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Review

Click chemistry approaches for developing carbonic anhydrase inhibitors and their applications

ORCID Icon & ORCID Icon
Article: 2166503 | Received 26 Nov 2022, Accepted 04 Jan 2023, Published online: 13 Jan 2023

References

  • Kolb HC, Finn MG, Sharpless KB. Click chemistry: diverse chemical function from a few good reactions. Angew Chem Int Ed. 2001;40(11):2004–2021.
  • Tornøe CW, Christensen C, Meldal M. Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(i)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J Org Chem. 2002;67(9):3057–3064.
  • Thirumurugan P, Matosiuk D, Jozwiak K. Click chemistry for drug development and diverse chemical-biology applications. Chem Rev. 2013;113(7):4905–4979.
  • Kaur J, Saxena M, Rishi N. An overview of recent advances in biomedical applications of click chemistry. Bioconjug Chem. 2021;32(8):1455–1471.
  • Jiang X, Hao X, Jing L, Wu G, Kang D, Liu X, Zhan P. Recent applications of click chemistry in drug discovery. Expert Opin Drug Discov. 2019;14(8):779–789.
  • Kim E, Koo H. Biomedical applications of copper-free click chemistry: in vitro, in vivo, and ex vivo. Chem Sci. 2019;10(34):7835–7851.
  • Hou J, Liu X, Shen J, Zhao G, Wang PG. The impact of click chemistry in medicinal chemistry. Expert Opin Drug Discov. 2012;7(6):489–501.
  • (a) Supuran CT. Emerging role of carbonic anhydrase inhibitors. Clin Sci. 2021;135(10):1233–1249. (b) Nocentini A, Angeli A, Carta F, Winum JY, Zalubovskis R, Carradori S, Capasso C, Donald WA, Supuran CT. Reconsidering anion inhibitors in the general context of drug design studies of modulators of activity of the classical enzyme carbonic anhydrase. J Enzyme Inhib Med Chem. 2021; 36(1):561–580.
  • Angeli A, Carta F, Nocentini A, Winum JY, Zalubovskis R, Akdemir A, Onnis V, Eldehna WM, Capasso C, Simone G, et al. Carbonic anhydrase inhibitors targeting metabolism and tumor Mi-croenvironment. Metabolites. 2020;10(10):412.
  • Supuran CT, Capasso C. Antibacterial carbonic anhydrase inhibitors: an update on the recent literature. Expert Opin Ther Pat. 2020;30(12):963–982.
  • Supuran CT. Multitargeting approaches involving carbonic anhydrase inhibitors: hybrid drugs against a variety of disorders. J Enzyme Inhib Med Chem. 2021;36(1):1702–1714.
  • Capasso C, Supuran CT. An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria: can bacterial car-bonic anhydrases shed new light on evolution of bacteria? J Enzyme Inhib Med Chem. 2015;30(2):325–332.
  • Angeli A, Pinteala M, Maier SS, Del Prete S, Capasso C, Simionescu BC, Supuran CT. Inhibition of α-, β-, γ-, δ-, ζ- and η-class carbonic anhydrases from bacteria, fungi, algae, diatoms and protozoans with famotidine. J Enzyme Inhib Med Chem. 2019;34(1):644–650.
  • (a) Supuran CT, Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov. 2008;7(2):168–181. (b) Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov. 2011;10(10):767–777.
  • Supuran CT. Carbonic anhydrase inhibition and the management of neuropathic pain. Expert Rev Neurother. 2016;16(8):961–968.
  • Bozdag M, Altamimi ASA, Vullo D, Supuran CT, Carta F. State of the Art on Carbonic Anhydrase Modulators for Biomedi-cal Purposes. CMC. 2019;26(15):2558–2573.
  • Supuran CT. Exploring the multiple binding modes of inhibitors to carbonic anhydrases for novel drug discovery. Expert Opin Drug Discov. 2020;15(6):671–686.
  • Supuran CT. Carbonic Anhydrase Inhibitors from Marine Natural Products. Mar. Drugs. 2022;20(11):721.
  • Scozzafava A, Menabuoni L, Mincione F, Briganti F, Mincione G, Supuran CT. Carbonic anhydrase inhibitors. 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(14):2641–2650.
