Diversely substituted sulfamides for fragment-based drug discovery of carbonic anhydrase inhibitors: synthesis and inhibitory profile

References

• 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
• Alterio V, Di Fiore A, D’Ambrosio K, et al. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem Rev 2012;112:4421–68.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Structure-based drug discovery of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2012;27:759–72.
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Supuran CT. Glaucoma and the applications of carbonic anhydrase inhibitors. Subcell Biochem 2014;75:349–59.
   PubMedGoogle Scholar
• Supuran CT. Acetazolamide for the treatment of idiopathic intracranial hypertension. Expert Rev Neurother 2015;15:851–6.
   PubMed Web of Science ®Google Scholar
• Swenson ER. Carbonic anhydrase inhibitros and high altitude ilnesses. Subcell Biochem 2014;75:361–86.
   PubMedGoogle Scholar
• Wongboonsin J, Thongprayoon C, Bathini T, et al. Acetazolamide therapy in patients with heart failure: a meta-analysis. J Clin Med 2019;8:349.
   PubMedGoogle Scholar
• Buzás GM, Supuran CT. The history and rationale of using carbonic anhydrase inhibitors in the treatment of peptic ulcers. In memoriam Ioan Puşcaş (1932–2015). J Enzyme Inhib Med Chem 2016;31:527–33.
   PubMed Web of Science ®Google Scholar
• Ciccone L, Cerri C, Nencetti S, Orlandini E. Carbonic anhydrase and epilepsy: state of the art and future perspectives. Molecules 2021;26:6380.
   PubMed Web of Science ®Google Scholar
• Mboge MY, McKenna R, Frost SC. Advances in anti-cancer drug development targeting carbonic anhydrase IX and XII. Top Anticancer Res 2015;5:3–42.
   PubMedGoogle Scholar
• Ward C, Meehan J, Gray ME, et al. The impact of tumour pH on cancer progression: strategies for clinical intervention. Explor Target Antitumor Ther 2020;1:71–100.
   PubMedGoogle Scholar
• Carta F, Vullo D, Osman SM, et al. Synthesis and carbonic anhydrase inhibition of a series of SLC-0111 analogs. Bioorg Med Chem 2017;25:2569–76.
   PubMed Web of Science ®Google Scholar
• https://clinicaltrials.gov/ct2/show/NCT03450018 [last accessed 14 Jan 2022].
   Google Scholar
• Assi R, Kantarjian H, Kadia TM, et al. Final results of a phase 2, open-label study of Indisulam, idarubicin, and cytarabine in patients with relapsed or refractory acute myeloid leukemia and high-risk myelodysplastic syndrome. Cancer 2018;124:2758–65.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Capasso C. Antibacterial carbonic anhydrase inhibitors: an update on the recent literature. Exp Opin Ther Pat 2020;30:963–82.
   PubMed Web of Science ®Google Scholar
• De Vita D, Angeli A, Pandofi F, et al. Inhibition of the α-carbonic anhydrase from Vibrio cholerae with amides and sulfonamides incorporating imidazole moieties. J Enzyme Inhib Med Chem 2017;32:798–804.
   PubMed Web of Science ®Google Scholar
• Rasti B, Mazraedoost S, Panahi H, et al. New insights into the selective inhibition of the β-carbonic anhydrases of pathogenic bacteria Burkholderia pseudomallei and Francisella tularensis: a proteochemometrics study. Mol Divers 2019;23:263–73.
   PubMed Web of Science ®Google Scholar
• Aspatwar A, Winum J-Y, Carta F, et al. Carbonic anhydrase inhibitors as novel drugs against mycobacterial β-carbonic anhydrases: an update on in vitro and in vivo studies. Molecules 2018;23:2911.
   PubMed Web of Science ®Google Scholar
• Nishimori I, Minakuchi T, Vullo D, et al. Inhibition studies of the β-carbonic anhydrases from the bacterial pathogen Salmonella enterica serovar Typhimurium with sulfonamides and sulfamates. Bioorg Med Chem 2011;19:5023–30.
   PubMed Web of Science ®Google Scholar
• Grande R, Carradori S, Puca V, et al. Selective inhibition of Helicobacter pylori carbonic anhydrases by carvacrol and thymol could impair biofilm production and the release of outer membrane vesicles. Int J Mol Sci 2021;22:11583.
   PubMed Web of Science ®Google Scholar
• Del Prete S, De Luca V, Bua S, et al. The effect of substituted benzene-sulfonamides and clinically licensed drugs on the catalytic activity of CynT2, a carbonic anhydrase crucial for Escherichia coli life cycle. Int J Mol Sci 2020;21:4175.
   PubMed Web of Science ®Google Scholar
• Winum J-Y, Scozzafava A, Montero J-L, Supuran CT. New zinc binding motifs in the design of selective carbonic anhydrase inhibitors. Mini-Rev Med Chen 2006;6:921–36.
