Cloning, expression and biochemical characterization of a β-carbonic anhydrase from the soil bacterium Enterobacter sp. B13

References

• Smith KS, Ferry JG. Prokaryotic carbonic anhydrases. FEMS Microbiol Rev 2000;24:335–66
   PubMed Web of Science ®Google Scholar
• Hashimoto M, Kato JI. Indispensability of the Escherichia coli carbonic anhydrases YadF and CynT in cell proliferation at a low CO2 partial pressure. Biosci Biotechnol Biochem 2003;67:919–22
   PubMed Web of Science ®Google Scholar
• Rodriguez-Navarro C, Jroundi F, Schiro M, et al. Influence of substrate mineralogy on bacterial mineralization of calcium carbonate: implications for stone conservation. Appl Environm Microbiol 2012;78:4017–29
   PubMed Web of Science ®Google Scholar
• Capasso C, De Luca V, Carginale V, et al. Biochemical properties of a novel and highly thermostable bacterial α-carbonic anhydrase from Sulfurihydrogenibium yellowstonense YO3AOP1. J Enzyme Inhib Med Chem 2012;27:892–7
   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
• Sung YC, Fuchs JA. Characterization of the cyn operon in Escherichia coli K12. J Biol Chem 1988;263:14769–75
   PubMed Web of Science ®Google Scholar
• Guilloton MB, Korte JJ, Lamblin AF, et al. Carbonic anhydrase in Escherichia coli. A product of the cyn operon. J Biol Chem 1992;267:3731–4
   PubMed Web of Science ®Google Scholar
• Cronk JD, Endrizzi JA, Cronk MR, et al. Crystal structure of E. coli beta-carbonic anhydrase, an enzyme with an unusual pH-dependent activity. Protein Sci 2001;10:911–22
   PubMed Web of Science ®Google Scholar
• Merlin C, Masters M, McAteer S, Coulson A. Why is carbonic anhydrase essential to Escherichia coli? J Bacteriol 2003;185:6415–24
   PubMed Web of Science ®Google Scholar
• Ramanan R, Kannan K, Sivanesan SD, Chakrabarti T. Prevalence and phylogenetic relationship of two β-carbonic anhydrases in affiliates of Enterobacteriaceae. Ann Microbiol 2013;63:1275–82
   Web of Science ®Google Scholar
• Chirică LC, Elleby B, Jonsson BH, Lindskog S. The complete sequence, expression in Escherichia coli, purification and some properties of carbonic anhydrase from Neisseria gonorrhoeae. Eur J Biochem 1997;244:755–60
   PubMedGoogle Scholar
• Joseph S, David WR. Molecular cloning: a laboratory manual. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2001:2–25
   Google Scholar
• Kotwica J, Ciuk MA, Joachimiak E, et al. Carbonic anhydrase activity in the vas deferens of the cotton leafworm–Spodoptera littoralis (Lepidoptera: Noctuidae) controlled by circadian clock. J Physiol Pharmacol 2006;57:107–23
   PubMed Web of Science ®Google Scholar
• Eminoğlu A, Ülker S, Sandallı C. Cloning, purification and characterization of acetyl xylane esterase from Anoxybacillus flavithermus DSM 2641(T) with activity on low molecular-weight acetates. Protein J 2015;34:237–42
   PubMed Web of Science ®Google Scholar
• Kim OS, Cho YJ, Lee K, et al. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 2012;62:716–21
   PubMed Web of Science ®Google Scholar
• Bjellqvist B, Hughes GJ, Pasquali C, et al. The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 1993;14:1023–31
   PubMed Web of Science ®Google Scholar
• Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673–80
   PubMed Web of Science ®Google Scholar
• Tamura K, Stecher G, Peterson D, et al. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013;30:2725–9
   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
• Innocenti A, Scozzafava A, Parkkila S, et al. Investigations of the esterase, phosphatase and sulfatase activities of the cytosolic mammalian carbonic anhydrase isoforms I, II and XIII with 4-nitrophenyl esters as substrates. Bioorg Med Chem Lett 2008;18:2267–71
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, et al. Biochemical characterization of the δ-carbonic anhydrase from the marine diatom Thalassiosira weissflogii, TweCA. J Enzyme Inhib Med Chem 2014;29:906–11
   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
• 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
• Nishimori I, Vullo D, Minakuchi T, et al. Anion inhibition studies of two new β-carbonic anhydrases from the bacterial pathogen Legionella pneumophila. Bioorg Med Chem Lett 2014;24:1127–32
   PubMed Web of Science ®Google Scholar
• Del Prete S, De Luca V, Scozzafava A, et al. Biochemical properties of a new α-carbonic anhydrase from the human pathogenic bacterium, Vibrio cholerae. J Enzyme Inhib Med Chem 2014;29:23–7
   PubMed Web of Science ®Google Scholar
• Del Prete S, De Luca V, Vullo D, et al. Biochemical characterization of the γ-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, Isik S, Vullo D, et al. DNA cloning, characterization, and inhibition studies of an alpha-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae. J Med Chem 2012;55:10742–8
   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
