2,170
Views
15
CrossRef citations to date
0
Altmetric
Research Papers

Coumarins effectively inhibit bacterial α-carbonic anhydrases

, , ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 333-338 | Received 05 Nov 2021, Accepted 23 Nov 2021, Published online: 03 Jan 2022

References

  • (a) Smith KS, Jakubzick C, Whittam TS, Ferry JG. Carbonic anhydrase is an ancient enzyme widespread in prokaryotes. Proc Natl Acad Sci U S A 1999;96:15184–9. (b) Abuaita BH, Withey JH. Bicarbonate induces Vibrio cholerae virulence gene expression by enhancing ToxT activity. Infect Immun 2009;77:4111–20. (c) Merlin C, Masters M, McAteer S, Coulson A. Why is carbonic anhydrase essential to Escherichia coli? J Bacteriol 2003;185:6415–24. (d) Del Prete S, Nocentini A, Supuran CT, Capasso C. 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.
  • (a) Supuran CT. Bacterial carbonic anhydrases as drug targets: toward novel antibiotics? Front Pharmacol 2011;2:34. (b) Flaherty DP, Seleem MN, Supuran CT. Bacterial carbonic anhydrases: underexploited antibacterial therapeutic targets. Future Med Chem 2021;13:1619–22. (c) Petreni A, De Luca V, Scaloni A, et al. Anion inhibition studies of the Zn(II)-bound ι-carbonic anhydrase from the Gram-negative bacterium Burkholderia territorii. J Enzyme Inhib Med Chem 2021;36:372–6. (d) Supuran CT, Capasso C. An Overview of the Bacterial Carbonic Anhydrases. Metabolites 2017;7:56.
  • (a) Supuran CT, Capasso C. Biomedical applications of prokaryotic carbonic anhydrases. Expert Opin Ther Pat 2018;28:745–54 (b) Supuran CT, Capasso C. Antibacterial carbonic anhydrase inhibitors: an update on the recent literature. Expert Opin Ther Pat 2020;30:963–82. (c) Campestre CD, Luca V, Carradori S, et al. Carbonic anhydrases: new perspectives on protein functional role and inhibition in Helicobacter pylori. Front Microbiol 2021;12:629163. (d) Capasso C, Supuran CT. An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria? J Enzyme Inhib Med Chem 2015;30:325–32.
  • (a) 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. (b) Abutaleb NS, Elkashif A, Flaherty DP, Seleem MN. In vivo antibacterial activity of acetazolamide. Antimicrob Agents Chemother 2021;65:e01715–20. (c) Abutaleb NS, Elhassanny AEM, Flaherty DP, Seleem MN. In vitro and in vivo activities of the carbonic anhydrase inhibitor, dorzolamide, against vancomycin-resistant enterococci. PeerJ 2021;9:e11059.
  • (a) Hewitt CS, Abutaleb NS, Elhassanny AEM, et al. Structure-activity relationship studies of acetazolamide-based carbonic anhydrase inhibitors with activity against Neisseria gonorrhoeae. ACS Infect Dis 2021;7:1969–84. (b) Nocentini A, Hewitt CS, Mastrolorenzo MD, et al. Anion inhibition studies of the α-carbonic anhydrases from Neisseria gonorrhoeae. J Enzyme Inhib Med Chem 2021;36:1061–6.
  • (a) 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. (b) 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. (c) Angeli A, Del Prete S, Osman SM, et al. Activation studies of the α- and β-carbonic anhydrases from the pathogenic bacterium Vibrio cholerae with amines and amino acids. J Enzyme Inhib Med Chem 2018;33:227–33. (d) 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.
  • (a) Urbanski LJ, Bua S, Angeli A, et al. Sulphonamide inhibition profile of Staphylococcus aureus β-carbonic anhydrase. J Enzyme Inhib Med Chem 2020;35:1834–9. (b) Fan SH, Ebner P, Reichert S, et al. MpsAB is important for Staphylococcus aureus virulence and growth at atmospheric CO2 levels. Nat Commun 2019;10:3627. (c) Supuran CT. Novel carbonic anhydrase inhibitors. Future Med Chem 2021;13:1935–7. (d) Supuran CT. Emerging role of carbonic anhydrase inhibitors. Clin Sci 2021;135:1233–49.
