Advances in structure-based drug discovery of carbonic anhydrase inhibitors

References

• Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nature Rev Drug Discov. 2008;7:168–181. DOI:10.1038/nrd2467.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria? J Enzyme Inhib Med Chem. 2015;30:325–332.
   PubMed Web of Science ®Google Scholar
• Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nature Rev Drug Discov. 2011;10:767–777.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Structure-based drug discovery of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2012;27:759–772.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Structure and function of carbonic anhydrases. Biochem J. 2016;473:2023–2032.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases: from biomedical applications of the inhibitors and activators to biotechnologic use for CO2 capture. J Enzyme Inhib Med Chem. 2013;28:229–230.
   PubMed Web of Science ®Google Scholar
• De Simone G, Supuran CT. (In)organic anions as carbonic anhydrase inhibitors. J Inorg Biochem. 2012;111:117–129.
   PubMed Web of Science ®Google Scholar
• Kikutani S, Nakajima K, Nagasato C, et al. Thylakoid luminal θ-carbonic anhydrase critical for growth and photosynthesis in the marine diatom Phaeodactylum tricornutum. Proc Natl Acad Sci USA. 2016;113:9828–9833.
   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 η-carbonic anhydrases. Bioorg Med Chem Lett. 2014;15(24):4389–4396.
   Web of Science ®Google Scholar
• 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;112:4421–4468. DOI:10.1021/cr200176r
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Menabuoni L, Mincione F, et al. Carbonic anhydrase inhibitors. A general approach for the preparation of water solublesulfonamides 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
• Carta F, Supuran CT, Scozzafava A. Novel therapies for glaucoma: a patent review 2007-2011. Expert OpinTher Pat. 2012;22:79–88. DOI:10.1517/13543776.2012.649006.
   PubMed Web of Science ®Google Scholar
• Masini E, Carta F, Scozzafava A, et al. Antiglaucoma carbonic anhydrase inhibitors: a patent review. Expert Opin Ther Pat. 2013;23:705–716. DOI:10.1517/13543776.2013.794788.
   PubMed Web of Science ®Google Scholar
• Carta F, Supuran CT. Diuretics with carbonic anhydrase inhibitory action: a patent and literature review (2005-2013). Expert Opin Ther Pat. 2013;23:681–691. DOI:10.1517/13543776.2013.780598.
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Supuran CT, Carta F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin Ther Pat. 2013;23:725–735. DOI:10.1517/13543776.2013.790957.
   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;14:4853–4858. DOI:10.1039/c6ob00803h.
   PubMed Web of Science ®Google Scholar
• Lou Y, McDonald PC, Oloumi 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
• Pettersen EO, Ebbesen P, Gieling RG, et al. Targeting tumour hypoxia to prevent cancer metastasis. From biology, biosensing and technology to drug development: the METOXIA consortium. J Enzyme Inhib Med Chem. 2015;30:689–721.
   PubMed Web of Science ®Google Scholar
• Supuran CT. The safety and clinical efficacy of acetazolamide for the treatment of idiopathic intracranial hypertension. Expert Rev Neurother. 2015;15:851–856.
   PubMed Web of Science ®Google Scholar
• Carta F, Di Cesare Mannelli L, Pinard M, et al. A class of sulfonamide carbonic anhydrase inhibitors with neuropathic pain modulating effects. Bioorg Med Chem. 2015;23:1828–1840.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibition and the management of neuropathic pain. Expert Rev Neurother. 2016;16:961–968.
   PubMed Web of Science ®Google Scholar
• Di Cesare Mannelli L, Micheli L, Carta F, et al. Carbonic anhydrase inhibition for the management of cerebral ischemia: in vivo evaluation of sulfonamide and coumarin inhibitors. J Enzyme Inhib Med Chem. 2016;31:894–899.
   PubMed Web of Science ®Google Scholar
• Margheri F, Ceruso M, Carta F, et al. Overexpression of the transmembrane carbonic anhydrase isoforms IX and XII in the inflamed synovium. J Enzyme Inhib Med Chem. 2016;31. DOI:10.1080/14756366.2016.1217857
   Web of Science ®Google Scholar
• Capasso C, Supuran CT. Sulfa and trimethoprim-like drugs - antimetabolites acting as carbonic anhydrase, dihydropteroate synthase and dihydrofolate reductase inhibitors. J Enzyme Inhib Med Chem. 2014;29:379–387.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Legionella pneumophila carbonic anhydrases: underexplored antibacterial drug targets. Pathogens. 2016;5:E44.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Inhibition of carbonic anhydrase from Trypanosoma cruzi for the management of Chagas disease: an underexplored therapeutic opportunity. Future Med Chem. 2016;8:311–324.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Drug interaction considerations in the therapeutic use of carbonic anhydrase inhibitors. Expert Opin Drug Metab Toxicol. 2016;12:423–431.
   PubMed Web of Science ®Google Scholar
• Briganti F, Mangani S, Scozzafava A, et al. Carbonic anhydrase catalyzes cyanamide hydration to urea: is it mimicking the physiological reaction ? J Biol Inorg Chem. 1999;4:528–536.
   PubMed Web of Science ®Google Scholar
• Ferraroni M, Del Prete S, Vullo D, et al. Crystal structure and kinetic studies of a tetrameric type II β-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae. Acta Crystallogr D Biol Crystallogr. 2015;71:2449–2456.
   PubMedGoogle Scholar
• De Simone G, Di Fiore A, Capasso C, et al. The zinc coordination pattern in the η-carbonic anhydrase from Plasmodium falciparum is different from all other carbonic anhydrase genetic families. Bioorg Med Chem Lett. 2015;25:1385–1389.
   PubMed Web of Science ®Google Scholar
• Alterio V, Hilvo M, Di Fiore A, 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
• Briganti F, Mangani S, Orioli P, et al. 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
• Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem. 2016;31:345–360.
   PubMed Web of Science ®Google Scholar
• Bonneau A, Maresca A, Winum JY, et al. Metronidazole-coumarin conjugates and 3-cyano-7-hydroxy-coumarin act as isoform-selective carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2013;28:397–401.
   PubMed Web of Science ®Google Scholar
• Nair SK, Ludwig PA, Christianson DW. Two-site binding of phenol in the active site of human carbonic anhydrase II: structural implications for substrate association. J Am Chem Soc. 1994;116:3659–3660.
   Web of Science ®Google Scholar
• Carta F, Temperini C, Innocenti A, et al. 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
• Innocenti A, Vullo D, Scozzafava A, et al. Carbonic anhydrase inhibitors. Interactions of phenols with the 12 catalytically active mammalian isoforms (CA I – XIV). Bioorg Med Chem Lett. 2008;18:1583–1587.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Vullo D, Scozzafava A, et al. Carbonic anhydrase inhibitors. Inhibition of mammalian isoforms I – XIV with a series of substituted phenols including paracetamol and salicylic acid. Bioorg Med Chem. 2008;16:7424–7428.