  • Leitans J, Sprudza A, Tanc M, Vozny I, Zalubovskis R, Tars K, Supuran CT. Supuran CT. 5-Substituted-(1,2,3-triazol-4-yl)thiophene-2-sulfonamides strongly inhibit human carbonic anhydrases I, II, IX and XII: solu-tion and X-ray crystallographic studies. Bioorg Med Chem. 2013;21(17):5130–5138.
  • Pala N, Micheletto L, Sechi M, Aggarwal M, Carta F, McKenna R, Supuran CT. Carbonic Anhydrase Inhibition with Ben-zenesulfonamides and Tetrafluorobenzenesulfonamides Obtained via Click Chemistry. ACS Med Chem Lett. 2014;5(8):927–930.
  • Swain B, Angeli A, Angapelly S, Thacker PS, Singh P, Supuran CT, Arifuddin M. Synthesis of a new series of 3-functionalised-1-phenyl-1,2,3-triazole sulfamoylbenzamides as carbonic anhydrase I, II, IV and IX inhibitors. J Enzyme Inhib Med Chem. 2019;34(1):1199–1209.
  • Aimene Y, Eychenne R, Mallet-Ladeira S, Saffon N, Winum JY, Nocentini A, Supuran CT, Benoist E, Seridi A. Novel Re(I) tricarbonyl coordination compounds based on 2-pyridyl-1,2,3-triazole derivatives bearing a 4-amino-substituted benzene-sulfonamide arm: synthesis, crystal structure, computational studies and inhibitory activity against carbonic anhydrase I, II, and IX isoforms. J Enzyme Inhib Med Chem. 2019; 34:773–782.
  • Singh P, Swain B, Thacker PS, Sigalapalli DK, Purnachander Yadav P, Angeli A, Supuran CT, Arifuddin M. Synthesis and carbonic anhydrase inhibition studies of sulfonamide based indole-1,2,3-triazole chalcone hybrids. Bioorg Chem. 2020; 99:103839.
  • Manzoor S, Petreni A, Raza MK, Supuran CT, Hoda N. Novel triazole-sulfonamide bearing pyrimidine moieties with carbonic anhydrase inhibitory action: Design, synthesis, computational and enzyme inhibition studies. Bioorg Med Chem Lett. 2021; 48:128249.
  • Ismail C, Nocentini A, Supuran CT, Winum JY, Gharbi R. 1,5-Benzodiazepines as a platform for the design of carbonic anhydrase inhibitors. Arch Pharm (Weinheim)). 2022;355(3):e2100405.
  • Ewies EF, Sabry E, Bekheit MS, Fouad MA, Vullo D, Supuran CT. Click chemistry-based synthesis of new benzenesulfonamide derivatives bearing triazole ring as selective carbonic anhydrase II inhibitors. Drug Dev Res. 2022;83(6):1281–1291.
  • Maresca A, Temperini C, Vu H, Pham NB, Poulsen SA, Scozzafava A, Quinn RJ, Supuran CT. Non-zinc mediated inhibition of carbonic anhydrases: coumarins are a new class of suicide inhibitors. J Am Chem Soc. 2009;131(8):3057–3062.
  • (a) Supuran CT. Coumarin carbonic anhydrase inhibitors from natural sources. J Enzyme Inhib Med Chem. 2020;35(1):1462–1470. (b) Supuran CT. Coumarins as carbonic anhydrase inhibitors. In: Carradori S. editor. Flavonoids and phenolics. Singapore: Bentham Science Publishers; 2022, p. 298–329.
  • Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem. 2016;31(3):345–360.
  • Nocentini A, Carta F, Ceruso M, Bartolucci G, Supuran CT. Click-tailed coumarins with potent and selective inhibitory ac-tion against the tumor-associated carbonic anhydrases IX and XII. Bioorg Med Chem. 2015;23(21):6955–6966.
  • Kumar A, Siwach K, Supuran CT, Sharma PK. A decade of tail-approach based design of selective as well as potent tumor associated carbonic anhydrase inhibitors. Bioorg Chem. 2022; 126:105920.
  • Nocentini A, Carta F, Tanc M, Selleri S, Supuran CT, Bazzicalupi C, Gratteri P. Deciphering the Mechanism of Human Carbonic Anhydrases Inhibition with Sulfocoumarins: Computational and Experimental Studies. Chemistry. 2018;24(31):7840–7844.
