1,352
Views
6
CrossRef citations to date
0
Altmetric
Research Papers

Coumarins inhibit η-class carbonic anhydrase from Plasmodium falciparum

, , ORCID Icon, ORCID Icon & ORCID Icon
Pages 680-685 | Received 23 Dec 2021, Accepted 28 Jan 2022, Published online: 09 Feb 2022

References

  • (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) 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. (b) 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. (c) 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. (d) 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. (e) Fuentes-Aguilar A, Merino-Montiel P, Montiel-Smith S, et al. 2-Aminobenzoxazole-appended coumarins as potent and selective inhibitors of tumour-associated carbonic anhydrases. J Enzyme Inhib Med Chem 2022;37:168–77.
  • (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. Coumarin carbonic anhydrase inhibitors from natural sources. J Enzyme Inhib Med Chem 2020;35:1462–70. (c) Supuran CT. Multitargeting approaches involving carbonic anhydrase inhibitors: hybrid drugs against a variety of disorders. J Enzyme Inhib Med Chem 2021;36:1702–14.
  • (a) 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. (b) 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. (c) 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) Mussi S, Rezzola S, Chiodelli P, et al. Antiproliferative effects of sulphonamide carbonic anhydrase inhibitors C18, SLC-0111 and acetazolamide on bladder, glioblastoma and pancreatic cancer cell lines. J Enzyme Inhib Med Chem 2022;37:280–6. (b) Supuran CT. Carbonic anhydrase inhibitors: an update on experimental agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs 2021;30:1197–208.  (c) Chen F, Licarete E, Wu X, et al. Pharmacological inhibition of carbonic anhydrase IX and XII to enhance targeting of acute myeloid leukaemia cells under hypoxic conditions. J Cell Mol Med 2021;25:11039–52. (d) McDonald PC, Chia S, Bedard PL, et al. A phase 1 study of SLC-0111, a novel inhibitor of carbonic anhydrase IX, in patients with advanced solid tumors. Am J Clin Oncol 2020;43:484–90.
  • (a) Supuran CT. Novel carbonic anhydrase inhibitors. Future Med Chem 2021;13:1935–7. (b) Chafe SC, Vizeacoumar FS, Venkateswaran G, et al. Genome-wide synthetic lethal screen unveils novel CAIX-NFS1/xCT axis as a targetable vulnerability in hypoxic solid tumors. Sci Adv 2021;7:eabj0364. (c) Berrino E, Michelet B, Martin-Mingot A, et al. Modulating the efficacy of carbonic anhydrase inhibitors through fluorine substitution. Angew Chem Int Ed Engl 2021; 60:23068–82. (d) Supuran CT. Emerging role of carbonic anhydrase inhibitors. Clin Sci 2021;135:1233–49.
  • (a) Alterio V, Langella E, Buonanno M, et al. Zeta-carbonic anhydrases show CS2 hydrolase activity: a new metabolic carbon acquisition pathway in diatoms? Comput Struct Biotechnol J 2021;19:3427–36. (b) Urbański LJ, Di Fiore A, Azizi L, et al. Biochemical and structural characterisation of a protozoan beta-carbonic anhydrase from Trichomonas vaginalis. J Enzyme Inhib Med Chem 2020;35:1292–9. (c) Amedei A, Capasso C, Nannini G, Supuran CT. Microbiota, bacterial carbonic anhydrases, and modulators of their activity: links to human diseases? Mediators Inflamm 2021; 2021:6926082.
  • (a) Nocentini A, Supuran CT, Capasso C. An overview on the recently discovered iota-carbonic anhydrases. J Enzyme Inhib Med Chem 2021;36:1988–95. (b) Jensen EL, Maberly SC, Gontero B. Insights on the functions and ecophysiological relevance of the diverse carbonic anhydrases in microalgae. Int J Mol Sci 2020; 21:2922. (c) Jensen EL, Receveur-Brechot V, Hachemane M, et al. Structural contour map of the iota carbonic anhydrase from the diatom Thalassiosira pseudonana using a multiprong approach. Int J Mol Sci 2021;22:8723.
  • (a) Pocker Y, Stone JT. The catalytic versatility of erythrocyte carbonic anhydrase. VI. Kinetic studies of noncompetitive inhibition of enzyme-catalyzed hydrolysis of p-nitrophenyl acetate. Biochemistry 1968;7:2936–45. (b) Pocker Y, Stone JT. The catalytic versatility of erythrocyte carbonic anhydrase. VII. Kinetic studies of esterase activity and competitive inhibition by substrate analogs. Biochemistry 1968;7:3021–31. (c) Pocker Y, Guilbert LJ. Catalytic versatility of erythrocyte carbonic anhydrase. Kinetic studies of the enzyme-catalyzed hydrolysis of methyl pyridyl carbonates. Biochemistry 1972; 11:180–90. (d) Pocker Y, Tanaka N. Inhibition of carbonic anhydrase by anions in the carbon dioxide-bicarbonate system. Science 1978;199:907–9. (e) Supuran CT, Conroy CW, Maren TH. Is cyanate a carbonic anhydrase substrate? Proteins 1997;27:272–8. (f) 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.
  • (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.
