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Review Article

A magnificent enzyme superfamily: carbonic anhydrases, their purification and characterization

, &
Pages 689-694 | Received 15 May 2015, Accepted 03 Jun 2015, Published online: 29 Jun 2015

References

  • Supuran CT. Carbonic anhydrases: from biomedical applications of the inhibitors and activators to biotechnologic use for CO2 capture. J Enzyme Inhib Med Chem 2013;28:229–30
  • Supuran CT. Structure-based drug discovery of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2012;27:759–72
  • Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81
  • Lindskog S. Purification and properties of bovine erythrocyte carbonic anhydrase. Biochim Biophys Acta 1960;39:218–26
  • Nyman PO. Purification and properties of carbonic anhydrase from human erythrocytes. Biochim Biophys Acta 1961;52:1–12
  • Laurent G, Charrel M, Castay M, et al. Identification des proteines érythrocytaires Y, X et X2 aux hydrases carboniques humaines. Compt Rend Soc Biol (Paris) 1962;154:1461–4
  • Rickli EE, Edsall JT. Zinc binding and the sulfhydryl group of human carbonic anhydrase. J Biol Chem 1962;237:258–60
  • Rickli EE, Ghazanfar SA, Gibbons BH, et al. Carbonic anhydrases from human erythrocytes. Preparation and properties of two enzymes. J Biol Chem 1964;239:1065–78
  • Laurent G, Charrel M, Luccioni F, et al. On carbonic anhydrases of human erythrocytes. I. Isolation and purification. Bull Soc Chim Biol (Paris) 1965;47:1101–24
  • Kannan KK, Notsrand B, Fridborg K, et al. Crystal structure of human erythrocyte carbonic anhydrase B. Three-dimensional structure at a nominal 2.2-A resolution. Proc Natl Acad Sci USA 1975;72:51–5
  • Nyman P, Lindskog S. Amino acid composition of various forms of bovine and human erythrocyte carbonic anhydrase. Biochim Biophys Acta 1964;85:141–51
  • Andersson B, Nyman PO, Strid L. Amino acid sequence of human erythrocyte carbonic anhydrase B. Biochem Biophys Res Commun 1972;48:670–7
  • Liljas A, Kannan KK, Bergstén PC, et al. Crystal structure of human carbonic anhydrase C. Nat New Biol 1972;235:131–7
  • Henderson LE, Henriksson D, Nyman PO. Amino acid sequence of human erythrocyte carbonic anhydrase C. Biochem Biophys Res Commun 1973;52:1388–94
  • Lin KT, Deutsch HF. Human carbonic anhydrases. XI. The complete primary structure of carbonic anhydrase B. J Biol Chem 1973;248:1885–93
  • Lin KT, Deutsch HF. Human carbonic anhydrases. XII. The complete primary structure of the C isozyme. J Biol Chem 1974;249:2329–37
  • Garg LC. Catalytic activity and inhibition of carbonic anhydrase of rat tissues. Biochem Pharmacol 1974;23:3153–61
  • Garg LC. The effect of sex hormones on rat liver carbonic anhydrase. J Pharmacol Exp Ther 1974;189:557–62
  • Holmes RS. Mammalian carbonic anhydrase isozymes: evidence for a third locus. J Exp Zool 1976;197:289–95
  • Balckburn MN, Chirgwin JM, James GT, et al. Pseudoisoenzymes of rabbit muscle phosphoglucose isomerase. J Biol Chem 1972;247:1170–9
  • Koester MK, Register AM, Noltmann EA. Basic muscle protein, a third genetic locus isoenzyme of carbonic anhydrase? Biochem Biophys Res Commun 1977;76:196–204
  • Fernley RT, Wright RD, Coghlan JP. A novel carbonic anhydrase from the ovine parotid gland. FEBS Lett 1979;105:299–302
  • Murakami H, Sly WS. Purification and characterization of human salivary carbonic anhydrase. J Biol Chem 1987;262:1382–8
  • Whitney PL, Briggle TV. Membrane-associated carbonic anhydrase purified from bovine lung. J Biol Chem 1982;257:12056–9
  • Wistrand PJ, Knuuttila KG. Renal membrane-bound carbonic anhydrase. Purification and properties. Kidney Int 1989;35:851–9
  • Zhu XL, Sly WS. Carbonic anhydrase IV from human lung. Purification, characterization, and comparison with membrane carbonic anhydrase from human kidney. J Biol Chem 1990;265:8795–801
