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Review Article

Activation of α-, β-, γ- δ-, ζ- and η- class of carbonic anhydrases with amines and amino acids: a review

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Pages 1652-1659 | Received 08 Aug 2019, Accepted 30 Aug 2019, Published online: 17 Sep 2019

References

  • Van Slyke DD, Hawkins JA. Studies of gas and electrolyte equilibria in blood XVI. The evolution of carbon dioxide from blood and buffer solutions. J Biol Chem 1930;87:265–79.
  • Meldrum NU, Roughton F. Carbonic anhydrase. Its preparation and properties. J Physiol (Lond) 1933;80:113–42.
  • (a) Supuran CT. Carbonic anhydrase activators. Future Med Chem 2018;10:561–73. (b) Temperini C, Scozzafava A, Supuran CT. Carbonic anhydrase activation and the drug design. Curr Pharm Des 2008;14:708–15. (c) Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81. (d) Akocak S, Ilies MA, Next-Generation primary sulfonamide carbonic anhydrase inhibitors. In: Supuran C.T., Cappasso C. (Eds.) Targeting carbonic anhydrases, future science, London; 2014, pp. 35–51; (e) Zamanova S, Shabana AM, Mondal UK, Ilies MA. Carbonic anhydrases as disease markers. Expert Opin Ther Targets 2019;29:509–33.
  • Bradfield JR. Plant carbonic anhydrase. Nature 1947;159:467.
  • (a) 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. (b) Smith KS, Jakubzick C, Whittam TS, Ferry JG. Carbonic anhydrase is an ancient enzyme widespread in prokaryotes. Proc Natl Acad Sci USA 1999;96:15184–9.
  • (a) Supuran CT. Applications of carbonic anhydrases inhibitors in renal and central nervous system diseases. Expert Opin Ther Pat 2018;28:713–21. (b) Supuran CT. Carbonic anhydrase inhibitors and their potential in a range of therapeutic areas. Expert Opin Ther Pat 2018;28:709–12. (c) Supuran CT. Carbonic anhydrase inhibitors as emerging agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs 2018;27:963–70. (d) Nocentini A, Supuran CT. Carbonic anhydrase inhibitors as antitumor/antimetastatic agents: a patent review (2008-2018). Expert Opin Ther Pat 2018;28:729–40. (e) Nocentini A, Supuran CT. Advances in the structural annotation of human carbonic anhydrases and impact on future drug discovery. Expert Opin Drug Discov 2019;1–23. (in press).
  • (a) Supuran CT, Capasso C. The η-class carbonic anhydrases as drug targets for antimalarial agents . Expert Opin Ther Targets 2015;19:551–63. (b) Capasso C, Supuran CT. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin Ther Targets 2015;19:1689–704. (c) Supuran CT, Capasso C. Biomedical applications of prokaryotic carbonic anhydrases. Expert Opin Ther Pat 2018;28:745–54.
  • (a) Ozensoy Guler O, Capasso C, Supuran CT. A magnificient enzyme superfamily: carbonic anhydrases, their purification and characterization. J Enzym Inhib Med Chem 2016;31:689–94. (b) De Simone G, Supuran CT. (In)organic anions as carbonic anhydrase inhibitors. J Inorg Biochem 2012;111:117–29. (c) Supuran CT. Carbonic anhydrase inhibition and the management of hypoxic tumors. Metabolites 2017;7:E48.
  • (a) Alterio V, Esposito D, Monti SM, et al. Crystal structure of the human carbonic anhydrase II adduct with 1-(4-sulfamoylphenyl-ethyl)-2,4,6-triphenylpyridinium perchlorate, a membrane-impermeant, isoform selective inhibitor. J Enzyme Inhib Med Chem 2018;33:151–7. (b) Innocenti A, Vullo D, Scozzafava A, et al. 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.(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. (d) 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.
  • (a) Del Prete S, Vullo D, Scozzafava A, et al. Cloning, characterization and anion inhibition study of the δ-class carbonic anhydrase (TweCA) from the marine diatom Thalassiosira weissflogii. Bioorg Med Chem 2014;22:531–7. (b) Vullo D, Del Prete S, Osman SM, et al. Sulfonamide inhibition studies of the δ-carbonic anhydrase from the diatom Thalassiosira weissflogii. Bioorg Med Chem Lett 2014;24:275–9. (c) 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.
  • (a) Supuran CT, Capasso C. An overview of the bacterial carbonic anhydrases. Metabolites 2017;7:56. (b) Clare BW, Supuran CT. Carbonic anhydrase activators. 3: Structure‐activity correlations for a series of isozyme II activators. J Pharm Sci 1994;83:768–73.(c) Supuran CT. Carbonic anhydrases and metabolism. Metabolites 2018;8:25. (d) Supuran CT. Carbon- versus sulphur-based zinc binding groups for carbonic anhydrase inhibitors? J Enzyme Inhib Med Chem 2018;33:485–95.