  • (a) Matsumoto Y, Miyake K, Ozawa K, et al. Bicarbonate and unsaturated fatty acids enhance capsular polysaccharide synthesis gene expression in oral streptococci, Streptococcus anginosus. J Biosci Bioeng 2019;128:511–7. (b) Capasso C, Supuran CT. An overview of the carbonic anhydrases from two pathogens of the oral cavity: Streptococcus mutans and Porphyromonas gingivalis. Curr Top Med Chem 2016;16:2359–68. (c) 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. (d) Burghout P, Vullo D, Scozzafava A, et al. Inhibition of the β-carbonic anhydrase from Streptococcus pneumoniae by inorganic anions and small molecules: Toward innovative drug design of antiinfectives? Bioorg Med Chem 2011;19:243–8.
  • (a) Del Prete S, De Luca V, Capasso C, et al. Recombinant thermoactive phosphoenolpyruvate carboxylase (PEPC) from Thermosynechococcus elongatus and its coupling with mesophilic/thermophilic bacterial carbonic anhydrases (CAs) for the conversion of CO2 to oxaloacetate. Bioorg Med Chem 2016;24:220–5. (b) De Luca V, Del Prete S, Vullo D, et al. Expression and characterization of a recombinant psychrophilic γ-carbonic anhydrase (NcoCA) identified in the genome of the Antarctic cyanobacteria belonging to the genus Nostoc. J Enzyme Inhib Med Chem 2016;31:810–7. (c) Vullo D, De Luca V, Del Prete S, et al. Sulfonamide inhibition studies of the γ-carbonic anhydrase from the Antarctic cyanobacterium Nostoc commune. Bioorg Med Chem 2015;23:1728–34. (d) 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.
  • (a) Rahman MM, Tikhomirova A, Modak JK, et al. Antibacterial activity of ethoxzolamide against Helicobacter pylori strains SS1 and 26695. Gut Pathog 2020;12:20. (b) Modak JK, Tikhomirova A, Gorrell RJ, et al. Anti-Helicobacter pylori activity of ethoxzolamide. J Enzyme Inhib Med Chem 2019;34:1660–7. (c) Modak JK, Liu YC, Supuran CT, Roujeinikova A. Structure-activity relationship for sulfonamide inhibition of Helicobacter pylori α-carbonic anhydrase. J Med Chem 2016;59:11098–109.
  • (a) Supuran CT. Exploring the multiple binding modes of inhibitors to carbonic anhydrases for novel drug discovery. Expert Opin Drug Discov 2020;15:671–86. (b) Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81. (c) Mishra CB, Tiwari M, Supuran CT. Progress in the development of human carbonic anhydrase inhibitors and their pharmacological applications: where are we today? Med Res Rev 2020;40:2485–565.
  • (a) De Simone G, Supuran CT. (In)organic anions as carbonic anhydrase inhibitors. J Inorg Biochem 2012;111:117–29. (b) Ozensoy Guler O, Capasso C, Supuran CT. A magnificent enzyme superfamily: carbonic anhydrases, their purification and characterization. J Enzyme Inhib Med Chem 2016;31:689–94. (c) Nocentini A, Angeli A, Carta F, et al. Reconsidering anion inhibitors in the general context of drug design studies of modulators of activity of the classical enzyme carbonic anhydrase. J Enzyme Inhib Med Chem 2021;36:561–80. (d) Supuran CT. Structure-based drug discovery of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2012;27:759–72. (e) Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60.
  • (a) Maresca A, Temperini C, Vu H, et al. Non-zinc mediated inhibition of carbonic anhydrases: coumarins are a new class of suicide inhibitors. J Am Chem Soc 2009;131:3057–62. (b) Maresca A, Temperini C, Pochet L, et al. Deciphering the mechanism of carbonic anhydrase inhibition with coumarins and thiocoumarins. J Med Chem 2010;53:335–44.
