Cloning, expression and purification of the complete domain of the η-carbonic anhydrase from Plasmodium falciparum

References

• Syrjanen L, Vermelho AB, Rodrigues Ide A, et al. Cloning, characterization, and inhibition studies of a beta-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
• Rodrigues Ide A, da Silva BA, dos Santos AL, 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
   PubMed Web of Science ®Google Scholar
• Rodrigues GC, Feijo 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
• Pan P, Vermelho AB, Scozzafava A, et al. Anion inhibition studies of the alpha-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
• 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
• Pan P, Vermelho AB, Capaci Rodrigues G, et al. Cloning, characterization, and sulfonamide and thiol inhibition studies of an alpha-carbonic anhydrase from Trypanosoma cruzi, the causative agent of Chagas disease. J Med Chem 2013;56:1761–71
   PubMed Web of Science ®Google Scholar
• de Menezes DD, Calvet CM, Rodrigues GC, et al. Hydroxamic acid derivatives: a promising scaffold for rational compound optimization in Chagas disease. J Enzyme Inhib Med Chem 2015. [Epub ahead of print]. doi: 10.3109/14756366.2015.1077330
   PubMed Web of Science ®Google Scholar
• Alafeefy AM, Ceruso M, Al-Jaber NA, et al. A new class of quinazoline-sulfonamides acting as efficient inhibitors against the alpha-carbonic anhydrase from Trypanosoma cruzi. J Enzyme Inhib Med Chem 2015;30:581–5
   PubMed Web of Science ®Google Scholar
• Guzel-Akdemir O, Akdemir A, Pan P, et al. Sulfonamides with strong inhibitory action against the alpha-carbonic anhydrase from Trypanosoma cruzi. J Med Chem 2013;56:5773–81
   PubMed Web of Science ®Google Scholar
• Kuijpers LM, Maltha J, Guiraud I, et al. Severe anemia associated with Plasmodium falciparum infection in children: consequences for additional blood sampling for research. Malar J 2016;15:304
   PubMed Web of Science ®Google Scholar
• Scholzen A, Sauerwein RW. Immune activation and induction of memory: lessons learned from controlled human malaria infection with Plasmodium falciparum. Parasitology 2016;143:224–35
   PubMed Web of Science ®Google Scholar
• Antony HA, Parija SC. Antimalarial drug resistance: an overview. Trop Parasitol 2016;6:30–41
   PubMedGoogle Scholar
• Packard RM. The origins of antimalarial-drug resistance. N Engl J Med 2014;371:397–9
   PubMed Web of Science ®Google Scholar
• Ludin P, Woodcroft B, Ralph SA, Maser P. In silico prediction of antimalarial drug target candidates. Int J Parasitol Drugs Drug Resist 2012;2:191–9
   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
• Capasso C, Supuran CT. An Overview of the selectivity and efficiency of the bacterial carbonic anhydrase inhibitors. Curr Med Chem 2015;22:2130–9
   PubMed Web of Science ®Google Scholar
• 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
• De Luca V, Del Prete S, Supuran CT, Capasso C. Protonography, a new technique for the analysis of carbonic anhydrase activity. J Enzyme Inhib Med Chem 2015;30:277–82
   PubMed Web of Science ®Google Scholar
• Akdemir A, Vullo D, Luca VD, et al. The extremo-alpha-carbonic anhydrase (CA) from Sulfurihydrogenibium azorense, the fastest CA known, is highly activated by amino acids and amines. Bioorg Med Chem Lett 2013;23:1087–90
   PubMed Web of Science ®Google Scholar
• McKenna R, Supuran CT. Carbonic anhydrase inhibitors drug design. Sub-Cell Biochem 2014;75:291–323
   PubMedGoogle 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