  • (a) Del Prete S, Vullo D, Fisher GM, et al. Discovery of new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum- the η-carbonic anhydrases. Bioorg Med Chem 2014;24:4389–96. (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.
  • Jensen EL, Clement R, Kosta A, et al. A new widespread subclass of carbonic anhydrase in marine phytoplankton. Isme J 2019;13:2094–106.
  • (a) Alterio V, Di Fiore A, D'Ambrosio K, et al. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem Rev 2012;112:4421–68. (b) 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. (c) Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60. (d) Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov 2017;12:61–88. (e) Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32.(f) Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–77. (g) 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. (h) Akocak S, Alam MR, Shabana AM, et al. PEGylated Bis-Sulfonamide carbonic anhydrase inhibitors can efficiently control the growth of several carbonic Anhydrase IX-Expressing carcinomas. J Med Chem 2016;59:5077–88.
  • (a) Pacchiano F, Carta F, McDonald PC, et al. Ureido-substituted benzenesulfonamides potently inhibit carbonic anhydrase IX and show antimetastatic activity in a model of breast cancer metastasis. J Med Chem 2011;54:1896–902. (b) 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. (c) Pacchiano F, Aggarwal M, Avvaru BS, et al. Selective hydrophobic pocket binding observed within the carbonic anhydrase II active site accommodate different 4-substituted-ureido-benzenesulfonamides and correlate to inhibitor potency. Chem Commun (Camb) 2010;46:8371–3. (d) 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.
  • (a) Krall N, Pretto F, Decurtins W, et al. A Small‐Molecule drug conjugate for the treatment of carbonic anhydrase IX expressing tumors. Angew Chem Int Ed Engl 2014;53:4231–5.(b) El-Gazzar MG, Nafie NH, Nocentini A, et al. Carbonic anhydrase inhibition with a series of novel benzenesulfonamide-triazole conjugates. J Enzyme Inhib Med Chem 2005; 20:333–40. (c) Eldehna WM, Abo-Ashour MF, Berrino E, et al. SLC-0111 enaminone analogs, 3/4-(3-aryl-3-oxopropenyl) aminobenzenesulfonamides, as novel selective subnanomolar inhibitors of the tumor-associated carbonic anhydrase isoform IX. Bioorg Chem 2019;83:549–58. (d) Abo-Ashour MF, Eldehna WM, Nocentini A, et al. Novel synthesized SLC-0111 thiazole and thiadiazole analogues: Determination of their carbonic anhydrase inhibitory activity and molecular modeling studies. Bioorg Chem 2019;87:794–802.
  • (a) Akocak S, Lolak N, Nocentini A, et al. Synthesis and biological evaluation of novel aromatic and heterocyclic bis-sulfonamide Schiff bases as carbonic anhydrase I, II, VII and IX inhibitors. Bioorg Med Chem 2017;25:3093–7. (b) Akocak S, Lolak N, Bua S, et al. Synthesis and biological evaluation of novel N,N`-diaryl cyanoguanidines acting as potent and selective carbonic anhydrase II inhibitors. Bioorg Chem 2018;77:245–51. (c) Lolak N, Akocak S, Bua S, et al. Design and synthesis of novel 1,3-diaryltriazene-substituted sulfonamides as potent and selective carbonic anhydrase II inhibitors. Bioorg Chem 2018;77:542–7. (d) Akocak S, Lolak N, Bua S, et al. Discovery of novel 1,3-diaryltriazene sulfonamides as carbonic anhydrase I, II, VII, and IX inhibitors. J Enzyme Inhib Med Chem 2018;33:1575–80.
  • (a) Lolak N, Akocak S, Bua S, Supuran CT. Design, synthesis and biological evaluation of novel ureido benzenesulfonamides incorporating 1,3,5-triazine moieties as potent carbonic anhydrase IX inhibitors. Bioorg Chem 2019;82:117–22. (b) Lolak N, Akocak S, Bua S, et al. Discovery of new ureido benzenesulfonamides incorporating 1,3,5-triazine moieties as carbonic anhydrase I, II, IX and inhibitors. Bioorg Med Chem 2019;27:1588–94. (c) Shabana AM, Mondal UK, Alam R, et al. pH-sensitive multiligand gold nanoplatform targeting carbonic anhydrase IX enhances the delivery of Doxorubicin to hypoxic tumor spheroids and overcomes the hypoxia-induced chemoresistance. ACS Appl Mater Interfaces 2018;10:17792–808.
