A failed tentative to design a super carbonic anhydrase having the biochemical properties of the most thermostable CA (SspCA) and the fastest (SazCA) enzymes

References

• Demirjian DC, Moris-Varas F, Cassidy CS. Enzymes from extremophiles. Curr Opin Chem Biol 2001;5:144–51
   PubMed Web of Science ®Google Scholar
• Gabani P, Singh OV. Radiation-resistant extremophiles and their potential in biotechnology and therapeutics. Appl Microbiol Biotechnol 2013;97:993–1004
   PubMed Web of Science ®Google Scholar
• Madigan MT, Marrs BL. Extremophiles. Sci Am 1997;276:82–7
   PubMed Web of Science ®Google Scholar
• Egorova K, Antranikian G. Industrial relevance of thermophilic Archaea. Curr Opin Microbiol 2005;8:649–55
   PubMed Web of Science ®Google Scholar
• Eichler J. Biotechnological uses of archaealextremozymes. Biotechnol Adv 2001;19:261–78
   PubMed Web of Science ®Google Scholar
• Marhuenda-Egea FC, Bonete MJ. Extreme halophilic enzymes in organic solvents. Curr Opin Biotechnol 2002;13:385–9
   PubMed Web of Science ®Google Scholar
• Schumacher K, Heine E, Hocker H. Extremozymes for improving wool properties. J Biotechnol 2001;89:281–8
   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 beta-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 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
• Alafeefy AM, Abdel-Aziz HA, Vullo D, et al. Inhibition of carbonic anhydrases from the extremophilic bacteria Sulfurihydrogenibium yellostonense (SspCA) and S. azorense (SazCA) with a new series of sulfonamides incorporating aroylhydrazone-, [1,2,4]triazolo[3,4-b][1,3,4]thiadiazinyl- or 2-(cyanophenylmethylene)-1,3,4-thiadiazol-3(2H)-yl moieties. Bioorg Med Chem 2014;22:141–7
   PubMed Web of Science ®Google Scholar
• Vullo D, Sai Kumar RS, Scozzafava A, et al. Anion inhibition studies of a beta-carbonic anhydrase from Clostridium perfringens. Bioorg Med Chem Lett 2013;23:6706–10
   PubMed Web of Science ®Google Scholar
• Vullo D, De Luca V, Scozzafava A, et al. The extremo-alpha-carbonic anhydrase from the thermophilic bacterium Sulfurihydrogenibium azorense is highly inhibited by sulfonamides. Bioorg Med Chem 2013;21:4521–5
   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 CO2 hydration reaction. Bioorg Med Chem 2013;21:1465–9
   PubMed Web of Science ®Google Scholar
• Di Fiore A, Capasso C, De Luca V, et al. X-ray structure of the first ‘extremo-alpha-carbonic anhydrase’, a dimeric enzyme from the thermophilic bacterium Sulfurihydrogenibium yellowstonense YO3AOP1. Acta Crystallogr D Biol Crystallogr 2013;69:1150–9
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, et al. A highly catalytically active gamma-carbonic anhydrase from the pathogenic anaerobe Porphyromonas gingivalis and its inhibition profile with anions and small molecules. Bioorg Med Chem Lett 2013;23:4067–71
   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
• 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
• 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
• 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
• 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
• Supuran CT. Carbonic anhydrase inhibitors: an editorial. Expert Opin Ther Pat 2013;23:677–9
   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
• 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
• Del Prete S, Vullo D, Fisher GM, et al. Discovery of a new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum – the eta-carbonic anhydrases. Bioorg Med Chem Lett 2014;24:4389–96
   PubMed Web of Science ®Google Scholar
• Vullo D, Del Prete S, Osman SM, et al. Sulfonamide inhibition studies of the delta-carbonic anhydrase from the diatom Thalassiosira weissflogii. Bioorg Med Chem Lett 2014;24:275–9
   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
• Del Prete S, Vullo D, De Luca V, et al. Biochemical characterization of the delta-carbonic anhydrase from the marine diatom Thalassiosira weissflogii, TweCA. J Enzyme Inhib Med Chem 2014;29:906–11
   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
• Vullo D, Kupriyanova EV, Scozzafava A, et al. Anion inhibition study of the beta-carbonic anhydrase (CahB1) from the cyanobacterium Coleofasciculus chthonoplastes (ex-Microcoleus chthonoplastes). Bioorg Med Chem 2014;22:1667–71
