Benzenesulfonamides with different rigidity-conferring linkers as carbonic anhydrase inhibitors: an insight into the antiproliferative effect on glioblastoma, pancreatic, and breast cancer cells

References

• Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81.
   PubMed Web of Science ®Google Scholar
• McKenna R, Supuran CT. Carbonic anhydrase inhibitors drug design. Subcell Biochem 2014;75:291–323.
   PubMedGoogle Scholar
• Alterio V, Fiore AD, 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
• Akman M, Belisario DC, Salaroglio IC, et al. Hypoxia, endoplasmic reticulum stress and chemoresistance: dangerous liaisons. J Exp Clin Cancer Res 2021;40:28.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Experimental carbonic anhydrase inhibitors for the treatment of hypoxic tumors. J Exp Pharmacol 2020;12:603–17.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Minassian LM, Cotechini T, Huitema E, Graham CH. Hypoxia-induced resistance to chemotherapy in cancer. Adv Exp Med Biol 2019;1136:123–39.
   PubMed Web of Science ®Google Scholar
• Kuchuk O, Tuccitto A, Citterio D, et al. pH regulators to target the tumor immune microenvironment in human hepatocellular carcinoma. Oncoimmunology 2018;7:e1445452.
   PubMed Web of Science ®Google Scholar
• Ward C, Langdon SP, Mullen P, et al. New strategies for targeting the hypoxic tumour microenvironment in breast cancer. Cancer Treat Rev 2013;39:171–9.
   PubMed Web of Science ®Google Scholar
• Tawfik HO, Petreni A, Supuran CT, El-Hamamsy MH. Discovery of new carbonic anhydrase IX inhibitors as anticancer agents by toning the hydrophobic and hydrophilic rims of the active site to encounter the dual-tail approach. Eur J Med Chem 2022;232:114190.
   PubMed Web of Science ®Google Scholar
• Koyuncu I, Temiz E, Durgun M, et al. Intracellular pH-mediated induction of apoptosis in HeLa cells by a sulfonamide carbonic anhydrase inhibitor. Int J Biol Macromol 2022;201:37–46.
   PubMed Web of Science ®Google Scholar
• Mussi S, Rezzola S, Chiodelli P, et al. Antiproliferative effects of sulphonamide carbonic anhydrase inhibitors C18, SLC-0111 and acetazolamide on bladder, glioblastoma and pancreatic cancer cell lines. J Enzyme Inhib Med Chem 2022;37:280–6.
   PubMed Web of Science ®Google Scholar
• (a) Lau J, Zhang Z, Jenni S, et al. PET imaging of carbonic anhydrase IX expression of HT-29 tumor xenograft mice with (68)Ga-labeled benzenesulfonamides. Mol Pharm 2016;13:1137–46.
   PubMed Web of Science ®Google Scholar
  (b) Mishra CB, Mongre RK, Prakash A, et al. Anti-breast cancer action of carbonic anhydrase IX inhibitor 4-[4-(4-Benzo[1,3]dioxol-5-ylmethyl-piperazin-1-yl)-benzylidene-hydrazinocarbonyl]-benzenesulfonamide (BSM-0004): in vitro and in vivo studies. J Enzyme Inhib Med Chem 2021;36:954–63.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Andreucci E, Ruzzolini J, Peppicelli S, et al. The carbonic anhydrase IX inhibitor SLC-0111 sensitises cancer cells to conventional chemotherapy. J Enzyme Inhib Med Chem 2019;34:117–23.
   PubMed Web of Science ®Google Scholar
• Hedlund EE, McDonald PC, Nemirovsky O, et al. Harnessing induced essentiality: targeting carbonic anhydrase IX and angiogenesis reduces lung metastasis of triple negative breast cancer xenografts. Cancers 2019;11:1002.
