Benzenesulfonamide derivatives as Vibrio cholerae carbonic anhydrases inhibitors: a computational-aided insight in the structural rigidity-activity relationships

References

• Silva DL, Lima CM, Magalhães VCR, Baltazar LM, Peres NTA, Caligiorne RB, Moura AS, Fereguetti T, Martins JC, Rabelo LF, et al. Fungal and bacterial coinfections increase mortality of severely ill COVID-19 patients. J Hosp Infect. 2021;113:145–154.
   PubMed Web of Science ®Google Scholar
• Bardet A, Fraslin AM, Marghadi J, Borget I, Faron M, Honoré C, Delaloge S, Albiges L, Planchard D, Ducreux M, et al. Impact of COVID-19 on healthcare organisation and cancer outcomes. Eur J Cancer. 2021;153:123–132.
   PubMed Web of Science ®Google Scholar
• Uwishema O, Okereke M, Onyeaka H, Hasan MM, Donatus D, Martin Z, Oluwatomisin LA, Mhanna M, Olumide AO, Sun J, et al. Threats and outbreaks of cholera in Africa amidst COVID-19 pandemic: a double burden on Africa’s health systems. Trop Med Health. 2021;49(1):93.
   PubMed Web of Science ®Google Scholar
• D'Mello-Guyett L, Gallandat K, Van den Bergh R, Taylor D, Bulit G, Legros D, Maes P, Checchi F, Cumming O. Prevention and control of cholera with household and community water, sanitation and hygiene (WASH) interventions: A scoping review of current international guidelines. PLOS One. 2020;15(1):e0226549.
   PubMed Web of Science ®Google Scholar
• WHO. [accessed 2023 Jan 31]. https://www.who.int/news-room/fact-sheets/detail/cholera.
   Google Scholar
• ECDC. [accessed 2023 Jan 31]. https://www.ecdc.europa.eu/en/all-topics-z/cholera/surveillance-and-disease-data/cholera-monthly.
   Google Scholar
• Owoicho O, Abechi P, Olwal CO. Cholera in the era of COVID-19 pandemic: a worrying trend in Africa? Int J Public Health. 2021;66:1604030.
   PubMed Web of Science ®Google Scholar
• Oladapo RK, Oyetola AB, Obidiro OP, Olajide A, Osuagwu-Nwogu E, Olaitan OM, Ngokere C, Monisola I, Ibraheem B, Afolayan A. Rising cholera cases: harnessing the momentum of COVID-19 to strengthen Nigeria’s health systems. Int J Health Plann Manage. 2021;36(6):2030–2034.
   PubMed Web of Science ®Google Scholar
• Faruque SM, Ahmed KM, Siddique AK, Zaman K, Alim AR, Albert MJ. Molecular analysis of toxigenic Vibrio cholerae O139 Bengal strains isolated in Bangladesh between 1993 and 1996: evidence for emergence of a new clone of the Bengal vibrios. J Clin Microbiol. 1997;35(9):2299–2306.
   PubMed Web of Science ®Google Scholar
• CDC. [accessed 2023 Jan 31]. https://www.cdc.gov/cholera/treatment/antibiotic-treatment.html. (accessed on 31/01/2023).
   Google Scholar
• Das B, Verma J, Kumar P, Ghosh A, Ramamurthy T. Antibiotic resistance in Vibrio cholerae: understanding the ecology of resistance genes and mechanisms. Vaccine. 2020;38(Suppl 1):A83–A92.
   PubMedGoogle Scholar
• Ahmadi MH. Global status of tetracycline resistance among clinical isolates of Vibrio cholerae: a systematic review and meta-analysis. Antimicrob Resist Infect Control. 2021;10(1):115.
   PubMed Web of Science ®Google Scholar
• Gupta P, Modgil V, Kant V, Kaur H, Narayan C, Mahindroo J, Verma R, Mohan B, Taneja N. Phenotypic and genotypic characterization of antimicrobial resistance in clinical isolates of Vibrio cholerae over a decade (2002–2016). Indian J Med Microbiol. 2022;40(1):24–29.
   PubMed Web of Science ®Google Scholar
• Mashe T, Domman D, Tarupiwa A, Manangazira P, Phiri I, Masunda K, Chonzi P, Njamkepo E, Ramudzulu M, Mtapuri-Zinyowera S, et al. Highly resistant cholera outbreak strain in Zimbabwe. N Engl J Med. 2020;383(7):687–689.
