2a8d › Citations

Identification of a novel noncatalytic bicarbonate binding site in eubacterial beta-carbonic anhydrase.

Cronk JD, Rowlett RS, Zhang KY, Tu C, Endrizzi JA, Lee J, Gareiss PC, Preiss JR
Biochemistry 45 4351-61 (2006)
Related entries: 2a8c, 2esf

Cited: 49 times
EuropePMC logo PMID: 16584170

Abstract

The structures of beta class carbonic anhydrases (beta-CAs) determined so far fall into two distinct subclasses based on the observed coordination of the catalytic zinc (Zn2+) ion. The subclass of beta-CAs that coordinate Zn2+ tetrahedrally with four protein-derived ligands is represented by the structures of orthologues from Porphyridium purpureum, Escherichia coli, and Mycobacterium tuberculosis. Here we present the structure of an additional member of that subclass, that from Haemophilus influenzae, as well as detailed kinetic analysis, revealing the correspondence between structural classification and kinetic profile for this subclass. In addition, we identify a unique, noncatalytic binding mode for the substrate bicarbonate that occurs in both the H. influenzae and E. coli enzymes. The kinetic and structural analysis indicates that binding of bicarbonate in this site of the enzyme may modulate its activity by influencing a pH-dependent, cooperative transition between active and inactive forms. We hypothesize that the two structural subclasses of beta-CAs may provide models for the proposed active and inactive forms of the H. influenzae and E. coli enzymes.

Articles - 2a8d mentioned but not cited (6)

  1. Structural studies of β-carbonic anhydrase from the green alga Coccomyxa: inhibitor complexes with anions and acetazolamide. Huang S, Hainzl T, Grundström C, Forsman C, Samuelsson G, Sauer-Eriksson AE. PLoS One 6 e28458 (2011)
  2. Allosteric site variants of Haemophilus influenzae beta-carbonic anhydrase. Rowlett RS, Tu C, Lee J, Herman AG, Chapnick DA, Shah SH, Gareiss PC. Biochemistry 48 6146-6156 (2009)
  3. Carbon Dioxide "Trapped" in a β-Carbonic Anhydrase. Aggarwal M, Chua TK, Pinard MA, Szebenyi DM, McKenna R. Biochemistry 54 6631-6638 (2015)
  4. Co(II)-substituted Haemophilus influenzae β-carbonic anhydrase: spectral evidence for allosteric regulation by pH and bicarbonate ion. Hoffmann KM, Samardzic D, Heever Kv, Rowlett RS. Arch Biochem Biophys 511 80-87 (2011)
  5. Evidence for a bicarbonate "escort" site in Haemophilus influenzae beta-carbonic anhydrase . Rowlett RS, Hoffmann KM, Failing H, Mysliwiec MM, Samardzic D. Biochemistry 49 3640-3647 (2010)
  6. Crystal Structure of β-Carbonic Anhydrase CafA from the Fungal Pathogen Aspergillus fumigatus. Kim S, Yeon J, Sung J, Jin MS. Mol Cells 43 831-840 (2020)


Reviews citing this publication (10)

  1. Structure-based drug discovery of carbonic anhydrase inhibitors. Supuran CT. J Enzyme Inhib Med Chem 27 759-772 (2012)
  2. Carbonic anhydrase as a model for biophysical and physical-organic studies of proteins and protein-ligand binding. Krishnamurthy VM, Kaufman GK, Urbach AR, Gitlin I, Gudiksen KL, Weibel DB, Whitesides GM. Chem Rev 108 946-1051 (2008)
  3. Anti-infective carbonic anhydrase inhibitors: a patent and literature review. Capasso C, Supuran CT. Expert Opin Ther Pat 23 693-704 (2013)
  4. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Capasso C, Supuran CT. Expert Opin Ther Targets 19 1689-1704 (2015)
  5. Thermostable Carbonic Anhydrases in Biotechnological Applications. Di Fiore A, Alterio V, Monti SM, De Simone G, D'Ambrosio K. Int J Mol Sci 16 15456-15480 (2015)
  6. Crystallography and Its Impact on Carbonic Anhydrase Research. Lomelino CL, Andring JT, McKenna R. Int J Med Chem 2018 9419521 (2018)
  7. Microbial Carbonic Anhydrases in Biomimetic Carbon Sequestration for Mitigating Global Warming: Prospects and Perspectives. Bose H, Satyanarayana T. Front Microbiol 8 1615 (2017)
  8. An Update on the Metabolic Roles of Carbonic Anhydrases in the Model Alga Chlamydomonas reinhardtii. Aspatwar A, Haapanen S, Parkkila S. Metabolites 8 E22 (2018)
  9. Role of carbonic anhydrases in pathogenic micro-organisms: a focus on Aspergillus fumigatus. Tobal JM, Balieiro MEDSF. J Med Microbiol 63 15-27 (2014)
  10. A matter of structure: structural comparison of fungal carbonic anhydrases. Lehneck R, Pöggeler S. Appl Microbiol Biotechnol 98 8433-8441 (2014)

