Sulphonamide inhibition studies of the β-carbonic anhydrase GsaCAβ present in the salmon platyhelminth parasite Gyrodactylus salaris

References

• Aspatwar A, Barker H, Aisala H, et al. Cloning, purification, kinetic and anion inhibition studies of a recombinant β-carbonic anhydrase from the Atlantic salmon parasite platyhelminth Gyrodactylus salaris. J Enzyme Inhib Med Chem 2022;37:1577–86.
   PubMed Web of Science ®Google Scholar
• Paladini G, Shinn AP, Taylor NGH, et al. Geographical distribution of Gyrodactylus salaris Malmberg, 1957 (Monogenea, Gyrodactylidae). Parasit Vectors 2021;14:34.
   PubMed Web of Science ®Google Scholar
• Zueva KJ, Lumme J, Veselov AE, et al. Genomic signatures of parasite-driven natural selection in north European Atlantic salmon (Salmo salar). Mar Genomics 2018;39:26–38.
   PubMed Web of Science ®Google Scholar
• Hansen H, Cojocaru CD, Mo TA. Infections with Gyrodactylus spp. (Monogenea) in Romanian fish farms: Gyrodactylus salaris Malmberg, 1957 extends its range. Parasit Vectors 2016;9:444.
   PubMed Web of Science ®Google Scholar
• Ramírez R, Bakke TA, Harris PD. Same barcode, different biology: differential patterns of infectivity, specificity and pathogenicity in two almost identical parasite strains. Int J Parasitol 2014;44:543–9.
   PubMed Web of Science ®Google Scholar
• Hopkins C. Introduced marine organisms in Norwegian waters, including Svalbard. Parasites and diseases. In: Leppakoski E, Gollasch S, Olenin S, eds. Invasive aquatic species of Europe. Distribution, impacts and management. Dordrecht: Springer Netherlands; 2002:13–25.
   Google Scholar
• (a) Schelkle B, Shinn AP, Peeler E, et al. Treatment of gyrodactylid infections in fish. Dis Aquat Organ 2009;86:65–75.
   PubMed Web of Science ®Google Scholar
  (b) Soleng A, Poléo AB, Alstad NE, et al. Aqueous aluminium eliminates Gyrodactylus salaris (Platyhelminthes, Monogenea) infections in Atlantic salmon. Parasitology 1999;119 (Pt 1):19–25.
   PubMedGoogle Scholar
  (c) Schmahl G. The chemotherapy of monogeneans which parasitize fish: a review. Folia Parasitol (Praha) 1991;38:97–106.
   PubMed Web of Science ®Google Scholar
• (a) Feldmeier H, Chitsulo L. Therapeutic and operational profiles of metrifonate and praziquantel in Schistosoma haematobium infection. Arzneimittelforschung 1999;49:557–65.
   PubMed Web of Science ®Google Scholar
  (b) Kramer CV, Zhang F, Sinclair D, et al. Drugs for treating urinary schistosomiasis. Cochrane Database Syst Rev 2014;2014:CD000053.
   PubMedGoogle Scholar
• (a) Skelly PJ, Nation CS, Da’Dara AA. Schistosoma mansoni and the purinergic halo. Trends Parasitol 2022;38:1080–8.
   PubMed Web of Science ®Google Scholar
  (b) Skelly PJ, Da’dara AA. Schistosome secretomes. Acta Trop 2022;236:106676.
   PubMed Web of Science ®Google Scholar
  (c) Nation CS, Da’Dara AA, Skelly PJ. NAD-catabolizing ectoenzymes of Schistosoma mansoni. Biochem J 2022;479:1165–80.
   PubMed Web of Science ®Google Scholar
  (d) Acharya S, Da’dara AA, Skelly PJ. Schistosome immunomodulators. PLoS Pathog 2021;17:e1010064.
   PubMed Web of Science ®Google Scholar
• (a) Da’dara AA, Angeli A, Ferraroni M, et al. Crystal structure and chemical inhibition of essential schistosome host-interactive virulence factor carbonic anhydrase SmCA. Commun Biol 2019;2:333.
