Open saccharin-based secondary sulfonamides as potent and selective inhibitors of cancer-related carbonic anhydrase IX and XII isoforms

References

• 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
• 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.
   PubMed Web of Science ®Google Scholar
• Winum JY, Scozzafava A, Montero JL, Supuran CT. Therapeutic potential of sulfamides as enzyme inhibitors. Med Res Rev 2006;26:767–92.
   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
• De Simone G, Supuran CT. Carbonic anhydrase IX: biochemical and crystallographic characterization of a novel antitumor target. Biochim Biophys Acta 2010;1804:404–9.
   PubMed Web of Science ®Google Scholar
• Lock FE, McDonald PC, Lou Y, et al. Targeting carbonic anhydrase IX depletes breast cancer stem cells within the hypoxic niche. Oncogene 2013;32:5210–19.
   PubMed Web of Science ®Google Scholar
• De Simone G, Alterio V, Supuran CT. Exploiting the hydrophobic and hydrophilic binding sites for designing carbonic anhydrase inhibitors. Expert Opin Drug Discov 2013;8:793–810.
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Menabuoni L, Mincione F, Supuran CT. Carbonic anhydrase inhibitors. A general approach fir the preparation of water-soluble sulfonamides incorporating polyamino-polycarboxylate tails and of their metal complexes possessing long-lasting, topical intraocular pressure-lowering properties. J Med Chem 2002;45:1466–76.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Beyza Oztürk Sarikaya S, Gülçin I, Supuran CT. Carbonic anhydrase inhibitors. Inhibition of mammalian isoforms I-XIV with a series of natural products polyphenols and phenolic acids. Bioorg Med Chem 2010;18:2159–64.
   PubMed Web of Science ®Google Scholar
• Bayram E, Senturk M, Kufrevioglu OI, Supuran CT. In vitro inhibition of salycilic acid derivatives on human cytosolic carbonic anhydrase isozymes I and II. Bioorg Med Chem 2008;16:9101–5.
   PubMed Web of Science ®Google Scholar
• Carradori S, Mollica A, De Monte C, et al. Nitric oxide donors and selective carbonic anhydrase inhibitors: a dual pharmacological approach for the treatment of glaucoma, cancer and osteoporosis. Molecules 2015;20:5667–79.
   PubMed Web of Science ®Google Scholar
• Maccallini C, Di Matteo M, Vullo D, et al. Indazole, pyrazole, and oxazole derivatives targeting nitric oxide synthases and carbonic anhydrases. ChemMedChem 2016;11:1695–9.
   PubMed Web of Science ®Google Scholar
• Gidaro MC, Alcaro F, Carradori S, et al. Eriocitrin and apigenin as new carbonic anhydrase VA inhibitors, from a virtual screening of Calabrian natural products. Planta Medica 2015;81:533–40.
   PubMed Web of Science ®Google Scholar
• De Monte C, Carradori S, Secci D, et al. Cyclic tertiary sulfamates: selective inhibition of the tumor-associated carbonic anhydrases IX and XII by N- and O-substituted acesulfame derivatives. Eur J Med Chem 2014;84:240–6.
   PubMed Web of Science ®Google Scholar
• D’Ascenzio M, Carradori S, De Monte C, et al. Design, synthesis and evaluation of N-substituted saccharin derivatives as selective inhibitors of tumor-associated carbonic anhydrase XII. Bioorg Med Chem 2014;22:1821–31.
   PubMed Web of Science ®Google Scholar
• Mollica A, Costante R, Akdemir A, et al. Exploring new probenecid-based carbonic anhydrase inhibitors: Synthesis, biological evaluation and docking studies. Bioorg Med Chem 2015;23:5311–18.
   PubMed Web of Science ®Google Scholar
• D’Ascenzio M, Carradori S, Secci D, et al. Selective inhibition of human carbonic anhydrases by novel amide derivatives of probenecid: synthesis, biological evaluation and molecular modeling studies. Bioorg Med Chem 2014;22:3982–8.
   PubMed Web of Science ®Google Scholar
• De Monte C, Carradori S, Gentili A, et al. Dual cyclooxygenase and carbonic anhydrase inhibition by nonsteroidal anti-inflammatory drugs for the treatment of cancer. Curr Med Chem 2015;22:2812–18.
   PubMed Web of Science ®Google Scholar
• Carradori S, Mollica A, Ceruso M, et al. New amide derivatives of Probenecid as selective inhibitors of carbonic anhydrase IX and XII: biological evaluation and molecular modeling studies. Bioorg Med Chem 2015;23:2975–81.