Articles citing this publication (33)

  1. Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Xu Y, Feng L, Jeffrey PD, Shi Y, Morel FM. Nature 452 56-61 (2008)
  2. Bacterial carbonic anhydrases as drug targets: toward novel antibiotics? Supuran CT. Front Pharmacol 2 34 (2011)
  3. Structure and inhibition of the CO2-sensing carbonic anhydrase Can2 from the pathogenic fungus Cryptococcus neoformans. Schlicker C, Hall RA, Vullo D, Middelhaufe S, Gertz M, Supuran CT, Mühlschlegel FA, Steegborn C. J Mol Biol 385 1207-1220 (2009)
  4. A multiprotein bicarbonate dehydration complex essential to carboxysome function in cyanobacteria. Cot SS, So AK, Espie GS. J Bacteriol 190 936-945 (2008)
  5. Carbonic anhydrase inhibitors. Characterization and inhibition studies of the most active beta-carbonic anhydrase from Mycobacterium tuberculosis, Rv3588c. Carta F, Maresca A, Covarrubias AS, Mowbray SL, Jones TA, Supuran CT. Bioorg Med Chem Lett 19 6649-6654 (2009)
  6. Crystal structure and kinetic studies of a tetrameric type II β-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae. Ferraroni M, Del Prete S, Vullo D, Capasso C, Supuran CT. Acta Crystallogr D Biol Crystallogr 71 2449-2456 (2015)
  7. Characterization of the first beta-class carbonic anhydrase from an arthropod (Drosophila melanogaster) and phylogenetic analysis of beta-class carbonic anhydrases in invertebrates. Syrjänen L, Tolvanen M, Hilvo M, Olatubosun A, Innocenti A, Scozzafava A, Leppiniemi J, Niederhauser B, Hytönen VP, Gorr TA, Parkkila S, Supuran CT. BMC Biochem 11 28 (2010)
  8. Anion inhibition studies of the α-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae. Vullo D, Isik S, Del Prete S, De Luca V, Carginale V, Scozzafava A, Supuran CT, Capasso C. Bioorg Med Chem Lett 23 1636-1638 (2013)
  9. Carbonic anhydrase is essential for Streptococcus pneumoniae growth in environmental ambient air. Burghout P, Cron LE, Gradstedt H, Quintero B, Simonetti E, Bijlsma JJ, Bootsma HJ, Hermans PW. J Bacteriol 192 4054-4062 (2010)
  10. Inhibition studies of the β-carbonic anhydrases from the bacterial pathogen Salmonella enterica serovar Typhimurium with sulfonamides and sulfamates. Nishimori I, Minakuchi T, Vullo D, Scozzafava A, Supuran CT. Bioorg Med Chem 19 5023-5030 (2011)
  11. Anion inhibition studies of a β-carbonic anhydrase from Clostridium perfringens. Vullo D, Sai Kumar RS, Scozzafava A, Capasso C, Ferry JG, Supuran CT. Bioorg Med Chem Lett 23 6706-6710 (2013)
  12. Crystal structures of two tetrameric β-carbonic anhydrases from the filamentous ascomycete Sordaria macrospora. Lehneck R, Neumann P, Vullo D, Elleuche S, Supuran CT, Ficner R, Pöggeler S. FEBS J 281 1759-1772 (2014)
  13. DABs are inorganic carbon pumps found throughout prokaryotic phyla. Desmarais JJ, Flamholz AI, Blikstad C, Dugan EJ, Laughlin TG, Oltrogge LM, Chen AW, Wetmore K, Diamond S, Wang JY, Savage DF. Nat Microbiol 4 2204-2215 (2019)
  14. Carbonic anhydrase inhibitors. Inhibition of the β-class enzymes from the fungal pathogens Candida albicans and Cryptococcus neoformans with branched aliphatic/aromatic carboxylates and their derivatives. Carta F, Innocenti A, Hall RA, Mühlschlegel FA, Scozzafava A, Supuran CT. Bioorg Med Chem Lett 21 2521-2526 (2011)
  15. Nontypeable Haemophilus influenzae carbonic anhydrase is important for environmental and intracellular survival. Langereis JD, Zomer A, Stunnenberg HG, Burghout P, Hermans PW. J Bacteriol 195 2737-2746 (2013)
  16. Three functional β-carbonic anhydrases in Pseudomonas aeruginosa PAO1: role in survival in ambient air. Lotlikar SR, Hnatusko S, Dickenson NE, Choudhari SP, Picking WL, Patrauchan MA. Microbiology (Reading) 159 1748-1759 (2013)