   PubMed Web of Science ®Google Scholar
• Boyd NH, Walker K, Fried J, et al. Addition of carbonic anhydrase 9 inhibitor SLC-0111 to temozolomide treatment delays glioblastoma growth in vivo. JCI Insight 2017;2:e92928.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Mboge MY, Mahon BP, Lamas N, et al. Structure activity study of carbonic anhydrase IX: selective inhibition with ureido-substituted benzenesulfonamides. Eur J Med Chem 2017;132:184–91.
   PubMed Web of Science ®Google Scholar
• Akdemir ÖG, Yazıcı KD, Vullo D, et al. New pyridinium salt derivatives of 2-(hydrazinocarbonyl)-3-phenyl-1H-indole-5-sulfonamide as selective inhibitors of tumour-related human carbonic anhydrase isoforms IX and XII. Anticancer Agents Med Chem 2022;22:2637–2646.
   PubMed Web of Science ®Google Scholar
• Bozdag M, Carta F, Ceruso M, et al. Discovery of 4-hydroxy-3-(3-(phenylureido)benzenesulfonamides as SLC-0111 analogues for the treatment of hypoxic tumors overexpressing carbonic anhydrase IX. J Med Chem 2018;61:6328–38.
   PubMed Web of Science ®Google Scholar
• Mboge MY, Combs J, Singh S, et al. Inhibition of carbonic anhydrase using SLC-149: support for a noncatalytic function of CAIX in breast cancer. J Med Chem 2021;64:1713–24.
   PubMed Web of Science ®Google Scholar
• Zhang Z. Aryl sulfonamide compounds as carbonic anhydrase inhibitors and their therapeutic use. 2017. WO 2017/004543 A1.
   Google Scholar
• Supuran CT, Scozzafava A, Jurca BC, Ilies MA. Carbonic anhydrase inhibitors. Part 49. Synthesis of substituted ureido- and thioureido derivatives of aromatic/heterocyclic sulfonamides with increased affinities for isozyme I. Eur J Med Chem 1998;33:83–93.
   Web of Science ®Google Scholar
• Kalifah 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
• Supuran CT. Carbonic anhydrase inhibitors: an update on experimental agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs 2021;30:1197–208.
   PubMed Web of Science ®Google Scholar
• Sarnella A, Ferrara Y, Auletta L, et al. Inhibition of carbonic anhydrases IX/XII by SLC-0111 boosts cisplatin effects in hampering head and neck squamous carcinoma cell growth and invasion. J Exp Clin Cancer Res 2022;41:122.
   PubMed Web of Science ®Google Scholar
• Daina A, Michielin O, Zoete V. SwissADME: a free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Sci Rep 2017;7:42717.
   PubMed Web of Science ®Google Scholar
• Lagorce D, Bouslama L, Becot J, et al. FAF-Drugs4: free ADME-tox filtering computations for chemical biology and early stages drug discovery. Bioinformatics 2017;33:3658–60.
   PubMed Web of Science ®Google Scholar
• Baell JB, Holloway GA. New substructure filters for removal of Pan assay interference compounds (PAINS) from screening libraries and for their exclusion in bioassays. J Med Chem 2010;53:2719–40.
   PubMed Web of Science ®Google Scholar
• D'Ambrosio K, Carradori S, Cesa S, et al. Catechols: a new class of carbonic anhydrase inhibitors. Chem Commun 2020;56:13033–6.
   PubMed Web of Science ®Google Scholar
• Carradori S, De Monte C, D'Ascenzio M, et al. Salen and tetrahydrosalen derivatives act as effective inhibitors of the tumor-associated carbonic anhydrase XII–a new scaffold for designing isoform-selective inhibitors. Bioorg Med Chem Lett 2013;23:6759–63.
   PubMed Web of Science ®Google Scholar
• Giacomini A, Taranto S, Rezzola S, et al. Inhibition of the FGF/FGFR system induces apoptosis in lung cancer cells via c-Myc downregulation and oxidative stress. Int J Mol Sci 2020;21:9376.
   PubMed Web of Science ®Google Scholar