1,137
Views
14
CrossRef citations to date
0
Altmetric
Research Paper

7-Acylamino-3H-1,2-benzoxathiepine 2,2-dioxides as new isoform-selective carbonic anhydrase IX and XII inhibitors

, , , , & ORCID Icon
Pages 650-656 | Received 26 Dec 2019, Accepted 23 Jan 2020, Published online: 21 Feb 2020

References

  • (a) Pustenko A, Stepanovs D, Žalubovskis R, et al. 3H-1,2-benzoxathiepine 2,2-dioxides: a new class of isoform-selective carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2017;32:767–75.; (b) Pustenko A, Nocentini A, Balašova A, et al. Aryl derivatives of 3H-1,2-benzoxathiepine 2,2-dioxide as carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2020;35:245–54.
  • 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.
  • Tanc M, Carta F, Bozdag M, et al. 7-Substituted-sulfocoumarins are isoform-selective, potent carbonic anhydrase II inhibitors. Bioorg Med Chem 2013;21:4502–10.
  • 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;31:1226–33.
  • Grandane A, Tanc M, Mannelli LDC, et al. Substituted sulfocoumarins are selective carbonic anhdydrase IX and XII inhibitors with significant cytotoxicity against colorectal cancer cells. J Med Chem 2015;58:3975–83.
  • (a) 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;131:3057–62; (b) Maresca A, Temperini C, Pochet L, et al. Deciphering the mechanism of carbonic anhydrase inhibition with coumarins and thiocoumarins. J Med Chem 2010;53:335–44; (c) 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;53:850–4; (d) 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;54:8271–7.
  • Zengin Kurt B, Sonmez F, Durdagi S, et al. Synthesis, biological activity and multiscale molecular modeling studies for coumaryl-carboxamide derivatives as selective carbonic anhydrase IX inhibitors. J Enzyme Inhib Med Chem 2017;32:1042–52.
  • (a) 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;20:7255–8; (b) 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;20:4511–4.
  • (a) Xu Y, Feng L, Jeffrey PD, et al. Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 2008;452:56–61; (b) 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;24:4389–96; (c) Jensen EL, Clement R, Kosta A, et al. A new widespread subclass of carbonic anhydrase in marine phytoplankton. ISME J 2019;13:2094–106.
  • (a) Capasso C, Supuran CT. Anti-infective carbonic anhydrase inhibitors: a patent and literature review. Expert Opin Ther Pat 2013;23:693–704; (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;30:325–32; (c) Capasso C, Supuran CT. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin Ther Targets 2015;19:1689–704; (d) Supuran CT, Capasso C. Biomedical applications of prokaryotic carbonic anhydrases. Expert Opin Ther Pat 2018;28:745–54; (e) Nishimori I, Minakuchi T, Morimoto K, et al. 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;49:2117–26.
  • (a) Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nature Rev Drug Discov 2008;7:168–81; (b) 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; (c) Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32; (d) Innocenti A, Gülçin I, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. Antioxidant polyphenols effectively inhibit mammalian isoforms I-XV. Bioorg Med Chem Lett 2010;20:5050–3.
  • (a) Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60; (b) Nocentini A, Supuran CT. Advances in the structural annotation of human carbonic anhydrases and impact on future drug discovery. Expert Opin Drug Discov 2019;14:1175–97; (c) Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov 2017;12:61–88; ( d) De Simone G, Supuran CT. (In)organic anions as carbonic anhydrase inhibitors. J Inorg Biochem 2012;111:117–29.
  • (a) Supuran CT. Carbonic anhydrase inhibitors as emerging agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs 2018;27:963–70; (b) Supuran CT. Carbonic anhydrase inhibitors and their potential in a range of therapeutic areas. Expert Opin Ther Pat 2018;28:709–12; (c) Supuran CT. Applications of carbonic anhydrases inhibitors in renal and central nervous system diseases. Expert Opin Ther Pat 2018;28:713–21; (d) Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nature Rev Drug Discov 2011;10:767–77; (e) Supuran CT, Alterio V, Di Fiore A, et al. Inhibition of carbonic anhydrase IX targets primary tumors, metastases, and cancer stem cells: three for the price of one. Med Res Rev 2018;38:1799–836.
  • (a) Supuran CT. Carbonic anhydrases and metabolism. Metabolites 2018;8:25; (b) Supuran CT. Carbonic anhydrase inhibition and the management of hypoxic tumors. Metabolites 2017;7:E48; (c) Da’dara AA, Angeli A, Ferraroni M, et al. Crystal structure and chemical inhibition of essential schistosome host-interactive virulence factor carbonic anhydrase SmCA. Commun Biol 2019;2:333.