• Supuran CT. Bacterial carbonic anhydrases as drug targets: toward novel antibiotics? Front Pharmacol 2011;2:34
   PubMed Web of Science ®Google Scholar
• Vullo D, Nishimori I, Minakuchi T, et al. Inhibition studies with anions and small molecules of two novel beta-carbonic anhydrases from the bacterial pathogen Salmonella enterica serovar Typhimurium. Bioorg Med Chem Lett 2011;21:3591–5
   PubMed Web of Science ®Google Scholar
• Joseph P, Ouahrani-Bettache S, Montero JL, et al. A new beta-carbonic anhydrase from Brucella suis, its cloning, characterization, and inhibition with sulfonamides and sulfamates, leading to impaired pathogen growth. Bioorg Med Chem 2011;19:1172–8
   PubMed Web of Science ®Google Scholar
• Joseph P, Turtaut F, Ouahrani-Bettache S, et al. Cloning, characterization, and inhibition studies of a beta-carbonic anhydrase from Brucella suis. J Med Chem 2010;53:2277–85
   PubMed Web of Science ®Google Scholar
• 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
• Nishimori I, Onishi S, Takeuchi H, et al. The alpha and beta classes carbonic anhydrases from Helicobacter pylori as novel drug targets. Curr Pharm Des 2008;14:622–30
   PubMed Web of Science ®Google Scholar
• Nishimori I, Minakuchi T, Kohsaki T, et al. Carbonic anhydrase inhibitors: the beta-carbonic anhydrase from Helicobacter pylori is a new target for sulfonamide and sulfamate inhibitors. Bioorg Med Chem Lett 2007;17:3585–94
   PubMed Web of Science ®Google Scholar
• Burghout P, Vullo D, Scozzafava A, et al. Inhibition of the β-carbonic anhydrase from Streptococcus pneumoniae by inorganic anions and small molecules: toward innovative drug design of antiinfectives? Bioorg Med Chem 2011;19:243–8
   PubMed Web of Science ®Google Scholar
• Guzel O, Maresca A, Scozzafava A, et al. Discovery of low nanomolar and subnanomolar inhibitors of the mycobacterial beta-carbonic anhydrases Rv1284 and Rv3273. J Med Chem 2009;52:4063–7
   PubMed Web of Science ®Google Scholar
• Nishimori I, Minakuchi T, Maresca A, et al. The β-carbonic anhydrases from Mycobacterium tuberculosis as drug targets. Curr Pharm Des 2010;16:3300–9
   PubMed Web of Science ®Google Scholar
• Suarez Covarrubias A, Larsson AM, Hogbom M, et al. Structure and function of carbonic anhydrases from Mycobacterium tuberculosis. J Biol Chem 2005;280:18782–9
   PubMed Web of Science ®Google Scholar
• Carta F, Maresca A, Covarrubias AS, et al. Carbonic anhydrase inhibitors. Characterization and inhibition studies of the most active beta-carbonic anhydrase from Mycobacterium tuberculosis, Rv3588c. Bioorg Med Chem Lett 2009;19:6649–54
   PubMed Web of Science ®Google Scholar
• Minakuchi T, Nishimori I, Vullo D, et al. Molecular cloning, characterization, and inhibition studies of the Rv1284 beta-carbonic anhydrase from Mycobacterium tuberculosis with sulfonamides and a sulfamate. J Med Chem 2009;52:2226–32
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Migliardini F, De Luca V, Carginale V, et al. Biomimetic CO2 capture using a highly thermostable bacterial α-carbonic anhydrase immobilized on a polyurethane foam. J Enzyme Inhib Med Chem 2014;29:146–50
   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
• 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
• Supuran CT. Carbonic anhydrase inhibitors: an editorial. Expert Opin Ther Pat 2013;23:677–79
   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
• 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
• 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
• 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
• 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
   PubMed Web of Science ®Google Scholar
• Pinard MA, Lotlikar SR, Boone CD, et al. Structure and inhibition studies of a type II beta-carbonic anhydrase psCA3 from Pseudomonas aeruginosa. Bioorg Med Chem 2015;23:4831–8
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibition/activation: trip of a scientist around the world in the search of novel chemotypes and drug targets. Curr Pharm Des 2010;16:3233–45
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibitors. Bioorg Med Chem Lett 2010;20:3467–74
   PubMed Web of Science ®Google Scholar
• De Simone G, Alterio V, Supuran CT. Exploiting the hydrophobic and hydrophilic binding sites for designing carbonic anhydrase inhibitors. Expert Opin Drug Discov 2013;8:793–810
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Maresca A, Carta F, Vullo D, et al. Dithiocarbamates strongly inhibit the β-class carbonic anhydrases from Mycobacterium tuberculosis. J Enzyme Inhib Med Chem 2013;28:407–11
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Passaponti M, Supuran CT, Gulcin I. 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
• Alp C, Maresca A, Alp NA, et al. Secondary/tertiary benzenesulfonamides with inhibitory action against the cytosolic human carbonic anhydrase isoforms I and II. J Enzyme Inhib Med Chem 2013;28:294–8
   PubMed Web of Science ®Google Scholar