   PubMed Web of Science ®Google Scholar
  (b) Angeli A, Pinteala M, Maier SS, et al. Sulfonamide inhibition studies of an α-carbonic anhydrase from Schistosoma mansoni, a platyhelminth parasite responsible for schistosomiasis. Int J Mol Sci 2020;21:1842.
   PubMed Web of Science ®Google Scholar
  (c) Angeli A, Ferraroni M, Da’dara AA, et al. Structural insights into Schistosoma mansoni Carbonic Anhydrase (SmCA) inhibition by selenoureido-substituted benzenesulfonamides. J Med Chem 2021;64:10418–28.
   PubMed Web of Science ®Google Scholar
• (a) Ferraroni M, Angeli A, Carradori S, et al. Inhibition of Schistosoma mansoni carbonic anhydrase by the antiparasitic drug clorsulon: X-ray crystallographic and in vitro studies. Acta Crystallogr D Struct Biol 2022;78(Pt 3):321–7.
   PubMedGoogle Scholar
  (b) Angeli A, Ferraroni M, Carta F, et al. Development of praziquantel sulphonamide derivatives as antischistosomal drugs. J Enzyme Inhib Med Chem 2022;37:1479–94.
   PubMed Web of Science ®Google Scholar
• Aspatwar A, Tolvanen MEE, Barker H, et al. Carbonic anhydrases in metazoan model organisms: molecules, mechanisms, and physiology. Physiol Rev 2022;102:1327–83.
   PubMed Web of Science ®Google Scholar
• Hooper PL, Swenson ER, Johnson RJ. Carbonic anhydrase inhibitors for the treatment of high-altitude hypoxemia. Am J Med 2019;132:e799–800.
   PubMed Web of Science ®Google Scholar
• 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
• 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
• (a) Supuran CT. Emerging role of carbonic anhydrase inhibitors. Clin Sci (Lond)) 2021;135:1233–49.
   PubMed Web of Science ®Google Scholar
  (b) Supuran CT. Carbonic anhydrase inhibitors and their potential in a range of therapeutic areas. Expert Opin Ther Pat 2018;28:709–12.
   PubMed Web of Science ®Google Scholar
  (c) Supuran CT. Applications of carbonic anhydrases inhibitors in renal and central nervous system diseases. Expert Opin Ther Pat 2018;28:713–21.
   PubMed Web of Science ®Google Scholar
  (d) Ferraroni M, Angeli A, Pinteala M, et al. Sulfonamide diuretic azosemide as an efficient carbonic anhydrase inhibitor. J Mol Struct 2022;1268:133672.
   Web of Science ®Google Scholar
• (a) Mishra CB, Kumari S, Angeli A, et al. Discovery of potent carbonic anhydrase inhibitors as effective anticonvulsant agents: drug design, synthesis, and in vitro and in vivo investigations. J Med Chem 2021;64:3100–14.
   PubMed Web of Science ®Google Scholar
  (b) Mishra CB, Kumari S, Angeli A, et al. Discovery of potent anti-convulsant carbonic anhydrase inhibitors: design, synthesis, in vitro and in vivo appraisal. Eur J Med Chem 2018;156:430–43.
   PubMed Web of Science ®Google Scholar
  (c) Shukralla AA, Dolan E, Delanty N. Acetazolamide: old drug, new evidence? Epilepsia Open 2022;7:378–92.
   PubMedGoogle Scholar
  (d) Ciccone L, Cerri C, Nencetti S, et al. Carbonic anhydrase inhibitors and epilepsy: state of the art and future perspectives. Molecules 2021;26:6380.
   PubMed Web of Science ®Google Scholar
• (a) Supuran CT. Multitargeting approaches involving carbonic anhydrase inhibitors: hybrid drugs against a variety of disorders. J Enzyme Inhib Med Chem 2021;36:1702–14.