   PubMed Web of Science ®Google Scholar
• Bayram E, Senturk M, Kufrevioglu OI, et al. In vitro effects of salicylic acid derivatives on human cytosolic carbonic anhydrase isozymesI and II. Bioorg Med Chem. 2008;16:9101–9105.
   PubMed Web of Science ®Google Scholar
• Tars K, Vullo D, Kazaks A, et al. Sulfocoumarins (1,2-benzoxathiine-2,2-dioxides): a class of potent and isoform-selective inhibitors of tumor-associated carbonic anhydrases. J Med Chem. 2013;56:293–300.
   PubMed Web of Science ®Google Scholar
• Buchieri MV, Riafrecha LE, Rodríguez OM, et al. Inhibition of the β-carbonic anhydrases from Mycobacterium tuberculosis with C-cinnamoyl glycosides: identification of the first inhibitor with anti-mycobacterial activity. Bioorg Med Chem Lett. 2013;23:740–743.
   PubMed Web of Science ®Google Scholar
• Riafrecha LE, Rodríguez OM, Vullo D, et al. Synthesis of C-cinnamoyl glycosides and their inhibitory activity against mammalian carbonic anhydrases. Bioorg Med Chem. 2013;21:1489–1494.
   PubMed Web of Science ®Google Scholar
• Ferraroni M, Carta F, Scozzafava A, et al. Thioxocoumarins show an alternative carbonic anhydrase inhibition mechanism compared to coumarins. J Med Chem. 2016;59:462–473.
   PubMed Web of Science ®Google Scholar
• Maresca A, Temperini C, Vu H, 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, et al. Deciphering the mechanism of carbonic anhydrase inhibition with coumarins and thiocoumarins. J Med Chem. 2010;53:335–344.
   PubMed Web of Science ®Google Scholar
• Temperini C, Innocenti A, Scozzafava A, et al. The coumarin-binding site in carbonic anhydrase accommodates structurally diverse inhibitors: the antiepileptic lacosamide as an example. J Med Chem. 2010;53:850–854.
   PubMed Web of Science ®Google Scholar
• Touisni N, Maresca A, McDonald PC, et al. Glycosylcoumarin 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
• Sharma A, Tiwari M, Supuran CT. Novel coumarins and benzocoumarins acting as isoform-selective inhibitors against the tumor-associated carbonic anhydrase IX. J Enzyme Inhib Med Chem. 2014;2:292–296.
   Web of Science ®Google Scholar
• Maresca A, Supuran CT. Coumarins incorporating hydroxy- and chloro- moieties selectively inhibit the transmembrane, tumor-associated carbonic anhydrase isoforms IX and XII over the cytosolic ones I and II. Bioorg Med Chem Lett. 2010;20:4511–4514.
   PubMed Web of Science ®Google Scholar
• Maresca A, Scozzafava A, Supuran CT. 7,8-Disubstituted- but not 6,7-disubstituted coumarins selectively inhibit the transmembrane, tumor-associated carbonic anhydrase isoforms IX and XII over the cytosolic ones I and II in the low nanomolar/subnanomolar range. Bioorg Med Chem Lett. 2010;20:7255–7258.
   PubMed Web of Science ®Google Scholar
• Carta F, Maresca A, Scozzafava A, et al. 5- and 6-membered (thio)lactones are prodrug type carbonic anhydrase inhibitors. Bioorg Med Chem Lett. 2012;22:267−70.
   PubMed Web of Science ®Google Scholar
• Isik S, Vullo D, Bozdag M, et al. 7-Amino-3,4-dihydro-1H-quinoline-2-one, a compound similar to thesubstitutedcoumarins, inhibits α-carbonic anhydrases without hydrolysis of the lactam ring. J Enzyme Inhib Med Chem. 2015;30:773–777.
   PubMed Web of Science ®Google Scholar
• D’Ambrosio K, Carradori S, Monti SM, et al. Out of the active site binding pocket for carbonic anhydrase inhibitors. Chem Commun. 2015;51:302–305.
   PubMed Web of Science ®Google Scholar
• Alp C, Ozsoy S, Alp NA, et al. Sulfapyridine-like benzenesulfonamide derivatives as inhibitors of carbonic anhydrase isoenzymes I, II and VI. J Enzyme Inhib Med Chem. 2012;27:818–824.
   PubMed Web of Science ®Google Scholar
• Ekinci D, Fidan I, Durdagi S, et al. Kinetic and in silico analysis of thiazolidin-based inhibitors of α-carbonic anhydrase isoenzymes. J Enzyme Inhib Med Chem. 2013;28:370–374.
   PubMed Web of Science ®Google Scholar
• Abdel-Aziz AA, El-Azab AS, Ekinci D, et al. Investigation of arenesulfonyl-2-imidazolidinones as potent carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2015;30:81–84.
   PubMed Web of Science ®Google Scholar
• Arslan M, Şentürk M, Fidan I, et al. Synthesis of 3,4-dihydroxypyrrolidine-2,5-dione and 3,5-dihydroxybenzoic acid derivatives and evaluation of the carbonic anhydrase I and II inhibition. J Enzyme Inhib Med Chem. 2015;30:896–900.
   PubMed Web of Science ®Google Scholar
• Liu F, Martin-Mingot A, Lecornué F, et al. Carbonic Anhydrases inhibitory effects of new benzenesulfonamides synthesized by using superacid chemistry. J Enzyme Inhib Med Chem. 2012;27:886–891.
   PubMed Web of Science ®Google Scholar
• Compain G, Martin-Mingot A, Maresca A, et al. Superacid synthesis of halogen containing N-substituted-4-aminobenzene sulfonamides: new selective tumor-associated carbonic anhydrase inhibitors. Bioorg Med Chem. 2013;21:1555–1563.
   PubMed Web of Science ®Google Scholar
• Métayer B, Mingot A, Vullo D, et al. New superacid synthesized (fluorinated) tertiary benzenesulfonamides acting as selective hCA IX inhibitors: toward a new mode of carbonic anhydrases inhibition by sulfonamides. Chem Commun. 2013;49:6015–6017.
   PubMed Web of Science ®Google Scholar
• Le Darz A, Mingot A, Bouazza F, et al. Fluorinated pyrrolidines and piperidines containing tertiary benzenesulfonamides: selective carbonic anhydrase II inhibitors. J Enzyme Inhib Med Chem. 2015;30:737–745.
   PubMed Web of Science ®Google Scholar
• D’Ascenzio M, Carradori S, De Monte C, et al. Design, synthesis and evaluation of N-substituted saccharin derivatives as selective inhibitors of tumor-associated carbonic anhydrase XII. Bioorg Med Chem. 2014;22:1821–1831.
