Biochemical and structural characterisation of a protozoan beta-carbonic anhydrase from Trichomonas vaginalis

References

• Lin WC, Chang WT, Chang TY, Shin JW. The pathogenesis of human cervical epithelium cells induced by interacting with trichomonas vaginalis. PLoS One 2015;10:e0124087
   PubMed Web of Science ®Google Scholar
• Schwebke JR, Burgess D. Trichomoniasis. Clin Microbiol Rev 2004;17:794–803.
   PubMed Web of Science ®Google Scholar
• Rowley J, Vander Hoorn S, Korenromp E, et al. Chlamydia, gonorrhoea, trichomoniasis and syphilis: global prevalence and incidence estimates, 2016. Bull World Health Organ 2019;97:548–62. P.
   PubMed Web of Science ®Google Scholar
• Available from: http://www.who.int/mediacentre/factsheets/fs110/en/.
   Google Scholar
• Lewis D. Trichomoniasis. Medicine 2014;42:369–71.
   Google Scholar
• Sherrard J, Ison C, Moody J, et al. United Kingdom National Guideline on the Management of Trichomonas vaginalis 2014. Int J STD AIDS 2014;25:541–9.
   PubMed Web of Science ®Google Scholar
• McClelland RS, Sangare L, Hassan WM, et al. Infection with Trichomonas vaginalis increases the risk of HIV-1 acquisition. J Infect Dis 2007;195:698–702.
   PubMed Web of Science ®Google Scholar
• Cotch MF, Pastorek JG, 2nd, Nugent RP, et al. Trichomonas vaginalis associated with low birth weight and preterm delivery. The Vaginal Infections and Prematurity Study Group. Sex Transm Dis 1997;24:353–60.
   PubMed Web of Science ®Google Scholar
• Zhang ZF, Begg CB. Is Trichomonas vaginalis a cause of cervical neoplasia? Results from a combined analysis of 24 studies. Int J Epidemiol 1994;23:682–90.
   PubMed Web of Science ®Google Scholar
• Twu O, Dessi D, Vu A, et al. Trichomonas vaginalis homolog of macrophage migration inhibitory factor induces prostate cell growth, invasiveness, and inflammatory responses. Proc Natl Acad Sci USA 2014;111:8179–84.
   PubMed Web of Science ®Google Scholar
• Waitkins SA, Thomas DJ. Isolation of Trichomonas vaginalis resistant to metronidazole. Lancet 1981;2:590.
   PubMed Web of Science ®Google Scholar
• Lewis DA, Habgood L, White R, et al. Managing vaginal trichomoniasis resistant to high-dose metronidazole therapy. Int J STD AIDS 1997;8:780–4.
   PubMed Web of Science ®Google Scholar
• Supuran C.T., De Simone, G. eds. Carbonic anhydrases as biocatalysts. In: From theory to medical and industrial applications. 1st ed. The netherlands: Elsevier; 2015: 398.
   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
• Kikutani S, Nakajima K, Nagasato C, et al. Thylakoid luminal θ-carbonic anhydrase critical for growth and photosynthesis in the marine diatom Phaeodactylum tricornutum. Proc Natl Acad Sci USA 2016;113:9828–33.
   PubMed Web of Science ®Google Scholar
• Jensen EL, Clement R, Kosta A, et al. A new widespread subclass of carbonic anhydrase in marine phytoplankton. Isme J 2019;13:2094–106.
   PubMed Web of Science ®Google Scholar
• De Simone G, Di Fiore A, Capasso C, Supuran CT. The zinc coordination pattern in the η-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
• Syrjanen L, Kuuslahti M, Tolvanen M, et al. The β-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
• Vullo D, Del Prete S, Di Fonzo P, et al. Comparison of the sulfonamide inhibition profiles of the beta- and gamma-carbonic anhydrases from the pathogenic Bacterium Burkholderia pseudomallei. Molecules 2017;22:421.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Bortezomib inhibits bacterial and fungal β-carbonic anhydrases. Bioorg Med Chem 2016;24:4406–9.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Hall RA, Schlicker C, et al. Carbonic anhydrase inhibitors. Inhibition of the beta-class enzymes from the fungal pathogens Candida albicans and Cryptococcus neoformans with aliphatic and aromatic carboxylates. Bioorg Med Chem 2009;17:2654–7.
   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
• 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
• Del Prete S, Vullo D, De Luca V, et al. Sulfonamide inhibition studies of the β-carbonic anhydrase from the pathogenic Bacterium Vibrio cholerae. Bioorg Med Chem 2016;24:1115–20.
