl tails act as potent inhibitors of human mitochondrial isoforms VA and VB. Bioorg Med Chem 2009;17:4894–4899.
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. Arylsulfonylureido- and arylureido-substituted aromatic and heterocyclic sulfonamides: towards selective inhibitors of carbonic anhydrase isozyme I. J Enzym Inhib 1999;14:343–363.
   PubMed Web of Science ®Google Scholar
• Garaj V, Puccetti L, Fasolis G, Winum JY, Montero JL, Scozzafava A et al. Carbonic anhydrase inhibitors: synthesis and inhibition of cytosolic/tumor-associated carbonic anhydrase isozymes I, II, and IX with sulfonamides incorporating 1,2,4-triazine moieties. Bioorg Med Chem Lett 2004;14:5427–5433.
   PubMed Web of Science ®Google Scholar
• Garaj V, Puccetti L, Fasolis G, Winum JY, Montero JL, Scozzafava A et al. Carbonic anhydrase inhibitors: novel sulfonamides incorporating 1,3,5-triazine moieties as inhibitors of the cytosolic and tumour-associated carbonic anhydrase isozymes I, II and IX. Bioorg Med Chem Lett 2005;15:3102–3108.
   PubMed Web of Science ®Google Scholar
• McDonald PC, Winum JY, Supuran CT, Dedhar S. Recent developments in targeting carbonic anhydrase IX for cancer therapeutics. Oncotarget 2012;3:84–97.
   PubMed Web of Science ®Google Scholar
• Carta F, Aggarwal M, Maresca A, Scozzafava A, McKenna R, Masini E et al. Dithiocarbamates strongly inhibit carbonic anhydrases and show antiglaucoma action in vivo. J Med Chem 2012;55:1721–1730.
   PubMed Web of Science ®Google Scholar
• Monti SM, Maresca A, Viparelli F, Carta F, De Simone G, Mühlschlegel FA et al. Dithiocarbamates are strong inhibitors of the beta-class fungal carbonic anhydrases from Cryptococcus neoformans, Candida albicans and Candida glabrata. Bioorg Med Chem Lett 2012;22:859–862.
   PubMed Web of Science ®Google Scholar
• Maresca A, Carta F, Vullo D, Supuran CT. Dithiocarbamates strongly inhibit the ß-class carbonic anhydrases from Mycobacterium tuberculosis. J Enzyme Inhib Med Chem 2012.
   Google Scholar
• Hall RA, Mühlschlegel FA. Fungal and nematode carbonic anhydrases: their inhibition in drug design. In Drug design of zinc-enzyme inhibitors: functional, structural, and disease applications, Supuran CT, Winum JY, Eds, Hoboken: John Wiley & Sons, 2009, pp. 301–322.
   Google Scholar
• Ohndorf UM, Schlicker C, Steegborn C. Crystallographic studies on carbonic anhydrases from fungal pathogens for structure-assisted drug development. In Drug design of zinc-enzyme inhibitors: functional, structural, and disease applications, Supuran CT, Winum JY., Eds., Hoboken: John Wiley & Sons, 2009, pp. 323–334.
   Google Scholar
• Carta F, Innocenti A, Hall RA, Mühlschlegel FA, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. Inhibition of the ß-class enzymes from the fungal pathogens Candida albicans and Cryptococcus neoformans with branched aliphatic/aromatic carboxylates and their derivatives. Bioorg Med Chem Lett 2011;21:2521–2526.
   PubMed Web of Science ®Google Scholar
• Nishimori I, Onishi S, Takeuchi H, Supuran CT. The alpha and beta classes carbonic anhydrases from Helicobacter pylori as novel drug targets. Curr Pharm Des 2008;14:622–630.
   PubMed Web of Science ®Google Scholar
• Minakuchi T, Nishimori I, Vullo D, Scozzafava A, Supuran CT. Molecular cloning, characterization, and inhibition studies of the Rv1284 beta-carbonic anhydrase from Mycobacterium tuberculosis with sulfonamides and a sulfamate. J Med Chem 2009;52:2226–2232.