  • Tars K, Vullo D, Kazaks A, Leitans J, Lends A, Grandane A, Zalubovskis R, Scozzafava A, Supuran CT. 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(1):293–300.
  • Grandane A, Tanc M, Zalubovskis R, Supuran CT. 6-Triazolyl-substituted sulfocoumarins are potent, selective inhibitors of the tumor-associated carbonic anhydrases IX and XII. Bioorg Med Chem Lett. 2014;24(5):1256–1260.
  • 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(8):2561–2573.
  • Nocentini A, Ceruso M, Carta F, Supuran CT. 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(6):1226–1233.
  • Tanc M, Carta F, Bozdag M, Scozzafava A, Supuran CT. 7-Substituted-sulfocoumarins are isoform-selective, potent carbonic anhydrase II inhibitors. Bioorg Med Chem. 2013;21(15):4502–4510.
  • Murray AB, Lomelino CL, Supuran CT, McKenna R. Seriously Sweet": Acesulfame K Exhibits Selective Inhibition Using Alternative Binding Modes in Carbonic Anhydrase Isoforms. J Med Chem. 2018;61(3):1176–1181.
  • Köhler K, Hillebrecht A, Schulze Wischeler J, Innocenti A, Heine A, Supuran CT, Klebe G. Saccharin inhibits carbonic anhy-drases: possible explanation for its unpleasant metallic aftertaste. Angew Chem Int Ed Engl. 2007;46(40):7697–7699.
  • Lopez M, Salmon AJ, Supuran CT, Poulsen SA. Carbonic anhydrase inhibitors developed through 'click tailing’. Curr Pharm Des. 2010;16(29):3277–3287.
  • Moeker J, Peat TS, Bornaghi LF, Vullo D, Supuran CT, Poulsen SA. Cyclic secondary sulfonamides: unusually good inhibi-tors of cancer-related carbonic anhydrase enzymes. J Med Chem. 2014;57(8):3522–3531.
  • Saada MC, Ombouma J, Montero JL, Supuran CT, Winum JY. Thiol-ene click chemistry for the synthesis of highly effective glycosyl sulfonamide carbonic anhydrase inhibitors. Chem Commun. 2013;49(50):5699–5701.
  • (a) Capasso C, Supuran CT. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin Ther Targets. 2015;19(12):1689–1704., (b) De Luca V, Giovannuzzi S, Supuran CT, Capasso C. May sulfonamide inhibitors of carbonic anhydrases from Mammaliicoccus sciuri prevent antimicrobial resistance due to gene transfer to other harmful staphylococci? IJMS. 2022;23(22):13827.
  • (a) Supuran CT, Capasso C. Biomedical applications of prokaryotic carbonic anhydrases. Expert Opin Ther Pat. 2018;28(10):745–754. (b) Angeli A, Urbański LJ, Capasso C, Parkkila S, Supuran CT. Activation studies with amino acids and amines of a β-carbonic anhydrase from Mammaliicoccus (Staphylococcus) sciuri previously annotated as Staphylococcus aureus (SauBCA) carbonic anhydrase. J Enzyme Inhib Med Chem. 2022;37(1):2786–2792.
  • Da’dara AA, Angeli A, Ferraroni M, Supuran CT, Skelly PJ. Crystal structure and chemical inhibition of essential schistosome host-interactive virulence factor carbonic anhydrase SmCA. Commun Biol. 2019; 2:333.
  • Bua S, Osman SM, Del Prete S, Capasso C, AlOthman Z, Nocentini A, Supuran CT. Click-tailed benzenesulfonamides as potent bacterial carbonic anhydrase inhibitors for targeting Mycobacterium tuberculosis and Vibrio cholerae. Bioorg Chem. 2019; 86:183–186.
  • Fisher GM, Tanpure RP, Douchez A, Andrews KT, Poulsen SA. Synthesis and evaluation of antimalarial properties of novel 4-aminoquinoline hybrid compounds. Chem Biol Drug Des. 2014;84(4):462–472.
  • (a) Krungkrai J, Krungkrai SR, Supuran CT. Carbonic anhydrase inhibitors: inhibition of Plasmodium falciparum carbonic anhydrase with aromatic/heterocyclic sulfonamides-in vitro and in vivo studies. Bioorg Med Chem Lett. 2008;18(20):5466–5471. (b) Vullo D, Del Prete S, Fisher GM, Andrews KT, Poulsen SA, Capasso C, Supuran CT. Sulfonamide inhibition studies of the η-class carbonic anhydrase from the malaria pathogen Plasmodium falciparum. Bioorg Med Chem. 2015;23(3):526–531.
