Inhibitory activity against carbonic anhydrase IX and XII as a candidate selection criterion in the development of new anticancer agents

References

• Bailey KM, Wojtkowiak JW, Hashim AI, Gillies RJ. Targeting the metabolic microenvironment of tumors. Adv Pharmacol 2012;65:63–107.
   Google Scholar
• Chiche J, Brahimi-Horn MC, Pouysségur J. Tumour hypoxia induces a metabolic shift causing acidosis: a common feature in cancer. J Cell Mol Med 2010;14:771–94.
   PubMed Web of Science ®Google Scholar
• Webb BA, Chimenti M, Jacobson MP, Barber DL. Dysregulated pH: a perfect storm for cancer progression. Nat Rev Cancer 2011;11:671–7.
   PubMed Web of Science ®Google Scholar
• McDonald PC, Chafe SC, Dedhar S. Overcoming hypoxia-mediated tumor progression: combinatorial approaches targeting pH regulation, angiogenesis and immune dysfunction. Front Cell Dev Biol 2016;4:16–27.
   PubMed Web of Science ®Google Scholar
• Singh S, Lomelino CL, Mboge MY, et al. Cancer drug development of carbonic anhydrase inhibitors beyond the active site. Molecules 2018;23:1045.
   PubMed Web of Science ®Google Scholar
• Pastorek J, Pastorekova S. Hypoxia-induced carbonic anhydrase IX as a target for cancer therapy: from biology to clinical use. Semin Cancer Biol 2015;31:52–64.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32.
   PubMed Web of Science ®Google Scholar
• Švastová E, Hulíková A, Rafajová M, et al. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett 2004;577:439–45.
   PubMed Web of Science ®Google Scholar
• Waheed A, Sly WS. Carbonic anhydrase XII functions in health and disease. Gene 2017;623:33–40.
   PubMed Web of Science ®Google Scholar
• Becker HM, Klier M, Deitmer JW. Carbonic anhydrases and their Interplay with acid/base-coupled membrane transporters. In: Frost S, McKenna R, eds. Carbonic anhydrase: mechanism, regulation, links to disease, and industrial applications. Subcellular Biochemistry. Vol 75. Dordrecht: Springer; 2014.
   Google Scholar
• Watson PH, Chia SK, Wykoff CC, et al. Carbonic anhydrase XII is a marker of good prognosis in invasive breast carcinoma. Br J Cancer 2003;88:1065–70.
   PubMed Web of Science ®Google Scholar
• Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–77.
   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
• Koch G. Medicinal chemistry. Chimia 2017;71:643.
   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.
   PubMed Web of Science ®Google Scholar
• Williams KJ, Gieling RG. Preclinical evaluation of ureidosulfamate carbonic anhydrase IX/XII inhibitors in the treatment of cancers. Int J Mol Sci 2019;20:6080.
   PubMed Web of Science ®Google Scholar
• Gieling RG, Babur M, Mamnani L, et al. Antimetastatic effect of sulfamate carbonic anhydrase IX inhibitors in breast carcinoma xenografts. J Med Chem 2012;55:5591–600.
   PubMed Web of Science ®Google Scholar
• Touisni N, Maresca A, McDonald PC, et al. Glycosyl coumarin carbonic anhydrase IX and XII inhibitors strongly attenuate the growth of primary breast tumors. J Med Chem 2011;54:8271–7.
   PubMed Web of Science ®Google Scholar
• Krasavin M, Žalubovskis R, Grandāne A, et al. Sulfocoumarins as dual inhibitors of human carbonic anhydrase isoforms IX/XII and of human thioredoxin reductase. J Enzyme Inhib Med Chem 2020;35:506–10.
   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
• Mboge MY, Chen Z, Wolff A, et al. Selective inhibition of carbonic anhydrase IX over carbonic anhydrase XII in breast cancer cells using benzene sulfonamides: disconnect between activity and growth inhibition. PLOS One 2018;13:e0207417.
