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Research Papers

Antiproliferative effects of sulphonamide carbonic anhydrase inhibitors C18, SLC-0111 and acetazolamide on bladder, glioblastoma and pancreatic cancer cell lines

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Pages 280-286 | Received 10 Oct 2021, Accepted 05 Nov 2021, Published online: 11 Dec 2021

References

  • a) Chan N, Koritzinsky M, Zhao H, et al. Chronic hypoxia decreases synthesis of homologous recombination proteins to offset chemoresistance and radioresistance. Cancer Res 2008;68:605–14. b) Kondo A, Safaei R, Mishima M, et al. Hypoxia-induced enrichment and mutagenesis of cells that have lost DNA mismatch repair. Cancer Res 2001;61:7603–7.c) Semenza GL. Intratumoral hypoxia and mechanisms of immune evasion mediated by hypoxia-inducible factors. Physiology 2021;36:73–83.
  • a) Hsieh CH, Lee CH, Liang JA, et al. Cycling hypoxia increases U87 glioma cell radioresistance via ROS induced higher and long-term HIF-1 signal transduction activity. Oncol Rep 2010;24:1629–36. b) Kato Y, Yashiro M, Fuyuhiro Y, et al. Effects of acute and chronic hypoxia on the radiosensitivity of gastric and esophageal cancer cells. Anticancer Res 2011;31:3369–75. c) Maxwell PH, Wiesener MS, Chang GW, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999; 399:271–5.
  • a) McDonald PC, Swayampakula M, Dedhar S. Coordinated regulation of metabolic transporters and migration/invasion by carbonic anhydrase IX. Metabolites 2018;8:20. b) Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–77. c) Supuran CT. Carbonic anhydrase inhibitors as emerging agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs 2018;27:963–70. d) Lou Y, McDonald PC, Oloumi A, et al. Targeting tumor hypoxia: suppression of breast tumor growth and metastasis by novel carbonic anhydrase IX inhibitors. Cancer Res 2011;71:3364–76.
  • a) Angeli A, Carta F, Nocentini A, et al. Carbonic anhydrase inhibitors targeting metabolism and tumor microenvironment. Metabolites 2020;10:412. b) Supuran CT. Carbonic anhydrase inhibition and the management of hypoxic tumors. Metabolites 2017;7:48. c) 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.
  • Chaplin DJ, Durand RE, Olive PL. Acute hypoxia in tumors: implications for modifiers of radiation effects. Int J Radiat Oncol Biol Phys 1986;12:1279–82.
  • Rofstad EK, Gaustad JV, Egeland TA, et al. Tumors exposed to acute cyclic hypoxic stress show enhanced angiogenesis, perfusion and metastatic dissemination. Int J Cancer 2010;127:1535–46.
  • Minassian LM, Cotechini T, Huitema E, Graham CH. Hypoxia-induced resistance to chemotherapy in cancer. Adv Exp Med Biol 2019;1136:123–39.
  • Samanta D, Gilkes DM, Chaturvedi P, et al. Hypoxia-inducible factors are required for chemotherapy resistance of breast cancer stem cells. Proc Natl Acad Sci U S A 2014;111:E5429–38.
  • Swietach P. What is pH regulation, and why do cancer cells need it? Cancer Metastasis Rev 2019;38:5–15.
  • a) Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473: 2023–32. b) Chafe SC, Vizeacoumar FS, Venkateswaran G, et al. Genome-wide synthetic lethal screen unveils novel CAIX-NFS1/xCT axis as a targetable vulnerability in hypoxic solid tumors. Sci Adv. 2021;7:eabj0364.
  • Güttler A, Theuerkorn K, Riemann A, et al. Cellular and radiobiological effects of carbonic anhydrase IX in human breast cancer cells. Oncol Rep 2019;41:2585–94.
  • a) Koyuncu I, Tülüce Y, Slahaddin Qadir H, et al. Evaluation of the anticancer potential of a sulphonamide carbonic anhydrase IX inhibitor on cervical cancer cells. J Enzyme Inhib Med Chem 2019;34:703–11. b) Koyuncu I, Gonel A, Durgun M, et al. Assessment of the antiproliferative and apoptotic roles of sulfonamide carbonic anhydrase IX inhibitors in HeLa cancer cell line. J Enzyme Inhib Med Chem 2019;34:75–86.
  • Hsin MC, Hsieh YH, Hsiao YH, et al. Carbonic anhydrase IX promotes human cervical cancer cell motility by regulating PFKFB4 expression. Cancers 2021;13:1174.
  • Chen CL, Chu JS, Su WC, et al. Hypoxia and metabolic phenotypes during breast carcinogenesis: expression of HIF-1alpha, GLUT1, and CAIX. Virchows Arch 2010;457:53–61.
  • a) Andring JT, Fouch M, Akocak S, et al. Structural basis of nanomolar inhibition of tumor-associated carbonic anhydrase IX: X-ray crystallographic and inhibition study of lipophilic inhibitors with acetazolamide backbone. J Med Chem 2020;63:13064–75. b) Briganti F, Pierattelli R, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. Part 37. Novel classes of carbonic anhydrase inhibitors and their interaction with the native and cobalt-substituted enzyme: kinetic and spectroscopic investigations. Eur J Med Chem 1996;31:1001–10. c) Carta F, Aggarwal M, Maresca A, et al. Dithiocarbamates: a new class of carbonic anhydrase inhibitors. Crystallographic and kinetic investigations. Chem Commun 2012;48:1868–70.
  • Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81.
  • Supuran CT. Experimental carbonic anhydrase inhibitors for the treatment of hypoxic tumors. J Exp Pharmacol 2020;12:603–17.
  • Supuran CT. Emerging role of carbonic anhydrase inhibitors. Clin Sci 2021;135:1233–49.
  • McDonald PC, Chia S, Bedard PL, et al. A phase 1 study of SLC-0111, a novel inhibitor of carbonic anhydrase IX, in patients with advanced solid tumors. Am J Clin Oncol 2020;43:484–90.
  • a) Nocentini A, Angeli A, Carta F, et al. 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;36:561–80. b) Menchise V, De Simone G, Alterio V, et al. Carbonic anhydrase inhibitors: stacking with Phe131 determines active site binding region of inhibitors as exemplified by the X-ray crystal structure of a membrane-impermeant antitumor sulfonamide complexed with isozyme II. J Med Chem 2005;48:5721–7.
  • a) Pacchiano F, Carta F, McDonald PC, et al. Ureido-substituted benzenesulfonamides potently inhibit carbonic anhydrase IX and show antimetastatic activity in a model of breast cancer metastasis. J Med Chem 2011;54:1896–902. b) Pacchiano F, Aggarwal M, Avvaru BS, et al. Selective hydrophobic pocket binding observed within the carbonic anhydrase II active site accommodate different 4-substituted-ureido-benzenesulfonamides and correlate to inhibitor potency. Chem Commun 2010;46:8371–3.
  • 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;246:2561–257.
  • Supuran CT, Scozzafava A. Benzolamide is not a membrane-impermeant carbonic anhydrase inhibitor. J Enzyme Inhib Med Chem 2004;19:269–73.
  • a) Scozzafava A, Briganti F, Ilies MA, Supuran CT. Carbonic anhydrase inhibitors: synthesis of membrane-impermeant low molecular weight sulfonamides possessing in vivo selectivity for the membrane-bound versus cytosolic isozymes. J Med Chem 2000;43:292–300. b) Akocak S, Güzel-Akdemir Ö, Kishore Kumar Sanku R, et al. Pyridinium derivatives of 3-aminobenzenesulfonamide are nanomolar-potent inhibitors of tumor-expressed carbonic anhydrase isozymes CA IX and CA XII. Bioorg Chem 2020;103:104204. c) Pastorekova S, Casini A, Scozzafava A, et al. Carbonic anhydrase inhibitors: the first selective, membrane-impermeant inhibitors targeting the tumor-associated isozyme IX. Bioorg Med Chem Lett 2004;14:869–73.
  • a) Supuran CT. Acetazolamide for the treatment of idiopathic intracranial hypertension. Expert Rev Neurother 2015;15:851–6.b) Supuran CT. Applications of carbonic anhydrases inhibitors in renal and central nervous system diseases. Expert Opin Ther Pat 2018;28:713–21.
  • Krasavin M, Kalinin S, Sharonova T, Supuran CT. Inhibitory activity against carbonic anhydrase IX and XII as a candidate selection criterion in the development of new anticancer agents. J Enzyme Inhib Med Chem 2020;35:1555–61.
  • Robertson N, Potter C, Harris AL. Role of carbonic anhydrase IX in human tumor cell growth, survival, and invasion. Cancer Res 2004;64:6160–5.
  • Parkkila S, Rajaniemi H, Parkkila AK, et al. Carbonic anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc Natl Acad Sci U S A 2000;97:2220–4.
  • a) McDonald PC, Chafe SC, Brown WS, et al. Regulation of pH by carbonic anhydrase 9 mediates survival of pancreatic cancer cells with activated KRAS in response to hypoxia. Gastroenterology 2019;157:823–37. b) Chafe SC, McDonald PC, Saberi S, et al. Targeting hypoxia-induced carbonic anhydrase IX enhances immune-checkpoint blockade locally and systemically. Cancer Immunol Res 2019;7:1064–78.
  • a) Peppicelli S, Andreucci E, Ruzzolini J, et al. The carbonic anhydrase IX inhibitor SLC-0111 as emerging agent against the mesenchymal stem cell-derived pro-survival effects on melanoma cells. J Enzyme Inhib Med Chem 2020;35:1185–93. b) Gros SJ, Holland-Cunz SG, Supuran CT, Braissant O. Personalized treatment response assessment for rare childhood tumors using microcalorimetry-exemplified by use of carbonic anhydrase IX and aquaporin 1 inhibitors. Int J Mol Sci 2019;20:4984. c) Petrenko M, Güttler A, Funtan A, et al. Combined 3-O-acetylbetulin treatment and carbonic anhydrase IX inhibition results in additive effects on human breast cancer cells. Chem Biol Interact 2021;333:109326.
  • D’Ascenzio M, Secci D, Carradori S, et al. 1,3-Dipolar cycloaddition, HPLC enantioseparation, and docking studies of saccharin/isoxazole and saccharin/isoxazoline derivatives as selective carbonic anhydrase IX and XII inhibitors. J Med Chem 2020;63:2470–88.