   PubMed Web of Science ®Google Scholar
• Campestre C, De Luca V, Carradori S, Grande R, Carginale V, Scaloni A, Supuran CT, Capasso C. Carbonic anhydrases: new perspectives on protein functional role and inhibition in Helicobacter pylori. Front Microbiol. 2021;12:629163.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Structure and function of carbonic anhydrases. Biochem J. 2016;473(14):2023–2032.
   PubMedGoogle Scholar
• De Luca V, Carginale V, Supuran CT, Capasso C. gram-negative bacterium Escherichia coli as a model for testing the effect of carbonic anhydrase inhibition on bacterial growth. J Enzyme Inhib Med Chem. 2022;37(1):2092–2098.
   PubMed Web of Science ®Google Scholar
• Hewitt CS, Abutaleb NS, Elhassanny AEM, Nocentini A, Cao X, Amos DP, Youse MS, Holly KJ, Marapaka AK, An AW, et al. Structure-activity relationship studies of acetazolamide-based carbonic anhydrase inhibitors with activity against Neisseria gonorrhoeae. ACS Infect Dis. 2021;7(7):1969–1984.
   PubMed Web of Science ®Google Scholar
• Abutaleb NS, Elkashif A, Flaherty DP, Seleem MN. In Vivo antibacterial activity of acetazolamide. Antimicrob Agents Chemother. 2021;65(4):e01715-e01720.
   Web of Science ®Google Scholar
• Kaur J, Cao X, Abutaleb NS, Elkashif A, Graboski AL, Krabill AD, AbdelKhalek AH, An W, Bhardwaj A, Seleem MN, et al. Optimization of acetazolamide-based scaffold as potent inhibitors of vancomycin-resistant Enterococcus. J Med Chem. 2020;63(17):9540–9562.
   PubMed Web of Science ®Google Scholar
• Abutaleb NS, Elhassanny AEM, Flaherty DP, Seleem MN. In vitro and in vivo activities of the carbonic anhydrase inhibitor, dorzolamide, against vancomycin-resistant enterococci. Peer J. 2021;9:e11059.
   PubMed Web of Science ®Google Scholar
• Abutaleb NS, Elhassanny AEM, Seleem MN. In vivo efficacy of acetazolamide in a mouse model of Neisseria gonorrhoeae infection. Microb Pathog. 2022;164:105454.
   PubMed Web of Science ®Google Scholar
• Mancuso F, De Luca L, Bucolo F, Vrabel M, Angeli A, Capasso C, Supuran CT, Gitto R. 4-sulfamoylphenylalkylamides as inhibitors of carbonic anhydrases expressed in Vibrio cholerae. ChemMedChem. 2021;16(24):3787–3794.
   PubMed Web of Science ®Google Scholar
• Akgul O, Angeli A, Selleri S, Capasso C, Supuran CT, Carta F. Taurultams incorporating arylsulfonamide: first in vitro inhibition studies of α-, β- and γ-class Carbonic Anhydrases from Vibrio cholerae and Burkholderia pseudomallei. Eur J Med Chem. 2021;219:113444.
   PubMed Web of Science ®Google Scholar
• Abuaita BH, Withey JH. Bicarbonate Induces Vibrio cholerae virulence gene expression by enhancing ToxT activity. Infect Immun. 2009;77(9):4111–4120.
   PubMed Web of Science ®Google Scholar
• Butler SM, Camilli A. Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat Rev Microbiol. 2005;3(8):611–620.
   PubMed Web of Science ®Google Scholar
• Szklarczyk D, Gable AL, Nastou KC, Lyon D, Kirsch R, Pyysalo S, Doncheva NT, Legeay M, Fang T, Bork P, et al. The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res. 2021;49(D1):D605–D612.
   PubMed Web of Science ®Google Scholar
• Zeller T, Klug G. Thioredoxins in bacteria: functions in oxidative stress response and regulation of thioredoxin genes. Naturwissenschaften. 2006;93(6):259–266.
   PubMed Web of Science ®Google Scholar
• Del Prete S, De Luca V, Scozzafava A, Carginale V, Supuran CT, Capasso C. Biochemical properties of a new α-carbonic anhydrase from the human pathogenic bacterium, Vibrio cholerae. J Enzyme Inhib Med Chem. 2014;29(1):23–27.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, Carginale V, Osman SM, AlOthman Z, Supuran CT, Capasso C. 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(8):1941–1946.