  • (a) Supuran CT. Coumarin carbonic anhydrase inhibitors from natural sources. J Enzyme Inhib Med Chem 2020;35:1462–70. (b) Maresca A, Supuran CT. Coumarins incorporating hydroxy- and chloro-moieties selectively inhibit the transmembrane, tumor-associated carbonic anhydrase isoforms IX and XII over the cytosolic ones I and II . Bioorg Med Chem Lett 2010;20:4511–4. (c) Maresca A, Scozzafava A, Supuran CT. 7,8-Disubstituted- but not 6,7-disubstituted coumarins selectively inhibit the transmembrane, tumor-associated carbonic anhydrase isoforms IX and XII over the cytosolic ones I and II in the low nanomolar/subnanomolar range. Bioorg Med Chem Lett 2010;20:7255–8. (d) Sharma A, Tiwari M, Supuran CT. Novel coumarins and benzocoumarins acting as isoform-selective inhibitors against the tumor-associated carbonic anhydrase IX. J Enzyme Inhib Med Chem 2014;29:292–6. (e) Touisni N, Maresca A, McDonald PC, et al. Glycosyl coumarin carbonic anhydrase IX and XII inhibitors strongly attenuate the growth of primary breast tumors. J Med Chem 2011;54:8271–7.
  • (a) Petreni A, Osman SM, Alasmary FA, et al. Binding site comparison for coumarin inhibitors and amine/amino acid activators of human carbonic anhydrases. Eur J Med Chem 2021;226:113875. (b) Supuran CT. Multitargeting approaches involving carbonic anhydrase inhibitors: hybrid drugs against a variety of disorders. J Enzyme Inhib Med Chem 2021;36:1702–14. (c) Fois B, Distinto S, Meleddu R, et al. Coumarins from Magydaris pastinacea as inhibitors of the tumour-associated carbonic anhydrases IX and XII: isolation, biological studies and in silico evaluation. J Enzyme Inhib Med Chem 2020;35:539–‐48. (d) Melis C, Distinto S, Bianco G, et al. Targeting tumor associated carbonic anhydrases IX and XII: highly isozyme selective coumarin and psoralen inhibitors. ACS Med Chem Lett 2018;9:725–9. (e) Meleddu R, Deplano S, Maccioni E, et al. Selective inhibition of carbonic anhydrase IX and XII by coumarin and psoralen derivatives. J Enzyme Inhib Med Chem 2021;36:685–92.
  • (a) Innocenti A, Supuran CT. Paraoxon, 4-nitrophenyl phosphate and acetate are substrates of α- but not of β-, γ- and ζ-carbonic anhydrases. Bioorg Med Chem Lett 2010;20:6208–12. (b) Innocenti A, Scozzafava A, Parkkila S, et al. Investigations of the esterase, phosphatase, and sulfatase activities of the cytosolic mammalian carbonic anhydrase isoforms I, II, and XIII with 4-nitrophenyl esters as substrates. Bioorg Med Chem Lett 2008;18:2267–71. (c) Lopez M, Vu H, Wang CK, et al. Promiscuity of carbonic anhydrase II. Unexpected ester hydrolysis of carbohydrate-based sulfamate inhibitors. J Am Chem Soc 2011;133:18452–62.
  • (a) Kaul T, Reddy PS, Mahanty S, et al. Biochemical and molecular characterization of stress-induced β-carbonic anhydrase from a C(4) plant, Pennisetum glaucum. J Plant Physiol 2011;168:601–10. (b) Lee RB, Smith JA, Rickaby RE. Cloning, expression and characterization of the δ-carbonic anhydrase of Thalassiosira weissflogii (Bacillariophyceae). J Phycol 2013;49:170–7.
  • Del Prete S, Vullo D, De Luca V, et al. Biochemical characterization of the δ-carbonic anhydrase from the marine diatom Thalassiosira weissflogii, TweCA. J Enzyme Inhib Med Chem 2014;29:906–11.
  • 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;246:2561–73.
  • (a) Supuran CT, Alterio V, Di Fiore A, et al. Inhibition of carbonic anhydrase IX targets primary tumors, metastases, and cancer stem cells: three for the price of one. Med Res Rev 2018;38:1799–836. (b) Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–77. (c) Thacker PS, Tiwari PL, Angeli A, et al. Synthesis and biological evaluation of coumarin-linked 4-anilinomethyl-1,2,3-triazoles as potent inhibitors of carbonic anhydrases IX and XIII involved in tumorigenesis. Metabolites 2021;11:225.
  • (a) Peperidou A, Bua S, Bozdag M, et al. Novel 6- and 7-substituted coumarins with inhibitory action against lipoxygenase and tumor-associated carbonic anhydrase IX. Molecules 2018;23:153. (b) Kartsev V, Geronikaki A, Bua S, et al. Extending the inhibition profiles of coumarin-based compounds against human carbonic anhydrases: synthesis, biological, and in silico evaluation. Molecules 2019;24:3580.