1,888
Views
11
CrossRef citations to date
0
Altmetric
Research Paper

Inhibition of α-, β- and γ-carbonic anhydrases from the pathogenic bacterium Vibrio cholerae with aromatic sulphonamides and clinically licenced drugs – a joint docking/molecular dynamics study

, ORCID Icon, , , , , ORCID Icon & ORCID Icon show all
Pages 469-479 | Received 05 Nov 2020, Accepted 01 Dec 2020, Published online: 20 Jan 2021

References

  • Baker-Austin C, Oliver JD, Alam M, et. al. Vibrio spp. infections. Nat Rev Dis Primers 2018;4:8.
  • Baker-Austin C, Trinanes J, Gonzalez-Escalona N, et al. Non-Cholera vibrios: the microbial barometer of climate change. Trends Microbiol 2017;25:76–84.
  • World Health Organization. Weekly epidemiological record. 2016;21:421–28.
  • World Health Organization. Weekly epidemiological record. 2018;93:489–500.
  • Zuckerman JN, Rombo L, Fisch A. The true burden and risk of cholera: implications for prevention and control. Lancet Infect Dis 2007;7:521–30.
  • World Health Organization. Weekly epidemiological record 2010;85:117–28.
  • Rabbani GH, Greenough WB. III. Food as a vehicle of transmission of cholera. J Diarrhoeal Dis Res 1999;17:1–9.
  • Sugimoto JD, Koepke AA, Kenah EE, et al. Household transmission of Vibrio cholerae in Bangladesh. PLoS Negl Trop Dis 2014;8:e3314e3314.
  • Goh KT, Teo SH, Lam S, et al. Person-to-person transmission of cholera in a psychiatric hospital. J Infect 1990;20:193–200.
  • Gangarosa EF, Beisel WR, Benyajati C, et al. The nature of the gastrointestinal lesion in asiatic cholera and its relation to pathogenesis: a biopsy study. Am J Trop Med Hyg 1960;9:125–35.
  • Abuaita BH, Withey JH. Bicarbonate induces vibrio cholerae virulence gene expression by enhancing ToxT activity. Infect Immun 2009;77:4111–20.
  • Weber GG, Klose KEK. The complexity of ToxT-dependent transcription in Vibrio cholerae. Indian J Med Res 2011;133:201–6.
  • Kirn TJ, Lafferty MJ, Sandoe CM, et al. Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol Microbiol 2000;35:896–910.
  • Herrington DA, Hall RH, Losonsky G, et al. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J Exp Med 1988;168:1487–92.
  • Fishman PH, Atikkan EE. Mechanism of action of cholera toxin: effect of receptor density and multivalent binding on activation of adenylate cyclase. J Membr Biol 1980;54:51–60.
  • De SN, Chatterje DN. Enterotoxicity of bacteria-free culture-filtrate of Vibrio cholerae. Nature 1959;183:1533–4.
  • Levine MM, Kaper JB, Black RE, et al. New knowledge on pathogenesis of bacterial enteric infections as applied to vaccine development. Microbiol Rev 1983;47:510–50.
  • World Health Organization. Prevention and control of cholera. WHO 2020 https://www.who.int/health-topics/cholera#tab=tab_2.
  • World Health Organization. Treatment diarrhoea: manual: a manual for physicians other senior health workers, 4th rev. World Health Organization 2005.
  • Alam NH, Ashraf H. Treatment of infectious diarrhea in children. Paediatr Drugs 2003;5:151–65.
  • Ahmed T, Ali M, Ullah MM, et al. Mortality in severely malnourished children with diarrhoea and use of a standardized management protocol. Lancet 1999;353:1919–22.
  • World Health Organization‎. Clinical management of acute diarrhoea: WHO/UNICEF joint statement. World Health Organization 2004.
  • Lindenbaum J, Greenough WB, Islam MR. Antibiotic therapy of Cholera in children. Bull World Health Organ 1967;37: 871–83.
  • Kaushik JS, Gupta P, Faridi MM, et al. Single-dose azithromycin versus ciprofloxacin for cholera in children: a randomized controlled trial. Indian Pediatr 2010;47:309–15.
  • Roy SK, Hossain MJ, Khatun W, et al. Zinc supplementation in children with cholera in Bangladesh: randomised controlled trial. BMJ 2008;336:266–8.