   PubMed Web of Science ®Google Scholar
• Bonardi A, Nocentini A, Osman SM, Alasmary FA, Almutairi TM, Abdullah DS, Gratteri P, Supuran CT. 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. J Enzyme Inhib Med Chem. 2021;36(1):469–479.
   PubMed Web of Science ®Google Scholar
• Bonardi A, Nocentini A, Cadoni R, Del Prete S, Dumy P, Capasso C, Gratteri P, Supuran CT, Winum JY. Benzoxaboroles: new potent inhibitors of the carbonic anhydrases of the pathogenic bacterium Vibrio cholerae. ACS Med Chem Lett. 2020;11(11):2277–2284.
   PubMed Web of Science ®Google Scholar
• Demir-Yazıcı K, Güzel-Akdemir Ö, Angeli A, Supuran CT, Akdemir A. Novel indole-based hydrazones as potent inhibitors of the α-class carbonic anhydrase from pathogenic bacterium Vibrio cholerae. IJMS. 2020;21(9):3131.
   Google Scholar
• Bua S, Berrino E, Del Prete S, Murthy VS, Vijayakumar V, Tamboli Y, Capasso C, Cerbai E, Mugelli A, Carta F, et al. Synthesis of novel benzenesulfamide derivatives with inhibitory activity against human cytosolic carbonic anhydrase I and II and Vibrio cholerae α- and β-class enzymes. J Enzyme Inhib Med Chem. 2018;33(1):1125–1136.
   PubMed Web of Science ®Google Scholar
• Berrino E, Bozdag M, Del Prete S, Alasmary FAS, Alqahtani LS, AlOthman Z, Capasso C, Supuran CT. Inhibition of α-, β-, γ-, and δ-carbonic anhydrases from bacteria and diatoms with N'-aryl-N-hydroxy-ureas. J Enzyme Inhib Med Chem. 2018;33(1):1194–1198.
   PubMed Web of Science ®Google Scholar
• Ali M, Angeli A, Bozdag M, Carta F, Capasso C, Farooq U, Supuran CT. Benzylaminoethylureido-tailed benzenesulfonamides show potent inhibitory activity against bacterial carbonic anhydrases. ChemMedChem. 2020;15(24):2444–2447.
   PubMed Web of Science ®Google Scholar
• Ceruso M, Del Prete S, Alothman Z, Capasso C, Supuran CT. Sulfonamides with potent inhibitory action and selectivity against the α-carbonic anhydrase from Vibrio cholerae. ACS Med Chem Lett. 2014;5(7):826–830.
   PubMed Web of Science ®Google Scholar
• De Vita D, Angeli A, Pandolfi F, Bortolami M, Costi R, Di Santo R, Suffredini E, Ceruso M, Del Prete S, Capasso C, et al. Inhibition of the α-carbonic anhydrase from Vibrio cholerae with amides and sulfonamides incorporating imidazole moieties. J Enzyme Inhib Med Chem. 2017;32(1):798–804.
   PubMed Web of Science ®Google Scholar
• Mancuso F, De Luca L, Angeli A, Berrino E, Del Prete S, Capasso C, Supuran CT, Gitto R. In silico-guided identification of new potent inhibitors of carbonic anhydrases expressed in Vibrio cholerae. ACS Med Chem Lett. 2020;11(11):2294–2299.
   PubMed Web of Science ®Google Scholar
• Liguori F, Carradori S, Ronca R, Rezzola S, Filiberti S, Carta F, Turati M, Supuran CT. Benzenesulfonamides with different rigidity-conferring linkers as carbonic anhydrase inhibitors: an insight into the antiproliferative effect on glioblastoma, pancreatic, and breast cancer cells. J Enzyme Inhib Med Chem. 2022;37(1):1857–1869.
   PubMed Web of Science ®Google Scholar
• Combs J, Bozdag M, Cravey LD, Kota A, McKenna R, Angeli A, Carta F, Supuran CT. New insights into conformationally restricted carbonic anhydrase inhibitors. Molecules. 2023;28(2):890.
   PubMed Web of Science ®Google Scholar
• Scozzafava A, Menabuoni L, Mincione F, Briganti F, Mincione G, Supuran CT. Carbonic anhydrase inhibitors. Synthesis of water-soluble, topically effective, intraocular pressure-lowering aromatic/heterocyclic sulfonamides containing cationic or anionic moieties: Is the tail more important than the ring? J Med Chem. 1999;42(14):2641–2650.
