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Review Article

Coumarin carbonic anhydrase inhibitors from natural sources

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Pages 1462-1470 | Received 27 May 2020, Accepted 21 Jun 2020, Published online: 11 Aug 2020

References

  • Sethna SM, Shah NM. The chemistry of coumarins. Chem Rev 1945;36:1–62.
  • Riveiro ME, De Kimpe N, Moglioni A, et al. Coumarins: old compounds with novel promising therapeutic perspectives. Curr Med Chem 2010;17:1325–38.
  • Pereira TM, Franco DP, Vitorio F, Kummerle AE. Coumarin compounds in medicinal chemistry: some important examples from the last years. Curr Top Med Chem 2018;18:124–48.
  • Stefanachi A, Leonetti F, Pisani L, et al. Coumarin: a natural, privileged and versatile scaffold for bioactive compounds. Molecules 2018;23:E250.
  • Carradori S, Secci D, Petzer JP. MAO inhibitors and their wider applications: a patent review. Expert Opin Ther Pat 2018;28:211–26.
  • 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.
  • Vu H, Pham NB, Quinn RJ. Direct screening of natural product extracts using mass spectrometry. J Biomol Screen 2008;13:265–75.
  • Menezes JC, Diederich M. Translational role of natural coumarins and their derivatives as anticancer agents. Future Med Chem 2019;11:1057–82.
  • Davis RA, Vullo D, Maresca A, et al. Natural product coumarins that inhibit human carbonic anhydrases. Bioorg Med Chem 2013;21:1539–43.
  • 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.
  • Lippi G, Gosselin R, Favaloro EJ. Current and emerging direct oral anticoagulants: state-of-the-art. Semin Thromb Hemost 2019;45:490–501.
  • Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81.
  • (a) De Simone G, Supuran CT. (In)organic anions as carbonic anhydrase inhibitors. J Inorg Biochem 2012;111:117–29. (b) Supuran CT. Carbon- versus sulphur-based zinc binding groups for carbonic anhydrase inhibitors? J Enzyme Inhib Med Chem 2018;33:485–95.
  • Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32.
  • Supuran CT, Capasso C. Biomedical applications of prokaryotic carbonic anhydrases. Expert Opin Ther Pat 2018;28:745–54.
  • Nocentini A, Supuran CT. Advances in the structural annotation of human carbonic anhydrases and impact on future drug discovery. Expert Opin Drug Discov 2019;14:1175–97.
  • 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.
  • (a) Supuran CT, Capasso C. An overview of the bacterial carbonic anhydrases. Metabolites 2017;7:56. (b) 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.
  • 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.
  • Supuran CT. Carbonic anhydrases and metabolism. Metabolites 2018;8:25.
  • (a) Supuran CT, Carbonic anhydrase inhibitors as emerging agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs 2018;27:963–70. (b) Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–77. (c) Supuran CT, Vullo D, Manole G, et al. Designing of novel carbonic anhydrase inhibitors and activators. Curr Med Chem Cardiovasc Hematol Agents 2004;2:49–68.
  • (a) Supuran CT. Applications of carbonic anhydrases inhibitors in renal and central nervous system diseases. Expert Opin Ther Pat 2018;28:713–21. (b) Milite C, Amendola G, Nocentini A, et al. Novel 2-substituted-benzimidazole-6-sulfonamides as carbonic anhydrase inhibitors: synthesis, biological evaluation against isoforms I, II, IX and XII and molecular docking studies. J Enzyme Inhib Med Chem 2019;34:1697–710. (c) Distinto S, Meleddu R, Ortuso F, et al. Exploring new structural features of the 4-[(3-methyl-4-aryl-2,3-dihydro-1,3-thiazol-2-ylidene)amino]benzenesulphonamide scaffold for the inhibition of human carbonic anhydrases. J Enzyme Inhib Med Chem 2019;34:1526–33.
  • (a) Supuran CT. Drug interaction considerations in the therapeutic use of carbonic anhydrase inhibitors. Expert Opin Drug Metab Toxicol 2016;12:423–31. (b) Köhler K, Hillebrecht A, Schulze Wischeler J, et al. Saccharin inhibits carbonic anhydrases: possible explanation for its unpleasant metallic aftertaste. Angew Chem Int Ed Engl 2007;46:7697–9.