   PubMed Web of Science ®Google Scholar
  (b) Mincione F, Nocentini A, Supuran CT. Advances in the discovery of novel agents for the treatment of glaucoma. Expert Opin Drug Discov 2021;16:1209–25.
   PubMed Web of Science ®Google Scholar
  (c) Bonardi A, Nocentini A, Bua S, et al. Sulfonamide inhibitors of human carbonic anhydrases designed through a three-tails approach: improving ligand/isoform matching and selectivity of action. J Med Chem 2020;63:7422–44.
   PubMed Web of Science ®Google Scholar
• (a) Supuran CT. Anti-obesity carbonic anhydrase inhibitors: challenges and opportunities. J Enzyme Inhib Med Chem 2022;37:2478–88.
   PubMed Web of Science ®Google Scholar
  (b) 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
  (c) Muñoz W, Lamm A, Poppers D, et al. Acetazolamide promotes decreased consumption of carbonated drinks and weight loss. Oxf Med Case Reports 2018;2018:omy081.
   PubMedGoogle Scholar
  (d) Supuran CT. Carbonic anhydrases and metabolism. Metabolites 2018;8:25.
   PubMed Web of Science ®Google Scholar
• (a) Angeli A, Carta F, Nocentini A, et al. Carbonic anhydrase inhibitors targeting metabolism and tumor microenvironment. Metabolites 2020;10:412.
   PubMed Web of Science ®Google Scholar
  (b) McDonald PC, Chafe SC, Supuran CT, et al. Cancer therapeutic targeting of hypoxia induced carbonic anhydrase IX: from bench to bedside. Cancers (Basel) 2022;14:3297.
   PubMed Web of Science ®Google Scholar
  (c) Chafe SC, Vizeacoumar FS, Venkateswaran G, et al. Genome-wide synthetic lethal screen unveils novel CAIX-NFS1/xCT axis as a targetable vulnerability in hypoxic solid tumors. Sci Adv 2021;7:eabj0364.
   PubMed Web of Science ®Google Scholar
  (d) Supuran CT. Carbonic anhydrase inhibitors as emerging agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs 2018;27:963–70.
   PubMed Web of Science ®Google Scholar
  (e) Supuran CT. Carbonic anhydrase inhibitors: an update on experimental agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs 2021;30:1197–208.
   PubMed Web of Science ®Google Scholar
• (a) Angeli A, Urbański LJ, Capasso C, et al. Activation studies with amino acids and amines of a β-carbonic anhydrase from Mammaliicoccus (Staphylococcus) sciuri previously annotated as Staphylococcus aureus (SauBCA) carbonic anhydrase. J Enzyme Inhib Med Chem 2022;37:2786–92.
   PubMed Web of Science ®Google Scholar
  (b) 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
  (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) Abutaleb NS, Elhassanny AEM, Nocentini A, et al. Repurposing FDA-approved sulphonamide carbonic anhydrase inhibitors for treatment of Neisseria gonorrhoeae. J Enzyme Inhib Med Chem 2022;37:51–61.
   PubMed Web of Science ®Google Scholar
  (e) 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
  (f) 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
  (g) De Luca V, Giovannuzzi S, Supuran CT, et al. May sulfonamide inhibitors of carbonic anhydrases from Mammaliicoccus sciuri Prevent antimicrobial resistance due to gene transfer to other harmful Staphylococci? Int J Mol Sci 2022;23:13827.
   PubMed Web of Science ®Google Scholar
  (h) 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
• (a) Angeli A, Velluzzi A, Selleri S, et al. Seleno containing compounds as potent and selective antifungal agents. ACS Infect Dis 2022;8:1905–19.
   PubMed Web of Science ®Google Scholar
  (b) De Luca V, Angeli A, Mazzone V, et al. Heterologous expression and biochemical characterisation of the recombinant β-carbonic anhydrase (MpaCA) from the warm-blooded vertebrate pathogen malassezia pachydermatis. J Enzyme Inhib Med Chem 2022;37:62–8.