   PubMed Web of Science ®Google Scholar
• Vullo D, Flemetakis E, Scozzafava A, et al. Anion inhibition studies of two alpha-carbonic anhydrases from Lotus japonicus, LjCAA1 and LjCAA2. J Inorg Biochem 2014;136:67–72
   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
• 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
• 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. 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
• Migliardini F, De Luca V, Carginale V, et al. Biomimetic CO2 capture using a highly thermostable bacterial alpha-carbonic anhydrase immobilized on a polyurethane foam. J Enzyme Inhib Med Chem 2014;29:146–50
   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 2014. [Epub ahead of print]. DOI:10.3109/14756366.2014.931383
   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
• 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 2014. [Epub ahead of print].doi:10.3109/14756366.2014.917085
   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
• 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
• Supuran CT. Bacterial carbonic anhydrases as drug targets: toward novel antibiotics? Front Pharmacol 2011;2:34
   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 2014. [Epub ahead of print]. doi:10.3109/14756366.2014.910202
   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 2014. [Epub ahead of print]
   Google Scholar
• Ceruso M, Del Prete S, Alothman Z, et al. Sulfonamides with potent inhibitory action and selectivity against the alpha-carbonic anhydrase from Vibrio cholerae. ACS Med Chem Lett 2014;5:826–30
   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
• 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, Leewattanapasuk W, Muhlschlegel FA, et al. Carbonic anhydrase inhibitors: inhibition of the beta-class enzyme from the pathogenic yeast Candida glabrata with sulfonamides, sulfamates and sulfamides. Bioorg Med Chem Lett 2013;23:2647–52
   PubMed Web of Science ®Google Scholar
• Vullo D, Isik S, Del Prete S, et al. Anion inhibition studies of the alpha-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae. Bioorg Med Chem Lett 2013;23:1636–8
   PubMed Web of Science ®Google Scholar
• 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
• 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
• 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
• Nishimori I, Vullo D, Minakuchi T, et al. Restoring catalytic activity to the human carbonic anhydrase (CA) related proteins VIII, X and XI affords isoforms with high catalytic efficiency and susceptibility to anion inhibition. Bioorg Med Chem Lett 2013;23:256–60
   PubMed Web of Science ®Google Scholar
• Monti SM, De Simone G, Dathan NA, et al. Kinetic and anion inhibition studies of a beta-carbonic anhydrase (FbiCA 1) from the C4 plant Flaveria bidentis. Bioorg Med Chem Lett 2013;23:1626–30
   PubMed Web of Science ®Google Scholar
• Guzel-Akdemir O, Akdemir A, Pan P, et al. A class of 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
• Alafeefy AM, Isik S, Al-Jaber NA, et al. Carbonic anhydrase inhibitors. Benzenesulfonamides incorporating cyanoacrylamide moieties strongly inhibit Saccharomyces cerevisiae beta-carbonic anhydrase. Bioorg Med Chem Lett 2013;23:3570–5
   PubMed Web of Science ®Google Scholar
• Akdemir A, Vullo D, De Luca V, 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
• Akdemir A, Guzel-Akdemir O, Scozzafava A, et al. Inhibition of tumor-associated human carbonic anhydrase isozymes IX and XII by a new class of substituted-phenylacetamido aromatic sulfonamides. Bioorg Med Chem 2013;21:5228–32
   PubMed Web of Science ®Google Scholar
• McKenna R, Supuran CT. Carbonic anhydrase inhibitors drug design. SubcellBiochem 2014;75:291–323
   Google Scholar
• Carta F, Aggarwal M, Maresca A, et al. Dithiocarbamates: a new class of carbonic anhydrase inhibitors. Crystallographic and kinetic investigations. Chem Commun (Camb) 2012;48:1868–70
   PubMed Web of Science ®Google Scholar
• Winum JY, Supuran CT. Recent advances in the discovery of zinc-binding motifs for the development of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2014. [Epub ahead of print]. doi:10.3109/14756366.2014.913587
   Web of Science ®Google Scholar