   PubMed Web of Science ®Google Scholar
• Zolfaghari Emameh R, Barker HR, Tolvanen ME, et al. Horizontal transfer of β-carbonic anhydrase genes from prokaryotes to protozoans, insects, and nematodes. Parasit Vectors 2016;9:152
   PubMed Web of Science ®Google Scholar
• Laitinen OH, Airenne KJ, Hytonen VP, et al. A multipurpose vector system for the screening of libraries in bacteria, insect and mammalian cells and expression in vivo. Nucleic Acids Res 2005;33:e42
   PubMed Web of Science ®Google Scholar
• Piao S, Xu Y, Ha NC. Crystallization and preliminary X-ray crystallographic analysis of MacA from Actinobacillus actinomycetemcomitans. Acta Crystallogr Sect F Struct Biol Cryst Commun 2008;64:391–3.
   PubMedGoogle Scholar
• Hilvo M, Baranauskiene L, Salzano AM, et al. Biochemical characterization of CA IX, one of the most active carbonic anhydrase isozymes. J Biol Chem 2008;283:27799–809.
   PubMed Web of Science ®Google Scholar
• Jancarik J, Scott WG, Milligan DL, et al. Crystallization and preliminary X-ray diffraction study of the ligand-binding domain of the bacterial chemotaxis-mediating aspartate receptor of Salmonella typhimurium. J Mol Biol 1991;221:31–4.
   PubMed Web of Science ®Google Scholar
• Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Meth Enzymol 1997;276:307–26.
   PubMed Web of Science ®Google Scholar
• Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallographica Section A 1994;50:157–63.
   Web of Science ®Google Scholar
• Strop P, Smith KS, Iverson TM, et al. Crystal structure of the “cab”-type beta class carbonic anhydrase from the archaeon Methanobacterium thermoautotrophicum. J Biol Chem 2001;276:10299–305.
   PubMed Web of Science ®Google Scholar
• Brunger AT. Version 1.2 of the Crystallography and NMR system. Nature Protocols 2007;2:2728–33.
   PubMed Web of Science ®Google Scholar
• Brunger AT, Adams PD, Clore GM, et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 1998;54:905–21.
   PubMed Web of Science ®Google Scholar
• Jones TA, Zou JY, Cowan SW, Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr Sec A, Foundat Crystallogra 1991;47:110–9.
   PubMed Web of Science ®Google Scholar
• Panjikar S, Parthasarathy V, Lamzin VS, et al. Auto-rickshaw: an automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment. Acta Crystallogr D Biol Crystallogr 2005;61:449–57.
   PubMed Web of Science ®Google Scholar
• Panjikar S, Parthasarathy V, Lamzin VS, et al. On the combination of molecular replacement and single-wavelength anomalous diffraction phasing for automated structure determination. Acta Crystallogr D Biol Crystallogr 2009;65:1089–97.
   PubMedGoogle Scholar
• Murshudov GN, Skubak P, Lebedev AA, Pannu NS, et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr 2011;67:355–67.
   PubMed Web of Science ®Google Scholar
• Winn MD, Ballard CC, Cowtan KD, Dodson EJ, et al. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 2011;67:235–42.
   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
• Nishimori I, Minakuchi T, Vullo D, et al. Inhibition studies of the β-carbonic anhydrases from the bacterial pathogen Salmonella enterica serovar Typhimurium with sulfonamides and sulfamates. Bioorg Med Chem 2011;19:5023–30.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Legionella pneumophila carbonic anhydrases: underexplored antibacterial drug targets. Pathogens 2016;5:44.
   PubMed Web of Science ®Google Scholar
• Kimber MS, Pai EF. The active site architecture of Pisum sativum beta-carbonic anhydrase is a mirror image of that of alpha-carbonic anhydrases. Embo J 2000;19:1407–18.
   PubMed Web of Science ®Google Scholar
• Covarrubias AS, Bergfors T, Jones TA, Högbom M. Structural mechanics of the pH-dependent activity of beta-carbonic anhydrase from Mycobacterium tuberculosis. J Biol Chem 2006;281:4993–9.
   PubMed Web of Science ®Google Scholar
• Sawaya MR, Cannon GC, Heinhorst S, et al. The structure of beta-carbonic anhydrase from the carboxysomal shell reveals a distinct subclass with one active site for the price of two. J Biol Chem 2006;281:7546–55.