   PubMed Web of Science ®Google Scholar
  (c) Supuran CT, Capasso C. A highlight on the inhibition of fungal carbonic anhydrases as drug targets for the antifungal armamentarium. Int J Mol Sci 2021;22:4324.
   PubMed Web of Science ®Google Scholar
• (a) Bonardi A, Parkkila S, Supuran CT. Inhibition studies of the protozoan α-carbonic anhydrase from Trypanosoma cruzi with phenols. J Enzyme Inhib Med Chem 2022; 37:2417–22.
   PubMed Web of Science ®Google Scholar
  (b) Urbański LJ, Angeli A, Mykuliak VV, et al. Biochemical and structural characterization of beta-carbonic anhydrase from the parasite Trichomonas vaginalis. J Mol Med (Berl) 2022;100:115–24.
   PubMed Web of Science ®Google Scholar
  (c) Syrjänen L, Vermelho AB, Rodrigues IDA, 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.
   PubMed Web of Science ®Google Scholar
  (d) Pal DS, Mondal DK, Datta R. Identification of metal dithiocarbamates as a novel class of antileishmanial agents. Antimicrob Agents Chemother 2015;59:2144–52.
   PubMed Web of Science ®Google Scholar
  (e) Pal DS, Abbasi M, Mondal DK, et al. Interplay between a cytosolic and a cell surface carbonic anhydrase in pH homeostasis and acid tolerance of Leishmania. J Cell Sci 2017;130:754–66.
   PubMed Web of Science ®Google Scholar
  (f) Reungprapavut S, Krungkrai SR, Krungkrai J. Plasmodium falciparum carbonic anhydrase is a possible target for malaria chemotherapy. J Enzyme Inhib Med Chem 2004;19:249–56.
   PubMed Web of Science ®Google Scholar
  (g) Krungkrai J, Krungkrai SR, Supuran CT. Carbonic anhydrase inhibitors: inhibition of Plasmodium falciparum carbonic anhydrase with aromatic/heterocyclic sulfonamides-in vitro and in vivo studies. Bioorg Med Chem Lett 2008;18:5466–71.
   PubMed Web of Science ®Google Scholar
• (a) Zolfaghari Emameh R, Kuuslahti M, Vullo D, et al. Ascaris lumbricoides β carbonic anhydrase: a potential target enzyme for treatment of ascariasis. Parasit Vectors 2015;8:479.
   PubMed Web of Science ®Google Scholar
  (b) Zolfaghari Emameh R, Barker H, Hytönen VP, et al. Beta carbonic anhydrases: novel targets for pesticides and anti-parasitic agents in agriculture and livestock husbandry. Parasit Vectors 2014;7:403.
   PubMed Web of Science ®Google Scholar
  (c) Zolfaghari Emameh R, Syrjänen L, Barker H, et al. Drosophila melanogaster: a model organism for controlling Dipteran vectors and pests. J Enzyme Inhib Med Chem 2015;30:505–13.
   PubMed Web of Science ®Google Scholar
• (a) Abbate F, Winum JY, Potter BV, et al. 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;14:231–4.
   PubMed Web of Science ®Google Scholar
  (b) 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.
   Web of Science ®Google Scholar
  (c) Gieling RG, Babur M, Mamnani L, et al. Antimetastatic effect of sulfamate carbonic anhydrase IX inhibitors in breast carcinoma xenografts. J Med Chem 2012;55:5591–600.
   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) Nishimori I, Minakuchi T, Morimoto K, et al. Carbonic anhydrase inhibitors: DNA cloning and inhibition studies of the alpha-carbonic anhydrase from Helicobacter pylori, a new target for developing sulfonamide and sulfamate gastric drugs. J Med Chem 2006;49:2117–26.
   PubMed Web of Science ®Google Scholar
  (b) 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
• (a) 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
  (b) Supuran CT. Carbonic anhydrase inhibitors from marine natural products. Mar Drugs. 2022;20:721.
   PubMed Web of Science ®Google Scholar