Aryl derivatives of 3H-1,2-benzoxaphosphepine 2-oxides as inhibitors of cancer-related carbonic anhydrase isoforms IX and XII

References

• Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–249.
   PubMed Web of Science ®Google Scholar
• Long J, Ji Z, Yuan P, Long T, Liu K, Li J, Cheng L. Nut consumption and risk of cancer: a meta-analysis of prospective studies. Cancer Epidemiol Biomarkers Prev. 2020;29(3):565–573.
   PubMed Web of Science ®Google Scholar
• (a) Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov. 2011;10(10):767–777.
   PubMed Web of Science ®Google Scholar
  (b) Supuran CT, Alterio V, Di Fiore A, D' Ambrosio K, Carta F, Monti SM, De Simone G. Inhibition of carbonic anhydrase IX targets primary tumors, metastases, and cancer stem cells: three for the price of one. Med Res Rev. 2018;38(6):1799–1836.
   PubMed Web of Science ®Google Scholar
  (c) Pastorekova S, Gillies RJ. The role of carbonic anhydrase IX in cancer development: links to hypoxia, acidosis, and beyond. Cancer Metastasis Rev. 2019;38(1-2):65–77.
   PubMed Web of Science ®Google Scholar
  (d) Singh S, Lomelino CL, Mboge MY, Frost SC, McKenna R. Cancer drug development of carbonic anhydrase inhibitors beyond the active site. Molecules. 2018;23:1045.
   PubMed Web of Science ®Google Scholar
  (e) Waheed A, Sly WS, Doisy EA. Carbonic anhydrase XII functions in health and disease. Gene. 2017;623:33–40.
   PubMed Web of Science ®Google Scholar
• (a) Robertson N, Potter C, Harris AL. Role of carbonic anhydrase IX in human tumor cell growth, survival, and invasion. Cancer Res. 2004;64(17):6160–6165.
   PubMed Web of Science ®Google Scholar
  (b) Chiche J, Ilc K, Laferriere J, Trottier E, Dayan F, Mazure NM, Brahimi-Horn MC, Pouysségur J. Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res. 2009;69(1):358–368.
   PubMed Web of Science ®Google Scholar
  (c) Angeli A, Carta F, Nocentini A, Winum J-Y, Zalubovskis R, Akdemir A, Onnis V, Eldehna WM, Capasso C, Simone G. Carbonic anhydrase inhibitors targeting metabolism and tumor microenvironment. Metabolites. 2020;10:412.
   PubMed Web of Science ®Google Scholar
• (a) Hewett-Emmett D, Tashian RE. Functional diversity, conservation, and convergence in the evolution of the alpha-, beta-, and gamma-carbonic anhydrase gene families. Mol Phylogenet Evol. 1996;5(1):50–77.
   PubMed Web of Science ®Google Scholar
  (b) Hassan MI, Shajee B, Waheed A, Ahmad F, Sly WS. Structure, function and applications of carbonic anhydrase isozymes. Bioorg Med Chem. 2013;21(6):1570–1582.
   PubMed Web of Science ®Google Scholar
• (a) Supuran CT. Structure and function of carbonic anhydrases. Biochem J. 2016;473(14):2023–2032.
   PubMedGoogle Scholar
  (b) Supuran CT. Carbonic anhydrases and metabolism. Metabolites. 2018;21:25.
   Google Scholar
• Kumar S, Rulhania S, Jaswal S, Monga V. Recent advances in the medicinal chemistry of carbonic anhydrase inhibitors. Eur J Med Chem. 2021;209:112923.
   PubMed Web of Science ®Google Scholar
• (a)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.
   PubMed Web of Science ®Google Scholar
  (b) Aggarwal M, Kondeti B, McKenna R. Insights towards sulfonamide drug specificity in α-carbonic anhydrases. Bioorg Med Chem. 2013;21(6):1526–1533.
   PubMed Web of Science ®Google Scholar
• Žalubovskis R. In a search for selective inhibitors of carbonic anhydrases: coumarin and its bioisosteres: synthesis and derivatization. Chem Heterocycl Comp. 2015;51(7):607–612.
   Web of Science ®Google Scholar
• (a) Maresca A, Temperini C, Vu H, Pham NB, Poulsen S-A, 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.