   PubMed Web of Science ®Google Scholar
• Teng YB, Jiang YL, He YX, et al. Structural insights into the substrate tunnel of Saccharomyces cerevisiae carbonic anhydrase Nce103. BMC Struct Biol 2009;9:67
   PubMed Web of Science ®Google Scholar
• Huang S, Hainzl T, Grundstrom C, et al. Structural studies of β-carbonic anhydrase from the green alga Coccomyxa: inhibitor complexes with anions and acetazolamide. PLoS One 2011;6:e28458
   PubMed Web of Science ®Google Scholar
• Mitsuhashi S, Mizushima T, Yamashita E, et al. X-ray structure of beta-carbonic anhydrase from the red alga, Porphyridium purpureum, reveals a novel catalytic site for CO(2) hydration. J Biol Chem 2000;275:5521–6.
   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
• Cronk JD, Rowlett RS, Zhang KY, et al. Identification of a novel noncatalytic bicarbonate binding site in eubacterial beta-carbonic anhydrase. Biochemistry 2006;45:4351–61.
   PubMed Web of Science ®Google Scholar
• Schlicker C, Hall RA, Vullo D, et al. Structure and inhibition of the CO2-sensing carbonic anhydrase Can2 from the pathogenic fungus Cryptococcus neoformans. J Mol Biol 2009;385:1207–20.
   PubMed Web of Science ®Google Scholar
• Ferraroni M, Del Prete S, Vullo D, et al. Crystal structure and kinetic studies of a tetrameric type II β-carbonic anhydrase from the pathogenic Bacterium Vibrio cholerae. Acta Crystallogr D Biol Crystallogr 2015;71:2449–56.
   PubMedGoogle 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
• McGurn LD, Moazami-Goudarzi M, White SA, et al. The structure, kinetics and interactions of the β-carboxysomal β-carbonic anhydrase, CcaA. Biochem J 2016;473:4559–72.
   PubMed Web of Science ®Google Scholar
• Lehneck R, Neumann P, Vullo D, et al. Crystal structures of two tetrameric β-carbonic anhydrases from the filamentous ascomycete Sordaria macrospora. Febs J 2014;281:1759–72.
   PubMed Web of Science ®Google Scholar
• Kim S, Kim NJ, Hong S, et al. The structural basis of the low catalytic activities of the two minor β-carbonic anhydrases of the filamentous fungus Aspergillus fumigatus. J Struct Biol 2019;208:61–8.
   PubMed Web of Science ®Google Scholar
• Dostal J, Brynda J, Blaha J, et al. Crystal structure of carbonic anhydrase CaNce103p from the pathogenic yeast Candida albicans. BMC Struct Biol 2018;18:14.
   PubMed Web of Science ®Google Scholar
• Holm L. Benchmarking fold detection by DaliLite v.5. Bioinformatics 2019;35:5326–7.
   PubMed Web of Science ®Google Scholar
• Pal DS, Mondal DK, Datta R. Identification of metal dithiocarbamates as a novel class of antileishmanial agents. Antimicrob Agents Chemother 2015;59:2144–52.
   PubMed Web of Science ®Google Scholar
• Pal DS, Abbasi M, Mondal DK, et al. Interplay between a cytosolic and a cell surface carbonic anhydrase in pH homeostasis and acid tolerance of Leishmania. J Cell Sci 2017;130:754–66.
   PubMed Web of Science ®Google Scholar
• D’Ambrosio K, Supuran CT, De Simone G. Are carbonic anhydrases suitable targets to fight protozoan parasitic diseases? Curr Med Chem 2018;25:5266–78.
   PubMed Web of Science ®Google Scholar
• Syrjanen L, Vermelho AB, Rodrigues Ide A, et al. Cloning, characterization, and inhibition studies of a β-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
• Zolfaghari Emameh R, Kuuslahti M, Vullo D, et al. Ascaris lumbricoides β carbonic anhydrase: a potential target enzyme for treatment of ascariasis. Parasit Vectors 2015;8:479.
   PubMed Web of Science ®Google Scholar
• Haapanen S, Bua S, Kuuslahti M, et al. Cloning, Characterization and Anion Inhibition Studies of a beta-Carbonic Anhydrase from the Pathogenic Protozoan Entamoeba histolytica. Molecules 2018;23:3112.
   PubMed Web of Science ®Google Scholar
• Rowlett RS. Structure and catalytic mechanism of the beta-carbonic anhydrases. Biochim Biophys Acta 2010;1804:362–73.
   PubMed Web of Science ®Google Scholar
• Suhanovsky MM, Sheppard K, Rowlett RS, β-Carbonic anhydrases: general features and medical implications. In: Supran CT, De Simone G, editors. Carbonic anhydrases as biocatalysts. USA: Elsevier B. V.; 2015. p. 247–74.
   Google Scholar