Inhibition studies of the protozoan α-carbonic anhydrase from Trypanosoma cruzi with phenols

References

• Vermelho AB, Mori M, Donald WA, Supuran CT. Challenges and promises for obtaining new antiprotozoal drugs: what’s going wrong? In: Vermelho AB, Supuran CT, eds. Antiprotozoal drug development and delivery. Cham (Switzerland): Springer Nature; 2022:321–330.
   Google Scholar
• (a) Nocentini A, Vermelho AB, Supuran CT. Targeting carbonic anhydrases from Trypanosoma cruzi and Leishmania spp. as a therapeutic strategy to obtain new aantiprotozoal drugs. In: Vermelho AB, Supuran CT, eds. Antiprotozoal drug development and delivery. Cham (Switzerland): Springer Nature; 2022:83–112.
   Google Scholar
  (b) Vermelho AB, Cardoso V, Mansoldo FRP, et al. Chagas disease: drug development and parasite targets. In: Vermelho AB, Supuran CT, eds. Antiprotozoal drug development and delivery. Cham (Switzerland): Springer Nature; 2022:49–82.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• (a) 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.
   PubMed Web of Science ®Google Scholar
  (b) 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.
   PubMed Web of Science ®Google Scholar
• (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.
   PubMed Web of Science ®Google Scholar
  (b) Capasso C, Supuran CT. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin Ther Targets 2015;19:1689–704.
   PubMed Web of Science ®Google Scholar
  (c) 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.
   PubMed Web of Science ®Google Scholar
  (d) D’Ambrosio K, Supuran CT, De Simone G. Are carbonic anhydrases suitable targets to fight protozoan parasitic diseases? Curr Med Chem 2019;25:5266–78.
   Web of Science ®Google Scholar
• (a) Nocentini A, Cadoni R, Dumy P, et al. Carbonic anhydrases from Trypanosoma cruzi and Leishmania donovani chagasi are inhibited by benzoxaboroles. J Enzyme Inhib Med Chem 2018;33:286–9.
   PubMed Web of Science ®Google Scholar
  (b) Vermelho AB, da Silva Cardoso V, 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.
   PubMed Web of Science ®Google Scholar
  (c) Nocentini A, Osman SM, Almeida IA, et al. Appraisal of anti-protozoan activity of nitroaromatic benzenesulfonamides inhibiting carbonic anhydrases from Trypanosoma cruzi and Leishmania donovani. J Enzyme Inhib Med Chem 2019;34:1164–71.
   PubMed Web of Science ®Google Scholar
  (d) Bonardi A, Vermelho AB, da Silva Cardoso V, et al. N-nitrosulfonamides as carbonic anhydrase inhibitors: a promising chemotype for targeting Chagas disease and Leishmaniasis. ACS Med Chem Lett 2019;10:413–8.
   PubMed Web of Science ®Google Scholar
  (e) Llanos MA, Sbaraglini ML, Villalba ML, et al. A structure-based approach towards the identification of novel antichagasic compounds: Trypanosoma cruzi carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2020;35:21–30.
   PubMed Web of Science ®Google Scholar
• (a) Vermelho AB, Rodrigues GC, Supuran CT. Why hasn’t there been more progress in new Chagas disease drug discovery? Expert Opin Drug Discov 2020;15:145–58.
   PubMed Web of Science ®Google Scholar
  (b) Mansoldo FRP, Carta F, Angeli A, et al. Chagas disease: perspectives on the past and present and challenges in drug discovery. Molecules 2020;25:5483.
   PubMed Web of Science ®Google Scholar
• Simonsson I, Jonsson BH, Lindskog S. Phenol, a competitive inhibitor of CO2 hydration catalyzed by carbonic anhydrase. Biochem Biophys Res Commun 1982;108:1406–12.
   PubMed Web of Science ®Google Scholar
• Nair SK, Ludwig PA, Christianson DW. Two-site binding of phenol in the active site of human carbonic anhydrase II: structural implications for substrate association. J Am Chem Soc 1994;116:3659–60.
   Web of Science ®Google Scholar
• (a) Innocenti A, Vullo D, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors: interactions of phenols with the 12 catalytically active mammalian isoforms (CA I-XIV). Bioorg Med Chem Lett 2008;18:1583–7.
   PubMed Web of Science ®Google Scholar
  (b) Innocenti A, Vullo D, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors: inhibition of mammalian isoforms I-XIV with a series of substituted phenols including paracetamol and salicylic acid. Bioorg Med Chem 2008;16:7424–8.
   PubMed Web of Science ®Google Scholar
  (c) Innocenti A, Hilvo M, Scozzafava A, et al. Carbonic anhydrase inhibitors: inhibition of the new membrane-associated isoform XV with phenols. Bioorg Med Chem Lett 2008;18:3593–6.
