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Short Communication

Discovery of novel 1,3-diaryltriazene sulfonamides as carbonic anhydrase I, II, VII, and IX inhibitors

, , & ORCID Icon
Pages 1575-1580 | Received 28 Jul 2018, Accepted 21 Aug 2018, Published online: 09 Oct 2018

References

  • (a) Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov 2017;12:61–88; (b) 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; (c) Supuran CT, Carbon-versus sulphur-based zinc binding groups for carbonic anhydrase inhibitors? J Enzyme Inhib Med Chem 2018;33:485–95.
  • (a) Supuran CT, Capasso C. The eta-class carbonic anhydrases as drug targets for antimalarial agents. Expert Opin Ther Targets 2015;1:551–63; (b) Del Prete S, De Luca V, De Simone G, et al. Cloning, expression and purification of the complete domain of the g-carbonic anhydrase from Plasmodium falciparum. J Enzyme Inhib Med Chem 2016;31:54–9; (c) Vullo D, Del Prete S, Fisher GM, et al. Sulfonamide inhibition studies of theg-class carbonic anhydrase from the malaria pathogen Plasmodium falciparum. Bioorg Med Chem 2015;23:526–31.
  • (a) Supuran C.T. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60; (b) Supuran C.T. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32; (c) Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81; (d) Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat. Rev. Drug Discov 2011;10:767–77; (e) Supuran CT, Vullo D, Manole G, Casini A, Scozzafava A. Designing of novel carbonic anhydrase inhibitors and activators. Curr Med Chem Cardiovasc Hematol Agents 2004;2:49–68.
  • (a) Akocak S, Ilies MA. Next-generation primary sulfonamide carbonic anhydrase inhibitors. In: Supuran C.T., Cappasso C., eds. Targeting Carbonic Anhydrases. London: Future Science; 2014:35–51; (b) 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; (c) Shabana AM, Mondal UK, Alam R., et al. pH-Senstive multiligand gold nanoplatform targeting carbonic anhydrase IX enhances the delivery of Doxorubicin to hypoxic tumor spheroids and overcomes the hypoxia-induced chemoresistance. ACS Appl Mater Interfaces 2018;10:17792–808.
  • 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; in press.
  • (a) Gul HI, Yamali C, Yesilyurt F, et al. Microwave-assisted synthesis and bioevaluation of new sulfonamides. J Enzym Inhib Med Ch 2017;32:369–74; (b) Gulçin İ., Abbasova M., Taslimi P., et al. Synthesis and biological evaluation of aminomethyl and alkoxymethyl derivatives as carbonic anhydrase, acetylcholinesterase and butyrylcholinesterase inhibitors. J Enzyme Inhib Med Chem 2017;32:1174–82; (c) Guzel-Akdemir O., Akdemir A., Karali N., et al. Discovery of novel isatin-based sulfonamides with potent and selective inhibition of the tumor-associated carbonic anhydrase isoforms IX and XII. Org Biomol Chem 2015;13:6493–9; (d) Alterio V, Di Fiore A, D'Ambrosio K, Supuran CT, De Simone, G. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem Rev 2012;112:4421–68; (e) Abbate F, Winum JY, Potter BV, Casini A, Montero JL, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors: X-ray crystallographic structure of the adduct of human isozyme II with EMATE, a dual inhibitor of carbonic anhydrases and steroid sulfatase. Bioorg Med Chem Lett 2004;14:231–34.
  • 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.
  • 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.
  • 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.
  • (a) Kimball DB, Haley MM., Triazenes: a versatile tool in organic synthesis. Angew Chem Int Ed 2002;41:3338–51; (b) Marchesi F, Turriziani M, Tortorelli G, et al. Triazene compounds: mechanism of action and related DNA repair systems. Pharmacol Res 2007;56:275–87.
  • (a) Akocak S, Lolak N, Nocentini A, et al. Synthesis and biological evaluation of novel aromatic and heterocyclic bis-sulfonamide Schiff bases as carbonic anhydrase I, II, VII and IX inhibitors. Bioorg Med Chem 2017;25:3093–7; (b) Akocak S, Lolak N, Bua S, et al. Synthesis and biological evaluation of novel N,N′-diaryl cyanoguanidines acting as potent and selective carbonic anhydrase II inhibitors. Bioorg Chem 2018;77:245–51; (c) Lolak N, Akocak S., Bua S, et al. Design and synthesis of novel 1,3-diaryltriazene-substituted sulfonamides as potent and selective carbonic anhydrase II inhibitors. Bioorg Chem 2018;77:542–47.
  • 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.
  • (a) Draghici B, Vullo D, Akocak S, et al. Ethylene bis-imidazoles are highly potent and selective activators for isozymes VA and VII of carbonic anhydrase, with a potential nootropic effect. Chem Commun 2014;50:5980–3; (b) Akocak S, Lolak N, Vullo D, et al. Synthesis and biological evaluation of histamine Schiff bases as carbonic anhydrase I, II, IV, VII, and IX activators. J Enzyme Inhib Med Chem 2017;32:1305–12; (c) Buzás GM, Supuran CT. The history and rationale of using carbonic anhydrase inhibitors in the treatment of peptic ulcers. In memoriam Ioan Puşcaş (1932–2015). J Enzyme Inhib Med Chem 2016;31:527–33; (d) Supuran CT. Bacterial carbonic anhydrases as drug targets: toward novel antibiotics? Front Pharmacol 2011;2:34; (e) Nishimori I, Onishi S, Takeuchi H, Supuran CT. The alpha and beta classes carbonic anhydrases from Helicobacter pylori as novel drug targets. Curr Pharm Des 2008;14:622–30.