   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;84:240–246.
   PubMed Web of Science ®Google Scholar
• D’Ascenzio M, Carradori S, Secci D, et al. Selective inhibition of human carbonic anhydrases by novel amide derivatives of probenecid: synthesis, biological evaluation and molecular modelling studies. Bioorg Med Chem. 2014;22:3982–3988.
   PubMed Web of Science ®Google Scholar
• Carradori S, Mollica A, Ceruso M, et al. New amide derivatives of Probenecid as selective inhibitors of carbonic anhydrase IX and XII: biological evaluation and molecular modelling studies. Bioorg Med Chem. 2015;23:2975–2981.
   PubMed Web of Science ®Google Scholar
• Mollica A, Costante R, Akdemir A, et al. Exploring new Probenecid-based carbonic anhydrase inhibitors: synthesis, biological evaluation and docking studies. Bioorg Med Chem. 2015;23:5311–5318.
   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;21:1410–1418.
   PubMed Web of Science ®Google Scholar
• Parkkila S, Innocenti A, Kallio H, et al. The protein tyrosine kinase inhibitors imatinib and nilotinib strongly inhibit several mammalian α-carbonic anhydrase isoforms. Bioorg Med Chem Lett. 2009;19:4102–4106.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Durdagi S, Doostdar N, et al. Nanoscale enzyme inhibitors: fullerenes inhibit carbonic anhydrase by occluding the active site entrance. Bioorg Med Chem. 2010;28:2822–2828.
   Web of Science ®Google Scholar
• Durdagi S, Vullo D, Pan P, et al. Protein-protein interactions: inhibition of mammalian carbonic anhydrases I-XV by the murine inhibitor of carbonic anhydrase and other members of the transferrin family. J Med Chem. 2012;55:5529–5535.
   PubMed Web of Science ®Google Scholar
• Chazalette C, Riviere-Baudet M, Scozzafava A, et al. Carbonic anhydrase inhibitors, interaction of boron derivatives with isozymes I and II: a new binding site for hydrophobic inhibitors at the entrance of the active site as shown by docking studies. J Enzyme Inhib. 2001;16:125–133.
   PubMed Web of Science ®Google Scholar
• Chazalette C, Rivière-Baudet M, Supuran CT, et al. Carbonic anhydrase inhibitors: allylsulfonamide, styrene sulfonamide, N-allyl sulfonamides and some of their Si, Ge, and B derivatives. J Enzyme Inhib. 2001;16:475–489.
   PubMed Web of Science ®Google Scholar
• Winum JY, Innocenti A, Scozzafava A, et al. Carbonic anhydrase inhibitors. Inhibition of the human cytosolic isoforms I and II and transmembrane, tumor-associated isoforms IX and XII with boronic acids. Bioorg Med Chem. 2009;17:3649–3652.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Winum JY, Hall RA, et al. Carbonic anhydrase inhibitors. Inhibition of the fungal beta-carbonic anhydrases from Candida albicans and Cryptococcus neoformans with boronic acids. Bioorg Med Chem Lett. 2009;19:2642–2645.
   PubMed Web of Science ®Google Scholar
• Alterio V, Cadoni R, Esposito D, et al. Benzoxaborole as a new chemotype for carbonic anhydrase inhibition. Chem Commun. 2016;52:11983–11986.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Bortezomib inhibits bacterial and fungal β-carbonic anhydrases. Bioorg Med Chem. 2016;24:4406–4409.
   PubMed Web of Science ®Google Scholar
• Vullo D, Milos M, Galic B, et al. Dipotassium-trioxohydroxy-tetrafluorotriborate, K₂[B₃O₃F₄OH], is a potent inhibitor of human carbonic anhydrases. J Enzyme Inhib Med Chem. 2015;30:341–344.
   PubMed Web of Science ®Google Scholar
• Ilies MA, Supuran CT, Scozzafava A. Carbonic anhydrase inhibitors. Part 91. Metal complexes of heterocyclic sulfonamides as potential pharmacological agents in the treatment of gastric Acid secretion imbalances. Met Based Drugs. 2000;7:57–62.
   PubMedGoogle Scholar
• Supuran CT, Manole G, Andruh M. Carbonic anhydrase inhibitors. Part 11. Coordination compounds of heterocyclic sulfonamides with lanthanides are potent inhibitors of isozymes I and II. J Inorg Biochem. 1993;49:97–103.
   PubMed Web of Science ®Google Scholar
• Sumalan SL, Casanova J, Alzuet G, et al. Synthesis and characterization of metal(II)-8-quinolinsulfonamidato (sa-) complexes (M = Co, Ni, Cu, and Zn). Crystal structure of [Zn(sa)2(NH3)]NH3 complex. Carbonic anhydrase inhibitory properties. J Inorg Biochem. 1996;62:31–39.
   PubMed Web of Science ®Google Scholar
• Borras J, Alzuet G, Ferrer S, et al. Metal complexes of heterocyclic sulfonamides as carbonic anhydrases inhibitors. In: Supuran CT, Scozzafava A, Conway J, editors. Carbonic anhydrase – Its Inhibitors and Activators. Boca Raton (FL): CRC Press; 2004. p. 183–207.
   Google Scholar
• Dilworth JR, Pascu SI, Waghorn PA, et al. Synthesis of sulfonamide conjugates of Cu(II), Ga(III), In(III), Re(V) and Zn(II) complexes: carbonic anhydrase inhibition studies and cellular imaging investigations. Dalton Trans. 2015;44:4859–4873.
   PubMed Web of Science ®Google Scholar
• Lau J, Zhang Z, Jenni S, et al. PET imaging of carbonic anhydrase IX expression of HT-29 tumor xenograft mice with (68)Ga-labeled benzenesulfonamides. Mol Pharm. 2016;13:1137–1146.
   PubMed Web of Science ®Google Scholar
• Sneddon D, Niemans R, Bauwens M, et al. Synthesis and in vivo biological evaluation of (68)Ga-labeled carbonic anhydrase IX targeting small molecules for positron emission tomography. J Med Chem. 2016;59:6431–6443.
   PubMed Web of Science ®Google Scholar
• El-Azab AS, Abdel-Aziz AA, Ayyad RR, et al. Inhibition of carbonic anhydrase isoforms I, II, IV, VII and XII with carboxylates and sulfonamides incorporating phthalimide/phthalic anhydride scaffolds. Bioorg Med Chem. 2016;24:20–25. DOI:10.1016/j.bmc.2015.11.034.
   PubMed Web of Science ®Google Scholar
• Lesburg CA, Huang C, Christianson DW, et al. Histidine --> carboxamide ligand substitutions in the zinc binding site of carbonic anhydrase II alter metal coordination geometry but retain catalytic activity. Biochemistry. 1997;36:15780–15791.