  • Montgomery JC, Venta PJ, Eddy RL, et al. Characterization of human gene for a newly discovered carbonic anhydrase, CA VII, and its location to chromosome 16. Genomics 1991;11:835–48
  • Pastoreková S, Závadová Z, Kostál M, et al. A novel quasi-viral agent, MaTu, is a two-component system. Virology 1992;187:620–6
  • Opavský R, Pastoreková S, Zelník V, et al. Human MN/CA9 gene, a novel member of the carbonic anhydrase family: structure and exon to protein domain relationships. Genomics 1996;33:480–7
  • Tureci O, Sahin U, Vollmar E, et al. Human carbonic anhydrase XII: cDNA cloning, expression, and chromosomal localization of a carbonic anhydrase gene that is overexpressed in some renal cell cancers. Proc Natl Acad Sci USA 1998;95:7608–13
  • Fujikawa-Adachi K, Nishimori I, Taguchi T, et al. Human carbonic anhydrase XIV (CA14): cDNA cloning, mRNA expression, and mapping to chromosome 1. Genomics 1999;61:74–81
  • Mori K, Ogawa Y, Ebihara K, et al. Isolation and characterization of CAXIV, a novel membrane-bound carbonic anhydrase from mouse kidney. J Biol Chem 1999;274:15701–5
  • Nagao Y, Platero JS, Waheed A, et al. Human mitochondrial carbonic anhydrase: cDNA cloning, expression, subcellular localization, and mapping to chromosome 16. Proc Natl Acad Sci USA 1993;90:7623–7
  • Heck RW, Tanhauser SM, Manda R, et al. Catalytic properties of mouse carbonic anhydrase V. J Biol Chem 1994;269:24742–6
  • Fujikawa-Adachi K, Nishimori I, Taguchi T, et al. Human mitochondrial carbonic anhydrase VB. cDNA cloning, mRNA expression, subcellular localization, and mapping to chromosome X. J Biol Chem 1999;274:21228–33
  • Lehtonen J, Shen B, Vihinen M, et al. Characterization of CA XIII, a novel member of the carbonic anhydrase isozyme family. J Biol Chem 2004;279:2719–27
  • Henriques OM. Die Bindungsweise des Kohlendioxyds im Blute. Berlin: Biochem Ztschrft 1928;200:1–24
  • Van Slyke DD, Hawkins JA. Studies of gas and electrolyte equilibria in blood. XVI. The evolution of carbon dioxide from blood and buffer solutions. J Biol Chem 1930;87:265–79
  • Meldrum NU, Roughton FJ. Some properties of carbonic anhydrase, the CO2 enzyme present in blood. J Physiol 1932;75:15–16
  • Meldrum NU, Roughton FJ. Carbonic anhydrase. Its preparation and properties. J Physiol 1933;80:113–42
  • Keilin D, Mann T. Carbonic anhydrase. Nature 1939;144:442–3
  • Keilin D, Mann T. Carbonic anhydrase. Purification and nature of the enzyme. Biochem J 1940;34:1163–76
  • Furth AJ. Purification and properties of horse erythrocyte carbonic anhydrases. J Biol Chem 1968;243:4832–41
  • Falkbring SO, Göthe PO, Nyman PO, et al. Affinity chromatography of carbonic anhydrase. FEBS Lett 1972;24:229–35
  • Whitney PL. Affinity chromatography of carbonic anhydrase. Anal Biochem 1974;57:467–76
  • Funakoshi S, Deutsch HF. Human carbonic anhydrases. II. Some physicochemical properties of native isozymes and of similar isozymes generated in vitro. J Biol Chem 1969;244:3438–46
  • Carter MJ, Parsons DS. The purification and properties of carbonic anhydrases from guinea-pig erythrocytes and mucosae of the gastrointestinal tract. Biochem J 1970;120:797–808
  • Maynard JR, Coleman JE. Elasmobranch carbonic anhydrase. Purification and properties of the enzyme from two species of shark. J Biol Chem 1971;246:4455–64
  • Khalifah RG, Strader DJ, Bryant SH, et al. Carbon-13 nuclear magnetic resonance probe of active-site ionizations in human carbonic anhydrase B. Biochemistry 1977;16:2241–7
  • Osborne WR, Tashian RE. An improved method for the purification of carbonic anhydrase isozymes by affinity chromatography. Anal Biochem 1975;64:297–303