  • (a) 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. (b) 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. (c) 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. (d) 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) Del Prete S, De Luca V, De Simone G, et al. Cloning, expression and purification of the complete domain of the η-carbonic anhydrase from Plasmodium falciparum. J Enzyme Inhib Med Chem 2016;31:54–9. (b) 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. (c) 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. (d) Del Prete S, De Luca V, Supuran CT, Capasso C. Protonography, a technique applicable for the analysis of η-carbonic anhydrase activity. J Enzyme Inhib Med Chem 2015;30:920–4.
  • (a) Reungprapavut S, Krungkrai SR, Krungkrai J. Plasmodium falciparum carbonic anhydrase is a possible target for malaria chemotherapy. J Enzyme Inhib Med Chem 2004;19:249–56. (b) Krungkrai J, Scozzafava A, Reungprapavut S, et al. Carbonic anhydrase inhibitors. Inhibition of Plasmodium falciparum carbonic anhydrase with aromatic sulfonamides: towards antimalarials with a novel mechanism of action? Bioorg Med Chem 2005;13:483–9. (c) Krungkrai J, Supuran CT. The alpha-carbonic anhydrase from the malaria parasite and its inhibition. Curr Pharm Des 2008;14:631–40.
  • (a) Supuran CT, Capasso C. The η-class carbonic anhydrases as drug targets for antimalarial agents. Expert Opin Ther Targets 2015;19:551–63. Apr (b) 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.
  • (a) Briganti F, Pierattelli R, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. Part 37. Novel classes of carbonic anhydrase inhibitors and their interaction with the native and cobalt-substituted enzyme: kinetic and spectroscopic investigations. Eur J Med Chem 1996;31:1001–10. (b) Pastorekova S, Casini A, Scozzafava A, et al. Carbonic anhydrase inhibitors: the first selective, membrane-impermeant inhibitors targeting the tumor-associated isozyme IX. Bioorg Med Chem Lett 2004;14:869–73. (c) Vullo D, Voipio J, Innocenti A, et al. Carbonic anhydrase inhibitors. Inhibition of the human cytosolic isozyme VII with aromatic and heterocyclic sulfonamides. Bioorg Med Chem Lett 2005;15:971–6. (d) Gieling RG, Babur M, Mamnani L, et al. Antimetastatic effect of sulfamate carbonic anhydrase IX inhibitors in breast carcinoma xenografts. J Med Chem 2012;55:5591–600. (e) Carta F, Supuran CT, Scozzafava A. Sulfonamides and their isosters as carbonic anhydrase inhibitors. Future Med Chem 2014;6:1149–65.
  • (a) Angeli A, Pinteala M, Maier SS, et al. Inhibition of α-, β-, γ-, δ-, ζ- and η-class carbonic anhydrases from bacteria, fungi, algae, diatoms and protozoans with famotidine. J Enzyme Inhib Med Chem 2019; 34:644–50. (b) Del Prete S, Vullo D, De Luca V, et al. Cloning, expression, purification and sulfonamide inhibition profile of the complete domain of the η-carbonic anhydrase from Plasmodium falciparum. Bioorg Med Chem Lett 2016;26:4184–90. (c) Del Prete S, Vullo D, De Luca V, et al. Anion inhibition profiles of the complete domain of the η-carbonic anhydrase from Plasmodium falciparum. Bioorg Med Chem 2016;24:4410–4. (d) Vullo D, Del Prete S, Fisher GM, et al. Sulfonamide inhibition studies of the η-class carbonic anhydrase from the malaria pathogen Plasmodium falciparum. Bioorg Med Chem 2015;23:526–31. (e) Krungkrai J, Krungkrai SR, Supuran CT. Carbonic anhydrase inhibitors: inhibition of Plasmodium falciparum carbonic anhydrase with aromatic/heterocyclic sulfonamides-in vitro and in vivo studies. Bioorg Med Chem Lett 2008; 18:5466–71.
  • 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) Sarikaya SB, Gülçin I, Supuran CT. Carbonic anhydrase inhibitors: inhibition of human erythrocyte isozymes I and II with a series of phenolic acids. Chem Biol Drug Des 2010 May;75:515–20. (b) Yıldırım A, Atmaca U, Keskin A, et al. N-Acylsulfonamides strongly inhibit human carbonic anhydrase isoenzymes I and II. Bioorg Med Chem 2015;23:2598–605. (c) Innocenti A, Gülçin I, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. Antioxidant polyphenols effectively inhibit mammalian isoforms I-XV. Bioorg Med Chem Lett 2010;20:5050–3.
  • (a) Zimmerman SA, Ferry JG, Supuran CT. Inhibition of the archaeal beta-class (Cab) and gamma-class (Cam) carbonic anhydrases. Curr Top Med Chem 2007;7:901–8. (b) Maresca A, Carta F, Vullo D, Supuran CT. Dithiocarbamates strongly inhibit the β-class carbonic anhydrases from Mycobacterium tuberculosis. J Enzyme Inhib Med Chem 2013;28:407–11.
  • (a) Winum JY, Temperini C, El Cheikh K, et al. Carbonic anhydrase inhibitors: clash with Ala65 as a means for designing inhibitors with low affinity for the ubiquitous isozyme II, exemplified by the crystal structure of the topiramate sulfamide analogue. J Med Chem 2006;49:7024–31. (b) Oztürk Sarikaya SB, Topal F, Sentürk M, et al. In vitro inhibition of α-carbonic anhydrase isozymes by some phenolic compounds. Bioorg Med Chem Lett 2011;21:4259–62.
  • (a) Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32. (b) 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. (c) Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81.
  • Lesburg CA, Huang C, Christianson DW, Fierke CA. Histidine -> carboxamide ligand substitutions in the zinc binding site of carbonic anhydrase II alter metal coordination geometry but retain catalytic activity. Biochemistry 1997;36:15780–91.