   PubMed Web of Science ®Google Scholar
• Aggarwal M, Boone CD, Kondeti B, et al. Effects of cryoprotectants on the structure and thermostability of the human carbonic anhydrase II-acetazolamide complex. Acta Crystallogr D Biol Crystallogr. 2013;69:860–865.
   PubMedGoogle Scholar
• Pinard MA, Aggarwal M, Mahon BP, et al. A sucrose-binding site provides a lead towards an isoform-specific inhibitor of the cancer-associated enzyme carbonic anhydrase IX. Acta Crystallogr F Struct Biol Commun. 2015;71:1352–1358.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Hilvo M, Scozzafava A, et al. Carbonic anhydrase inhibitors: the very weak inhibitors dithiothreitol, beta-mercaptoethanol, tris(carboxyethyl)phosphine and threitol interfere with the binding of sulfonamides to isozymes II and IX. Bioorg Med Chem Lett. 2008;18:1898–1903.
   PubMed Web of Science ®Google Scholar
• Pala N, Dallocchio R, Dessì A, et al. Virtual screening-driven identification of human carbonic anhydrase inhibitors incorporating an original, new pharmacophore. Bioorg Med Chem Lett. 2011;21:2515–2520.
   PubMed Web of Science ®Google Scholar
• Lomelino CL, Sechi M, McKenna M, et al. Gem-diols as a new class of carbonic anhydrase inhibitors binding to the metal ion. Forthcoming.
   Google Scholar
• Innocenti A, Hilvo M, Scozzafava A, et al. Carbonic anhydrase inhibitors: inhibition of the new membrane-associated isoform XV with phenols. Bioorg Med Chem Lett. 2008;18:3593–3596.
   PubMed Web of Science ®Google Scholar
• Riafrecha LE, Bua S, Supuran CT, et al. Synthesis and carbonic anhydrase inhibitory effects of new N-glycosylsulfonamides incorporating the phenol moiety. Bioorg Med Chem Lett. 2016;26:3892–3895.
   PubMed Web of Science ®Google Scholar
• Işık S, Vullo D, Durdagi S, et al. Interaction of carbonic anhydrase isozymes I, II, and IX with some pyridine and phenol hydrazinecarbothioamide derivatives. Bioorg Med Chem Lett. 2015;25:5636–5641.
   PubMed Web of Science ®Google Scholar
• Maresca A, Akyuz G, Osman SM, et al. Inhibition of mammalian carbonic anhydrase isoforms I-XIV with a series of phenolic acid esters. Bioorg Med Chem. 2015;23:7181–7188.
   PubMed Web of Science ®Google Scholar
• Karioti A, Ceruso M, Carta F, et al. New natural product carbonic anhydrase inhibitors incorporating phenol moieties. Bioorg Med Chem. 2015;23:7219–7225.
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Kalın P, Supuran CT, et al. The impact of hydroquinone on acetylcholine esterase and certain human carbonic anhydrase isoenzymes (hCA I, II, IX, and XII). J Enzyme Inhib Med Chem. 2015;30:941–946.
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Passaponti M, Supuran CT, et al. Carbonic anhydrase inhibitors: guaiacol and catechol derivatives effectively inhibit certain human carbonic anhydrase isoenzymes (hCA I, II, IX and XII). J Enzyme Inhib Med Chem. 2015;30:586–591.
   PubMed Web of Science ®Google Scholar
• Carradori S, De Monte C, D’Ascenzio M, et al. Salen and tetrahydrosalen derivatives act as effective inhibitors of the tumor-associated carbonic anhydrase XII--a new scaffold for designing isoform-selective inhibitors. Bioorg Med Chem Lett. 2013;23:6759–6763.
   PubMed Web of Science ®Google Scholar
• Bilginer S, Unluer E, Gul HI, et al. Carbonic anhydrase inhibitors. Phenols incorporating 2- or 3-pyridyl-ethenylcarbonyl and tertiary amine moieties strongly inhibit Saccharomyces cerevisiae β-carbonic anhydrase. J Enzyme Inhib Med Chem. 2014;29:495–499.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Gülçin I, Scozzafava A, et al. Carbonic anhydrase inhibitors. Antioxidant polyphenols effectively inhibit mammalian isoforms I-XV. Bioorg Med Chem Lett. 2010;20:5050–5053. DOI:10.1016/j.bmcl.2010.07.038.
   PubMed Web of Science ®Google Scholar
• Ekinci D, Karagoz L, Ekinci D, et al. Carbonic anhydrase inhibitors: in vitro inhibition of α isoforms (hCA I, hCA II, bCA III, hCA IV) by flavonoids. J Enzyme Inhib Med Chem. 2013;28:283–288. DOI:10.3109/14756366.2011.643303.
   PubMed Web of Science ®Google Scholar
• Davis RA, Hofmann A, Osman A, et al. Natural product-based phenols as novel probes for mycobacterial and fungal carbonic anhydrases. J Med Chem. 2011;54:1682–1692. DOI:10.1021/jm1013242.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Oztürk Sarikaya SB, Gülçin I, et al. Carbonic anhydrase inhibitors. Inhibition of mammalian isoforms I-XIV with a series of natural product polyphenols and phenolic acids. Bioorg Med Chem. 2010;18:2159–2164. DOI:10.1016/j.bmc.2010.01.076.
   PubMed Web of Science ®Google Scholar
• Boztaş M, Çetinkaya Y, Topal M, et al. Synthesis and carbonic anhydrase isoenzymes I, II, IX, and XII inhibitory effects of dimethoxybromophenol derivatives incorporating cyclopropane moieties. J Med Chem. 2015;58:640–650. DOI:10.1021/jm501573b.
   PubMed Web of Science ®Google Scholar
• Cau Y, Mori M, Supuran CT, et al. Mycobacterial carbonic anhydrase inhibition with phenolic acids and esters: kinetic and computational investigations. Org Biomol Chem. 2016;14:8322–8330. DOI:10.1039/c6ob01477a
   PubMed Web of Science ®Google Scholar
• Riviere-Baudet M, Supuran CT. Carbonic anhydrase inhibitors. Part 40. Germyl amines and germaniols inhibit carbonic anhydrase isozyme II but not isozyme I. Main Group Met Chem. 1996;19:579–584. DOI:10.1515/MGMC.1996.19.9.579.
   Web of Science ®Google Scholar
• Karioti A, Carta F, Supuran CT. An update on natural products with carbonic anhydrase inhibitory activity. Curr Pharm Des. 2016;22:1570–1591.
   PubMed Web of Science ®Google Scholar
• Boone CD, Tu C, McKenna R. Structural elucidation of the hormonal inhibition mechanism of the bile acid cholate on human carbonic anhydrase II. Acta Crystallogr D Biol Crystallogr. 2014;70:1758–1763. DOI:10.1107/S1399004714007457.