  • Campos NSP, Souza BS, Silva GCPD, Porto VA, Chalbatani GM, Lagreca G, Janji B, Suarez ER. Carbonic Anhydrase IX: A Renewed Target for Cancer Immunotherapy. Cancers. 2022;14(6):1392.
  • Tian Y, Liang Z, Xu H, Mou Y, Guo C. Design, synthesis and cytotoxicity of novel dihydroartemisinin-coumarin hybrids via click chemistry. Molecules. 2016;21(6):758.
  • Berrino E, Angeli A, Zhdanov DD, Kiryukhina AP, Milaneschi A, De Luca A, Bozdag M, Carradori S, Selleri S, Bartolucci G, et al. Azidothymidine "Clicked" into 1,2,3-Triazoles: first report on carbonic anhy-drase-telomerase dual-hybrid inhibitors. J Med Chem. 2020;63(13):7392–7409.
  • Hao S, Cheng X, Wang X, An R, Xu H, Guo M, Li C, Wang Y, Hou Z, Guo C. Design, synthesis and biological evaluation of novel carbohydrate-based sulfonamide derivatives as antitumor agents. Bioorg Chem. 2020; 104:104237.
  • Chu N, Wang Y, Jia H, Han J, Wang X, Hou Z. Design, synthesis and biological evaluation of new carbohydrate-based coumarin derivatives as selective carbonic anhydrase IX inhibitors via "Click" reaction. Molecules. 2022;27(17):5464.
  • Tatiparti K, Sau S, Gawde KA, Iyer AK. Copper-Free 'Click’ chemistry-based synthesis and characterization of carbonic anhydrase-IX anchored albumin-paclitaxel nanoparticles for targeting tumor hypoxia. IJMS. 2018;19(3):838.
  • Alsaab HO, Sau S, Alzhrani RM, Cheriyan VT, Polin LA, Vaishampayan U, Rishi AK, Iyer AK. Tumor hypoxia directed mul-timodal nanotherapy for overcoming drug resistance in renal cell carcinoma and reprogramming macrophages. Biomaterials. 2018; 183:280–294.
  • Mocharla VP, Walsh JC, Padgett HC, Su H, Fueger B, Weber WA, Czernin J, Kolb HC. From in situ to in vivo: an in situ click-chemistry-derived carbonic anhydrase II imaging agent for positron emission tomography. ChemMedChem. 2013;8(1):43–48.
  • Chun JH, Lu S, Lee YS, Pike VW. Fast and high-yield microreactor syntheses of ortho-substituted [(18)F]fluoroarenes from reactions of [(18)F]fluoride ion with diaryliodonium salts. J Org Chem. 2010;75(10):3332–3338.
  • Christie KN, Thomson C. The distribution of carbonic anhydrase II in human, pig and rat oesophageal epithelium. Histochem J. 2000;32(12):753–757.
  • Supuran CT. Structure and function of carbonic anhydrases. Biochem J. 2016;473(14):2023–2032.
  • Jia L, Li X, Cheng D, Zhang L. Fluorine-18 click radiosynthesis and microPET/CT evaluation of a small peptide-a potential PET probe for carbonic anhydrase IX. Bioorg Med Chem. 2019;27(5):785–789.
  • Rana S, Nissen F, Lindner T, Altmann A, Mier W, Debus J, Haberkorn U, Askoxylakis V. Screening of a novel peptide tar-geting the proteoglycan-like region of human carbonic anhydrase IX. Mol Imaging. 2013;12(8). DOI:10.2310/7290.2013.00066.
  • Chen KT, Nguyen K, Ieritano C, Gao F, Seimbille Y. A flexible synthesis of 68Ga-labeled carbonic anhydrase IX (CAIX)-targeted molecules via CBT/1,2-aminothiol click reaction. Molecules. 2018;24(1):23.
  • Jeon J, Shen B, Xiong L, Miao Z, Lee KH, Rao J, Chin FT. Efficient method for site-specific 18F-labeling of biomole-cules using the rapid condensation reaction between 2-cyanobenzothiazole and cysteine. Bioconjug Chem. 2012;23(9):1902–1908.