   PubMed Web of Science ®Google Scholar
  (b) Supuran CT. Coumarin carbonic anhydrase inhibitors from natural sources. J Enzyme Inhib Med Chem. 2020;35(1):1462–1470.
   PubMed Web of Science ®Google Scholar
• (a) Bonneau A, Maresca A, Winum J-Y, Supuran CT. Metronidazole-coumarin conjugates and 3-cyano-7-hydroxy-coumarin act as isoform-selective carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2013;28(2):397–401.
   PubMed Web of Science ®Google Scholar
  (b) 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;29(2):292–296.
   PubMed Web of Science ®Google Scholar
• Maresca A, Temperini C, Pochet L, Masereel B, Scozzafava A, Supuran CT. Deciphering the mechanism of carbonic anhydrase inhibition with coumarins and thiocoumarins. J Med Chem. 2010;53(1):335–344.
   PubMed Web of Science ®Google Scholar
• Onyılmaz M, Koca M, Bonardi A, Degirmenci M, Supuran CT. Isocoumarins: a new class of selective carbonic anhydrase IX and XII inhibitors. J Enzyme Inhib Med Chem. 2022;37(1):743–748.
   PubMed Web of Science ®Google Scholar
• (a) 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.
   PubMed Web of Science ®Google Scholar
  (b) Krasavin M, Žalubovskis R, Grandāne A, Domračeva I, Zhmurov P, Supuran CT. Sulfocoumarins as dual inhibitors of human carbonic anhydrase isoforms IX/XII and of human thioredoxin reductase. J Enzyme Inhib Med Chem. 2020;35(1):506–510.
   PubMed Web of Science ®Google Scholar
• (a) 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.
   PubMed Web of Science ®Google Scholar
  (b) 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.
   PubMed Web of Science ®Google Scholar
• (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.
   PubMed Web of Science ®Google Scholar
  (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.
   PubMed Web of Science ®Google Scholar
  (c) Grandane A, Tanc M, Žalubovskis R, Supuran CT. Synthesis of 6-aryl-substituted sulfocoumarins and investigation of their carbonic anhydrase inhibitory action. Bioorg Med Chem. 2015;23(7):1430–1436.
   PubMed Web of Science ®Google Scholar
  (d) Grandane A, Tanc M, Di Cesare Mannelli L, Carta F, Ghelardini C, Žalubovskis R, Supuran CT. 6-Substituted sulfocoumarins are selective carbonic anhdydrase IX and XII inhibitors with significant cytotoxicity against colorectal cancer cells. J Med Chem. 2015;58(9):3975–3983.
   PubMed Web of Science ®Google Scholar
  (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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• (a) Pustenko A, Stepanovs D, Žalubovskis R, Vullo D, Kazaks A, Leitans J, Tars K, Supuran CT. 3H-1,2-benzoxathiepine 2,2-dioxides: a new class of isoform-selective carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2017;32(1):767–775.
   PubMed Web of Science ®Google Scholar
  (b) Pustenko A, Nocentini A, Balašova A, Alafeefy A, Krasavin M, Žalubovskis R, Supuran CT. Aryl derivatives of 3H-1,2-benzoxathiepine 2,2-dioxide as carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2020;35(1):245–254.
   PubMed Web of Science ®Google Scholar
  (c) Pustenko A, Nocentini A, Balašova A, Krasavin M, Žalubovskis R, Supuran CT. 7-Acylamino-3H-1,2-benzoxathiepine 2,2-dioxides as new isoform-selective carbonic anhydrase IX and XII inhibitors. J Enzyme Inhib Med Chem. 2020;35(1):650–656.
   PubMed Web of Science ®Google Scholar
• Pustenko A, Balašova A, Nocentini A, Supuran CT, Žalubovskis R. 3H-1,2-Benzoxaphosphepine 2-oxides as selective inhibitors of carbonic anhydrase IX and XII. J Enzyme Inhib Med Chem. 2023;38(1):216–224.
   PubMed Web of Science ®Google Scholar
• (a) Rodriguez JB, Gallo-Rodriguez C. The role of the phosphorus atom in drug design. ChemMedChem. 2019;14:190–216.