• Monti SM, Maresca A, Viparelli F, et al. Dithiocarbamates are strong inhibitors of the beta-class fungal carbonic anhydrases from Cryptococcus neoformans, Candida albicans and Candida glabrata. Bioorg Med Chem Lett 2012;22:859–62
   PubMed Web of Science ®Google Scholar
• Adak AK, Leonov AP, Ding N, et al. Bishydrazide glycoconjugates for lectin recognition and capture of bacterial pathogens. Bioconjugate Chem 2010;21:2065–75
   PubMed Web of Science ®Google Scholar
• Supuran CT. Legionella pneumophila carbonic anhydrases: underexplored antibacterial drug targets. Pathogens 2016;5:E44
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, et al. Comparison of the sulfonamide inhibition profiles of the alpha-, beta- and gamma-carbonic anhydrases from the pathogenic bacterium Vibrio cholerae. Bioorg Med Chem Lett 2016;26:1941–6
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, Scozzafava A, et al. Cloning, characterization and anion inhibition study of the delta-class carbonic anhydrase (TweCA) from the marine diatom Thalassiosira weissflogii. Bioorg Med Chem 2014;22:531–7
   PubMed Web of Science ®Google Scholar
• Vullo D, Luca VD, Scozzafava A, et al. The alpha-carbonic anhydrase from the thermophilic bacterium Sulfurihydrogenibium yellowstonense YO3AOP1 is highly susceptible to inhibition by sulfonamides. Bioorg Med Chem 2013;21:1534–8
   PubMed Web of Science ®Google Scholar
• Vullo D, De Luca V, Scozzafava A, et al. Anion inhibition studies of the fastest carbonic anhydrase (CA) known, the extremo-CA from the bacterium Sulfurihydrogenibium azorense. Bioorg Med Chem Lett 2012;22:7142–5
   PubMed Web of Science ®Google Scholar
• Vullo D, De Luca V, Scozzafava A, et al. The first activation study of a bacterial carbonic anhydrase (CA). The thermostable alpha-CA from Sulfurihydrogenibium yellowstonense YO3AOP1 is highly activated by amino acids and amines. Bioorg Med Chem Lett 2012;22:6324–7
   PubMed Web of Science ®Google Scholar
• Luca VD, Vullo D, Scozzafava A, et al. An alpha-carbonic anhydrase from the thermophilic bacterium Sulphurihydrogenibium azorense is the fastest enzyme known for the CO(2) hydration reaction. Bioorg Med Chem 2013;21:1465–9
   PubMed Web of Science ®Google Scholar
• De Luca V, Vullo D, Scozzafava A, et al. Anion inhibition studies of an alpha-carbonic anhydrase from the thermophilic bacterium Sulfurihydrogenibium yellowstonense YO3AOP1. Bioorg Med Chem Lett 2012;22:5630–4
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D,D, Luca V, et al. Anion inhibition profiles of alpha-, beta- and gamma-carbonic anhydrases from the pathogenic bacterium Vibrio cholerae. Bioorg Med Chem 2016;24:3413–17
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. An overview of the carbonic anhydrases from two pathogens of the oral cavity: Streptococcus mutans and Porphyromonas gingivalis. Curr Top Med Chem 2016;16:2359–68
   PubMed Web of Science ®Google Scholar
• Vullo D, Del Prete S, Osman SM, et al. Anion inhibition study of the beta-class carbonic anhydrase (PgiCAb) from the oral pathogen Porphyromonas gingivalis. Bioorg Med Chem Lett 2014;24:4402–6
   PubMed Web of Science ®Google Scholar
• Vullo D, Del Prete S, Osman SM, et al. Sulfonamide inhibition studies of the gamma-carbonic anhydrase from the oral pathogen Porphyromonas gingivalis. Bioorg Med Chem Lett 2014;24:240–4
   PubMed Web of Science ®Google Scholar