  • Gao F, Ieritano C, Chen KT, Dias GM, Rousseau J, Bénard F, Seimbille Y. Two bifunctional desferrioxamine che-lators for bioorthogonal labeling of biovectors with zirconium-89. Org Biomol Chem. 2018;16(28):5102–5106.
  • Sakurai K, Yamada R, Okada A, Tawa M, Ozawa S, Inoue M. Selective fluorescence detection of small-molecule-binding proteins by using a dual photoaffinity labeling system. Chembiochem. 2013;14(4):421–425.
  • Teruya K, Rankin GM, Chrysanthopoulos PK, Tonissen KF, Poulsen SA. Characterisation of Photoaffinity-Based Chemical Probes by Fluorescence Imaging and Native-State Mass Spectrometry. Chembiochem. 2017;18(8):739–754.
  • Park H, Koo JY, Srikanth YV, Oh S, Lee J, Park J, Park SB. Nonspecific protein labeling of photoaffinity linkers correlates with their molecular shapes in living cells. Chem Commun. 2016;52(34):5828–5831.
  • Zhao B, Burgess K. Click-addressable cassette for photoaffinity labeling. ACS Med Chem Lett. 2018;9(2):155–158.
  • Lou Y, McDonald PC, Oloumi A, Chia S, Ostlund C, Ahmadi A, Kyle A, Auf Dem Keller U, Leung S, Huntsman D, et al. Targeting tumor hypoxia: suppression of breast tumor growth and metastasis by novel carbonic anhydrase IX inhibitors. Cancer Res. 2011;71(9):3364–3376.
  • Mori K, Sakurai K. Clickable gold-nanoparticles as generic probe precursors for facile photoaffinity labeling application. Org Biomol Chem. 2021;19(6):1268–1273.
  • Ji X, Ji K, Chittavong V, Aghoghovbia RE, Zhu M, Wang B. Click and fluoresce: a bioorthogonally activated smart probe for wash-free fluorescent labeling of biomolecules. J Org Chem. 2017;82(3):1471–1476.
  • Lossouarn A, Puteaux C, Bailly L, Tognetti V, Joubert L, Renard PY, Sabot C. Metalloenzyme-mediated thiol-Yne addition towards photoisomerizable fluorescent dyes. Chemistry. 2022; 21:e202202180.
  • Svastová E, Hulíková A, Rafajová M, Zat’ovicová M, Gibadulinová A, Casini A, Cecchi A, Scozzafava A, Supuran CT, Pas-Torek J, et al. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett. 2004;577(3):439–445.
  • Carta F, Ferraroni M, Scozzafava A, Supuran CT. Fluorescent sulfonamide carbonic anhydrase inhibitors incorporating 1,2,3-triazole moieties: Kinetic and X-ray crystallographic studies. Bioorg Med Chem. 2016;24(2):104–112.
  • Alterio V, Vitale RM, Monti SM, Pedone C, Scozzafava A, Cecchi A, De Simone G, Supuran CT. Carbonic anhydrase inhibi-tors: 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(25):8329–8335.
  • (a) Supuran CT. Carbonic anhydrase inhibitors as emerging agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs. 2018;27(12):963–970. (b) Supuran CT. Carbonic anhydrase inhibitors: an update on experimental agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs. 2021;30(12):1197–1208.
  • Compain P. Multivalent Effect in Glycosidase Inhibition: The End of the Beginning. Chem Rec. 2020;20(1):10–22.
  • Abellán-Flos M, Tanç M, Supuran CT, Vincent SP. Exploring carbonic anhydrase inhibition with multimeric coumarins displayed on a fullerene scaffold. Org Biomol Chem. 2015;13(27):7445–7451.
  • Abellán-Flos M, Tanç M, Supuran CT, Vincent SP. Multimeric xanthates as carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2016;31(6):946–952.
  • Mustafa S, Hamid A, Naeem A, Sultana Q. Effect of pH, temperature and time on the stability of potassium ethyl xanthate. J Chem Soc Pak. 2004; 26:363–365.
  • Kanfar N, Tanc M, Dumy P, Supuran CT, Ulrich S, Winum JY. Effective access to multivalent inhibitors of carbonic anhydrases promoted by peptide bioconjugation. Chemistry. 2017;23(28):6788–6794.