  • Brown ED, Wright GD. Antibacterial drug discovery in the resistance era. Nature 2016;529:336–43.
  • Del Prete S, Isik S, Vullo D, et al. DNA cloning, characterization, and inhibition studies of an α-carbonic anhydrase from the pathogenic bacterium vibrio cholerae. J Med Chem 2012;55:10742–8.
  • 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.
  • Vullo D, Isik S, Del Prete S, et al. Anion inhibition studies of the α-carbonic anhydrase from the pathogenic bacterium vibrio cholerae. Bioorg Med Chem Lett 2013;23:1636–8.
  • Maren TH. Carbonic anhydrase: chemistry, physiology, and inhibition. Physiol Rev 1967;47:595–781.
  • Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81.
  • Ferry JF. The gamma class of carbonic anhydrases. Biochim Biophys Acta 2010;1804:374–81.
  • 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.
  • 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.
  • Alterio V, Langella E, Viparelli F, et al. Structural and inhibition insights into carbonic anhydrase CDCA1 from the marine diatom Thalassiosira weissflogii. Biochimie 2012;94:1232–41.
  • Supuran CT, Capasso C. Biomedical applications of prokaryotic carbonic anhydrases. Expert Opin Ther Pat 2018;28:745–54.
  • Jensen EL, Clement R, Kosta A, et al. A new widespread subclass of carbonic anhydrase in marine phytoplankton. Isme J 2019;13:2094–106.
  • Del Prete S, Nocentini A, Supuran CT, et al. Bacterial ι-carbonic anhydrase: a new active class of carbonic anhydrase identified in the genome of the Gram-negative bacterium Burkholderia territorii. J Enzyme Inhib Med Chem 2020;35:1060–8.
  • Smith KS, Ferry JG. Prokaryotic carbonic anhydrases. FEMS Microbiol Rev 2000;24:335–59.
  • Del Prete S, Vullo D, De Luca V, et al. Biochemical characterization of recombinant β-carbonic anhydrase (PgiCAb) identified in the genome of the oral pathogenic bacterium Porphyromonas gingivalis. J Enzyme Inhib Med Chem 2015;30:359–70.
  • 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.
  • Vullo D, Del Prete S, Osman SM, et al. Sulfonamide inhibition studies of the γ-carbonic anhydrase from the oral pathogen Porphyromonas gingivalis. Bioorg Med Chem Lett 2014;24:240–4.
  • 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.
  • Cummins EP, Selfridge AC, Sporn PH, et al. Carbon dioxide-sensing in organisms and its implications for human disease. Cell Mol Life Sci 2014;71:831–45.
  • Del Prete S, Vullo D, De Luca V, et al. Comparison of the sulfonamide inhibition profiles of the α-, β- and γ-carbonic anhydrases from the pathogenic bacterium Vibrio cholerae. Bioorg Med Chem Lett 2016;26:1941–6.
  • Di Fiore A, D'Ambrosio K, Ayoub J, et al. α-Carbonic anhydrases. In: Supuran CT, Nocentini A, editors. Carbonic anhydrases. biochemistry and pharmacology of an evergreen pharmaceutical target. Amsterdam: Elsevier; 2019;19–54.
  • 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.
  • Murray AB, McKenna R, β-Carbonic anhydrases. In: Supuran CT, Nocentini A, editors. Carbonic Anhydrases. Biochemistry and pharmacology of an evergreen pharmaceutical target. Amsterdam: Elsevier; 2019;55–77.
  • Supuran CT, Capasso C. Carbonic anhydrases from pathogens: bacterial carbonic anhydrases and their inhibitors as potential antiinfectives. In: Supuran CT, Nocentini A, editors. Carbonic anhydrases. Biochemistry and pharmacology of an evergreen pharmaceutical target. Amsterdam: Elsevier; 2019;387–417.
  • Bonardi A, Gratteri P, Nocentini A. Carbonic anhydrases from pathogens: fungal carbonic anhydrases and their inhibitors as potential antifungal agents. In: Supuran CT, Nocentini A, editors. Carbonic anhydrases. Biochemistry and pharmacology of an evergreen pharmaceutical target. Amsterdam: Elsevier; 2019;419–48.