  • Briganti F, Mangani S, Orioli P, et al. Carbonic anhydrase activators: X-ray crystallographic and spectroscopic investigations for the interaction of isozymes I and II with histamine. Biochemistry 1997;36:10384–92.
  • (a) Temperini C, Scozzafava A, Vullo D, Supuran CT. Carbonic anhydrase activators. Activation of isozymes I, II, IV, VA, VII, and XIV with l- and d-histidine and crystallographic analysis of their adducts with isoform II: engineering proton-transfer processes within the active site of an enzyme. Chemistry 2006;12:7057–66. (b) Temperini C, Scozzafava A, Vullo D, Supuran CT. Carbonic anhydrase activators. Activation of isoforms I, II, IV, VA, VII, and XIV with L- and D-phenylalanine and crystallographic analysis of their adducts with isozyme II: stereospecific recognition within the active site of an enzyme and its consequences for the drug design. J Med Chem 2006;49:3019–27. (c) Temperini C, Innocenti A, Scozzafava A, Supuran CT. Carbonic anhydrase activators: kinetic and X-ray crystallographic study for the interaction of D- and L-tryptophan with the mammalian isoforms I-XIV. Bioorg Med Chem 2008;16:8373–8. (d) Temperini C, Innocenti A, Scozzafava A, et al. Carbonic anhydrase activators: L-Adrenaline plugs the active site entrance of isozyme II, activating better isoforms I, IV, VA, VII, and XIV. Bioorg Med Chem Lett 2007;17:628–35.
  • (a) Akocak S, Lolak N, Vullo D, et al. Synthesis and biological evaluation of histamine Schiff bases as carbonic anhydrase I, II, IV, VII, and IX activators. J Enzyme Inhib Med Chem 2017;32:1305–12. (b) Akocak S, Lolak N, Bua S, et al. α-Carbonic anhydrases are strongly activated by spinaceamine derivatives. Bioorg Med Chem 2019;27:800–4. (c) Akocak S, Lolak N, Bua S, et al. Activation of human α-carbonic anhydrase isoforms I, II, IV and VII with bis-histamine Schiff bases and bis-spinaceamine substituted derivatives. J Enzyme Inhib Med Chem 2019;34:1193–8. (d) Dave K, Scozzafava A, Vullo D, et al. Pyridinium derivatives of histamine are potent activators of cytosolic carbonic anhydrase isoforms, I, II and VII. Org Biomol Chem 2011;9:2790–800. (e) Dave K, Ilies MA, Scozzafava A, et al. An inhibitor-like binding mode of a carbonic anhydrase activator within the active site of isoform II. Bioorg Med Chem Lett 2011;21:2764–8.
  • (a) Bhatt A, Mondal UK, Supuran CT, et al. Crystal structure of Carbonic Anhydrase II in complex with an activating ligand: Implications in neuronal function. Mol Neurobiol 2018;55:7431–7. (b) Temperini C, Scozzafava A, Supuran CT. Carbonic anhydrase activators: the first X-ray crystallographic study of an adduct of isoform I. Bioorg Med Chem Lett 2006;16:5152–6. (c) Temperini C, Scozzafava A, Puccetti L, Supuran CT. Carbonic anhydrase activators: X-ray crystal structure of the adduct of human isozyme II with L-histidine as a platform for the design of stronger activators. Bioorg Med Chem Lett 2005;15:5136–41. (d) Draghici B, Vullo D, Akocak S, et al. Ethylene bis-imidazoles are highly potent and selective activators for isozymes VA and VII of carbonic anhydrase, with a potential nootropic effect. Chem Commun 2014;50:5980–3.
  • (a) 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. (b) Sanku RKK, John JS, Ilies MA, Walker EA. Potential learning and memory disruptors and enhancers in a simple, 1-day operant task in mice. Behavioural Pharmacol 2018;29:482–92.
  • Wang X, Schröder HC, Schlossmacher U, et al. Modulation of the initial mineralization process of SaOS-2 cells by carbonic anhydrase activators and polyphosphate. Calcif Tissue Int 2014;94:495–509.
  • Parkkila S, Vullo D, Puccetti L, et al. Carbonic anhydrase activators: Activation of isozyme XIII with amino acids and amines. Bioorg Med Chem Lett 2006;16:3955–9.
  • Vullo D, Nishimori I, Scozzafa A, Supuran CT. Carbonic anhydrase activators: Activation of the human cytosolic isozyme III and membrane-associated isoform IV with amino acids and amines. Bioorg Med Chem Lett 2008;18:4303–7.
  • Vullo D, Nishimori I, Innocenti A, et al. Carbonic anhydrase activators: An activation study of the human mitochondrial isoforms VA and VB with amino acids and amines. Bioorg Med Chem Lett 2007;17:1336–40.
