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Research Paper

Antileishmanial activity of sulphonamide nanoemulsions targeting the β-carbonic anhydrase from Leishmania species

, ORCID Icon, , , & ORCID Icon
Pages 850-857 | Received 26 Mar 2018, Accepted 06 Apr 2018, Published online: 30 Apr 2018

References

  • 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.
  • 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.
  • Supuran CT, Capasso C. Protozoan carbonic anhydrases. In: Supuran CT, Capasso C, eds. Zinc enzyme inhibitors – Volume 1: enzymes from microorganisms. Berlin, Germany: Springer; 2017:114–134.
  • Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32.
  • Lomelino CL, Supuran CT, McKenna R. Non-classical inhibition of carbonic anhydrase. Int J Mol Sci 2016;17:E1150.
  • Nocentini A, Vullo D, Del Prete S, et al. Inhibition of the β-carbonic anhydrase from the dandruff-producing fungus Malassezia globosa with monothiocarbamates. J Enzyme Inhib Med Chem 2017;32:1064–70.
  • (a) Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81. (b) Supuran CT. carbonic anhydrase activators. Future Med Chem 2018;10:561–73. (c) 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. (d) Angeli A, Vaiano F, Mari F, et al. Psychoactive substances belonging to the amphetamine class potently activate brain carbonic anhydrase isoforms VA, VB, VII, and XII. J Enzyme Inhib Med Chem 2017;32:1253–9. (e) Licsandru E, Tanc M, Kocsis I, et al. A class of carbonic anhydrase I - selective activators. J Enzyme Inhib Med Chem 2017;32:37–46.
  • (a) Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016; 31:345–60. (b) 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) Supuran CT. Structure-based drug discovery of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2012; 27:759–72. (b) Supuran CT. Carbonic anhydrase inhibition and the management of hypoxic tumors. Metabolites 2017;7:E48.
  • Scozzafava A, Supuran CT, Carta F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin Ther Patents 2013;23:725–35.
  • Nocentini A, Carta F, Ceruso M, et al. Click-tailed coumarins with potent and selective inhibitory action against the tumor-associated carbonic anhydrases IX and XII. Bioorg Med Chem 2015;23:6955–66.
  • 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.
  • Supuran CT, Capasso C. New light on bacterial carbonic anhydrases phylogeny based on the analysis of signal peptide sequences. J Enzyme Inhib Med Chem 2016;31:1254–60.
  • 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.
  • Capasso C, Supuran CT. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin Ther Targets 2015;19:1689–704.
  • (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) Kusuzaki K, Matsubara T, Murata H, et al. Natural extracellular nanovesicles and photodynamic molecules: is there a future for drug delivery? J Enzyme Inhib Med Chem 2017;32:908–16. (c) Ward C, Langdon SP, Mullen P, et al. New strategies for targeting the hypoxic tumour microenvironment in breast cancer. Cancer Treat Rev 2013;39:171–9.
  • Vermelho AB, Capaci GR, Rodrigues IA, et al. Carbonic anhydrases from Trypanosoma and Leishmania as anti-protozoan drug targets. Bioorg Med Chem 2017;25:1543–55.
  • Prete SD, 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.
  • (a) Supuran CT. Inhibition of carbonic anhydrase from Trypanosoma cruzi for the management of Chagas disease: an underexplored therapeutic opportunity. Future Med Chem 2016;8:311–24. (b) 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. (c) 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. (d) 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.
  • Capasso C, Supuran CT. An overview of the selectivity and efficiency of the bacterial carbonic anhydrase inhibitors. Curr Med Chem 2015;22:2130–9.
  • Moraes ARDP, Tavares GD, Rocha FJS, et al. Effects of nanoemulsions prepared with essential oils of copaiba- and andiroba against Leishmania infantum and Leishmania amazonensis infections. Exp Parasitol 2018;187:12–21.
  • Fernandes Rodrigues JC, Concepcion JL, Rodrigues C, et al. In vitro activities of ER-119884 and E5700, two potent squalene synthase inhibitors, against Leishmania amazonensis: antiproliferative, biochemical, and ultrastructural effects. Antimicrob Agents Chemother 2008;52:4098–114.
  • Dagnino APA, Mesquita CS, Dorneles GP, et al. Phloroglucinol derivatives from Hypericum species trigger mitochondrial dysfunction in Leishmania amazonensis. Parasitology 2018;27:1–11.
  • Pan P, Vermelho AB, Capaci Rodrigues G, et al. Cloning, characterization, and sulfonamide and thiol inhibition studies of an α-carbonic anhydrase from Trypanosoma cruzi, the causative agent of Chagas disease. J Med Chem 2013;56:1761–71.
  • Güzel-Akdemir Ö, Akdemir A, Pan P, et al. A class of sulfonamides with strong inhibitory action against the α-carbonic anhydrase from Trypanosoma cruzi. J Med Chem 2013;56:5773–81.