  • Supuran CT. Carbonic anhydrase inhibitors and their potential in a range of therapeutic areas. Expert Opin Ther Pat 2018;28:709–12.
  • Supuran CT. The management of glaucoma and macular degeneration. Expert Opin Ther Pat 2019;29:745–7.
  • Supuran CT, Altamimi ASA, Carta F. Carbonic anhydrase inhibition and the management of glaucoma: a literature and patent review 2013-2019. Expert Opin Ther Pat 2019;29:781–92.
  • Di Fiore A, De Simone G, Alterio V, et al. The anticonvulsant sulfamide JNJ-26990990 and its S,S-dioxide analog strongly inhibit carbonic anhydrases: solution and X-ray crystallographic studies. Org Biomol Chem 2016;14:4853–8.
  • Aggarwal M, Kondeti B, McKenna R. Anticonvulsant/antiepileptic carbonic anhydrase inhibitors: a patent review. Expert Opin Ther Pat 2013;23:717–24.
  • Scozzafava A, Supuran CT, Carta F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin Ther Pat 2013;23:725–35.
  • Poli G, Bozdag M, Berrino E, et al. N-aryl-N′-ureido-O-sulfamates as potent and selective inhibitors of hCA VB over hCA VA: deciphering the binding mode of new potential agents in mitochondrial dysfunctions. Bioorg Chem 2020;100:103896.
  • 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.
  • 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;43:484–490.
  • Nocentini A, Supuran CT. Carbonic anhydrase inhibitors as antitumor/antimetastatic agents: a patent review (2008–2018). Expert Opin Ther Pat 2018;28:729–40.
  • McDonald PC, Chafe SC, Brown WS, et al. Regulation of pH by carbonic anhydrase 9 mediates survival of pancreatic cancer cells with activated KRAS in response to hypoxia. Gastroenterology 2019;157:823–37.
  • Supuran CT. Carbonic anhydrase inhibition and the management of neuropathic pain. Expert Rev Neurother 2016;16:961–8.
  • Carta F, Di Cesare Mannelli L, Pinard M, et al. A class of sulfonamide carbonic anhydrase inhibitors with neuropathic pain modulating effects. Bioorg Med Chem 2015;23:1828–40.
  • Di Cesare Mannelli L, Micheli L, Carta F, et al. Carbonic anhydrase inhibition for the management of cerebral ischemia: in vivo evaluation of sulfonamide and coumarin inhibitors. J Enzyme Inhib Med Chem 2016;31:894–9.
  • Margheri F, Ceruso M, Carta F, et al. Overexpression of the transmembrane carbonic anhydrase isoforms IX and XII in the inflamed synovium. J Enzyme Inhib Med Chem 2016;31:60–3.
  • Bua S, Di Cesare Mannelli L, Vullo D, et al. Design and synthesis of novel nonsteroidal anti-inflammatory drugs and carbonic anhydrase inhibitors hybrids (NSAIDs-CAIs) for the treatment of rheumatoid arthritis. J Med Chem 2017;60:1159–70.
  • Akgul O, Di Cesare Mannelli L, Vullo D, et al. Discovery of novel nonsteroidal anti-inflammatory drugs and carbonic anhydrase inhibitors hybrids (NSAIDs-CAIs) for the management of rheumatoid arthritis. J Med Chem 2018;61:4961–77.
  • Supuran CT. Acetazolamide for the treatment of idiopathic intracranial hypertension. Expert Rev Neurother 2015;15:851–6.
  • Fossati S, Giannoni P, Solesio ME, et al. The carbonic anhydrase inhibitor methazolamide prevents amyloid beta-induced mitochondrial dysfunction and caspase activation protecting neuronal and glial cells in vitro and in the mouse brain. Neurobiol Dis 2016;86:29–40.
  • Provensi G, Carta F, Nocentini A, et al. A new kid on the block? Carbonic anhydrases as possible new targets in Alzheimer’s disease. Int J Mol Sci 2019;20:4724.
  • Canto de Souza L, Provensi G, Vullo D, et al. Carbonic anhydrase activation enhances object recognition memory in mice through phosphorylation of the extracellular signal-regulated kinase in the cortex and the hippocampus. Neuropharmacology 2017;118:148–56.
