Synthesis of an acridine orange sulfonamide derivative with potent carbonic anhydrase IX inhibitory action

References

• Kusuzaki K, Murata H, Matsubara T, et al. Review. Acridine orange could be an innovative anticancer agent under photon energy. In Vivo 2007;21:205–14.
   PubMed Web of Science ®Google Scholar
• Matsubara T, Kusuzaki K, Matsumine A, et al. Acridine orange used for photodynamic therapy accumulates in malignant musculoskeletal tumors depending on pH gradient. Anticancer Res 2006;26:187–93.
   PubMed Web of Science ®Google Scholar
• Nakamura T, Kusuzaki K, Matsubara T, et al. A new limb salvage surgery in cases of high-grade soft tissue sarcoma using photodynamic surgery, followed by photo- and radiodynamic therapy with acridine orange. J Surg Oncol 2008;97:523–8.
   PubMed Web of Science ®Google Scholar
• Matsubara T, Kusuzaki K, Matsumine A, et al. Photodynamic therapy with acridine orange in musculoskeletal sarcomas. J Bone Joint Surg Br 2010;92:760–2.
   PubMedGoogle Scholar
• Kusuzaki K, Hosogi S, Ashihara E, et al. Translational research of photodynamic therapy with acridine orange which targets cancer acidity. Curr Pharm Des 2012;18:1414–20.
   PubMed Web of Science ®Google Scholar
• Fotia C, Avnet S, Kusuzaki K, et al. Acridine orange is an effective anti-cancer drug that affects mitochondrial function in osteosarcoma cells. Curr Pharm Des 2015;21:4088–94.
   PubMed Web of Science ®Google Scholar
• Perut F, Carta F, Bonuccelli G, et al. Carbonic anhydrase IX inhibition is an effective strategy for osteosarcoma treatment. Expert Opin Ther Targets 2015;19:1593–605.
   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
• 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
• Capasso C, Supuran CT. An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria? J Enzyme Inhib Med Chem 2015;30:325–32.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Structure-based drug discovery of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2012;27:759–72.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibitors. Bioorg Med Chem Lett 2010;20:3467–74.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Bacterial carbonic anhydrases as drug targets: toward novel antibiotics? Front Pharmacol 2011;2:34.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, et al. Biochemical characterization of recombinant beta-carbonic anhydrase (PgiCAb) identified in the genome of the oral pathogenic bacterium Porphyromonas gingivalis. J Enzyme Inhib Med Chem 2015;30:366–70.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases: from biomedical applications of the inhibitors and activators to biotechnological use for CO(2) capture. J Enzyme Inhib Med Chem 2013;28:229–30.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. Anti-infective carbonic anhydrase inhibitors: a patent and literature review. Expert Opin Ther Pat 2013;23:693–704.
   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
• Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016; 473:2023–32.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Casini A, Scozzafava A, Mincione F, et al. Carbonic anhydrase inhibitors: water-soluble 4-sulfamoylphenylthioureas as topical intraocular pressure-lowering agents with long-lasting effects. J Med Chem 2000;43:4884–92.
   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
• Carta F, Aggarwal M, Maresca A, et al. Dithiocarbamates strongly inhibit carbonic anhydrases and show antiglaucoma action in vivo. J Med Chem 2012;55:1721–30.
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Menabuoni L, Mincione F, Supuran CT. Carbonic anhydrase inhibitors. A general approach for the preparation of water solublesulfonamides 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
• Fabrizi F, Mincione F, Somma T, et al. A new approach to antiglaucoma drugs: carbonic anhydrase inhibitors with or without NO donating moieties. Mechanism of action and preliminary pharmacology. J Enzyme Inhib Med Chem 2012;27:138–47.
   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
• Dubois L, Lieuwes NG, Maresca A, et al. Imaging of CA IX with fluorescent labelledsulfonamides distinguishes hypoxic and (re)-oxygenated cells in a xenograft tumor model. Radiother Oncol 2009;92:423–8.
   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
• 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
• 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 (Camb) 2010;46:8371–3.