   PubMedGoogle 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. DOI:10.1002/chem.201503748.
   PubMed Web of Science ®Google Scholar
• Martin DP, Cohen SM. Nucleophile recognition as an alternative inhibition mode for benzoic acid based carbonic anhydrase inhibitors. Chem Commun. 2012;48:5259–5261. DOI:10.1039/c2cc32013d.
   PubMed Web of Science ®Google Scholar
• Woods LA, Dolezal O, Ren B, et al. Native state mass spectrometry, surface plasmon resonance, and X-ray crystallography correlate strongly as a fragment screening combination. J Med Chem. 2016;59:2192–2204. DOI:10.1021/acs.jmedchem.5b01940.
   PubMed Web of Science ®Google Scholar
• Abdel-Aziz AA, El-Azab AS, Ceruso M, et al. Carbonic anhydrase inhibitory activity of sulfonamides and carboxylic acids incorporating cyclic imide scaffolds. Bioorg Med Chem Lett. 2014;24:5185–5189. DOI:10.1016/j.bmcl.2014.09.076.
   PubMed Web of Science ®Google Scholar
• Barresi E, Salerno S, Marini AM, et al. Sulfonamides incorporating heteropolycyclic scaffolds show potent inhibitory action against carbonic anhydrase isoforms I, II, IX and XII. Bioorg Med Chem. 2016;24:921–927. DOI:10.1016/j.bmc.2016.01.018.
   PubMed Web of Science ®Google Scholar
• Cvijetić IN, Tanç M, Juranić IO, et al. 5-Aryl-1H-pyrazole-3-carboxylic acids as selective inhibitors of human carbonic anhydrases IX and XII. Bioorg Med Chem. 2015;23:4649–4659. DOI:10.1016/j.bmc.2015.05.052.
   PubMed Web of Science ®Google Scholar
• Nasr G, Cristian A, Barboiu M, et al. Carbonic anhydrase inhibitors. Inhibition of human cytosolic isoforms I and II with (reduced) Schiff’s bases incorporating sulfonamide, carboxylate and carboxymethyl moieties. Bioorg Med Chem. 2014;22:2867–2874. DOI:10.1016/j.bmc.2014.03.041.
   PubMed Web of Science ®Google Scholar
• Sechi M, Innocenti A, Pala N, et al. Inhibition of α-class cytosolic human carbonic anhydrases I, II, IX and XII, and β-class fungal enzymes by carboxylic acids and their derivatives: new isoform-I selective nanomolar inhibitors. Bioorg Med Chem Lett. 2012;22:5801–5806. DOI:10.1016/j.bmcl.2012.07.094.
   PubMed Web of Science ®Google Scholar
• Maresca A, Vullo D, Scozzafava A, et al. Inhibition of the β-class carbonic anhydrases from Mycobacterium tuberculosis with carboxylic acids. J Enzyme Inhib Med Chem. 2013;28:392–396. DOI:10.3109/14756366.2011.650168.
   PubMed Web of Science ®Google Scholar
• Carta F, Innocenti A, Hall RA, et al. Carbonic anhydrase inhibitors. Inhibition of the β-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. DOI:10.1016/j.bmcl.2011.02.057.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Hall RA, Schlicker C, et al. Carbonic anhydrase inhibitors. Inhibition of the beta-class enzymes from the fungal pathogens Candida albicans and Cryptococcus neoformans with aliphatic and aromatic carboxylates. Bioorg Med Chem. 2009;17:2654–2657. DOI:10.1016/j.bmc.2009.02.058.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Vullo D, Scozzafava A, et al. Carbonic anhydrase inhibitors. Interaction of isozymes I, II, IV, V, and IX with carboxylates. Bioorg Med Chem Lett. 2005;15:573–578. DOI:10.1016/j.bmcl.2004.11.057.
   PubMed Web of Science ®Google Scholar
• Mori M, Cau Y, Vignaroli G, et al. Hit recycling : discovery of a potent carbonic anhydrase inhibitor by in silico target fishing. ACS Chem Biol. 2015;10:1964–1969. DOI:10.1021/acschembio.5b00337.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Vullo D, Scozzafava A, et al. Carbonic anhydrase inhibitors. Inhibition of isozymes I, II, IV, V, and IX with anions isosteric and isoelectronic with sulfate, nitrate, and carbonate. Bioorg Med Chem Lett. 2005;15:567–571. DOI:10.1016/j.bmcl.2004.11.056.
   PubMed Web of Science ®Google Scholar
• Davis RA, Vullo D, Supuran CT, et al. Natural product polyamines that inhibit human carbonic anhydrases. Biomed Res Int. 2014;2014:374079. DOI:10.1155/2014/374079.
   PubMed Web of Science ®Google Scholar
• Briganti F, Mangani S, Scozzafava A, et al. Carbonic anhydrase catalyzes cyanamide hydration to urea: is it mimicking the physiological reaction? J Biol Inorg Chem. 1999;4:528–536.
   PubMed Web of Science ®Google Scholar
• Guerri A, Briganti F, Scozzafava A, et al. Mechanism of cyanamide hydration catalyzed by carbonic anhydrase II suggested by cryogenic X-ray diffraction. Biochemistry. 2000;39:12391–12397.
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Supuran CT. Hydroxyurea is a carbonic anhydrase inhibitor. Bioorg Med Chem. 2003;11:2241–2246.
   PubMed Web of Science ®Google Scholar
• Temperini C, Innocenti A, Scozzafava A, et al. N-hydroxyurea--a versatile zinc binding function in the design of metalloenzyme inhibitors. Bioorg Med Chem Lett. 2006;16:4316–4320. DOI:10.1016/j.bmcl.2006.05.068.
   PubMed Web of Science ®Google Scholar
• Scolnick LR, Clements AM, Liao J, et al. Novel binding mode of hydroxamate inhibitors to human carbonic anhydrase II. J Am Chem Soc. 1997;119:850–851. DOI:10.1021/ja963832z.
   Web of Science ®Google Scholar
• Di Fiore A, Maresca A, Supuran CT, et al. Hydroxamate represents a versatile zinc binding group for the development of new carbonic anhydrase inhibitors. Chem Commun. 2012;48:8838–8840. DOI:10.1039/c2cc34275h.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Hydroxamates as carbonic anhydrase inhibitors. In: Gupta SP, editor. Hydroxamic acids: a unique family of chemicals with multiple biological activities. Heidelberg: Springer Verlag; 2013. p. 55–69.