  • Ferraroni M. γ-Carbonic anhydrases. In: Supuran CT, Nocentini A, editors. Carbonic anhydrases. Biochemistry and pharmacology of an evergreen pharmaceutical target. Amsterdam: Elsevier; 2019;79–105.
  • Del Prete S, Vullo D, Di Fonzo P, et al. Sulfonamide inhibition profile of the γ-carbonic anhydrase identified in the genome of the pathogenic bacterium Burkholderia pseudomallei the etiological agent responsible of melioidosis. Bioorg Med Chem Lett 2017;27:490–5.
  • Del Prete S, Vullo D, Osman SM, et al. Sulfonamide inhibition study of the carbonic anhydrases from the bacterial pathogen Porphyromonas gingivalis: the β-class (PgiCAb) versus the γ-class (PgiCA) enzymes. Bioorg Med Chem 2014;22:4537–43.
  • De Luca V, Vullo D, Del Prete S, et al. Cloning, characterization and anion inhibition studies of a γ-carbonic anhydrase from the Antarctic bacterium Colwellia psychrerythraea. Bioorg Med Chem 2016;24:835–40.
  • De Luca V, Vullo D, Del Prete S, et al. Cloning, characterization and anion inhibition studies of a new γ-carbonic anhydrase from the Antarctic bacterium Pseudoalteromonas haloplanktis. Bioorg Med Chem 2015;23:4405–9.
  • Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60.
  • Bonardi A, Nocentini A, Cadoni R, et al. Benzoxaboroles: new potent inhibitors of the carbonic anhydrases of the pathogenic bacterium Vibrio cholerae. ACS Med Chem. Lett 2020; doi:https://doi.org/10.1021/acsmedchemlett.0c00403.
  • Schrödinger Suite Release 2019-1, Schrödinger, LLC, New York, NY, 2019:(a) Prime, v.5.5; (b) Maestro v.11.9; (c) Epik, v.4.7; (d) Impact, v.8.2; (e) Macromodel v.12.3. (f) Glide, v.8.2; (g) Desmond, v.5.7; (h) Jaguar, v. 10.3.
  • a. Pustenko A, Nocentini A, Gratteri P, et al. The antibiotic furagin and its derivatives are isoform-selective human carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2020;35:1011–20; b. Said MA, Eldehna WM, Nocentini A, et al. Synthesis, biological and molecular dynamics investigations with a series of triazolopyrimidine/triazole-based benzenesulfonamides as novel carbonic anhydrase inhibitors. Eur J Med Chem 2020;185:111843; c. Nocentini A, Bonardi A, Gratteri P, et al. Steroids interfere with human carbonic anhydrase activity by using alternative binding mechanisms. J Enzyme Inhib Med Chem 2018;33:1453–9.
  • a. Abdelrahman MA, Ibrahim HS, Nocentini A, et al. Novel 3-substituted coumarins as selective human carbonic anhydrase IX and XII inhibitors: Synthesis, biological and molecular dynamics analysis. Eur J Med Chem 2020;209:112897; b. Abo-Ashour MF, Eldehna WM, Nocentini A, et al. 3-Hydrazinoisatin-based benzenesulfonamides as novel carbonic anhydrase inhibitors endowed with anticancer activity: Synthesis, in vitro biological evaluation and in silico insights. Eur J Med Chem 2019;184:111768.
  • Bonardi A, Nocentini A, Bua S, et al. Sulfonamide inhibitors of human carbonic anhydrases designed through a three-tails approach: improving ligand/isoform matching and selectivity of action. J Med Chem 2020;63:7422–44.
  • Modakh YK, Liu YC, Machuca MA, et al. Structural basis for the inhibition of helicobacter pylori α-carbonic anhydrase by sulfonamides. PLoS One 2015;10:e0127149.
  • 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
  • Murray AB, Aggarwal M, Pinard M, et al. Structural mapping of anion inhibitors to β-Carbonic Anhydrase psCA3 from Pseudomonas aeruginosa. ChemMedChem 2018;13:2024–9.
  • Kaur J, Cao X, Abutaleb NS, et al. Optimization of acetazolamide-based scaffold as potent inhibitors of vancomycin-resistant enterococcus. J Med Chem 2020;63:9540–62.
  • Berman HM, Westbrook J, Feng Z, et al. The Protein Data Bank. Nucleic Acids Res 2000; 28:235–42.