  • (a) Senturk M, Gulcin I, Beydemir S, et al. In vitro inhibition of human carbonic anhydrase I and II isozymes with natural phenolic compounds. Chem Biol Drug Des 2011;77:494–9; (b) Carradori S, Secci D, De Monte C, et al. A novel library ofsaccharin and acesulfame derivatives as potent and selective inhibitors of carbonic anhydrase IX and XII isoforms. Bioorg Med Chem 2016;24:1095–105; (c) Nocentini A, Bua S, Lomelino CL, et al. Discovery of new sulfonamide carbonic anhydrase IX inhibitors incorporating nitrogenous bases. ACS Med Chem Lett 2017;8:1314–19.
  • (a) Ilies MA, Vullo D, Pastorek J, et al. Carbonic anhydrase inhibitors. Inhibition of tumor-associated isozyme IX by halogenosulfanimamide and halogenophenylaminobenzolamide derivatives. J Med Chem 2003;46:2187–96; (c) Ward C, Langdon SP, Mullen P, et al. New strategies for targeting the hypoxic tumour microenvironment in breast cancer. Cancer Treat Rev 2013;39:171–79; (d) 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 tumour-associated carbonic anhydrase isozymes I, II and IX. Bioorg Med Chem Lett. 2005;15:3102–08; (e) Casey JR, Morgan PE, Vullo D, et al. Carbonic anhydrase inhibitors. Design of selective, membrane-impermeant inhibitors targeting the human tumor-associated isozyme IX. J Med Chem 2004;47:2337–47.
  • (a) Krall N, Pretto F, Decurtins W, et al. A small‐molecule drug conjugate for the treatment of carbonic anhydrase ix expressing tumors. Angew Chem Int Ed Engl 2014;53:4231–35; (b) Rehman SU, Chohan ZH, Gulnaz F, et al. In-vitro antibacterial, antifungal and cytotoxic activities of some coumarins and their metal complexes. J Enzyme Inhib Med Chem 2005;20:333–40; (c) Clare BW, Supuran CT. Carbonic anhydrase activators. 3: Structure‐activity correlations for a series of isozyme II activators. J Pharm Sci 1994;83:768–73; (d) Dubois L, Peeters S, Lieuwes NG, et al. Specific inhibition of carbonic anhydrase IX activity enhances the in vivo therapeutic effect of tumor irradiation. Radiother Oncol 2011;99:424–31; (e) Chohan ZH, Munawar A, Supuran CT. Transition metal ion complexes of Schiff-bases. Synthesis, characterization and antibacterial properties. Met Based Drugs 2001;8:137–43; (f) Zimmerman SA, Ferry JG, Supuran CT. Inhibition of the archaeal β-class (Cab) and γ-class (Cam) carbonic anhydrases. Curr Top Med Chem 2007;7:901–08.
  • (a) Supuran CT, Nicolae A, Popescu A. Carbonic anhydrase inhibitors. Part 35. Synthesis of Schiff bases derived from sulfanilamide and aromatic aldehydes: the first inhibitors with equally high affinity towards cytosolic and membrane-bound isozymes. Eur J Med Chem 1996;31:431–38; (b) Ozensoy Guler O, Capasso C, Supuran CT. A magnificent enzyme superfamily: carbonic anhydrases, their purification and characterization. J Enzyme Inhib Med Chem 2016; 31: 689–94; (c) De Simone G, Langella E, Esposito D, et al. Insights into the binding mode of sulphamates and sulphamides to hCA II: crystallographic studies and binding free energy calculations. J Enzyme Inhib Med Chem. 2017;32:1002–11; (d) Alper Türkoğlu E, Şentürk M, Supuran CT, Ekinci D. Carbonic anhydrase inhibitory properties of some uracil derivatives. J Enzyme Inhib Med Chem 2017;32:74–7; (e) Soydan E, Güler A, Bıyık S, et al. Carbonic anhydrase from Apis mellifera: purification and inhibition by pesticides. J Enzyme Inhib Med Chem 2017;32:47–50.
  • (a) Unsalan S., Cikla P., Kucukguzel SG., et al. Synthesis and characterization of triazenes derived from sulfonamides. Marmara Pharm J 2011;15:11–7; (b) Zovko TC., Brozovic A., Piantanida I., et al. Synthesis and biological evaluation of 4-nitro-substituted 1,3-diaryltriazenes as a novel class of potent antitumor agents. Eur J Med Chem 2011;46:2971–83; (c) Hill DT., Stanley KG., Williams JE., et al. 1,3-Diaryltriazenes: a new class of anorectic agents. J Med Chem 1983;26:865–9.
  • (a) 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; (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; (c) Supuran CT, Mincione F, Scozzafava A, et al. Carbonic anhydrase inhibitors—part 52. Metal complexes of heterocyclic sulfonamides: a new class of strong topical intraocular pressure-lowering agents in rabbits. Eur J Med Chem 1998;33:247–54; (d) 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 tumour-associated carbonic anhydrase isozymes I, II and IX. Bioorg Med Chem Lett 2005;15:3102–8; (e) Şentürk M, Gülçin İ, Beydemir Ş, et al. In vitro inhibition of human carbonic anhydrase I and II isozymes with natural phenolic compounds. Chem Biol Drug Des 2011;77:494–9; (f) 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.