   PubMed Web of Science ®Google Scholar
• Bozdag M, Ferraroni M, Nuti E, Vullo D, Rossello A, Carta F, Scozzafava A, Supuran CT. Combining the tail and the ring approaches for obtaining potent and isoform-selective carbonic anhydrase inhibitors: solution and X-ray crystallographic studies. Bioorg Med Chem. 2014;22(1):334–340.
   PubMed Web of Science ®Google Scholar
• Wilkinson BL, Bornaghi LF, Houston TA, Innocenti A, Supuran CT, Poulsen S-A. A novel class of carbonic anhydrase inhibitors: glycoconjugate benzene sulfonamides prepared by “click-tailing. J Med Chem. 2006;49(22):6539–6548.
   PubMed Web of Science ®Google Scholar
• Khalifah RG. The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. J Biol Chem. 1971;246(8):2561–2573.
   PubMed Web of Science ®Google Scholar
• Lagorce D, Bouslama L, Becot J, Miteva MA, Villoutreix BO. FAF-drugs4: free ADME-tox filtering computations for chemical biology and early stages drug discovery. Bioinformatics. 2017;33(22):3658–3660.
   PubMed Web of Science ®Google Scholar
• Veber DF, Johnson SR, Cheng HY, Smith BR, Ward KW, Kopple KD. Molecular properties that influence the oral bioavailability of drug candidates. J Med Chem. 2002;45(12):2615–2623.
   PubMed Web of Science ®Google Scholar
• Tunyasuvunakool K, Adler J, Wu Z, Green T, Zielinski M, Žídek A, Bridgland A, Cowie A, Meyer C, Laydon A, et al. Highly accurate protein structure prediction for the human proteome. Nature. 2021;596(7873):590–596.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Isik S, Vullo D, De Luca V, Carginale V, Scozzafava A, Supuran CT, Capasso C. DNA cloning, characterization, and inhibition studies of an α-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae. J Med Chem. 2012;55(23):10742–10748.
   PubMed Web of Science ®Google Scholar
• Schrödinger Release 2021-4. Maestro, Glide, Protein Preparation Wizard, Epik, SiteMap, QikProp, MacroModel, Desmond, Prime. New York (NY): Schrödinger, LLC; 2021.
   Google Scholar
• Filipski KJ, Varma MV, El-Kattan AF, Ambler CM, Ruggeri RB, Goosen TC, Cameron KO. Intestinal targeting of drugs: rational design approaches and challenges. Curr Top Med Chem. 2013;13(7):776–802.
   PubMed Web of Science ®Google Scholar
• Anthouard R, DiRita VJ. Small-molecule inhibitors of toxT expression in Vibrio cholerae. mBio. 2013;4(4):e00403–e00413.
   PubMed Web of Science ®Google Scholar
• Vullo D, Del Prete S, De Luca V, Carginale V, Ferraroni M, Dedeoglu N, Osman SM, AlOthman Z, Capasso C, Supuran CT. Anion inhibition studies of the β-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae. Bioorg Med Chem Lett. 2016;26(5):1406–1410.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, Carginale V, Ferraroni M, Osman SM, AlOthman Z, Supuran CT, Capasso C. Sulfonamide inhibition studies of the β-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae. Bioorg Med Chem. 2016;24(5):1115–1120.
   PubMed Web of Science ®Google Scholar
• Greenwood JR, Calkins D, Sullivan AP, Shelley JC. Towards the comprehensive, rapid, and accurate prediction of the favorable tautomeric states of drug-like molecules in aqueous solution. J Comput Aided Mol Des. 2010;24(6-7):591–604.
   PubMed Web of Science ®Google Scholar
• Shelley JC, Cholleti A, Frye LL, Greenwood JR, Timlin MR, Uchimaya M. Epik: a software program for pK (a) prediction and protonation state generation for drug-like molecules. J Comput Aided Mol Des. 2007;21(12):681–691.
   PubMed Web of Science ®Google Scholar
• Bozdag M, Ferraroni M, Ward C, Carta F, Bua S, Angeli A, Langdon SP, Kunkler IH, Al-Tamimi AS, Supuran CT. Carbonic anhydrase inhibitors based on sorafenib scaffold: Design, synthesis, crystallographic investigation and effects on primary breast cancer cells. Eur J Med Chem. 2019;182:111600.
   PubMed Web of Science ®Google Scholar
• Behnke CA, Le Trong I, Godden JW, Merritt EA, Teller DC, Bajorath J, Stenkamp RE. Atomic resolution studies of carbonic anhydrase II. Acta Crystallogr D Biol Crystallogr. 2010;66(Pt 5):616–627.
