1,187
Views
7
CrossRef citations to date
0
Altmetric
Research Paper

Novel thiazolone-benzenesulphonamide inhibitors of human and bacterial carbonic anhydrases

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Article: 2163243 | Received 25 Nov 2022, Accepted 22 Dec 2022, Published online: 11 Jan 2023

References

  • Supuran CT. Structure and function of carbonic anhydrases. Biochem J. 2016;473(14):2023–2032.
  • Supuran CT, Scozzafava A. Carbonic anhydrases as targets for medicinal chemistry. Bioorg Med Chem. 2007;15(13):4336–4350.
  • Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov. 2008;7(2):168–181.
  • Alterio V, Di Fiore A, D'Ambrosio K, Supuran CT, De Simone G. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem Rev. 2012;112(8):4421–4468.
  • Scott KA, Njardarson JT. Analysis of US FDA-approved drugs containing sulfur atoms. Top Curr Chem. 2018;376(1):5.
  • (a) Capasso C, Supuran CT. Anti-infective carbonic anhydrase inhibitors: a patent and literature review. Expert Opin Ther Pat. 2013;23(6):693–704. (b) 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(2):325–332. (c) Supuran CT, Capasso C. An overview of the bacterial carbonic anhydrases. Metabolites. 2017;7(4):56.
  • Smith DA, Jones RM. The sulfonamide group as a structural alert: a distorted story? Curr Opin Drug Discov Dev. 2008;11(1):72–79.
  • (a) Supuran CT, Scozzafava A, Casini A. Carbonic anhydrase inhibitors. Med Res Rev. 2003;23(2):146–189. (b) Carta F, Supuran CT, Scozzafava A. Sulfonamides and their isosters as carbonic anhydrase inhibitors. Future Med Chem. 2014;6(10):1149–1165.
  • (a) Grandane A, Tanc M, Zalubovskis R, Supuran CT. 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(5):1522–1528. (b) 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. (c) 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 microenvironment. Metabolites. 2020;10:412. (d) Ivanova J, Carta F, Vullo D, Leitans J, Kazaks A, Tars K, Žalubovskis R, Supuran CT. N-Substituted and ring opened saccharin derivatives selectively inhibit transmembrane, tumor-associated carbonic anhydrases IX and XII. Bioorg Med Chem. 2017;25(13):3583–3589. (e) Grandāne A, Nocentini A, Domračeva I, Žalubovskis R, Supuran CT. Development of oxathiino [6, 5-b] pyridine 2, 2-dioxide derivatives as selective inhibitors of tumor-related carbonic anhydrases IX and XII. Eur J Med Chem. 2020;200:112300. (f) 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;36:561–580. (g) Grandane A, Nocentini A, Werner T, Zalubovskis R, Supuran CT. Benzoxepinones: a new isoform-selective class of tumor associated carbonic anhydrase inhibitors. Bioorg Med Chem. 2020;28(11):115496. (h) Podolski-Renić A, Dinić J, Stanković T, Jovanović M, Ramović A, Pustenko A, Žalubovskis R, Pešić M. Sulfocoumarins, specific carbonic anhydrase IX and XII inhibitors, interact with cancer multidrug resistant phenotype through pH regulation and reverse P-glycoprotein mediated resistance. Eur J Pharm Sci. 2019;138:105012.
  • Galati S, Yonchev D, Rodríguez-Pérez R, Vogt M, Tuccinardi T, Bajorath J. Predicting isoform-selective carbonic anhydrase inhibitors via machine learning and rationalizing structural features important for selectivity. ACS Omega. 2021;6(5):4080–4089.
  • Angeli A, Carta F, Nocentini A, Winum J-Y, Zalubovskis R, Akdemir A, Onnis V, Eldehna WM, Capasso C, Simone GD, et al. Carbonic anhydrase inhibitors targeting metabolism and tumor microenvironment. Metabolites. 2020;10(10):412.