  17. Structural Mapping of Anion Inhibitors to β-Carbonic Anhydrase psCA3 from Pseudomonas aeruginosa. Murray AB, Aggarwal M, Pinard M, Vullo D, Patrauchan M, Supuran CT, McKenna R. ChemMedChem 13 2024-2029 (2018)
  18. Structural insights into the substrate tunnel of Saccharomyces cerevisiae carbonic anhydrase Nce103. Teng YB, Jiang YL, He YX, He WW, Lian FM, Chen Y, Zhou CZ. BMC Struct Biol 9 67 (2009)
  19. Sulphonamide inhibition profile of Staphylococcus aureus β-carbonic anhydrase. Urbanski LJ, Bua S, Angeli A, Kuuslahti M, Hytönen VP, Supuran CT, Parkkila S. J Enzyme Inhib Med Chem 35 1834-1839 (2020)
  20. A bicarbonate cofactor modulates 1,4-dihydroxy-2-naphthoyl-coenzyme a synthase in menaquinone biosynthesis of Escherichia coli. Jiang M, Chen M, Guo ZF, Guo Z. J Biol Chem 285 30159-30169 (2010)
  21. Biochemical and structural characterisation of a protozoan beta-carbonic anhydrase from Trichomonas vaginalis. Urbański LJ, Di Fiore A, Azizi L, Hytönen VP, Kuuslahti M, Buonanno M, Monti SM, Angeli A, Zolfaghari Emameh R, Supuran CT, De Simone G, Parkkila S. J Enzyme Inhib Med Chem 35 1292-1299 (2020)
  22. Structures of the γ-class carbonic anhydrase homologue YrdA suggest a possible allosteric switch. Park HM, Park JH, Choi JW, Lee J, Kim BY, Jung CH, Kim JS. Acta Crystallogr D Biol Crystallogr 68 920-926 (2012)
  23. Activation studies of the β-carbonic anhydrases from Escherichia coli with amino acids and amines. Nocentini A, Del Prete S, Mastrolorenzo MD, Donald WA, Capasso C, Supuran CT. J Enzyme Inhib Med Chem 35 1379-1386 (2020)
  24. Anion Inhibition Studies of the Beta-Carbonic Anhydrase from Escherichia coli. Del Prete S, De Luca V, Nocentini A, Scaloni A, Mastrolorenzo MD, Supuran CT, Capasso C. Molecules 25 E2564 (2020)
  25. Structural basis for carbon dioxide binding by 2-ketopropyl coenzyme M oxidoreductase/carboxylase. Pandey AS, Mulder DW, Ensign SA, Peters JW. FEBS Lett 585 459-464 (2011)
  26. Sulfonamide inhibition studies of the β carbonic anhydrase from Drosophila melanogaster. Syrjänen L, Parkkila S, Scozzafava A, Supuran CT. Bioorg Med Chem Lett 24 2797-2801 (2014)
  27. Crystal structure of carbonic anhydrase CaNce103p from the pathogenic yeast Candida albicans. Dostál J, Brynda J, Blaha J, Macháček S, Heidingsfeld O, Pichová I. BMC Struct Biol 18 14 (2018)
  28. Crystal Structure of a Tetrameric Type II β-Carbonic Anhydrase from the Pathogenic Bacterium Burkholderia pseudomallei. Angeli A, Ferraroni M, Pinteala M, Maier SS, Simionescu BC, Carta F, Del Prete S, Capasso C, Supuran CT. Molecules 25 E2269 (2020)
  29. Crystal Structure of a Highly Thermostable α-Carbonic Anhydrase from Persephonella marina EX-H1. Kim S, Sung J, Yeon J, Choi SH, Jin MS. Mol Cells 42 460-469 (2019)
  30. Major contribution of the type II beta carbonic anhydrase CanB (Cj0237) to the capnophilic growth phenotype of Campylobacter jejuni. Al-Haideri H, White MA, Kelly DJ. Environ Microbiol 18 721-735 (2016)
  31. Purification and inhibition studies with anions and sulfonamides of an α-carbonic anhydrase from the Antarctic seal Leptonychotes weddellii. Cincinelli A, Martellini T, Innocenti A, Scozzafava A, Supuran CT. Bioorg Med Chem 19 1847-1851 (2011)
  32. Comparison between α- and β-carbonic anhydrases: can Zn(His)3(H2O) and Zn(His)(Cys)2(H2O) sites lead to equivalent enzymes? Pannetier F, Ohanessian G, Frison G. Dalton Trans 40 2696-2698 (2011)
  33. Surface histidine mutations for the metal affinity purification of a β-carbonic anhydrase. Hoffmann KM, Wood KM, Labrum AD, Lee DK, Bolinger IM, Konis ME, Blount AG, Prussia GA, Schroll MM, Watson JM. Anal Biochem 458 66-68 (2014)


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