   PubMed Web of Science ®Google Scholar
• A study of SLC-0111 and gemcitabine for metastatic pancreatic ductal cancer in subjects positive for CAIX (SLC-0111-17-01); 2018. Available from: https://clinicaltrials.gov/ct2/show/NCT03450018.
   Google Scholar
• Han T, Goralski M, Gaskill N, et al. Anticancer sulfonamides target splicing by inducing RBM39 degradation via recruitment to DCAF15. Science 2017;356:eaal3755.
   PubMed Web of Science ®Google Scholar
• Uehara T, Minoshima Y, Sagane K, et al. Selective degradation of splicing factor CAPERα by anticancer sulfonamides. Nat Chem Biol 2017;13:675–80.
   PubMed Web of Science ®Google Scholar
• Podolski-Renić A, Dinić J, Stanković T, et al. 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
• Murri-Plesko MT, Hulikova A, Oosterwijk E, et al. Antibody inhibiting enzymatic activity of tumour-associated carbonic anhydrase isoform IX. Eur J Pharmacol 2011;657:173–83.
   PubMed Web of Science ®Google Scholar
• Battke C, Kremmer E, Mysliwietz J, et al. Generation and characterization of the first inhibitory antibody targeting tumour-associated carbonic anhydrase XII. Cancer Immunol Immunother 2011;60:649–58.
   PubMed Web of Science ®Google Scholar
• Pastorekova S, Gillies RJ. The role of carbonic anhydrase IX in cancer development: links to hypoxia, acidosis, and beyond. Cancer Metastasis Rev 2019;38:65–77.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibition and the management of hypoxic tumors. Metabolites 2017;7:48.
   PubMed Web of Science ®Google Scholar
• Sławiński J, Szafrański K, Vullo D, Supuran CT. Carbonic anhydrase inhibitors. Synthesis of heterocyclic 4-substituted pyridine-3-sulfonamide derivatives and their inhibition of the human cytosolic isozymes I and II and transmembrane tumor-associated isozymes IX and XII. Eur J Med Chem 2013;69:701–10.
   PubMed Web of Science ®Google Scholar
• Żołnowska B, Sławiński J, Pogorzelska A, et al. Carbonic anhydrase inhibitors. Synthesis, and molecular structure of novel series N-substituted N′-(2-arylmethylthio-4-chloro-5-methylbenzenesulfonyl)guanidines and their inhibition of human cytosolic isozymes I and II and the transmembrane tumor-associated isozymes IX and XII. Eur J Med Chem 2014;71:135–47.
   PubMed Web of Science ®Google Scholar
• Ibrahim HS, Allam HA, Mahmoud WR, et al. Dual-tail arylsulfone-based benzenesulfonamides differently match the hydrophobic and hydrophilic halves of human carbonic anhydrases active sites: selective inhibitors for the tumor-associated HCA IX isoform. Eur J Med Chem 2018;152:1–9.
   PubMed Web of Science ®Google Scholar
• Koyuncu I, Gonel A, Kocyigit A, et al. Selective inhibition of carbonic anhydrase-IX by sulphonamide derivatives induces pH and reactive oxygen species-mediated apoptosis in cervical cancer HeLa cells. J Enzyme Inhib Med Chem 2018;33:1137–49.
   PubMed Web of Science ®Google Scholar
• Gul HI, Yamali C, Sakagami H, et al. New anticancer drug candidates sulfonamides as selective HCA IX or HCA XII inhibitors. Bioorg Chem 2018;77:411–9.
   PubMed Web of Science ®Google Scholar
• Peerzada MN, Khan P, Ahmad K, et al. Synthesis, characterization and biological evaluation of tertiary sulfonamide derivatives of pyridyl-indole based heteroaryl chalcone as potential carbonic anhydrase IX inhibitors and anticancer agents. Eur J Med Chem 2018;155:13–23.
   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
• Vanchanagiri K, Emmerich D, Bruschke M, et al. Synthesis and biological investigation of new carbonic anhydrase IX (CAIX) inhibitors. Chem Biol Interact 2018;284:12–23.