• Singh S, Supuran CT. 3D-QSAR CoMFA studies on sulfonamide inhibitors of the Rv3588c β-carbonic anhydrase from Mycobacterium tuberculosis and design of not yet synthesized new molecules. J Enzyme Inhib Med Chem 2014;29:449–55
   PubMed Web of Science ®Google Scholar
• Prete SD, Vullo D, Osman SM, et al. Sulfonamide inhibition study of the carbonic anhydrases from the bacterial pathogen Porphyromonas gingivalis: the beta-class (PgiCAb) versus the gamma-class (PgiCA) enzymes. Bioorg Med Chem 2014;22:4537–43
   PubMed Web of Science ®Google Scholar
• Nishimori I, Vullo D, Minakuchi T, et al. Anion inhibition studies of two new beta-carbonic anhydrases from the bacterial pathogen Legionella pneumophila. Bioorg Med Chem Lett 2014;24:1127–32
   PubMed Web of Science ®Google Scholar
• Nishimori I, Vullo D, Minakuchi T, et al. Sulfonamide inhibition studies of two beta-carbonic anhydrases from the bacterial pathogen Legionella pneumophila. Bioorg Med Chem 2014;22:2939–46
   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
• Del Prete S, De Luca V, Vullo D, et al. Biochemical characterization of the gamma-carbonic anhydrase from the oral pathogen Porphyromonas gingivalis, PgiCA. J Enzyme Inhib Med Chem 2014;29:532–7
   PubMed Web of Science ®Google Scholar
• Del Prete S, De Luca V, Scozzafava A, et al. Biochemical properties of a new alpha-carbonic anhydrase from the human pathogenic bacterium, Vibrio cholerae. J Enzyme Inhib Med Chem 2014;29:23–7
   PubMed Web of Science ®Google Scholar
• Ceruso M, Vullo D, Scozzafava A, Supuran CT. Sulfonamides incorporating fluorine and 1,3,5-triazine moieties are effective inhibitors of three beta-class carbonic anhydrases from Mycobacterium tuberculosis. J Enzyme Inhib Med Chem 2014;29:686–9
   PubMed Web of Science ®Google Scholar
• Ceruso M, Del Prete S, AlOthman Z, et al. Synthesis of sulfonamides with effective inhibitory action against Porphyromonas gingivalis gamma-carbonic anhydrase. Bioorg Med Chem Lett 2014;24:4006–10
   PubMed Web of Science ®Google Scholar
• Vullo D, Del Prete S, Fisher GM, et al. Sulfonamide inhibition studies of the eta-class carbonic anhydrase from the malaria pathogen Plasmodium falciparum. Bioorg Med Chem 2015;23:526–31
   PubMed Web of Science ®Google Scholar
• Riafrecha LE, Vullo D, Supuran CT, Colinas PA. C-glycosides incorporating the 6-methoxy-2-naphthyl moiety are selective inhibitors of fungal and bacterial carbonic anhydrases. J Enzyme Inhib Med Chem 2015;30:857–61
   PubMed Web of Science ®Google Scholar
• Riafrecha LE, Vullo D, Ouahrani-Bettache S, et al. Inhibition of β-carbonic anhydrases from Brucella suis with C-cinnamoyl glycosides incorporating the phenol moiety. J Enzyme Inhib Med Chem 2015;30:1017–20
   PubMed Web of Science ®Google Scholar
• Ombouma J, Vullo D, Kohler S, et al. N-glycosyl-N-hydroxysulfamides as potent inhibitors of Brucella suis carbonic anhydrases. J Enzyme Inhib Med Chem 2015;30:1010–12
   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
• Dedeoglu N, DeLuca V, Isik S, et al. Sulfonamide inhibition study of the beta-class carbonic anhydrase from the caries producing pathogen Streptococcus mutans. Bioorg Med Chem Lett 2015;25:2291–7
   PubMed Web of Science ®Google Scholar
• Dedeoglu N, De Luca V, Isik S, et al. Cloning, characterization and anion inhibition study of a beta-class carbonic anhydrase from the caries producing pathogen Streptococcus mutans. Bioorg Med Chem 2015;23:2995–3001
   PubMed Web of Science ®Google Scholar
• Ceruso M, Carta F, Osman SM, et al. Inhibition studies of bacterial, fungal and protozoan beta-class carbonic anhydrases with Schiff bases incorporating sulfonamide moieties. Bioorg Med Chem 2015;23:4181–7