  • Menezes Dda R, Calvet CM, Rodrigues GC, et al. Hydroxamic acid derivatives: a promising scaffold for rational compound optimization in Chagas disease. J Enzyme Inhib Med Chem 2016;31:964–73.
  • Rodrigues GC, Feijó DF, Bozza MT, et al. Design, synthesis, and evaluation of hydroxamic acid derivatives as promising agents for the management of Chagas disease. J Med Chem 2014;57:298–308.
  • Pan P, Vermelho AB, Scozzafava A, et al. Anion inhibition studies of the α-carbonic anhydrase from the protozoan pathogen Trypanosoma cruzi, the causative agent of Chagas disease. Bioorg Med Chem 2013;21:4472–6.
  • Syrjänen L, Vermelho AB, Rodrigues Ide A, et al. Cloning, characterization, and inhibition studies of a β-carbonic anhydrase from Leishmania donovani chagasi, the protozoan parasite responsible for leishmaniasis. J Med Chem 2013;56:7372–81.
  • de Campos VE, Ricci-Júnior E, Mansur CR. Nanoemulsions as delivery systems for lipophilic drugs. J Nanosci Nanotechnol 2012;12:2881–90.
  • Senna JP, Ricci-Júnior E, Mansur CRE. Development and evaluation of nanoemulsions containing phthalocyanines for use in photodynamic cancer therapy. J Nanosci Nanotechno 2015;15:4205–14.
  • Vermelho AB, Cardoso VS, Ricci Junior E, et al. Nanoemulsions of sulfonamide carbonic anhydrase inhibitors strongly inhibit the growth of Trypanosoma cruzi. J Enzyme Inhib Med Chem 2018;33:139–46.
  • 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) 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;3:1001–10. (b) 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;31:431–8. (c) 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. (d) Tars K, Vullo D, Kazaks K, et al. Sulfocoumarins (1,2-benzoxathiine-2,2-dioxides): a class of potent and isoform-selective inhibitors of tumor-associated carbonic anhydrases. J Med Chem 2013;56:293–300.
  • (a) Supuran CT, Clare BW. Carbonic anhydrase inhibitors. Part 57. Quantum chemical QSAR of a group of 1,3,4-thiadiazole and 1,3,4-thiadiazoline disulfonamides with carbonic anhydrase inhibitory properties. Eur J Med Chem 1999;34:41–50. (b) Mastrolorenzo A, Rusconi S, Scozzafava A, et al. Inhibitors of HIV-1 protease: current state of the art 10 years after their introduction. From antiretroviral drugs to antifungal, antibacterial and antitumor agents based on aspartic protease inhibitors. Curr Med Chem 2007;14:2734–48.
  • (a) Puccetti L, Fasolis G, Vullo D, et al. Carbonic anhydrase inhibitors. Inhibition of cytosolic/tumor-associated carbonic anhydrase isozymes I, II, IX, and XII with Schiff’s bases incorporating chromone and aromatic sulfonamide moieties, and their zinc complexes. Bioorg Med Chem Lett 2005;15:3096–101. (b) 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.
  • Zetasizer Nano. User manual. Malvern: Malvern Instruments. Man0485, n. 1.1, 2004. Available from: http://www.malvern.com/en/support/resource-center/usermanuals/MAN0485EN.aspx. [last access 15 Jan 2018].
  • Rodrigues IA, Silva BA, Santos ALS, et al. A new experimental culture medium for cultivation of Leishmania amazonensis: its efficacy for the continuous in vitro growth and differentiation of infective promastigote forms. Parasitol Res 2010;106:1249–52.
  • Rolon M, Vega C, Escario JA, Gómez-Barrio A. Development of resazurin microtiter assay for drug sensibility testing of Trypanosoma cruzi epimastigotes. Parasitol Res 2006;99:103–7.
  • Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983;983:55–63.
  • Katsuno K, Burrows JN, Duncan K, et al. Hit and lead criteria in drug discovery for infectious diseases of the developing world. Nat Rev Drug Discov 2015;14:751–8.
  • Ishnava KB, Shah PP. Anticariogenic and hemolytic activity of selected seed protein extracts in vitro conditions. J Dent 2014;11:576.
  • Pham TT, Loiseau PM, Barratt G. Strategies for the design of orally bioavailable antileishmanial treatments. Int J Pharm 2013;454:539–52.
  • Chattopadhyay A, Jafurulla M. A novel mechanism for an old drug: amphotericin B in the treatment of visceral leishmaniasis. Biochem Biophys Res Commun 2011;416:7–12.
  • Lo´pez-Arencibia A, Garci´a VD, Marti´n-Navarro CM, et al. In vitro activities of hexaazatrinaphthylenes against Leishmania spp. Antimicrob Agents Chemother 2015;59:2867–74.
  • Gupta PK, Jaiswal AK, Asthana S, et al. Synergistic enhancement of parasiticidal activity of amphotericin B using copaiba oil in nanoemulsified carrier for oral delivery: an approach for non-toxic chemotherapy. Br J Pharmacol 2015;172:3596–610.
  • Santos DCMD, de Souza MLS, Teixeira EM, et al. A new nanoemulsion formulation improves antileishmanial activity and reduces toxicity of amphotericin B. J Drug Target 2018;26:357–64.
  • Islamuddin M, Sahal D, Afrin F. Apoptosis-like death in Leishmania donovani promastigotes induced by eugenol-rich oil of Syzygium aromaticum. J Med Microbiol 2014;63:74–85.