   PubMed Web of Science ®Google Scholar
• Carta F, Garaj V, Maresca A, et al. Sulfonamides incorporating 1,3,5-triazine moieties selectively and potently inhibit carbonic anhydrase transmembrane isoforms IX, XII and XIV over cytosolic isoforms I and II: solution and X-ray crystallographic studies. Bioorg Med Chem 2011;19:3105–19.
   PubMed Web of Science ®Google Scholar
• Garaj V, Puccetti L, Fasolis G, et al. Carbonic anhydrase inhibitors: synthesis and inhibition of cytosolic/tumor-associated carbonic anhydrase isozymes I, II and IX with sulfonamides incorporating 1,2,4-triazine moieties. Bioorg Med Chem Lett 2004;14:5427–33.
   PubMed Web of Science ®Google Scholar
• Garaj V, Puccetti L, Fasolis G, et al. Carbonic anhydrase inhibitors. Novel sulfonamides incorporating 1,3,5-triazine moieties as inhibitors of the cytosolic and tumor-associated carbonic anhydrase isozymes I, II and IX. Bioorg Med Chem Lett 2005;15:3102–8.
   PubMed Web of Science ®Google Scholar
• McDonald PC, Winum JY, Supuran CT, Dedhar S. Recent developments in targeting carbonic anhydrase IX for cancer therapeutics. Oncotarget 2012;3:84–97.
   PubMed Web of Science ®Google Scholar
• Carta F, Scozzafava A, Supuran CT. Sulfonamides (RSO2NH2): a patent review 2008–2012. Expert Opin Ther Pat 2012;22:747–58.
   PubMed Web of Science ®Google Scholar
• Masini E, Carta F, Scozzafava A, Supuran CT. Antiglaucoma carbonic anhydrase inhibitors: a patent review. Expert Opin Ther Pat 2013;23:705–16.
   PubMed Web of Science ®Google Scholar
• Monti SM, Supuran CT, De Simone G. Anticancer carbonic anhydrase inhibitors: a patent review (2008–2013). Expert Opin Ther Pat 2013;23:737–49.
   PubMed Web of Science ®Google Scholar
• Carta F, Supuran CT. Diuretics with carbonic anhydrase inhibitory action: a patent and literature review (2005–2013). Expert Opin Ther Pat 2013;23:681–91.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibitors as emerging drugs for the treatment of obesity. Expert Opin Emerg Drugs 2012;17:11–15.
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Supuran CT, Carta F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin Ther Pat 2013;23:725–35.
   PubMed Web of Science ®Google Scholar
• Supuran CT. The safety and clinical efficacy of acetazolamide for the treatment of idiopathic intracranial hypertension. Expert Rev Neurother 2015;15:851–6.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov 2017;12:61–88.
   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, et al. Carbonic anhydrase inhibitors. Synthesis of water-soluble, topically effective, intraocular pressure-lowering aromatic/heterocyclic sulfonamides containing cationic or anionic moieties: is the tail more important than the ring? J Med Chem 1999;42:2641–50.
   PubMed Web of Science ®Google Scholar
• Borras J, Scozzafava A, Menabuoni L, et al. Carbonic anhydrase inhibitors. Part 73. Synthesis of water-soluble, topically effective intraocular pressure lowering aromatic/heterocyclic sulfonamides containing 8-quinoline-sulfonyl moieties: is the tail more important than the ring? Bioorg Med Chem 1999;7:2397–406.
   PubMed Web of Science ®Google Scholar
• Winum JY, Supuran CT. Recent advances in the discovery of zinc-binding motifs for the development of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2015;30:321–4.
   PubMed Web of Science ®Google Scholar
• 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.
   Web of Science ®Google Scholar
• Supuran CT, Carbonic anhydrase inhibitors. In: Puscas I, ed. Carbonic anhydrase and modulation of physiologic and pathologic processes in the organism. Timisoara: Helicon; 1994:29–111.
   Google Scholar
• Clare BW, Supuran CT. Carbonic anhydrase activators. Part 3. Structure–activity correlations for a series of isozyme II activators. J Pharm Sci 1994;83:768–73.