   PubMed Web of Science ®Google Scholar
• Yue EW, Sparks R, Polam P, et al. INCB24360 (Epacadostat), a highly potent and selective indoleamine-2,3-dioxygenase 1 (IDO1) inhibitor for immuno-oncology. ACS Med Chem Lett 2017;8:486–91.
   PubMed Web of Science ®Google Scholar
• Langtry HD, Grant SM, Goa KL. Famotidine. An updated review of its pharmacodynamic and pharmacokinetic properties, and therapeutic use in peptic ulcer disease and other allied diseases. Drugs 1989;38:551–90.
   PubMed Web of Science ®Google Scholar
• Angeli A, Ferraroni M, Nocentini A, et al. Polypharmacology of epacadostat: a potent and selective inhibitor of the tumor associated carbonic anhydrases IX and XII. Chem Commun (Camb) 2019;55:5720–3.
   PubMed Web of Science ®Google Scholar
• Angeli A, Ferraroni M, Supuran CT. Famotidine, an antiulcer agent, strongly inhibits Helicobacter pylori and human carbonic anhydrases. ACS Med Chem Lett 2018;9:1035–8.
   PubMed Web of Science ®Google Scholar
• Krasavin M, Kalinin S, Zozulya S, et al. Screening of benzenesulfonamide in combination with chemically diverse fragments against carbonic anhydrase by differential scanning fluorimetry. J Enzyme Inhib Med Chem 2020;35:306–10.
   PubMed Web of Science ®Google Scholar
• Li Q. Application of fragment-based drug discovery to versatile targets. Front Mol Biosci 2020;7:180.
   PubMed Web of Science ®Google Scholar
• According to the Reaxys database, only 9,106 sulfamides (NSO2NH2) were associated with the keywords “carbonic anhydrase inhibitor” compared to 108,988 sulfonamides searchable in the same context (information retrieved on January 18, 2022).
   Google Scholar
• Bonardi A, Nocentini A, Bua S, et al. Sulfonamide inhibitors of human carbonic anhydrases designed through a three-tails approach: improving ligand/isoform matching and selectivity of action. J Med Chem 2020;63:7422–44.
   PubMed Web of Science ®Google Scholar
• Ferreira LG, Andricopulo AD. From protein structure to small-molecules: recent advances and applications to fragment-based drug discovery. Curr Top Med Chem 2017;17:2260–70.
   PubMed Web of Science ®Google Scholar
• Xu Z, Tice CM, Zhao W, et al. Structure-based design and synthesis of 1,3-oxazinan-2-one inhibitors of 11β-hydroxysteroid dehydrogenase type 1. J Med Chem 2011;54:6050–62.
   PubMed Web of Science ®Google Scholar
• Casini A, Winum J-Y, Montero J-L, et al. Carbonic anhydrase inhibitors: inhibition of cytosolic isozymes I and II with sulfamide derivatives. Bioorg. Med. Chem. Lett 2003;13:837–40.
   PubMed Web of Science ®Google Scholar
• https://www.molinspiration.com/.
   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;246:2561–73.
   PubMed Web of Science ®Google Scholar
• Wilkinson BL, Bornaghi LF, Houston TA, et al. A novel class of carbonic anhydrase inhibitors: glycoconjugate benzene sulfonamides prepared by “click-tailing”. J Med Chem 2006;49:6539–48.
   PubMed Web of Science ®Google Scholar
• Lopez M, Salmon AJ, Supuran CT, Poulsen S-A. Carbonic anhydrase inhibitors developed through ‘click tailing’. Curr Pharm Des 2010;16:3277–87.
   PubMed Web of Science ®Google Scholar
• Wilkinson BL, Bornaghi LF, Houston TA, et al. Carbonic anhydrase inhibitors: inhibition of isozymes I, II, and IX with triazole-linked O-glycosides of benzene sulfonamides. J Med Chem 2007;50:1651–7.
   PubMed Web of Science ®Google Scholar
• Pala N, Micheletto L, Sechi M, et al. Carbonic anhydrase inhibition with benzenesulfonamides and tetrafluorobenzenesulfonamides obtained via click chemistry. ACS Med Chem Lett 2014;5:927–30.
   PubMed Web of Science ®Google Scholar
• Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 1997;53:240–55.
   PubMed Web of Science ®Google Scholar
• Emsley P, Lohkamp B, Scott W, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 2010;66:486–501.
   PubMed Web of Science ®Google Scholar
• Lamzin VS, Perrakis A, Wilson KS. The ARP/WARP suite for automated construction and refinement of protein models. In: Rossmann MG, Arnold E, eds. Int. Tables for crystallography. Vol. F: Crystallography of biological macromolecules. Dordrecht, The Netherlands: Kluwer Academic Publishers; 2001:720–722.
   Google Scholar
• Lovell SC, Davis IW, Arendall WB, III, et al. Structure validation by Cα geometry: ϕ,ψ and Cβ deviation. Proteins Struct Funct Genet 2003;50:437–50.
   PubMed Web of Science ®Google Scholar
• Pettersen EF, Goddard TD, Huang CC, et al. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 2004;25:1605–12.
   PubMed Web of Science ®Google Scholar