   PubMed Web of Science ®Google Scholar
  (d) Davis RA, Innocenti A, Poulsen SA, Supuran CT. Carbonic anhydrase inhibitors. Identification of selective inhibitors of the human mitochondrial isozymes VA and VB over the cytosolic isozymes I and II from a natural product-based phenolic library. Bioorg Med Chem 2010;18:14–8.
   PubMed Web of Science ®Google Scholar
  (e) Davis RA, Hofmann A, Osman A, et al. Natural product-based phenols as novel probes for mycobacterial and fungal carbonic anhydrases. J Med Chem 2011;54:1682–92.
   PubMed Web of Science ®Google Scholar
• (a) Innocenti A, Gülçin I, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. Antioxidant polyphenols effectively inhibit mammalian isoforms I–XV. Bioorg Med Chem Lett 2010;20:5050–3.
   PubMed Web of Science ®Google Scholar
  (b) Sarikaya SB, Gülçin I, Supuran CT. Carbonic anhydrase inhibitors: inhibition of human erythrocyte isozymes I and II with a series of phenolic acids. Chem Biol Drug Des 2010;75:515–20.
   PubMed Web of Science ®Google Scholar
  (c) Innocenti A, Beyza Öztürk Sarıkaya S, Gülçin İ, Supuran CT. Carbonic anhydrase inhibitors. Inhibition of mammalian isoforms I–XIV with a series of natural product polyphenols and phenolic acids. Bioorg Med Chem 2010;18:2159–64.
   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
• (a) 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
  (b) Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60.
   PubMed Web of Science ®Google Scholar
• (a) 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
  (b) Nocentini A, Angeli A, Carta F, et al. Reconsidering anion inhibitors in the general context of drug design studies of modulators of activity of the classical enzyme carbonic anhydrase. J Enzyme Inhib Med Chem 2021;36:561–80.
   PubMed Web of Science ®Google Scholar
  (c) Mishra CB, Tiwari M, Supuran CT. Progress in the development of human carbonic anhydrase inhibitors and their pharmacological applications: where are we today? Med Res Rev 2020;40:2485–565.
   PubMed Web of Science ®Google Scholar
• (a) Supuran CT. Novel carbonic anhydrase inhibitors. Future Med Chem 2021;13:1935–7.
   PubMed Web of Science ®Google Scholar
  (b) Supuran CT. Emerging role of carbonic anhydrase inhibitors. Clin Sci (Lond) 2021;135:1233–49.
   PubMed Web of Science ®Google Scholar
  (c) Zimmerman SA, Ferry JG, Supuran CT. Inhibition of the archaeal beta-class (Cab) and gamma-class (Cam) carbonic anhydrases. Curr Top Med Chem 2007;7:901–8.
   PubMed Web of Science ®Google Scholar
  (d) Mori M, Supuran CT. Acipimox inhibits human carbonic anhydrases. J Enzyme Inhib Med Chem 2022;37:672–9.
   PubMed Web of Science ®Google Scholar
• (a) Andring J, Combs J, McKenna R. Aspirin: a suicide inhibitor of carbonic anhydrase II. Biomolecules 2020;10:527.
   PubMed Web of Science ®Google Scholar
  (b) D’Ambrosio K, Carradori S, Cesa S, et al. Catechols: a new class of carbonic anhydrase inhibitors. Chem Commun (Camb) 2020;56:13033–6.
   PubMed Web of Science ®Google Scholar
  (c) Simone DG, Bua S, Supuran CT, Alterio V. Benzyl alcohol inhibits carbonic anhydrases by anchoring to the zinc coordinated water molecule. Biochem Biophys Res Commun 2021;548:217–21.
   PubMed Web of Science ®Google Scholar
  (d) Di Fiore A, De Luca V, Langella E, et al. Biochemical, structural, and computational studies of a γ-carbonic anhydrase from the pathogenic bacterium Burkholderia pseudomallei. Comput Struct Biotechnol J 2022;20:4185–94.
   PubMed Web of Science ®Google Scholar
• (a) Maresca A, Temperini C, Vu H, et al. Non-zinc mediated inhibition of carbonic anhydrases: coumarins are a new class of suicide inhibitors. J Am Chem Soc 2009;131:3057–62.
   PubMed Web of Science ®Google Scholar
  (b) Maresca A, Temperini C, Pochet L, et al. Deciphering the mechanism of carbonic anhydrase inhibition with coumarins and thiocoumarins. J Med Chem 2010;53:335–44.