  • Vullo D, Innocenti A, Nishimori I, et al. Carbonic anhydrase activators: Activation of the human isoforms VII (cytosolic) and XIV (transmembrane) with amino acids and amines. Bioorg Med Chem Lett 2007;17:4107–12.
  • (a) Pastorekova S, Vullo D, Nishimori I, et al. Carbonic anhydrase activators: Activation of the human tumor-associated isozymes IX and XII with amino acids and amines. Bioorg Med Chem 2008;16:3530–6. (b) Innocenti A, Hilvo M, Parkkila S, et al. Carbonic anhydrase activators: Activation of the membrane-associated isoform XV with amino acids and amines. Bioorg Med Chem Lett 2009;19:3430–3.
  • Nguyen GTH, Tran TN, Podgorski MN, et al. Nanoscale ion emitters in native mass spectrometry for measuring Ligand-Protein binding affinities. ACS Cent Sci 2019;5:308–18.
  • Innocenti A, Zimmerman SA, Scozzafava A, et al. Carbonic anhydrase activators: Activation of the archaeal β-class (Cab) and γ-class (Cam) carbonic anhydrases with amino acids and amines. Bioorg Med Chem Lett 2008;18:6194–8.
  • Vullo D, Del Prete S, Capasso C, Supuran CT. Carbonic anhydrase activators: Activation of the β-carbonic anhydrase from Malassezia globosa with amino acids and amines. Bioorg Med Chem Lett 2016;26:1381–5.
  • Isik S, Kockar F, Aydin M, et al. Carbonic anhydrase activators: Activation of the β-carbonic anhydrase Nce103 from the yeast Saccharomyces cerevisiae with amino acids and amines. Bioorg Med Chem Lett 2009;19:1662–5.
  • Innocenti A, Leewattanapasuk W, Manole G, et al. Carbonic anhydrase activators: Activation of the β-carbonic anhydrase from the pathogenic yeast Candida glabrata with amino acids and amines. Bioorg Med Chem Lett 2010;20:1701–4.
  • (a) 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. (b) Angeli A, Del Prete S, Donald WA, et al. The γ-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae is potently activated by amines and amino acids. Bioorg Chem 2018;77:1–5.
  • Angeli A, Del Prete S, Osman SM, et al. Activation studies with amines and amino acids of the β-carbonic anhydrase encoded by the Rv3273 gene from the pathogenic bacterium Mycobacterium tuberculosis. J Enzyme Inhib Med Chem 2018;33:364–9.
  • (a) 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. (b) Stefanucci A, Angeli A, Dimmito MP, et al. Activation of β- and γ-carbonic anhydrases from pathogenic bacteria with tripeptides. J Enzyme Inhib Med Chem 2018;33:945–50.
  • Bua S, Haapanen S, Kuuslahti M, et al. Activation studies of the β-carbonic anhydrase from the pathogenic protozoan Entamoeba histolytica with amino acids and amines. Metabolites 2019;9:26–33.
  • Angeli A, Donald WA, Parkkila S, Supuran CT. Activation studies with amines and amino acids of the β-carbonic anhydrase from the pathogenic protozoan Leishmania donovani chagasi. Bioorg. Chem 2018;78:406–10.
  • (a) Vullo D, Del Prete S, Osman SM, et al. Burkholderia pseudomallei γ-carbonic anhydrase is strongly activated by amino acids and amines. Bioorg Med Chem Lett 2017;27:77–80. (b) Vullo D, Del Prete S, Osman SM, et al. Comparison of the amine/amino acid activation profiles of the β- and γ-carbonic anhydrases from the pathogenic bacterium Burkholderia pseudomallei. J Enzyme Inhib Med Chem 2018;33:25–30.
  • Angeli A, Del Prete S, Osman SM, et al. Activation studies of the γ-carbonic anhydrases from the Antarctic marine bacteria Pseudoalteromonas haloplanktis and Colwellia psychrerythraea with amino acids and amines. Marine Drugs 2019;17:238–46.
  • Angeli A, Alasmary FAS, Del Prete S, et al. The first study of a δ-carbonic anhydrase: TweCAδ from the diatom Thalassiosira weissflogii is effectively activated by amines and amino acids. J Enzyme Inhib Med Chem 2018;33:680–5.
  • Angeli A, Buonanno M, Donald WA, et al. The zinc - but not cadmium – containing ζ-carbonic from the diatom Thalassiosira weissflogii is potently activated by amines and amino acids . Bioorg Chem 2018;80:261–5.
  • Angeli A, Del Prete S, Alasmary FAS, et al. The first activation studies of the η-carbonic anhydrase from the malaria parasite Plasmodium falciparum with amines and amino acids. Bioorg Chem 2018;80:94–8.