   PubMed Web of Science ®Google Scholar
• Ghorab MM, Alsaid MS, Ceruso M, et al. Carbonic anhydrase inhibitors: synthesis, molecular docking, cytotoxic and inhibition of the human carbonic anhydrase isoforms I, II, IX, XII with novel benzenesulfonamides incorporating pyrrole, pyrrolopyrimidine and fused pyrrolopyrimidine moieties. Bioorg Med Chem 2014;22:3684–95.
   PubMed Web of Science ®Google Scholar
• Mojzych M, Bielawska A, Bielawski K, et al. Pyrazolo[4,3-e][1,2,4]triazine sulfonamides as carbonic anhydrase inhibitors with antitumor activity. Bioorg Med Chem 2014;22:2643–7.
   PubMed Web of Science ®Google Scholar
• Wang ZC, Duan YT, Qiu HY, et al. Novel metronidazole-sulfonamide derivatives as potent and selective carbonic anhydrase inhibitors: design, synthesis and biology analysis. RSC Adv 2014;4:33029–38.
   Web of Science ®Google Scholar
• Yilmaz Ö, Özbaş Turan S, Akbuʇa J, et al. Synthesis of pro-apoptotic indapamide derivatives as anticancer agents. J Enzyme Inhib Med Chem 2015;30:967–80.
   PubMed Web of Science ®Google Scholar
• Mojzych M, Ceruso M, Bielawska A, et al. New pyrazolo[4,3-e][1,2,4]triazine sulfonamides as carbonic anhydrase inhibitors. Bioorg Med Chem 2015;23:3674–80.
   PubMed Web of Science ®Google Scholar
• Abdel Gawad NM, Amin NH, Elsaadi MT, Mohamed FM. Synthesis of 4-(thiazol-2-ylamino)-benzenesulfonamides with carbonic anhydrase I, II and IX inhibitory activity and cytotoxic effects against breast cancer cell lines. Bioorg Med Chem 2016;24:3043–51.
   PubMed Web of Science ®Google Scholar
• Eldehna WM, Abo-ashour MF, Nocentini A, et al. Novel 4/3-((4-Oxo-5-(2-oxoindolin-3-ylidene)thiazolidin-2-ylidene)amino) benzenesulfonamides: synthesis, carbonic anhydrase inhibitory activity, anticancer activity and molecular modelling studies. Eur J Med Chem 2017;139:250–62.
   PubMed Web of Science ®Google Scholar
• Eldehna WM, Nocentini A, Al-Rashood ST, et al. Tumor-associated carbonic anhydrase isoform IX and XII inhibitory properties of certain isatin-bearing sulfonamides endowed with in vitro antitumor activity towards colon cancer. Bioorg Chem 2018;81:425–32.
   PubMed Web of Science ®Google Scholar
• Cecchi A, Hulikova A, Pastorek J, et al. Carbonic anhydrase inhibitors. Design of fluorescent sulfonamides as probes of tumor-associated carbonic anhydrase IX that inhibit isozyme IX-mediated acidification of hypoxic tumors. J Med Chem 2005;48:4834–41.
   PubMed Web of Science ®Google Scholar
• Li Y, Wang H, Oosterwijk E, et al. Expression and activity of carbonic anhydrase IX is associated with metabolic dysfunction in MDA-MB-231 breast cancer cells. Cancer Invest 2009;27:613–23.
   PubMed Web of Science ®Google Scholar
• Klier M, Jamali S, Ames S, et al. Catalytic activity of human carbonic anhydrase isoform IX is displayed both extra- and intracellularly. FEBS J 2016;283:191–200.
   PubMed Web of Science ®Google Scholar
• Winum JY, Carta F, Ward C, et al. Ureido-substituted sulfamates show potent carbonic anhydrase IX inhibitory and antiproliferative activities against breast cancer cell lines. Bioorg Med Chem Lett 2012;22:4681–5.