   PubMed Web of Science ®Google Scholar
  (b)Yu H, Yang H, Shi E, Tang W. Development and clinical application of phosphorus-containing drugs. Med Drug Discov. 2020;8:100063.
   PubMedGoogle Scholar
  (c) Ceradini D, Shubin K. New methods for the synthesis of phosphono-δ-lactones (microreview). Chem Heterocycl Comp. 2021;57(12):1167–1169.
   Web of Science ®Google Scholar
  (d) Balašova A, Žalubovskis R. Synthetic methods toward phosphacoumarins (microreview). Chem Heterocycl Comp. 2022;58(6-7):310–312.
   Web of Science ®Google Scholar
• (a) Bonnac L, Innocenti A, Winum J-Y, Casini A, Montero J-L, Scozzafava A, Barragan V, Supuran CT. Carbonic anhydrase inhibitors: aliphatic N-phosphorylated sulfamates – a novel zinc-anchoring group leading to nanomolar inhibitors. J Enzyme Inhib Med Chem. 2004;19(3):275–278.
   PubMed Web of Science ®Google Scholar
  (b) Winum J-W, Innocenti A, Gagnard V, Montero J-L, Scozzafava A, Vullo D, Supuran CT. Carbonic anhydrase inhibitors. Interaction of isozymes I, II, IV, V, and IX with organic phosphates and phosphonates. Bioorg Med Chem Lett. 2005;15(6):1683–1686.
   PubMed Web of Science ®Google Scholar
  (c) Nocentini A, Alterio V, Bua S, Micheli L, Esposito D, Buonanno M, Bartolucci G, Osman SM, ALOthman ZA, Cirilli R, et al. Phenyl(thio)phosphon(amid)ate benzenesulfonamides as potent and selective inhibitors of human carbonic anhydrases II and VII counteract allodynia in a mouse model of oxaliplatin-induced neuropathy. J Med Chem. 2020;63(10):5185–5200.,.
   PubMed Web of Science ®Google Scholar
  (d) Gülçin İ, Trofimov B, Kaya R, Taslimi P, Sobenina L, Schmidt E, Petrova O, Malysheva S, Gusarova N, Farzaliyev V, et al. Synthesis of nitrogen, phosphorus, selenium and sulfur-containing heterocyclic compounds: determination of their carbonic anhydrase, acetylcholinesterase, butyrylcholinesterase and α-glycosidase inhibition properties. Bioorg Chem. 2020;103:104171.
   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(8):2561–2573.
   PubMed Web of Science ®Google Scholar
• (a) Supuran CT, Ilies MA, Scozzafava A. Carbonic anhydrase inhibitors. Part 29. Interaction of isozymes I, II and IV with benzolamide-like derivatives. Bioorg Med Chem. 1998;33:739–752.
   Google Scholar
  (b) Sentürk M, Gülçin I, Daştan A, Küfrevioğlu OI, Supuran CT. Carbonic anhydrase inhibitors. Inhibition of human erythrocyte isozymes I and II with a series of antioxidant phenols. Bioorg Med Chem. 2009;17(8):3207–3211.
   PubMed Web of Science ®Google Scholar
• Leitans J, Kazaks A, Balode A, Ivanova J, Zalubovskis R, Supuran CT, Tars K. Efficient expression and crystallization system of cancer-associated carbonic anhydrase isoform IX. J Med Chem. 2015;58(22):9004–9009.
   PubMed Web of Science ®Google Scholar
• (a) Aspatwar A, Parvathaneni NK, Barker H, Anduran E, Supuran CT, Dubois L, Lambin P, Parkkila S, Winum J-W. Design, synthesis, in vitro inhibition and toxicological evaluation of human carbonic anhydrases I, II and IX inhibitors in 5-nitroimidazole series. J Enzyme Inhib Med Chem. 2020;35(1):109–117.
   PubMed Web of Science ®Google Scholar
  (b) Pustenko A, Nocentini A, Gratteri P, Bonardi A, Vozny I, Žalubovskis R, Supuran CT. The antibiotic furagin and its derivatives are isoform-selective human carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2020;35(1):1011–1020.
   PubMed Web of Science ®Google Scholar
  (c) 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.
   PubMed Web of Science ®Google Scholar