   PubMed Web of Science ®Google Scholar
• Nishimori I, Minakuchi T, Vullo D, Scozzafava A, Innocenti A, Supuran CT. Carbonic anhydrase inhibitors. Cloning, characterization, and inhibition studies of a new beta-carbonic anhydrase from Mycobacterium tuberculosis. J Med Chem 2009;52:3116–3120.
   PubMed Web of Science ®Google Scholar
• Güzel O, Maresca A, Scozzafava A, Salman A, Balaban AT, Supuran CT. Discovery of low nanomolar and subnanomolar inhibitors of the mycobacterial beta-carbonic anhydrases Rv1284 and Rv3273. J Med Chem 2009;52:4063–4067.
   PubMed Web of Science ®Google Scholar
• Carta F, Maresca A, Covarrubias AS, Mowbray SL, Jones TA, Supuran CT. Carbonic anhydrase inhibitors. Characterization and inhibition studies of the most active beta-carbonic anhydrase from Mycobacterium tuberculosis, Rv3588c. Bioorg Med Chem Lett 2009;19:6649–6654.
   PubMed Web of Science ®Google Scholar
• Nishimori I, Minakuchi T, Maresca A, Carta F, Scozzafava A, Supuran CT. The ß-carbonic anhydrases from Mycobacterium tuberculosis as drug targets. Curr Pharm Des 2010;16:3300–3309.
   PubMed Web of Science ®Google Scholar
• Winum JY, Köhler S, Supuran CT. Brucella carbonic anhydrases: new targets for designing anti-infective agents. Curr Pharm Des 2010;16:3310–3316.
   PubMed Web of Science ®Google Scholar
• Vullo D, Nishimori I, Minakuchi T, Scozzafava A, Supuran CT. Inhibition studies with anions and small molecules of two novel ß-carbonic anhydrases from the bacterial pathogen Salmonella enterica serovar Typhimurium. Bioorg Med Chem Lett 2011;21:3591–3595.
   PubMed Web of Science ®Google Scholar
• Cronk JD, Endrizzi JA, Cronk MR, O’neill JW, Zhang KY. Crystal structure of E. coli beta-carbonic anhydrase, an enzyme with an unusual pH-dependent activity. Protein Sci 2001;10:911–922.
   PubMed Web of Science ®Google Scholar
• Cronk JD, Rowlett RS, Zhang KY, Tu C, Endrizzi JA, Lee J et al. Identification of a novel noncatalytic bicarbonate binding site in eubacterial beta-carbonic anhydrase. Biochemistry 2006;45:4351–4361.
   PubMed Web of Science ®Google Scholar
• Maresca A, Vullo D, Scozzafava A, Supuran CT. Inhibition of the alpha- and beta- carbonic anhydrases from the gastric pathogen Helycobacter pylori with anions. J Enzyme Inhib Med Chem 2012.
   Google Scholar
• Maresca A, Vullo D, Scozzafava A, Manole G, Supuran CT. Inhibition of the ß-class carbonic anhydrases from Mycobacterium tuberculosis with carboxylic acids. J Enzyme Inhib Med Chem 2012.
   Google Scholar
• Vullo D, Nishimori I, Scozzafava A, Köhler S, Winum JY, Supuran CT. Inhibition studies of a beta-carbonic anhydrase from Brucella suis with a series of water soluble glycosyl sulfanilamides. Bioorg Med Chem Lett 2010;20:2178–2182.
   PubMed Web of Science ®Google Scholar
• Nishimori I, Minakuchi T, Kohsaki T, Onishi S, Takeuchi H, Vullo D et al. Carbonic anhydrase inhibitors: the beta-carbonic anhydrase from Helicobacter pylori is a new target for sulfonamide and sulfamate inhibitors. Bioorg Med Chem Lett 2007;17:3585–3594.
   PubMed Web of Science ®Google Scholar