  • (a) Supuran CT, Ilies MA, Scozzafava A. Carbonic anhydrase inhibitors. Part 29. Interaction of isozymes I, II and IV with benzolamide-like derivatives. Eur J Med Chem 1998;33:739–52; (b) Köhler K, Hillebrecht A, Schulze Wischeler J, et al. Saccharin inhibits carbonic anhydrases: possible explanation for its unpleasant metallic aftertaste. Ang ew Chem Int Ed Engl 2007;46:7697–9; (c) Scozzafava A, Menabuoni L, Mincione F, et al. Carbonic anhydrase inhibitors: perfluoroalkyl/aryl-s ubstituted derivatives of aromatic/heterocyclic sulfonamides as topical intraocular pressure-lowering agents with prolonged duration of action. J Med Chem 2000;43:4542–51; (d) Sentürk M, Gülçin I, Daştan A, et al. Carbonic anhydrase inhibitors. Inhibition of human erythrocyte isozymes I and II with a series of antioxidant phenols. Bioorg Med Chem 2009;17:3207–11.
  • (a) Supuran CT, Altamimi ASA, Carta F. Carbonic anhydrase inhibition and the management of glaucoma: a literature and patent review 2013-2019. Expert Opin Ther Pat 2019;29:781–92; ( b) Supuran CT. Carbon-versus sulphur-based zinc binding groups for carbonic anhydrase inhibitors? J Enzyme Inhib Med Chem 2018;33:485–95; (c) Bilginer S, Gul HI, Erdal FS, et al. Synthesis, cytotoxicities, and carbonic anhydrase inhibition potential of 6-(3-aryl-2-propenoyl)-2(3H)-benzoxazolones. J Enzyme Inhib Med Chem 2019;34:1722–9.
  • (a) 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;31:60–3; (b) Bua S, Di Cesare Mannelli L, Vullo D, et al. Design and synthesis of novel nonsteroidal anti-inflammatory drugs and carbonic anhydrase inhibitors hybrids (NSAIDs-CAIs) for the treatment of rheumatoid arthritis. J Med Chem 2017;60:1159–70; (c) Akgul O, Di Cesare Mannelli L, Vullo D, et al. Discovery of novel nonsteroidal anti-inflammatory drugs and carbonic anhydrase inhibitors hybrids (NSAIDs-CAIs) for the management of rheumatoid arthritis. J Med Chem 2018;61:4961–77.
  • (a) 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;23:1828–40; (b) Supuran CT. Carbonic anhydrase inhibition and the management of neuropathic pain. Expert Rev Neurother 2016;16:961–8.
  • 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. Enzyme Inhib Med Chem 2016;31:894–9.
  • 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.
  • (a) Vermelho AB, da Silva Cardoso V, Ricci Junior E, et al. Nanoemulsions of sulfonamide carbonic anhydrase inhibitors strongly inhibit the growth of Trypanosoma cruzi. J Enzyme Inhib Med Chem 2018;33:139–46; (b) Nocentini A, Carta F, Tanc M, et al. Deciphering the mechanism of human carbonic anhydrases inhibition with sulfocoumarins: computational and experimental studies. Chemistry 2018;24:7840–4; (c) Awadallah FM, Bua S, Mahmoud WR, et al. Inhibition studies on a panel of human carbonic anhydrases with N1-substituted secondary sulfonamides incorporating thiazolinone or imidazolone-indole tails. J Enzyme Inhib Med Chem 2018;33:629–38.
  • (a) Bua S, Bozdag M, Del Prete S, et al. Mono- and di-thiocarbamate inhibition studies of the δ-carbonic anhydrase TweCAδ from the marine diatom Thalassiosira weissflogii. J Enzyme Inhib Med Chem 2018;33:707–13; (b) Ferraroni M, Gaspari R, Scozzafava A, et al. Dioxygen, an unexpected carbonic anhydrase ligand. J Enzyme Inhib Med Chem 2018;33:999–1005; (c) El-Gazzar MG, Nafie NH, Nocentini A, et al. Carbonic anhydrase inhibition with a series of novel benzenesulfonamide-triazole conjugates. J Enzyme Inhib Med Chem 2018;33:1565–74; (d) Akocak S, Lolak N, Bua S, Supuran CT. Discovery of novel 1,3-diaryltriazene sulfonamides as carbonic anhydrase I, II, VII, and IX inhibitors. J Enzyme Inhib Med Chem 2018;33:1575–80.
  • (a) Nocentini A, Bonardi A, Gratteri P, et al. Steroids interfere with human carbonic anhydrase activity by using alternative binding mechanisms. J Enzyme Inhib Med Chem 2018;33:1453–9; (b) Nocentini A, Trallori E, Singh S, et al. 4-Hydroxy-3-nitro-5-ureido-benzenesulfonamides selectively target the tumor-associated carbonic anhydrase isoforms IX and XII showing hypoxia-enhanced antiproliferative profiles. J Med Chem 2018;61:10860–74; (c) Chohan ZH, Munawar A, Supuran CT. Transition metal ion complexes of Schiff bases. Synthesis, characterization and antibacterial properties. Met Based Drugs 2001;8:137–43; (d) Oztürk Sarikaya SB, Topal F, Sentürk M, et al. In vitro inhibition of α-carbonic anhydrase isozymes by some phenolic compounds. Bioorg Med Chem Lett 2011;21:4259–62.
  • (a) Awadallah FM, Bua S, Mahmoud WR, et al. Inhibition studies on a panel of human carbonic anhydrases with N1-substituted secondary sulfonamides incorporating thiazolinone or imidazolone-indole tails. J Enzyme Inhib Med Chem 2018;33:629–38; (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.