   PubMed Web of Science ®Google Scholar
  (c) Maresca A, Supuran CT. Coumarins incorporating hydroxy- and chloro-moieties selectively inhibit the transmembrane, tumor-associated carbonic anhydrase isoforms IX and XII over the cytosolic ones I and II. Bioorg Med Chem Lett 2010;20:4511–4.
   PubMed Web of Science ®Google Scholar
  (d) Temperini C, Innocenti A, Scozzafava A, et al. The coumarin-binding site in carbonic anhydrase accommodates structurally diverse inhibitors: the antiepileptic lacosamide as an example and lead molecule for novel classes of carbonic anhydrase inhibitors. J Med Chem 2010;53:850–4.
   PubMed Web of Science ®Google Scholar
• (a) Petreni A, Osman SM, Alasmary FA, et al. Binding site comparison for coumarin inhibitors and amine/amino acid activators of human carbonic anhydrases. Eur J Med Chem 2021;226:113875.
   PubMed Web of Science ®Google Scholar
  (b) Fuentes-Aguilar A, Merino-Montiel P, Montiel-Smith S, et al. 2-Aminobenzoxazole-appended coumarins as potent and selective inhibitors of tumour-associated carbonic anhydrases. J Enzyme Inhib Med Chem 2022;37:168–77.
   PubMed Web of Science ®Google Scholar
  (c) Giovannuzzi S, Hewitt CS, Nocentini A, et al. Coumarins effectively inhibit bacterial α-carbonic anhydrases. J Enzyme Inhib Med Chem 2022;37:333–8.
   PubMed Web of Science ®Google Scholar
  (d) Onyılmaz M, Koca M, Bonardi A, et al. Isocoumarins: a new class of selective carbonic anhydrase IX and XII inhibitors. J Enzyme Inhib Med Chem 2022;37:743–8.
   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 Commun (Camb) 2015;51:302–5.
   PubMed Web of Science ®Google Scholar
• (a) Ekinci D, Kurbanoglu NI, Salamci E, et al. Carbonic anhydrase inhibitors: inhibition of human and bovine isoenzymes by benzenesulphonamides, cyclitols and phenolic compounds. J Enzyme Inhib Med Chem 2012;27:845–8.
   PubMed Web of Science ®Google Scholar
  (b) Oztürk Sarikaya SB, Topal F, Sentürk M, et al. In vitro inhibition of α-carbonic anhydrase isozymes by some phenolic compounds. Bioorg Med Chem Lett 2011;21:4259–62.
   PubMed Web of Science ®Google Scholar
  (c) Sentürk M, Gülçin 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.
   PubMed Web of Science ®Google Scholar
• (a) Carta F, Vullo D, Maresca A, et al. Mono-/dihydroxybenzoic acid esters and phenol pyridinium derivatives as inhibitors of the mammalian carbonic anhydrase isoforms I, II, VII, IX, XII and XIV. Bioorg Med Chem 2013;21:1564–9.
   PubMed Web of Science ®Google Scholar
  (b) Maresca A, Akyuz G, Osman SM, et al. Inhibition of mammalian carbonic anhydrase isoforms I-XIV with a series of phenolic acid esters. Bioorg Med Chem 2015; 23:7181–8.
   PubMed Web of Science ®Google Scholar
  (c) Burmaoğlu S, Dilek E, Yılmaz AO, Supuran CT. Synthesis of two phloroglucinol derivatives with cinnamyl moieties as inhibitors of the carbonic anhydrase isozymes I and II: an in vitro study. J Enzyme Inhib Med Chem 2016;31:208–12.
   PubMed Web of Science ®Google Scholar
• (a) Ekinci D, Karagoz L, Ekinci D, et al. Carbonic anhydrase inhibitors: in vitro inhibition of α isoforms (hCA I, hCA II, bCA III, hCA IV) by flavonoids. J Enzyme Inhib Med Chem 2013;28:283–8.
   PubMed Web of Science ®Google Scholar
  (b) Scozzafava A, Passaponti M, Supuran CT, Gülçin İ. Carbonic anhydrase inhibitors: guaiacol and catechol derivatives effectively inhibit certain human carbonic anhydrase isoenzymes (hCA I, II, IX and XII). J Enzyme Inhib Med Chem 2015;30:586–91.
   PubMed Web of Science ®Google Scholar
  (c) Karioti A, Ceruso M, Carta F, et al. New natural product carbonic anhydrase inhibitors incorporating phenol moieties. Bioorg Med Chem 2015;23:7219–25.
   PubMed Web of Science ®Google Scholar
  (d) Karioti A, Carta F, Supuran CT. Phenols and polyphenols as carbonic anhydrase inhibitors. Molecules 2016;21:1649.