  • Blandina P, Provensi G, Passsani MB, et al. Carbonic anhydrase modulation of emotional memory. Implications for the treatment of cognitive disorders. J Enzyme Inhib Med Chem 2020;35:1206–14.
  • (a) Supuran CT. Carbonic anhydrase activators. Future Med Chem 2018;10:561–73. (b) Akocak S, Supuran CT. Activation of α-, β-, γ- δ-, ζ- and η- class of carbonic anhydrases with amines and amino acids: a review. J Enzyme Inhib Med Chem 2019;34:1652–9.
  • Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov 2017;12:61–88.
  • Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60.
  • De Simone G, Alterio V, Supuran CT. Exploiting the hydrophobic and hydrophilic binding sites for designing carbonic anhydrase inhibitors. Expert Opin Drug Discov 2013;8:793–810.
  • Supuran CT. Exploring the multiple binding modes of inhibitors to carbonic anhydrases for novel drug discovery. Expert Opin Drug Discov 2020;15:671–686.
  • (a) Innocenti A, Vullo D, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors: interactions of phenols with the 12 catalytically active mammalian isoforms (CA I-XIV)). Bioorg Med Chem Lett 2008;18:1583–7. (b) Boztaş M, Çetinkaya Y, Topal M, et al. Synthesis and carbonic anhydrase isoenzymes I, II, IX, and XII inhibitory effects of dimethoxybromophenol derivatives incorporating cyclopropane moieties. J Med Chem 2015;58:640–50.
  • (a) Innocenti A, Vullo D, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors: inhibition of mammalian isoforms I-XIV with a series of substituted phenols including paracetamol and salicylic acid. Bioorg Med Chem 2008;16:7424–8. (b) 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.
  • 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.
  • 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.
  • 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’Ambrosio K, Carradori S, Monti SM, et al. Out of the active site binding pocket for carbonic anhydrase inhibitors. Chem Commun 2015;51:302–5.
  • Chiaramonte N, Maach S, Biliotti C, et al. Synthesis and carbonic anhydrase activating properties of a series of 2-amino-imidazolines structurally related to clonidine1. J Enzyme Inhib Med Chem 2020;35:1003–10.
  • Angeli A, Vaiano F, Mari F, et al. Psychoactive substances belonging to the amphetamine class potently activate brain carbonic anhydrase isoforms VA, VB, VII, and XII. J Enzyme Inhib Med Chem 2017;32:1253–9.
  • Vistoli G, Aldini G, Fumagalli L, et al. Activation effects of carnosine- and histidine-containing dipeptides on human carbonic anhydrases: a comprehensive study. Int J Mol Sci 2020;21:1761.
  • Temperini C, Innocenti A, Scozzafava A, et al. The coumarin-binding site in carbonic anhydrase accommodates structurally diverse inhibitors: the antiepileptic lacosamide as an example and lead molecule for novel classes of carbonic anhydrase inhibitors. J Med Chem 2010;53:850–4.
  • Supuran CT. An update on drug interaction considerations in the therapeutic use of carbonic anhydrase inhibitors. Expert Opin Drug Metab Toxicol 2020;16:297–307.
  • 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.
  • 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.
  • Tanc M, Carta F, Scozzafava A, Supuran CT. α-carbonic anhydrases possess thioesterase activity. ACS Med Chem Lett 2015;6:292–5.
  • 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.
  • 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.
  • Mercer DK, Robertson J, Wright K, et al. A prodrug approach to the use of coumarins as potential therapeutics for superficial mycoses. PLoS One 2013;8:e80760.
  • Xia W, Gooden D, Liu L, et al. Photo-activated psoralen binds the ErbB2 catalytic kinase domain, blocking ErbB2 signaling and triggering tumor cell apoptosis. PLoS One 2014;9:e88983.
  • 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.
  • Lou Y, McDonald PC, Oloumi A, et al. Targeting tumor hypoxia: suppression of breast tumor growth and metastasis by novel carbonic anhydrase IX inhibitors. Cancer Res 2011;71:3364–76.
  • Carta F, Maresca A, Scozzafava A, et al. 5- And 6-membered (thio)lactones are prodrug type carbonic anhydrase inhibitors. Bioorg Med Chem Lett 2012;22:267–70.