   PubMed Web of Science ®Google Scholar
• Grandane A, Tanc M, Di Cesare Mannelli L, et al. 6-Substituted sulfocoumarins are selective carbonic anhydrase IX and XII inhibitors with significant cytotoxicity against colorectal cancer cells. J Med Chem 2015;58:3975–83.
   PubMed Web of Science ®Google Scholar
• Allam HA, Fahim SH, Abo-Ashour MF, et al. Application of hydrazino and hydrazido linkers to connect benzenesulfonamides with hydrophilic/phobic tails for targeting the middle region of human carbonic anhydrases active site: selective inhibitors of HCA IX. Eur J Med Chem 2019;179:547–56.
   PubMed Web of Science ®Google Scholar
• Bozdag M, Ferraroni M, Ward C, et al. Carbonic anhydrase inhibitors based on sorafenib scaffold: design, synthesis, crystallographic investigation and effects on primary breast cancer cells. Eur J Med Chem 2019;182:111600.
   PubMed Web of Science ®Google Scholar
• Eldehna WM, Abo-ashour MF, Nocentini A, et al. Enhancement of the tail hydrophobic interactions within the carbonic anhydrase IX active site via structural extension: design and synthesis of novel N-substituted isatins-SLC-0111 hybrids as carbonic anhydrase inhibitors and antitumor agents. Eur J Med Chem 2018;162:147–160.
   Google Scholar
• Tanini D, Ricci L, Capperucci A, et al. Synthesis of novel tellurides bearing benzensulfonamide moiety as carbonic anhydrase inhibitors with antitumor activity. Eur J Med Chem 2019;181:111586.
   PubMed Web of Science ®Google Scholar
• Krasavin M, Shetnev A, Sharonova T, et al. Continued exploration of 1,2,4-oxadiazole periphery for carbonic anhydrase-targeting primary arene sulfonamides: discovery of subnanomolar inhibitors of membrane-bound HCA IX isoform that selectively kill cancer cells in hypoxic environment. Eur J Med Chem 2019;164:92–105.
   PubMed Web of Science ®Google Scholar
• Krasavin M, Shetnev A, Baykov S, et al. Pyridazinone-substituted benzenesulfonamides display potent inhibition of membrane-bound human carbonic anhydrase IX and promising antiproliferative activity against cancer cell lines. Eur J Med Chem 2019;168:301–14.
   PubMed Web of Science ®Google Scholar
• Abo-Ashour MF, Eldehna WM, Nocentini A, et al. 3-Hydrazinoisatin-based benzenesulfonamides as novel carbonic anhydrase inhibitors endowed with anticancer activity: synthesis, in vitro biological evaluation and in silico insights. Eur J Med Chem 2019;184:111768.
   PubMed Web of Science ®Google Scholar
• Said MA, Eldehna WM, Nocentini A, et al. Sulfonamide-based ring-fused analogues for CAN508 as novel carbonic anhydrase inhibitors endowed with antitumor activity: design, synthesis, and in vitro biological evaluation. Eur J Med Chem 2020;189:112019.
   PubMed Web of Science ®Google Scholar
• Khalil OM, Kamal AM, Bua S, et al. Pyrrolo and pyrrolopyrimidine sulfonamides act as cytotoxic agents in hypoxia via inhibition of transmembrane carbonic anhydrases. Eur J Med Chem 2020;188:112021.
   PubMed Web of Science ®Google Scholar
• Akocak S, Alam MR, Shabana AM, et al. PEGylated bis-sulfonamide carbonic anhydrase inhibitors can efficiently control the growth of several carbonic anhydrase IX-expressing carcinomas. J Med Chem 2016;59:5077–88.
   PubMed Web of Science ®Google Scholar
• Coviello V, Marchi B, Sartini S, et al. 1,2-Benzisothiazole derivatives bearing 4-, 5-, or 6-alkyl/arylcarboxamide moieties inhibit carbonic anhydrase isoform IX (CAIX) and cell proliferation under hypoxic conditions. J Med Chem 2016;59:6547–52.