   PubMed Web of Science ®Google Scholar
• (a) Entezari Heravi Y, Bua S, Nocentini A, et al. Inhibition of Malassezia globosa carbonic anhydrase with phenols. Bioorg Med Chem 2017;25:2577–82.
   PubMed Web of Science ®Google Scholar
  (b) Nocentini A, Bua S, Del Prete S, et al. Natural polyphenols selectively inhibit β-carbonic anhydrase from the dandruff-producing fungus Malassezia globosa: activity and modeling studies. ChemMedChem 2018;13:816–23.
   PubMed Web of Science ®Google Scholar
  (c) Paloukopoulou C, Govari S, Soulioti A, et al. Phenols from Origanum dictamnus L. and Thymus vulgaris L. and their activity against Malassezia globosa carbonic anhydrase. Nat Prod Res 2022;36:1558–64.
   PubMed Web of Science ®Google Scholar
• (a) Nocentini A, Osman SM, Del Prete S, et al. Extending the γ-class carbonic anhydrases inhibition profiles with phenolic compounds. Bioorg Chem 2019;93:103336.
   PubMed Web of Science ®Google Scholar
  (b) Alissa SA, Alghulikah HA, ALOthman ZA, et al. Inhibition survey with phenolic compounds against the δ- and η-class carbonic anhydrases from the marine diatom Thalassiosira weissflogii and protozoan Plasmodium falciparum. J Enzyme Inhib Med Chem 2020;35:377–82.
   PubMed Web of Science ®Google Scholar
  (c) Grande R, Carradori S, Puca V, et al. Selective inhibition of Helicobacter pylori carbonic anhydrases by carvacrol and thymol could impair biofilm production and the release of outer membrane vesicles. Int J Mol Sci 2021;22:11583.
   PubMed Web of Science ®Google Scholar
  (d) Giovannuzzi S, Hewitt CS, Nocentini A, et al. Inhibition studies of bacterial α-carbonic anhydrases with phenols. J Enzyme Inhib Med Chem 2022;37:666–71.
   PubMed Web of Science ®Google Scholar
• (a) Supuran CT, Capasso C. Biomedical applications of prokaryotic carbonic anhydrases. Expert Opin Ther Pat 2018;28:745–54.
   PubMed Web of Science ®Google Scholar
  (b) Supuran CT, Capasso C. Antibacterial carbonic anhydrase inhibitors: an update on the recent literature. Expert Opin Ther Pat 2020;30:963–82.
   PubMed Web of Science ®Google Scholar
  (c) Hewitt CS, Abutaleb NS, Elhassanny AEM, et al. Structure-activity relationship studies of acetazolamide-based carbonic anhydrase inhibitors with activity against Neisseria gonorrhoeae. ACS Infect Dis 2021;7:1969–84.
   PubMed Web of Science ®Google Scholar
  (d) Nocentini A, Hewitt CS, Mastrolorenzo MD, et al. Anion inhibition studies of the α-carbonic anhydrases from Neisseria gonorrhoeae. J Enzyme Inhib Med Chem 2021;36:1061–6.
   PubMed Web of Science ®Google Scholar
  (e) An W, Holly KJ, Nocentini A, et al. Structure-activity relationship studies for inhibitors for vancomycin-resistant Enterococcus and human carbonic anhydrases. J Enzyme Inhib Med Chem 2022;37:1838–44.
   PubMed Web of Science ®Google Scholar
• (a) Abutaleb NS, Elhassanny AEM, Seleem MN. In vivo efficacy of acetazolamide in a mouse model of Neisseria gonorrhoeae infection. Microb Pathog 2022;164:105454.
   PubMed Web of Science ®Google Scholar
  (b) Flaherty DP, Seleem MN, Supuran CT. Bacterial carbonic anhydrases: underexploited antibacterial therapeutic targets. Future Med Chem 2021;13:1619–22.
   PubMed Web of Science ®Google Scholar
  (c) Abutaleb NS, Elkashif A, Flaherty DP, Seleem MN. In vivo antibacterial activity of acetazolamide. Antimicrob Agents Chemother 2021;65:e01715–20.
   PubMed Web of Science ®Google Scholar
• (a) Fan SH, Matsuo M, Huang L, et al. The MpsAB Bicarbonate transporter is superior to carbonic anhydrase in biofilm-forming bacteria with limited Co2 diffusion. Microbiol Spectr 2021;9:e0030521.
   PubMed Web of Science ®Google Scholar
  (b) Fan SH, Liberini E, Götz F. Staphylococcus aureus genomes harbor only MpsAB-like bicarbonate transporter but not carbonic anhydrase as dissolved inorganic carbon supply system. Microbiol Spectr 2021;9:e0097021.
   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