  • Nemr MT, AboulMagd AM, Hassan HM, Hamed AA, Hamed MI, Elsaadi MT. Design, synthesis and mechanistic study of new benzenesulfonamide derivatives as anticancer and antimicrobial agents via carbonic anhydrase IX inhibition. RSC Adv. 2021;11(42):26241–26257.
  • (a) Havrylyuk D, Zimenkovsky B, Vasylenko O, Zaprutko L, Gzella A, Lesyk R. Synthesis of novel thiazolone-based compounds containing pyrazoline moiety and evaluation of their anticancer activity. Eur J Med Chem. 2009;44(4):1396–1404. (b) Roaiah HM, Ghannam IA, Ali IH, El Kerdawy AM, Ali MM, Abbas SE, El‐Nakkady SS. Design, synthesis, and molecular docking of novel indole scaffold‐based VEGFR‐2 inhibitors as targeted anticancer agents. Arch Pharm. 2018;351(2):1700299.
  • (a) Othman IM, Mahross MH, Gad-Elkareem MA, Rudrapal M, Gogoi N, Chetia D, Aouadi K, Snoussi M, Kadri A. Toward a treatment of antibacterial and antifungal infections: design, synthesis and in vitro activity of novel arylhydrazothiazolylsulfonamides analogues and their insight of DFT, docking and molecular dynamic simulations. J Mol Struct. 2021;1243(10):130862–1562. (b) Kalaria PN, Makawana JA, Satasia SP, Raval DK, Zhu HL. Design, synthesis and molecular docking of novel bipyrazolyl thiazolone scaffold as a new class of antibacterial agents. MedChemComm. 2014;5:1555.
  • (a) Abdoli M, Angeli A, Bozdag M, Carta F, Kakanejadifard A, Saeidian H, Supuran CT. Synthesis and carbonic anhydrase I, II, VII, and IX inhibition studies with a series of benzo [d] thiazole-5-and 6-sulfonamides. J Enzyme Inhib Med Chem. 2017;32(1):1071–1078. (b) Abdoli M, Bozdag M, Angeli A, Supuran C. Benzamide-4-sulfonamides are effective human carbonic anhydrase I, II, VII, and IX inhibitors. Metabolites. 2018;8(2):37. (c) Abdoli M, Giovannuzzi S, Supuran CT, Žalubovskis R. 4-(3-Alkyl/benzyl-guanidino) benzenesulfonamides as selective carbonic anhydrase VII inhibitors. J Enzyme Inhib Med Chem. 2022;37(1):1568–1576. (d) Abdoli M, Bonardi A, Supuran CT, Žalubovskis R. 4-Cyanamidobenzenesulfonamide derivatives: a novel class of human and bacterial carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2023;38(1):156–165. (e) Ivanova J, Abdoli M, Nocentini A, Žalubovskis R, Supuran CT. 1, 2, 3-Benzoxathiazine-2, 2-dioxides–effective inhibitors of human carbonic anhydrases. J Enzyme Inhib Med Chem. 2023;38(1):225–238. (f) Abdoli M, De Luca V, Capasso C, Supuran CT, Žalubovskis R. Benzenesulfonamides incorporating hydantoin moieties effectively inhibit eukaryotic and human carbonic anhydrases. Int J Mol Sci. 2022;23(22):14115.
  • 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.
  • (a) Nishimori I, Minakuchi T, Morimoto K, Sano S, Onishi S, Takeuchi H, Vullo D, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors: DNA cloning and inhibition studies of the alpha-carbonic anhydrase from Helicobacter pylori, a new target for developing sulfonamide and sulfamate gastric drugs. J Med Chem. 2006;49(6):2117–2126. (b) Supuran CT, Clare BW. Carbonic anhydrase inhibitors. Part 57. Quantum chemical QSAR of a group of 1,3,4-thiadiazole and 1,3,4-thiadiazoline disulfonamides with carbonic anhydrase inhibitory properties. Eur J Med Chem. 1999;34:41–50. (c) Gieling RG, Babur M, Mamnani L, Burrows N, Telfer BA, Carta F, Winum JY, Scozzafava A, Supuran CT, Williams KJ. Antimetastatic effect of sulfamate carbonic anhydrase IX inhibitors in breast carcinoma xenografts. J Med Chem. 2012;55(11):5591–600.