   PubMed Web of Science ®Google Scholar
• Di Cesare Mannelli L, Micheli L, Carta F, et al. Carbonic anhydrase inhibition for the management of cerebral ischemia: in vivo evaluation of sulfonamide and coumarin inhibitors. J Enzyme Inhib Med Chem 2016;31:894–9.
   PubMed Web of Science ®Google Scholar
• Kalinin S, Supuran CT, Krasavin M. Multicomponent chemistry in the synthesis of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2016;31:185–99.
   PubMed Web of Science ®Google Scholar
• Elslager EF. 9-Substituted 3,6-bis(dimethylamino)acridines. J Med Chem 1962;27:4346–8.
   Google Scholar
• Elslager EF, Haley NF, McLean R, et al. Inhibition of platelet aggregation. 2. 9-{[(Dialkylamino)alkyl]thio}-3-(dimethylamino)acridines and related acridine derivatives. J Med Chem 1971;14:782–8.
   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;246:2561–73.
   PubMed Web of Science ®Google Scholar
• Yamali C, Gul HI, Sakagami H, Supuran CT. Synthesis and bioactivities of halogen bearing phenolic chalcones and their corresponding bis Mannich bases. J Enzyme Inhib Med Chem 2016;31:125–31.
   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 14 blueberry Italian cultivars. J Enzyme Inhib Med Chem 2016;31:1–6.
   PubMed Web of Science ®Google Scholar
• Margheri F, Ceruso M, Carta F, et al. Overexpression of the transmembrane carbonic anhydrase isoforms IX and XII in the inflamed synovium. J Enzyme Inhib Med Chem 2016;31:60–3.
   PubMed Web of Science ®Google Scholar
• Mishra CB, Kumari S, Angeli A, et al. Design, synthesis and biological evaluation of N-(5-methyl-isoxazol-3-yl/1,3,4-thiadiazol-2-yl)-4-(3-substitutedphenylureido) benzenesulfonamides as human carbonic anhydrase isoenzymes I, II, VII and XII inhibitors. J Enzyme Inhib Med Chem 2016;31:174–9.
   PubMed Web of Science ®Google Scholar
• Diaz JR, Fernández Baldo M, Echeverría G, et al. A substituted sulfonamide and its Co (II), Cu (II), and Zn (II) complexes as potential antifungal agents. J Enzyme Inhib Med Chem 2016;31:51–62.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Kalinin S, Tanç M, et al. Isoform-selective inhibitory profile of 2-imidazoline-substituted benzene sulfonamides against a panel of human carbonic anhydrases. J Enzyme Inhib Med Chem 2016;31:197–202.
   PubMed Web of Science ®Google Scholar
• Federici C, Lugini L, Marino ML, et al. Lansoprazole and carbonic anhydrase IX inhibitors sinergize against human melanoma cells. J Enzyme Inhib Med Chem 2016;31:119–25.
   PubMed Web of Science ®Google Scholar
• Chohan ZH, Scozzafava A, Supuran CT. Unsymmetrical 1,1′-disubstituted ferrocenes: synthesis of Co(ii), Cu(ii), Ni(ii) and Zn(ii) chelates of ferrocenyl -1-thiadiazolo-1′-tetrazole, -1-thiadiazolo-1′-triazole and -1-tetrazolo-1'-triazole with antimicrobial properties. J Enzyme Inhib Med Chem 2002;17:261–6.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, Fisher GM, et al. Discovery of a new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum – the η-carbonic anhydrases. Bioorg Med Chem Lett 2014;24:4389–96.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Scozzafava A, Mastrolorenzo A. Bacterial proteases: current therapeutic use and future prospects for the development of new antibiotics. Expert Opin Ther Pat 2001;11:221–59.
   Web of Science ®Google Scholar
• Supuran CT, Barboiu M, Luca C, et al. Carbonic anhydrase activators. Part 14. Synthesis of mono- and bis-pyridinium salt derivatives of 2-amino-5-(2-aminoethyl)- and 2-amino-5-(3-aminopropyl)-1,3,4-thiadiazole, and their interaction with isozyme II. Eur J Med Chem 1996;31:597–606.
   Web of Science ®Google Scholar