  • Ferraroni M, Carta F, Scozzafava A, Supuran CT. Thioxocoumarins show an alternative carbonic anhydrase inhibition mechanism compared to coumarins. J Med Chem 2016;59:462–73.
  • Isik S, Vullo D, Bozdag M, et al. 7-Amino-3,4-dihydro-1H-quinolin-2-one, a compound similar to the substituted coumarins, inhibits α-carbonic anhydrases without hydrolysis of the lactam ring. J Enzyme Inhib Med Chem 2015;30:773–7.
  • Tars K, Vullo D, Kazaks A, et al. Sulfocoumarins (1,2-benzoxathiine-2,2-dioxides): a class of potent and isoform-selective inhibitors of tumor-associated carbonic anhydrases. J Med Chem 2013;56:293–300.
  • Pustenko A, Stepanovs D, Žalubovskis R, et al. 3H-1,2-benzoxathiepine 2,2-dioxides: a new class of isoform-selective carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2017;32:767–75.
  • Krasavin M, Žalubovskis R, Grandāne A, et al. Sulfocoumarins as dual inhibitors of human carbonic anhydrase isoforms IX/XII and of human thioredoxin reductase. J Enzyme Inhib Med Chem 2020;35:506–10.
  • Angeli A, Trallori E, Carta F, et al. Heterocoumarins are selective carbonic anhydrase IX and XII inhibitors with cytotoxic effects against cancer cells lines. ACS Med Chem Lett 2018;9:947–51.
  • Andring J, Combs J, McKenna R. Aspirin: a suicide inhibitor of carbonic anhydrase II. Biomolecules 2020;10:527.
  • Mori M, Capasso C, Carta F, et al. A deadly spillover: SARS-CoV-2 outbreak. Expert Opin Ther Pat 2020;1–5. DOI:10.1080/13543776.2020.1760838
  • Peppicelli S, Andreucci E, Ruzzolini J, et al. The carbonic anhydrase IX inhibitor SLC-0111 as emerging agent against the mesenchymal stem cell-derived pro-survival effects on melanoma cells. J Enzyme Inhib Med Chem 2020;35:1185–93.
  • Dogné JM, Hanson J, Supuran C, Pratico D. Coxibs and cardiovascular side-effects: from light to shadow. Curr Pharm Des 2006;12:971–5.
  • (a) Modak JK, Tikhomirova A, Gorrell RJ, et al. Anti-Helicobacter pylori activity of ethoxzolamide. J Enzyme Inhib Med Chem 2019;34:1660–7. (b) Vullo D, Kumar RSS, Scozzafava A, et al. Sulphonamide inhibition studies of the β-carbonic anhydrase from the bacterial pathogen Clostridium perfringens. J Enzyme Inhib Med Chem 2018;33:31–6. (c) Rahman MM, Tikhomirova A, Modak JK, et al. Antibacterial activity of ethoxzolamide against Helicobacter pylori strains SS1 and 26695. Gut Pathog 2020;12:20. (d) Angeli A, Del Prete S, Pinteala M, et al. The first activation study of the β-carbonic anhydrases from the pathogenic bacteria Brucella suis and Francisella tularensis with amines and amino acids. J Enzyme Inhib Med Chem. 2019;34:1178–85.
  • (a) Vermelho AB, Rodrigues GC, Supuran CT. Why hasn’t there been more progress in new Chagas disease drug discovery? Expert Opin Drug Discov 2020;15:145–58. (b) Supuran CT, Capasso C. The eta-class carbonic anhydrases as drug targets for antimalarial agents. Expert Opin Ther Targets 2015;19:551–63. (c) Capasso C, Supuran CT. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin Ther Targets 2015;19:1689–704.
  • Nocentini A, Osman SM, Almeida IA, et al. Appraisal of anti-protozoan activity of nitroaromatic benzenesulfonamides inhibiting carbonic anhydrases from Trypanosoma cruzi and Leishmania donovani. J Enzyme Inhib Med Chem 2019;34:1164–71.
  • Da’dara AA, Angeli A, Ferraroni M, et al. Crystal structure and chemical inhibition of essential schistosome host-interactive virulence factor carbonic anhydrase SmCA. Commun Biol 2019;2:333.