• Carta F, Akdemir A, Scozzafava A, et al. Xanthates and trithiocarbonates strongly inhibit carbonic anhydrases and show antiglaucoma effects in vivo. J Med Chem 2013;56:4691–700
   PubMed Web of Science ®Google Scholar
• Davis RA, Vullo D, Supuran CT, Poulsen SA. Natural product polyamines that inhibit human carbonic anhydrases. Biomed Res Int 2014;2014:374079. doi:10.1155/2014/374079
   PubMed Web of Science ®Google Scholar
• Carradori S, De Monte C, D'Ascenzio M, et al. Salen and tetrahydrosalen derivatives act as effective inhibitors of the tumor-associated carbonic anhydrase XII – a new scaffold for designing isoform-selective inhibitors. Bioorg Med Chem Lett 2013;23:6759–63
   PubMed Web of Science ®Google Scholar
• Supuran CT. Amide derivatives of benzene-sulfonanilide, pharmaceutical composition thereof and method for cancer treatment using the same (US20120095092). Expert Opin Ther Pat 2012;22:1251–5
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibitors and activators for novel therapeutic applications. Future Med Chem 2011;3:1165–80
   PubMed Web of Science ®Google Scholar
• Durdagi S, Senturk M, Ekinci D, et al. Kinetic and docking studies of phenol-based inhibitors of carbonic anhydrase isoforms I, II, IX and XII evidence a new binding mode within the enzyme active site. Bioorg Med Chem 2011;19:1381–9
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibition with natural products: novel chemotypes and inhibition mechanisms. Mol Divers 2011;15:305–16
   PubMed Web of Science ®Google Scholar
• Carta F, Temperini C, Innocenti A, et al. Polyamines inhibit carbonic anhydrases by anchoring to the zinc-coordinated water molecule. J Med Chem 2010;53:5511–22
   PubMed Web of Science ®Google Scholar
• Lehneck R, Neumann P, Vullo D, et al. Crystal structures of two tetrameric beta-carbonic anhydrases from the filamentous ascomycete Sordaria macrospora. FEBS J 2014;281:1759–72
   PubMed Web of Science ®Google Scholar
• Di Fiore A, Truppo E, Supuran CT, et al. Crystal structure of the C183S/C217S mutant of human CA VII in complex with acetazolamide. Bioorg Med Chem Lett 2010;20:5023–6
   PubMed Web of Science ®Google Scholar
• Avvaru BS, Wagner JM, Maresca A, et al. Carbonic anhydrase inhibitors. The X-ray crystal structure of human isoform II in adduct with an adamantyl analogue of acetazolamide resides in a less utilized binding pocket than most hydrophobic inhibitors. Bioorg Med Chem Lett 2010;20:4376–81
   PubMed Web of Science ®Google Scholar
• Temperini C, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. X-ray crystal studies of the carbonic anhydrase II-trithiocarbonate adduct – an inhibitor mimicking the sulfonamide and urea binding to the enzyme. Bioorg Med Chem Lett 2010;20:474–8
   PubMed Web of Science ®Google Scholar
• Alterio V, Hilvo M, Di Fiore A, et al. Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX. Proc Natl Acad Sci USA 2009;106:16233–8
   PubMed Web of Science ®Google Scholar
• Di Fiore A, Monti SM, Hilvo M, et al. Crystal structure of human carbonic anhydrase XIII and its complex with the inhibitor acetazolamide. Proteins 2009;74:164–75
   PubMed Web of Science ®Google Scholar
• Temperini C, Scozzafava A, Puccetti L, Supuran CT. Carbonic anhydrase activators: X-ray crystal structure of the adduct of human isozyme II with L-histidine as a platform for the design of stronger activators. Bioorg Med Chem Lett 2005;15:5136–41
   PubMed Web of Science ®Google Scholar
• Guzel O, Innocenti A, Vullo D, et al. 3-Phenyl-1H-indole-5-sulfonamides: structure-based drug design of a promising class of carbonic anhydrase inhibitors. Curr Pharm Des 2010;16:3317–26
   PubMed Web of Science ®Google Scholar
• Temperini C, Innocenti A, Guerri A, et al. Phosph(on)ate as a zinc-binding group in metalloenzyme inhibitors: X-ray crystal structure of the antiviral drug foscarnet complexed to human carbonic anhydrase I. Bioorg Med Chem Lett 2007;17:2210–15
   PubMed Web of Science ®Google Scholar
• Winum JY, Temperini C, El Cheikh K, et al. Carbonic anhydrase inhibitors: clash with Ala65 as a means for designing inhibitors with low affinity for the ubiquitous isozyme II, exemplified by the crystal structure of the topiramate sulfamide analogue. J Med Chem 2006;49:7024–31
   PubMed Web of Science ®Google Scholar