   PubMed Web of Science ®Google Scholar
• See more at ClinicalTrials.gov: Safety Study of SLC-0111 in Subjects With Advanced-Solid Tumors-Clinical Trials_gov.mht
   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
• Supuran CT, Winum JY, eds. Drug design of zinc-enzyme inhibitors: functional, structural, and disease applications. Hoboken, NJ: Wiley; 2009: Part II.
   Google Scholar
• Langella E, D'Ambrosio K, D’Ascenzio M, et al. A combined crystallographic and theoretical study explains the capability of carboxylic acids to adopt multiple binding modes within carbonic anhydrase active site. Chem Eur J 2016;22:97–100.
   PubMed Web of Science ®Google Scholar
• D’Ambrosio K, Carradori S, Monti SM, et al. Out of the active site binding pocket for carbonic anhydrase inhibitors. Chem Comm 2015;51:302–5.
   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
• Mollica A, Locatelli M, Macedonio G, et al. Microwave-assisted extraction, HPLC analysis and inhibitory effects on carbonic anhydrase I, II, VA and VII isoforms of fourteen blueberry Italian cultivars. J. Enzyme Inhib. Med. Chem 2016. [Epub ahead of print]. doi: 10.1080/14756366.2016.1214951.
   Web of Science ®Google Scholar
• Wilkinson BL, Bornaghi LF, Houston TA, et al. A novel class of carbonic anhydrase inhibitors: glycoconjugate benzene sulfonamides prepared by “click-tailing”. J Med Chem 2006;49:6539–98.
   PubMed Web of Science ®Google Scholar
• Güzel-Akdemir Ö, Akdemir A, Isik S, et al. o-Benzenedisulfonimido–sulfonamides are potent inhibitors of the tumor-associated carbonic anhydrase isoforms CA IX and CA XII. Bioorg Med Chem 2013;21:1386–91.
   PubMed Web of Science ®Google Scholar
• Liu F, Martin-Mingot A, Lecornué F, et al. Carbonic anhydrases inhibitory effects of new benzenesulfonamides synthesized by using superacid chemistry. J Enzyme Inhib Med Chem 2012;27:886–91.
   PubMed Web of Science ®Google Scholar
• Métayer B, Mingot A, Vullo D, et al. New superacid synthesized (fluorinated) tertiary benzenesulfonamides acting as selective hCA IX inhibitors: toward a new mode of carbonic anhydrase inhibition by sulfonamides. Chem Commun 2013;49:6015–17.
   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
• Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60.
   PubMed Web of Science ®Google Scholar
• Ivanova J, Leitans J, Tanc M, et al. X-ray crystallography-promoted drug design of carbonic anhydrase inhibitors. Chem Commun (Camb.) 2015;51:7108–11.
   PubMed Web of Science ®Google Scholar
• Carradori S, Secci D, De Monte C, et al. A novel library of saccharin and acesulfame derivatives as potent and selective inhibitors of carbonic anhydrase IX and XII isoforms. Bioorg Med Chem 2016;24:1095–105.
   PubMed Web of Science ®Google Scholar
• Rice LM, Grogan CH, Reid EE. N-Alkyl saccharins and their reduction products. J Am Chem Soc 1953;75:4304–5.
   Web of Science ®Google Scholar
• Hettler H. Chapman-Mumm rearrangement of pseudosaccharinethers. Tetrahedron Lett 1968;9:1793–6.
   Google Scholar
• Fichert T, Massing U. A new strategy for the preparation of secondary amines via o-(tetrahydropyranyloxymethyl)-benzamides. Tetrahedron Lett 1998;39:5017–18.
   Web of Science ®Google Scholar
• Bozdag M, Ferraroni M, Nuti E, et al. Combining the tail and the ring approaches for obtaining potent and isoform-selective carbonic anhydrase inhibitors: solution and X-ray crystallographic studies. Bioorg Med Chem 2014;22:334–40.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. Sulfa and trimethoprim-like drugs – antimetabolites acting as carbonic anhydrase, dihydropteroate synthase and dihydrofolate reductase inhibitors. J Enzyme Inhib Med Chem 2014;29:379–87.
   PubMed Web of Science ®Google Scholar
• Akdemir A, De Monte C, Carradori S, Supuran CT. Computational investigation of the selectivity of salen and tetrahydrosalen compounds towards the tumor-associated hCA XII isozyme. J Enzyme Inhib Med Chem 2015;30:114–18.
   PubMed Web of Science ®Google Scholar