  • Merabti A, Roger M, Nguyen C, Nocentini A, Gerbier P, Richeter S, Gary-Bobo M, Supuran CT, Clement S, Winum JY. Carbonic anhydrase inhibitors featuring a porphyrin scaffold: synthesis, optical and biological properties. Chemistry. 2022; 21:e202101538.
  • (a) Supuran CT. Carbonic anhydrase inhibitors: an update on experimental agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs. 2021;30(12):1197–1208.
  • McDonald PC, Chafe SC, Supuran CT, Dedhar S. Cancer Therapeutic Targeting of Hypoxia Induced Carbonic Anhydrase IX: From Bench to Bedside. Cancers (Basel). 2022; 14(14):3297.
  • (a) Supuran CT. Anti-obesity carbonic anhydrase inhibitors: challenges and opportunities. J Enzyme Inhib Med Chem. 2022;37(1):2478–2488. (b) Supuran CT. Carbonic anhydrases and metabolism. Metabolites. 2018;8(2):25.
  • (a) Carta F, Supuran CT. Diuretics with carbonic anhydrase inhibitory action: a patent and literature review (2005 - 2013). Expert Opin Ther Pat. 2013;23(6):681–691. (b) Supuran CT. Diuretics: from classical carbonic anhydrase inhibitors to novel applications of the sulfonamides. Curr Pharm Des. 2008;14(7):641–648.
  • (a) Thiry A, Dogné JM, Supuran CT, Masereel B. Anticonvulsant sulfonamides/sulfamates/sulfamides with carbonic anhydrase inhibitory activity: drug design and mechanism of action. Curr Pharm Des. 2008;14(7):661–671. (b) De Simone G, Scozzafava A, Supuran CT. Which carbonic anhydrases are targeted by the antiepileptic sulfonamides and sulfamates? Chem Biol Drug Des. 2009;74(3):317–321.
  • Supuran CT. Acetazolamide for the treatment of idiopathic intracranial hypertension. Expert Rev Neurother. 2015;15(8):851–856.
  • Supuran CT. Bacterial carbonic anhydrases as drug targets: toward novel antibiotics? Front Pharmacol. 2011;2:34.
  • (a) Del Prete S, Nocentini A, Supuran CT, Capasso C. Bacterial ι-carbonic anhydrase: a new active class of carbonic anhydrase identified in the genome of the Gram-negative bacterium Burkholderia territorii. J Enzyme Inhib Med Chem. 2020;35(1):1060–1068. (b) De Luca V, Carginale V, Supuran CT, Capasso C. The gram-negative bacterium Escherichia coli as a model for testing the effect of carbonic anhydrase inhibition on bacterial growth. J Enzyme Inhib Med Chem. 2022;37(1):2092–2098., (c) Nocentini A, Supuran CT, Capasso C. An overview on the recently discovered iota-carbonic anhydrases. J Enzyme Inhib Med Chem. 2021;36(1):1988–1995.
  • (a) An W, Holly KJ, Nocentini A, Imhoff RD, Hewitt CS, Abutaleb NS, Cao X, Seleem MN, Supuran CT, Flaherty DP. Structure-activity relationship studies for inhibitors for vancomycin-resistant Enterococcus and human carbonic anhydrases. J Enzyme Inhib Med Chem. 2022;37(1):1838–1844. (b) Giovannuzzi S, Hewitt CS, Nocentini A, Capasso C, Costantino G, Flaherty DP, Supuran CT. Inhibition studies of bacterial α-carbonic anhydrases with phenols. J Enzyme Inhib Med Chem. 2022;37(1):666–671. (c) Giovannuzzi S, Hewitt CS, Nocentini A, Capasso C, Flaherty DP, Supuran CT. Coumarins effectively inhibit bacterial α-carbonic anhydrases. J Enzyme Inhib Med Chem. 2022;37(1):333–338.