   Google Scholar
• Scozzafava A, Supuran CT. Carbonic anhydrase and matrix metalloproteinase inhibitors. Sulfonylated amino acid hydroxamates with MMP inhibitory properties act as efficient inhibitors of carbonic anhydrase isozymes I, II and IV, and N-hydroxysulfonamides inhibit both these zinc enzymes. J Med Chem. 2000;43:3677–3687.
   PubMed Web of Science ®Google Scholar
• Santos MA, Marques S, Gil M, et al. Protease inhibitors: synthesis of bacterial collagenase and matrix metalloproteinase inhibitors incorporating succinylhydroxamate and iminodiacetic acid hydroxamate moieties. J Enzyme Inhib Med Chem. 2003;18:233–242. DOI:10.1080/1475636031000081134.
   PubMed Web of Science ®Google Scholar
• Nuti E, Orlandini E, Nencetti S, et al. Carbonic anhydrase and matrix metalloproteinase inhibitors. Inhibition of human tumor-associated isozymes IX and cytosolic isozyme I and II with sulfonylatedhydroxamates. Bioorg Med Chem. 2007;15:2298–2311. DOI:10.1016/j.bmc.2007.01.023.
   PubMed Web of Science ®Google Scholar
• Santos MA, Marques S, Vullo D, et al. Carbonic anhydrase inhibitors. Inhibition of cytosolic/tumor-associated isoforms I, II and IX with iminodiacetic carboxylates/hydroxamates also incorporating benzenesulfonamide moieties. Bioorg Med Chem Lett. 2007;17:1538–1543. DOI:10.1016/j.bmcl.2006.12.107.
   PubMed Web of Science ®Google Scholar
• Marques SM, Nuti E, Rossello A, et al. Dual inhibitors of matrix metalloproteinases and carbonic anhydrases: iminodiacetyl-based hydroxamate-benzenesulfonamide conjugates. J Med Chem. 2008;51:7968–7979. DOI:10.1021/jm800964f.
   PubMed Web of Science ®Google Scholar
• Khalifah RG. The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. J Biol Chem. 1971;246:2561–2573.
   PubMed Web of Science ®Google Scholar
• Kannan KK, Petef M, Fridborg K, et al. Structure and function of carbonic anhydrases. Imidazole binding to human carbonic anhydrase B and the mechanism of action of carbonic anhydrases. FEBS Lett. 1977;73:115–119.
   PubMed Web of Science ®Google Scholar
• Mangani S, Liljas A. Crystal structure of the complex between human carbonic anhydrase II and the aromatic inhibitor 1,2,4-triazole. J Mol Biol. 1993;232:9–14. DOI:10.1006/jmbi.1993.1365.
   PubMed Web of Science ®Google Scholar
• Duda D, Tu C, Qian M, et al. Structural and kinetic analysis of the chemical rescue of the proton transfer function of carbonic anhydrase II. Biochemistry. 2001;40:1741–1748.
   PubMed Web of Science ®Google Scholar
• Rusconi S, Innocenti A, Vullo D, et al. Carbonic anhydrase inhibitors. Interaction of isozymes I, II, IV, V, and IX with phosphates, carbamoyl phosphate, and the phosphonate antiviral drug foscarnet. Bioorg Med Chem Lett. 2004;14:5763–5767. DOI:10.1016/j.bmcl.2004.09.064.
   PubMed Web of Science ®Google Scholar
• Winum JY, Innocenti A, Gagnard V, et al. Carbonic anhydrase inhibitors. Interaction of isozymes I, II, IV, V, and IX with organic phosphates and phosphonates. Bioorg Med Chem Lett. 2005;15:1683–1686. DOI:10.1016/j.bmcl.2005.01.049.
   PubMed Web of Science ®Google Scholar
• Temperini C, Innocenti A, Guerri A, et al. Phosph(on)ate as a zinc-binding group in metalloenzyme inhibitors: X-ray crystal structure of the antiviral drug foscarnet complexed to human carbonic anhydrase I. Bioorg Med Chem Lett. 2007;17:2210–2215. DOI:10.1016/j.bmcl.2007.01.113
   PubMed Web of Science ®Google Scholar
• Reich R, Hoffman A, Veerendhar A, et al. Carbamoylphosphonates control tumor cell proliferation and dissemination by simultaneously inhibiting carbonic anhydrase IX and matrix metalloproteinase-2. Toward nontoxic chemotherapy targeting tumor microenvironment. J Med Chem. 2012;55:7875–7882. DOI:10.1021/jm300981b.
   PubMed Web of Science ®Google Scholar
• Reich R, Hoffman A, Suresh RR, et al. Carbamoylphosphonates inhibit autotaxin and metastasis formation in vivo. J Enzyme Inhib Med Chem. 2015;30:767–772. DOI:10.3109/14756366.2014.968146.
   PubMed Web of Science ®Google Scholar
• Tauro M, Loiodice F, Ceruso M, et al. Dual carbonic anhydrase/matrix metalloproteinase inhibitors incorporating bisphosphonic acid moieties targeting bone tumors. Bioorg Med Chem Lett. 2014;24:2617–2620. DOI:10.1016/j.bmcl.2014.04.077.
   PubMed Web of Science ®Google Scholar
• Tauro M, Loiodice F, Ceruso M, et al. Arylamino bisphosphonates: potent and selective inhibitors of the tumor-associated carbonic anhydrase XII. Bioorg Med Chem Lett. 2014;24:1941–1943. DOI:10.1016/j.bmcl.2014.03.001.
   PubMed Web of Science ®Google Scholar
• Fenesan I, Popescu R, Scozzafava A, et al. Carbonic anhydrase inhibitors; phosphoryl-sulfonamides -a new class of high affinity inhibitors of isozymes I and II. J Enzyme Inhib. 2000;15:297–310.
   PubMed Web of Science ®Google Scholar
• Timotheatou D, Ioannou PV, Scozzafava A, et al. Carbonic anhydrase interaction with lipothioarsenites: a novel class of isozymes I and II inhibitors. Met Based Drugs. 1996;3:263–268. DOI:10.1155/MBD.1996.263.
   PubMedGoogle Scholar
• Supuran CT, Serves SV, Ioannou PV. Carbonic anhydrase inhibitors. Part 33. Isozyme II inhibition with 2,3-dihydroxypropylarsonic acids and arsonolipids. J Inorg Biochem. 1996;62:207–212. DOI:10.1016/0162-0134(95)00154-9.
   Web of Science ®Google Scholar
• Ioannou PV, Kordalis NL, Scozzafava A, et al. Carbonic anhydrase inhibitors Part 87. Inhibition of carbonic anhydrase isozymes I, II and IV with arsinolipids. Main Group Met Chem. 1999;22:693–695. DOI:10.1515/MGMC.1999.22.12.693.