  • Shinar H, Navon G. Kinetic and magnetic properties of cobalt(III) ion in the active site of carbonic anhydrase. Eur J Biochem 1979;93:313–22
  • Hall GE, Schraer R. Characterization of a high activity carbonic anhydrase isozyme purified from erythrocytes of Salmo gairdneri. Comp Biochem Physiol B 1983;75:81–92
  • Bergenhem N, Carlsson U, Klasson K. Rapid ion-exchange chromatography for preparative separation of proteins. Application to porcine and bovine carbonic anhydrases. J Chromatogr 1985;319:59–65
  • Yang SY, Tsuzuki M, Miyachi S. Carbonic anhydrase of Chlamydomonas: purification and studies on its induction using antiserum against Chlamydomonas carbonic anhydrase. Plant Cell Physiol 1985;26:25–34
  • Abou-Rebyeh H, Josić D, Gottschall K, et al. Purification of carbonic anhydrase isoenzymes by high-performance affinity chromatography and hydrophobic interaction chromatography. J Chromatogr 1991;566:351–9
  • Schmidt AM, Müller HN, Skerra A. A Zn(II)-binding site engineered into retinol-binding protein exhibits metal-ion specificity and allows highly efficient affinity purification with a newly designed metal ligand. Chem Biol 1996;3:645–53
  • Demir N, Demir Y, Bakan E, et al. A different structural feature for carbonic anhydrases in human erythrocytes. Prep Biochem Biotechnol 1997;27:279–87
  • Bergenhem NC, Hallberg M, Wisén S. Molecular characterization of the human carbonic anhydrase-related protein (HCA-RP VIII). Biochim Biophys Acta 1998;1384:294–8
  • Vince JW, Reithmeier RA. Carbonic anhydrase II binds to the carboxyl terminus of human band 3, the erythrocyte C1-/HCO3- exchanger. J Biol Chem 1998;273:28430–7
  • Vince JW, Carlsson U, Reithmeier RA. Localization of the Cl-/HCO3- anion exchanger binding site to the amino-terminal region of carbonic anhydrase II. Biochemistry 2000;39:13344–9
  • Mårtensson LG, Jonsson BH, Freskgård PO, et al. Characterization of folding intermediates of human carbonic anhydrase II: probing substructure by chemical labeling of SH groups introduced by site-directed mutagenesis. Biochemistry 1993;32:224–31
  • Persson M, Harbridge JR, Hammarström P, et al. Comparison of electron paramagnetic resonance methods to determine distances between spin labels on human carbonic anhydrase II. Biophys J 2001;80:2886–97
  • Krungkrai SR, Suraveratum N, Rochanakij S, et al. Characterisation of carbonic anhydrase in Plasmodium falciparum. Int J Parasitol 2001;31:661–8
  • Demir N, Demir Y, Nadaroglu H. Carbonic anhydrase from bovine bone. Prep Biochem Biotechnol 2001;31:33–47
  • Demir Y, Demir N, Alayli A. Cytosolic and non-cytosolic carbonic anhydrase enzymes from bovine leukocytes. Prep Biochem Biotechnol 2001;31:421–31
  • Ozensoy O, Arslan O, Sinan S. A new method for purification of carbonic anhydrase isozymes by affinity chromatography. Biochemistry (Mosc) 2004;69:216–19
  • Arslan O. Inhibition of bovine carbonic anhydrase by new sulfonamide compounds. Biochemistry (Mosc) 2001;66:982–13
  • Demir Y, Nadaroğlu H, Demir N. Purification and characterization of carbonic anhydrase from bovine stomach and effects of some known inhibitors on enzyme activity. J Enzyme Inhib Med Chem 2005;20:75–80
  • Nishimori I, Minakuchi T, Onishi S, et al. Carbonic anhydrase inhibitors. Cloning, characterization and inhibition studies of the cytosolic isozyme III with anions. J Enzyme Inhib Med Chem 2009;24:70–6
  • Piermarini PM, Kim EY, Boron WF. Evidence against a direct interaction between intracellular carbonic anhydrase II and pure C-terminal domains of SLC4 bicarbonate transporters. J Biol Chem 2007;282:1409–21
  • da Costa Ores J, Sala L, Cerveira GP, et al. Purification of carbonic anhydrase from bovine erythrocytes and its application in the enzymic capture of carbon dioxide. Chemosphere 2012;88:255–9