   PubMed Web of Science ®Google Scholar
• De Simone G, Di Fiore A, Capasso C, Supuran CT. The zinc coordination pattern in the eta-carbonic anhydrase from Plasmodium falciparum is different from all other carbonic anhydrase genetic families. Bioorg Med Chem Lett 2015;25:1385–9
   PubMed Web of Science ®Google Scholar
• Cassera MB, Zhang Y, Hazleton KZ, Schramm VL. Purine and pyrimidine pathways as targets in Plasmodium falciparum. Curr Top Med Chem 2011;11:2103–15
   PubMed Web of Science ®Google Scholar
• Del Prete S,D, Luca V, Vullo D, et al. A new procedure for the cloning, expression and purification of the beta-carbonic anhydrase from the pathogenic yeast Malassezia globosa, an anti-dandruff drug target. J Enzyme Inhib Med Chem 2015. [Epub ahead of print]. doi: 10.3109/14756366.2015.1102137
   Web of Science ®Google Scholar
• 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
• Carta F, Osman SM, Vullo D, et al. Poly(amidoamine) dendrimers show carbonic anhydrase inhibitory activity against alpha-, beta-, gamma- and eta-class enzymes. Bioorg Med Chem 2015;23:6794–8
   PubMed Web of Science ®Google Scholar
• Del Prete S, De Luca V, Iandolo E, et al. Protonography, a powerful tool for analyzing the activity and the oligomeric state of the gamma-carbonic anhydrase identified in the genome of Porphyromonas gingivalis. Bioorg Med Chem 2015;23:3747–50
   PubMed Web of Science ®Google Scholar
• Del Prete S, De Luca V, Supuran CT, Capasso C. Protonography, a technique applicable for the analysis of eta-carbonic anhydrase activity. J Enzyme Inhib Med Chem 2015;30:920–4
   PubMed Web of Science ®Google Scholar
• Supuran CT, Capasso C. The η-class carbonic anhydrases as drug targets for antimalarial agents. Expert Opin Ther Targets 2015;19:551–63
   PubMed Web of Science ®Google Scholar
• Syrjanen L, Kuuslahti M, Tolvanen M, et al. The beta-carbonic anhydrase from the malaria mosquito Anopheles gambiae is highly inhibited by sulfonamides. Bioorg Med Chem 2015;23:2303–9
   PubMed Web of Science ®Google Scholar
• Krungkrai J, Supuran CT. The alpha-carbonic anhydrase from the malaria parasite and its inhibition. Curr Pharm Des 2008;14:631–40
   PubMed Web of Science ®Google Scholar
• Krungkrai J, Scozzafava A, Reungprapavut S, et al. Carbonic anhydrase inhibitors. Inhibition of Plasmodium falciparum carbonic anhydrase with aromatic sulfonamides: towards antimalarials with a novel mechanism of action? Bioorg Med Chem 2005;13:483–9
   PubMed Web of Science ®Google Scholar
• 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
• 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
• Krungkrai SR, Suraveratum N, Rochanakij S, Krungkrai J. Characterisation of carbonic anhydrase in Plasmodium falciparum. Int J Parasitol 2001;31:661–8
   PubMed Web of Science ®Google Scholar
• Leese MP, Leblond B, Smith A, et al. 2-Substituted estradiol bis-sulfamates, multitargeted antitumor agents: synthesis, in vitro SAR, protein crystallography, and in vivo activity. J Med Chem 2006;49:7683–96
   PubMed Web of Science ®Google Scholar
• Mount DW. Using the basic local alignment search tool (BLAST). CSH Protoc 2007;2007:pdb top17
   PubMedGoogle Scholar
• Altschul SF, Gish W, Miller W, et al. Basic local alignment search tool. J Mol Biol 1990;215:403–10
   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
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680–5
   PubMed Web of Science ®Google Scholar