   PubMed Web of Science ®Google Scholar
• Angeli A, Tanini D, Peat TS, et al. Discovery of new selenoureido analogues of 4-(4-fluorophenylureido)benzenesulfonamide as carbonic anhydrase inhibitors. ACS Med Chem Lett 2017;8:963–8.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Bua S, Lomelino CL, et al. Discovery of new sulfonamide carbonic anhydrase IX inhibitors incorporating nitrogenous bases. ACS Med Chem Lett 2017;8:1314–9.
   PubMed Web of Science ®Google Scholar
• Kazokaitė J, Niemans R, Dudutienė V, et al. Novel fluorinated carbonic anhydrase IX inhibitors reduce hypoxia-induced acidification and clonogenic survival of cancer cells. Oncotarget 2018;9:26800–16.
   PubMedGoogle Scholar
• Angeli A, Trallori E, Ferraroni M, et al. Discovery of new 2, 5-disubstituted 1,3-selenazoles as selective human carbonic anhydrase IX inhibitors with potent anti-tumor activity. Eur J Med Chem 2018;157:1214–22.
   PubMed Web of Science ®Google Scholar
• Queen A, Khan P, Idrees D, et al. Biological evaluation of P-toluene sulphonylhydrazone as carbonic anhydrase IX inhibitors: an approach to fight hypoxia-induced tumors. Int J Biol Macromol 2018;106:840–50.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Yamali C, Gul HI, Ece A, et al. Synthesis, biological evaluation and in silico modelling studies of 1,3,5-trisubstituted pyrazoles carrying benzenesulfonamide as potential anticancer agents and selective cancer-associated HCA IX isoenzyme inhibitors. Bioorg Chem 2019;92:103222.
   PubMed Web of Science ®Google Scholar
• Shamsi F, Hasan P, Queen A, et al. Synthesis and SAR studies of novel 1,2,4-oxadiazole-sulfonamide based compounds as potential anticancer agents for colorectal cancer therapy. Bioorg Chem 2020;98:103754.
   PubMed Web of Science ®Google Scholar
• Kurt BZ, Dag A, Doğan B, et al. Synthesis, biological activity and multiscale molecular modeling studies of bis-coumarins as selective carbonic anhydrase IX and XII inhibitors with effective cytotoxicity against hepatocellular carcinoma. Bioorg Chem 2019;87:838–50.
   PubMed Web of Science ®Google Scholar
• Zengin Kurt B, Sonmez F, Ozturk D, et al. Synthesis of coumarin-sulfonamide derivatives and determination of their cytotoxicity, carbonic anhydrase inhibitory and molecular docking studies. Eur J Med Chem 2019;183:111702.
   PubMed Web of Science ®Google Scholar
• Eldehna WM, Abdelrahman MA, Nocentini A, et al. Bioorganic chemistry synthesis, biological evaluation and in silico studies with 4-benzylidene-2-phenyl-5(4H)-imidazolone-based benzenesulfonamides as novel selective carbonic anhydrase IX inhibitors endowed with anticancer activity. Bioorg Chem 2019;90:103102.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Petreni A, Bonardi A, Lomelino C, et al. Inclusion of a 5-fluorouracil moiety in nitrogenous bases derivatives as human carbonic anhydrase IX and XII inhibitors produced a targeted action against MDA-MB-231 and T47D breast cancer cells. Eur J Med Chem 2020;190:112112.
   PubMed Web of Science ®Google Scholar
• Hann MM. Molecular obesity, potency and other addictions in drug discovery. Med Chem Commun 2011;2:349–55.
   Web of Science ®Google Scholar
• Copeland RA, Pompliano DL, Meek TD. Drug-target residence time and its implications for lead optimization. Nat Rev Drug Discov 2006;5:730–9.
   PubMed Web of Science ®Google Scholar
• Gleeson MP, Hersey A, Montanari D, Overington J. Probing the links between in vitro potency, ADMET and physicochemical parameters. Nat Rev Drug Discov 2011;10:197–208.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibitors and their potential in a range of therapeutic areas. Expert Opin Ther Pat 2018;28:709–12.
   PubMed Web of Science ®Google Scholar