   PubMedGoogle Scholar
• Ferraroni M, Del Prete S, Vullo D, Capasso C, Supuran CT. 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(Pt 12):2449–2456.
   PubMedGoogle Scholar
• Farid R, Day T, Friesner RA, Pearlstein RA. New insights about HERG blockade obtained from protein modeling, potential energy mapping, and docking studies. Bioorg Med Chem. 2006;14(9):3160–3173.
   PubMed Web of Science ®Google Scholar
• Sherman W, Day T, Jacobson MP, Friesner RA, Farid R. Novel procedure for modeling ligand/receptor induced fit effects. J Med Chem. 2006;49(2):534–553.
   PubMed Web of Science ®Google Scholar
• Sherman W, Beard HS, Farid R. Use of an induced fit receptor structure in virtual screening. Chem Biol Drug Des. 2006;67(1):83–84.
   PubMed Web of Science ®Google Scholar
• Friesner RA, Murphy RB, Repasky MP, Frye LL, Greenwood JR, Halgren TA, Sanschagrin PC, Mainz DT. Extra precision glide: docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. J Med Chem. 2006;49(21):6177–6196.
   PubMed Web of Science ®Google Scholar
• Halgren TA, Murphy RB, Friesner RA, Beard HS, Frye LL, Pollard WT, Banks JL. Glide: a new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. J Med Chem. 2004;47(7):1750–1759.
   PubMed Web of Science ®Google Scholar
• Friesner RA, Banks JL, Murphy RB, Halgren TA, Klicic JJ, Mainz DT, Repasky MP, Knoll EH, Shelley M, Perry JK, et al. Glide: a new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J Med Chem. 2004;47(7):1739–1749.
   PubMed Web of Science ®Google Scholar
• Jacobson MP, Pincus DL, Rapp CS, Day TJ, Honig B, Shaw DE, Friesner RA. A hierarchical approach to all-atom protein loop prediction. Proteins. 2004;55(2):351–367.
   PubMed Web of Science ®Google Scholar
• Jacobson MP, Friesner RA, Xiang Z, Honig B. On the role of the crystal environment in determining protein side-chain conformations. J Mol Biol. 2002;320(3):597–608.
   PubMed Web of Science ®Google Scholar
• Kim S, Yeon J, Sung J, Jin MS. Crystal structure of β-carbonic anhydrase CafA from the fungal pathogen Aspergillus fumigatus. Mol Cells. 2020;43(9):831–840.
   PubMed Web of Science ®Google Scholar
• UniProt Consortium. UniProt: the universal protein knowledgebase in 2023. Nucleic Acids Res. 2023;51(D1):D523–D531.
   PubMed Web of Science ®Google Scholar
• Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421.
   PubMed Web of Science ®Google Scholar
• Somalinga V, Buhrman G, Arun A, Rose RB, Grunden AM. A high-resolution crystal structure of a psychrohalophilic α-carbonic anhydrase from Photobacterium profundum reveals a unique dimer interface. PLOS One. 2016;11(12):e0168022.
   PubMed Web of Science ®Google Scholar
• Park HM, Park JH, Choi JW, Lee J, Kim BY, Jung CH, Kim JS. Structures of the γ-class carbonic anhydrase homologue YrdA suggest a possible allosteric switch. Acta Crystallogr D Biol Crystallogr. 2012;68(Pt 8):920–926.
   PubMedGoogle Scholar
• Bowers KJ. Scalable algorithms for molecular dynamics simulations on commodity clusters. SC '06: Proceedings of the 2006 ACM/IEEE Conference on Supercomputing; Tampa, FL, USA; 2006, p. 43.
   Google Scholar
• PyMOL. The PyMOL Molecular Graphics System, Version 2.5 Schrödinger, LLC, 2021.
   Google Scholar
• Mugnaini C, Sannio F, Brizzi A, Del Prete R, Simone T, Ferraro T, De Luca F, Corelli F, Docquier JD. Screen of unfocused libraries identified compounds with direct or synergistic antibacterial activity. ACS Med Chem Lett. 2020;11(5):899–905.
   PubMed Web of Science ®Google Scholar
• Clinical and Laboratory Standards Institute (CLSI). 2015. M07-A10: Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard. 10th ed. Wayne (PA): Clinical and Laboratory Standards Institute.
   Google Scholar