   Web of Science ®Google Scholar
• Kose LP, Gulcin I, Yıldırım A, et al. The human carbonic anhydrase isoenzymes I and II inhibitory effects of some hydroperoxides, alcohols, and acetates. J Enzyme Inhib Med Chem. 2016;31:1248–1253. DOI:10.3109/14756366.2015.1120723.
   PubMed Web of Science ®Google Scholar
• Olander J, Kaiser ET. The binding of thiophenols to bovine carbonic anhydrase. Biochem Biophys Res Commun. 1971;45:1083–1088.
   PubMed Web of Science ®Google Scholar
• Barrese AA 3rd, Genis C, Fisher SZ, et al. Inhibition of carbonic anhydrase II by thioxolone: a mechanistic and structural study. Biochemistry. 2008;47:3174–3184. DOI:10.1021/bi702385k.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Maresca A, Scozzafava A, et al. Carbonic anhydrase inhibitors: thioxolone versus sulfonamides for obtaining isozyme-selective inhibitors? Bioorg Med Chem Lett. 2008;18:3938–3941. DOI:10.1016/j.bmcl.2008.06.024.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Scozzafava A, Saramet I, et al. Carbonic anhydrase inhibitors: inhibition of isozymes I, II and IV with heterocyclic mercaptans, sulfenamides, sulfonamides and their metal complexes. J Enzyme Inhib. 1998;13:177–194.
   PubMed Web of Science ®Google Scholar
• Almajan GL, Innocenti A, Puccetti L, et al. Carbonic anhydrase inhibitors. Inhibition of the cytosolic and tumor-associated carbonic anhydrase isozymes I, II, and IX with a series of 1,3,4-thiadiazole- and 1,2,4-triazole-thiols. Bioorg Med Chem Lett. 2005;15:2347–2352. DOI:10.1016/j.bmcl.2005.02.088.
   PubMed Web of Science ®Google Scholar
• Zareef M, Innocenti A, Iqbal R, et al. Carbonic anhydrase inhibitors. Inhibition of human tumor-associated isozymes IX and cytosolic isozymes I and II with some 1,3,4-oxadiazole-thiols. J Enzyme Inhib Med Chem. 2006;21:351–359. DOI:10.1080/14756360600741503.
   PubMed Web of Science ®Google Scholar
• Almajan GL, Barbuceanu SF, Innocenti A, et al. Carbonic anhydrase inhibitors. Inhibition of the cytosolic and tumor-associated carbonic anhydrase isozymes I, II and IX with some 1,3,4-oxadiazole- and 1,2,4-triazole-thiols. J Enzyme Inhib Med Chem. 2008;23:101–107. DOI:10.1080/14756360701342417.
   PubMed Web of Science ®Google Scholar
• Abdel-Hamid MK, Abdel-Hafez AA, El-Koussi NA, et al. Design, synthesis, and docking studies of new 1,3,4-thiadiazole-2-thione derivatives with carbonic anhydrase inhibitory activity. Bioorg Med Chem. 2007;15:6975–6984. DOI:10.1016/j.bmc.2007.07.044.
   PubMed Web of Science ®Google Scholar
• Pan P, Vermelho AB, Capaci Rodrigues G, et al. Cloning, characterization, and sulfonamide and thiol inhibition studies of an α-carbonic anhydrase from Trypanosoma cruzi, the causative agent of Chagas disease. J Med Chem. 2013;56:1761–1771. DOI:10.1021/jm4000616.
   PubMed Web of Science ®Google Scholar
• Syrjänen L, Vermelho AB, Rodrigues Ide A, et al. Cloning, characterization, and inhibition studies of a β-carbonic anhydrase from Leishmania donovani chagasi, the protozoan parasite responsible for leishmaniasis. J Med Chem. 2013;56:7372–7381. DOI:10.1021/jm400939k.
   PubMed Web of Science ®Google Scholar
• Carta F, Aggarwal M, Maresca A, et al. Dithiocarbamates: a new class of carbonic anhydrase inhibitors. Crystallographic and kinetic investigations. Chem Commun. 2012;48:1868–1870. DOI:10.1039/c2cc16395k.
   PubMed Web of Science ®Google Scholar
• Carta F, Aggarwal M, Maresca A, et al. Dithiocarbamates strongly inhibit carbonic anhydrases and show antiglaucoma action in vivo. J Med Chem. 2012;55:1721–1730. DOI:10.1021/jm300031j.
   PubMed Web of Science ®Google Scholar
• Monti SM, Maresca A, Viparelli F, et al. Dithiocarbamates strongly inhibit the beta-class fungal carbonic anhydrases from Cryptococcus neoformans, Candida albicans and Candida glabrata. Bioorg Med Chem Lett. 2012;22:859–862. DOI:10.1016/j.bmcl.2011.12.033.
   PubMed Web of Science ®Google Scholar
• Vullo D, Durante M, Di Leva FS, et al. Monothiocarbamates strongly inhibit carbonic anhydrases in vitro and possess intraocular pressure lowering activity in an animal model of glaucoma. J Med Chem. 2016;59:5857–5867. DOI:10.1021/acs.jmedchem.6b00462
   PubMed Web of Science ®Google Scholar
• Carta F, Akdemir A, Scozzafava A, et al. Xanthates and trithiocarbonates strongly inhibit carbonic anhydrases and show antiglaucoma effects in vivo. J Med Chem. 2013;56:4691–4700. DOI:10.1021/jm400414j.
   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
• Bozdag M, Carta F, Vullo D, et al. Synthesis of a new series of dithiocarbamates with effective human carbonic anhydrase inhibitory activity and antiglaucoma action. Bioorg Med Chem. 2015;23:2368–2376.
   PubMed Web of Science ®Google Scholar
• Bozdag M, Carta F, Vullo D, et al. Dithiocarbamates with potent inhibitory activity against the Saccharomyces cerevisiae β-carbonic anhydrase. J Enzyme Inhib Med Chem. 2016;31:132–136.
   PubMed Web of Science ®Google Scholar
• Grandane A, Tanc M, Zalubovskis R, et al. Synthesis of 6-tetrazolyl-substituted sulfocoumarins acting as highly potent and selective inhibitors of the tumor-associated carbonic anhydrase isoforms IX and XII. Bioorg Med Chem. 2014;22:1522–1528.
   PubMed Web of Science ®Google Scholar
• Grandane A, Tanc M, Zalubovskis R, et al. 6-Triazolyl-substituted sulfocoumarins are potent, selective inhibitors of the tumor-associated carbonic anhydrases IX and XII. Bioorg Med Chem Lett. 2014;24:1256–1260.
   PubMed Web of Science ®Google Scholar
• Grandane A, Tanc M, Žalubovskis R, et al. Synthesis of 6-aryl-substituted sulfocoumarins and investigation of their carbonic anhydrase inhibitory action. Bioorg Med Chem. 2015;23:1430–1436.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Ceruso M, Carta F, et al. 7-Aryl-triazolyl-substituted sulfocoumarins are potent, selective inhibitors of the tumor-associated carbonic anhydrase IX and XII. J Enzyme Inhib Med Chem. 2016;31:1226–1233.