  • Oviya M, Sukumaran V, Giri SS. Immobilization and characterization of carbonic anhydrase purified from E. coli MO1 and its influence on CO2 sequestration. World J Microbiol Biotechnol 2013;29:1813–20
  • Uygun M, Karagözler AA, Denizli A. Molecularly imprinted cryogels for carbonic anhydrase purification from bovine erythrocyte. Artif Cells Nanomed Biotechnol 2014;42:128–37
  • Hoffmann KM, Wood KM, Labrum AD, et al. Surface histidine mutations for the metal affinity purification of a β-carbonic anhydrase. Anal Biochem 2014;458:66–8
  • Sahin A, Isık S, Arslan O, et al. A new affinity gel for the purification of α-carbonic anhydrases. J Enzyme Inhib Med Chem 2015;30:224–8
  • Bozdag M, Isik S, Beyaztas S, et al. Synthesis of a novel affinity gel for the purification of carbonic anhydrases. J Enzyme Inhib Med Chem 2015;30:240–4
  • Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nature Rev Drug Discovery 2011;10:767−77
  • 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
  • Harju AK, Bootorabi F, Kuuslahti M, et al. Carbonic anhydrase III: a neglected isozyme is stepping into the limelight. J Enzyme Inhib Med Chem 2013;28:231–9
  • Çavdar H, Ekinci D, Talaz O, et al. α-Carbonic anhydrases are sulfatases with cyclic diol monosulfate esters. J Enzyme Inhib Med Chem 2012;27:148–54
  • Durdagi S, Scozzafava G, Vullo D, et al. Inhibition of mammalian carbonic anhydrases I-XIV with grayanotoxin III: solution and in silico studies. J Enzyme Inhib Med Chem 2014;29:469–75
  • Bilginer S, Unluer E, Gul HI, et al. Carbonic anhydrase inhibitors. Phenols incorporating 2- or 3-pyridyl- ethenylcarbonyl and tertiary amine moieties strongly inhibit Saccharomyces cerevisiaeβ-carbonic anhydrase. J Enzyme Inhib Med Chem 2014;29:495–9
  • Carta F, Scozzafava A, Supuran CT. Sulfonamides (RSO2NH2): a patent review 2008-2012. Expert Opin Ther Pat 2012;22:747–58
  • Fabrizi F, Mincione F, Somma T, et al. A new approach to antiglaucoma drugs: carbonic anhydrase inhibitors with or without NO donating moieties. Mechanism of action and preliminary pharmacology. J Enzyme Inhib Med Chem 2012;27:138–47
  • Carta F, Supuran CT, Scozzafava A. Novel therapies for glaucoma: a patent review 2007-2011. Expert Opin Ther Pat 2012;22:79–88
  • Masini E, Carta F, Scozzafava A, et al. Antiglaucoma carbonic anhydrase inhibitors: a patent review. Expert Opin Ther Pat 2013;23:705–16
  • Supuran CT, Maresca A, Gregáň F, et al. Three new aromatic sulfonamide inhibitors of carbonic anhydrases I, II, IV and XII. J Enzyme Inhib Med Chem 2013;28:289–93
  • 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
  • Monti SM, Supuran CT, De Simone G. Anticancer carbonic anhydrase inhibitors: a patent review (2008-2013). Expert Opin Ther Pat 2013;23:737–49
  • Ebbesen P, Pettersen EO, Gorr TA, et al. Taking advantage of tumor cell adaptations to hypoxia for developing new tumor markers and treatment strategies. J Enzyme Inhib Med Chem 2009;24:1–39
  • Carta F, Supuran CT. Diuretics with carbonic anhydrase inhibitory action: a patent and literature review (2005-2013). Expert Opin Ther Pat 2013;23:681–91
  • Supuran CT. Carbonic anhydrase inhibitors as emerging drugs for the treatment of obesity. Expert Opin Emerg Drugs 2012;17:11–15
  • Scozzafava A, Supuran CT, Carta F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin Ther Pat 2013;23:725–35
  • Capasso C, Supuran CT. Antiinfective carbonic anhydrase inhibitors: a patent and literature review. Expert Opin Ther Pat 2013;23:693−704
  • Dedeoglu N, De Luca V, Isik S, et al. Cloning, characterization and anion inhibition study of a β-class carbonic anhydrase from the caries producing pathogen Streptococcus mutans. Bioorg Med Chem 2015;23:2995–3001

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