  • (a) Abutaleb NS, Elhassanny AEM, Nocentini A, Hewitt CS, Elkashif A, Cooper BR, Supuran CT, Seleem MN, Flaherty DP. Repurposing FDA-approved sulphonamide carbonic anhydrase inhibitors for treatment of Neisseria gonorrhoeae. J Enzyme Inhib Med Chem. 2022;37(1):51–61. (b) Flaherty DP, Seleem MN, Supuran CT. Bacterial carbonic anhydrases: underexploited antibacterial therapeutic targets. Future Med Chem. 2021;13(19):1619–1622. (c) Nocentini A, Hewitt CS, Mastrolorenzo MD, Flaherty DP, Supuran CT. Anion inhibition studies of the α-carbonic anhydrases from Neisseria gonorrhoeae. J Enzyme Inhib Med Chem. 2021;36(1):1061–1066.
  • (a) Hewitson KS, Vullo D, Scozzafava A, Mastrolorenzo A, Supuran CT. Molecular cloning, characterization, and inhibition studies of a β-carbonic anhydrase from Malassezia globosa, a potential antidandruff target. J Med Chem. 2012;55(7):3513–3520. (b) Abdoli M, De Luca V, Capasso C, Supuran CT, Žalubovskis R. Benzenesulfonamides incorporating hydantoin moieties effectively inhibit eukaryoticand human carbonic anhydrases. IJMS. 2022;23(22):14115.
  • (a) Angeli A, Velluzzi A, Selleri S, Capasso C, Spadini C, Iannarelli M, Cabassi CS, Carta F, Supuran CT. Seleno containing compounds as potent and selective antifungal agents. ACS Infect Dis. 2022;8(9):1905–1919. (b) De Luca V, Angeli A, Mazzone V, Adelfio C, Carginale V, Scaloni A, Carta F, Selleri S, Supuran CT, Capasso C. Heterologous expression and biochemical characterisation of the recombinant β-carbonic anhydrase (MpaCA) from the warm-blooded vertebrate pathogen malassezia pachydermatis. J Enzyme Inhib Med Chem. 2022;37(1):62–68.
  • (a) Supuran CT, Capasso C. A highlight on the inhibition of fungal carbonic anhydrases as drug targets for the antifungal armamentarium. IJMS. 2021; 22(9):4324. (b) Del Prete S, Angeli A, Ghobril C, Hitce J, Clavaud C, Marat X, Supuran CT, Capasso C. Sulfonamide inhibition profile of the β-carbonic anhydrase from Malassezia restricta, an opportunistic pathogen triggering scalp conditions. Metabolites. 2020;10(1):39.
  • Supuran CT. Carbonic anhydrase activators. Future Med Chem. 2018;10(5):561–573.
  • (a) Canto de Souza L, Provensi G, Vullo D, Carta F, Scozzafava A, Costa A, Schmidt SD, Passani MB, Supuran CT, Blandina P. Carbonic anhydrase activation enhances object recognition memory in mice through phosphorylation of the extracellular signal-regulated kinase in the cortex and the hippocampus. Neuropharmacology. 2017;118:148–156. (b) Blandina P, Provensi G, Passsani MB, Capasso C, Supuran CT. Carbonic anhydrase modulation of emotional memory. Implications for the treatment of cognitive disorders. J Enzyme Inhib Med Chem. 2020;35(1):1206–1214. (c) Schmidt SD, Costa A, Rani B, Godfried Nachtigall E, Passani MB, Carta F, Nocentini A, de Carvalho Myskiw J, Furini CRG, Supuran CT, et al. The role of carbonic anhydrases in extinction of contextual fear memory. Proc Natl Acad Sci USA. 2020; 117(27):16000–16008.
  • (a) Provensi G, Nocentini A, Passani MB, Blandina P, Supuran CT. Activation of carbonic anhydrase isoforms involved in modulation of emotional memory and cognitive disorders with histamine agonists, antagonists and derivatives. J Enzyme Inhib Med Chem. 2021;36(1):719–726. (b) Schmidt SD, Nachtigall EG, Marcondes LA, Zanluchi A, Furini CRG, Passani MB, Supuran CT, Blandina P, Izquierdo I, Provensi G, et al. Modulation of carbonic anhydrases activity in the hippocampus or prefrontal cortex differentially affects social recognition memory in rats. Neuroscience. 2022;497:184–195. (c) Provensi G, Costa A, Rani B, Becagli MV, Vaiano F, Passani MB, Tanini D, Capperucci A, Carradori S, Petzer JP, et al. New β-arylchalcogeno amines with procognitive properties targeting Carbonic Anhydrases and Monoamine Oxidases. Eur J Med Chem. 2022;244:114828.