   PubMed Web of Science ®Google Scholar
• Tanc M, Carta F, Scozzafava A, et al. 6-Substituted 1,2-benzoxathiine-2,2-dioxides are isoform-selective inhibitors of human carbonic anhydrases IX, XII and VA. Org Biomol Chem. 2015;13:77–80.
   PubMed Web of Science ®Google Scholar
• Grandane A, Tanc M, Di Cesare Mannelli L, et al. 6-Substituted sulfocoumarins are selective carbonic anhdydrase IX and XII inhibitors with significant cytotoxicity against colorectal cancer cells. J Med Chem. 2015;58:3975–3983.
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Menabuoni L, Mincione F, et al. Carbonic anhydrase inhibitors. Part 74. Synthesis of water-soluble, topically effective, intraocular pressure-lowering aromatic/heterocyclic sulfonamides containing cationic or anionic moieties: is the tail more important than the ring? J Med Chem. 1999;42:2641–2650.
   PubMed Web of Science ®Google Scholar
• Pacchiano F, Carta F, McDonald PC, 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
• Pacchiano F, Aggarwal M, Avvaru BS, 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 (Cambridge). 2010;46:8371–8373.
   PubMed Web of Science ®Google Scholar
• Vomasta D, Innocenti A, König B, et al. Carbonic anhydrase inhibitors: Two-prong versus mono-prong inhibitors of isoforms I, II, IX, and XII exemplified by photochromic cis-1,2-α-dithienylethene derivatives. Bioorg Med Chem Lett. 2009;19:1283–1286.
   PubMed Web of Science ®Google Scholar
• Tanpure RP, Ren B, Peat TS, et al. Carbonic anhydrase inhibitors with dual-tail moieties to match the hydrophobic and hydrophilic halves of the carbonic anhydrase active site. J Med Chem. 2015;58:1494–1501.
   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;58:6630–6638.
   PubMed Web of Science ®Google Scholar
• Ivanova J, Leitans J, Tanc M, et al. X-ray crystallography-promoted drug design of carbonic anhydrase inhibitors. Chem Commun. 2015;51:7108–7111.
   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
• Leitans J, Sprudza A, Tanc M, et al. 5-Substituted-(1,2,3-triazol-4-yl)thiophene-2-sulfonamides strongly inhibit human carbonic anhydrases I, II, IX and XII: solution and X-ray crystallographic studies. Bioorg Med Chem. 2013;21:5130–5138.
   PubMed Web of Science ®Google Scholar
• Bozdag M, Alafeefy AM, Vullo D, et al. Benzenesulfonamides incorporating bulky aromatic/heterocyclic tails with potent carbonic anhydrase inhibitory activity. Bioorg Med Chem. 2015;23:7751–7764.
   PubMed Web of Science ®Google Scholar
• Bozdag M, Pinard M, Carta F, et al. A class of 4-sulfamoylphenyl-ω-aminoalkyl ethers with effective carbonic anhydrase inhibitory action and antiglaucoma effects. J Med Chem. 2014;57:9673–9686.
   PubMed Web of Science ®Google Scholar
• Bozdag M, Ferraroni M, Carta F, et al. Structural insights on carbonic anhydrase inhibitory action, isoform selectivity, and potency of sulfonamides and coumarins incorporating arylsulfonylureido groups. J Med Chem. 2014;57:9152–9167.
   PubMed Web of Science ®Google Scholar
• Bozdag M, Ferraroni M, Nuti E, et al. Combining the tail and the ring approaches for obtaining potent and isoform-selective carbonic anhydrase inhibitors: solution and X-ray crystallographic studies. Bioorg Med Chem. 2014;22:334–340.
   PubMed Web of Science ®Google Scholar
• Lomelino CL, Mahon BP, McKenna R, et al. Kinetic and X-ray crystallographic investigations on carbonic anhydrase isoforms I, II, IX and XII of a thioureido analog of SLC-0111. Bioorg Med Chem. 2016;24:976–981.
   PubMed Web of Science ®Google Scholar
• Lau J, Liu Z, Lin KS, et al. Trimeric radiofluorinated sulfonamide derivatives to achieve in vivo selectivity for carbonic anhydrase IX-targeted PET imaging. J Nucl Med. 2015;56:1434–1440.
   PubMed Web of Science ®Google Scholar
• Pan J, Lau J, Mesak F, et al. Synthesis and evaluation of 18F-labeled carbonic anhydrase IX inhibitors for imaging with positron emission tomography. J Enzyme Inhib Med Chem. 2014;29:249–255.
   PubMed Web of Science ®Google Scholar
• Peeters SG, Dubois L, Lieuwes NG, et al. [18F]VM4-037 microPET imaging and biodistribution of two in vivo CAIX-expressing tumor models. Mol Imaging Biol. 2015;17:615–619.
   PubMed Web of Science ®Google Scholar
• Akurathi V, Dubois L, Lieuwes NG, et al. Synthesis and biological evaluation of a 99mTc-labelled sulfonamide conjugate for in vivo visualization of carbonic anhydrase IX expression in tumor hypoxia. Nucl Med Biol. 2010;37:557–564.
   PubMed Web of Science ®Google Scholar
• Akurathi V, Dubois L, Celen S, et al. Development and biological evaluation of ⁹⁹mTc-sulfonamide derivatives for in vivo visualization of CA IX as surrogate tumor hypoxia markers. Eur J Med Chem. 2014;71:374–384.
   PubMed Web of Science ®Google Scholar
• Salmon AJ, Williams ML, Wu QK, et al. Metallocene-based inhibitors of cancer-associated carbonic anhydrase enzymes IX and XII. J Med Chem. 2012;55:5506–5517.
   PubMed Web of Science ®Google Scholar
• Loughrey BT, Williams ML, Healy PC, et al. Novel organometallic cationic ruthenium(II) pentamethylcyclopentadienyl benzenesulfonamide complexes targeted to inhibit carbonic anhydrase. J Biol Inorg Chem. 2009;14:935–945.
   PubMed Web of Science ®Google Scholar
• Can D, Spingler B, Schmutz P, et al. [(Cp-R)M(CO)3] (M=Re or 99mTc) Arylsulfonamide, arylsulfamide, and arylsulfamate conjugates for selective targeting of human carbonic anhydrase IX. Angew Chem Int Ed Engl. 2012;51:3354–3357.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Vullo D, Bartolucci G, et al. N-Nitrosulfonamides: a new chemotype for carbonic anhydrase inhibition. Bioorg Med Chem. 2016;24:3612–3617.
   PubMed Web of Science ®Google Scholar