  • (a) Abbate F, Winum JY, Potter BV, Casini A, Montero JL, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors: X-ray crystallographic structure of the adduct of human isozyme II with EMATE, a dual inhibitor of carbonic anhydrases and steroid sulfatase. Bioorg Med Chem Lett. 2004;14(1):231–234. (b) Gülçin İ, Scozzafava A, Supuran CT, Akıncıoğlu H, Koksal Z, Turkan F, Alwasel S. The effect of caffeic acid phenethyl ester (CAPE) on metabolic enzymes including acetylcholinesterase, butyrylcholinesterase, glutathione S-transferase, lactoperoxidase, and carbonic anhydrase isoenzymes I, II, IX, and XII. J Enzyme Inhib Med Chem. 2016;31(6):1095–1101.
  • (a) Zimmerman SA, Ferry JG, Supuran CT. Inhibition of the archaeal beta-class (Cab) and gamma-class (Cam) carbonic anhydrases. Curr Top Med Chem. 2007;7(9):901–908. (b) Supuran CT, Barboiu M, Luca C, Pop E, Brewster ME, Dinculescu A. Carbonic anhydrase activators. Part 14. Synthesis of mono- and bis- pyridinium salt derivatives of 2-amino-5-(2-aminoethyl)- and 2-amino-5-(3-aminopropyl)-1,3,4-thiadiazole, and their interaction with isozyme II. Eur J Med Chem. 1996; 31:597–606. (c) Aspatwar A, Barker H, Aisala H, Zueva K, Kuuslahti M, Tolvanen M, Primmer CR, Lumme J, Bonardi A, Tripathi A, et al. Cloning, purification, kinetic and anion inhibition studies of a recombinant β-carbonic anhydrase from the Atlantic salmon parasite platyhelminth Gyrodactylus salaris. J Enzyme Inhib Med Chem. 2022;37:1577–1586.
  • (a) Nishimori I, Minakuchi T, Vullo D, Scozzafava A, Supuran CT. Inhibition studies of the β-carbonic anhydrases from the bacterial pathogen Salmonella enterica serovar Typhimurium with sulfonamides and sulfamates. Bioorg Med Chem. 2011;19(16):5023–5030. (b) Vullo D, Nishimori I, Minakuchi T, Scozzafava A, Supuran CT. Inhibition studies with anions and small molecules of two novel β-carbonic anhydrases from the bacterial pathogen Salmonella enterica serovar Typhimurium. Bioorg Med Chem Lett. 2011;21(12):3591–3595. (c) Supuran CT. Bacterial carbonic anhydrases as drug targets: toward novel antibiotics? Front Pharmacol. 2011;2:34.
  • (a) Urbanski LJ, Vullo D, Parkkila S, Supuran CT. An anion and small molecule inhibition study of the β-carbonic anhydrase from Staphylococcus aureus. J Enzyme Inhib Med Chem. 2021;36(1):1088–1092. (b) Urbanski LJ, Bua S, Angeli A, Kuuslahti M, Hytönen VP, Supuran CT, Parkkila S. Sulphonamide inhibition profile of Staphylococcus aureus β-carbonic anhydrase. J Enzyme Inhib Med Chem. 2020;35(1):1834–1839. (c) 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;37:2786–2792.
  • 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.
  • Mahboobi S, Sellmer A, Höcher H, Eichhorn E, Bär T, Schmidt M, Maier T, Stadlwieser JF, Beckers TL. [4-(Imidazol-1-yl)thiazol-2-yl]phenylamines. A novel class of highly potent colchicine site binding tubulin inhibitors: synthesis and cytotoxic activity on selected human cancer cell lines. J Med Chem. 2006;49(19):5769–5776.
  • Supuran CT. Carbonic anhydrase inhibition and the management of neuropathic pain. Expert Rev Neurother. 2016;16(8):961–968.