State of the Art on Carbonic Anhydrase Modulators for Biomedical Purposes

Author(s): Murat Bozdag , Abdulmalik Saleh Alfawaz Altamimi , Daniela Vullo , Claudiu T. Supuran* , Fabrizio Carta* .

Journal Name: Current Medicinal Chemistry

Volume 26 , Issue 15 , 2019

  Journal Home
Translate in Chinese

Abstract:

The current review is intended to highlight recent advances in the search of new and effective modulators of the metalloenzymes Carbonic Anhydrases (CAs, EC 4.2.1.1) expressed in humans (h). CAs reversibly catalyze the CO2 hydration reaction, which is of crucial importance in the regulation of a plethora of fundamental processes at cellular level as well as in complex organisms. The first section of this review will be dedicated to compounds acting as activators of the hCAs (CAAs) and their promising effects on central nervous system affecting pathologies mainly characterized from memory and learning impairments. The second part will focus on the emerging chemical classes acting as hCA inhibitors (CAIs) and their potential use for the treatment of diseases.

Keywords: metalloenzymes, carbonic anhydrases, enzyme activators, enzyme inhibitors, tumors, reumathoid arthritis, glaucoma.

[1]
Supuran, C.T. Carbonic anhydrases: Novel therapeutic applications for inhibitors and activators. Nat. Rev. Drug Discov., 2008, 7(2), 168-181.
[http://dx.doi.org/10.1038/nrd2467] [PMID: 18167490]
[2]
Del Prete, S.; Vullo, D.; Fisher, G.M.; Andrews, K.T.; Poulsen, S.A.; Capasso, C.; Supuran, C.T. Discovery of a new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum--the η-carbonic anhydrases. Bioorg. Med. Chem. Lett., 2014, 24(18), 4389-4396.
[http://dx.doi.org/10.1016/j.bmcl.2014.08.015] [PMID: 25168745]
[3]
Domsic, J.F.; McKenna, R. Sequestration of carbon dioxide by the hydrophobic pocket of the carbonic anhydrases. Biochim. Biophys. Acta, 2010, 1804(2), 326-331.
[http://dx.doi.org/10.1016/j.bbapap.2009.07.025] [PMID: 19679198]
[4]
Tu, C.K.; Silverman, D.N.; Forsman, C.; Jonsson, B.H.; Lindskog, S. Role of histidine 64 in the catalytic mechanism of human carbonic anhydrase II studied with a site-specific mutant. Biochemistry, 1989, 28(19), 7913-7918.
[http://dx.doi.org/10.1021/bi00445a054] [PMID: 2514797]
[5]
Supuran, C.T. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin. Drug Discov., 2017, 12(1), 61-88.
[http://dx.doi.org/10.1080/17460441.2017.1253677] [PMID: 27783541]
[6]
Neri, D.; Supuran, C.T. Interfering with pH regulation in tumours as a therapeutic strategy. Nat. Rev. Drug Discov., 2011, 10(10), 767-777.
[http://dx.doi.org/10.1038/nrd3554] [PMID: 21921921]
[7]
Masini, E.; Carta, F.; Scozzafava, A.; Supuran, C.T. Antiglaucoma carbonic anhydrase inhibitors: A patent review. Expert Opin. Ther. Pat., 2013, 23(6), 705-716.
[http://dx.doi.org/10.1517/13543776.2013.794788] [PMID: 23627893]
[8]
Scozzafava, A.; Supuran, C.T.; Carta, F. Antiobesity carbonic anhydrase inhibitors: A literature and patent review. Expert Opin. Ther. Pat., 2013, 23(6), 725-735.
[http://dx.doi.org/10.1517/13543776.2013.790957] [PMID: 23607332]
[9]
Carta, F.; Supuran, C.T. Diuretics with carbonic anhydrase inhibitory action: A patent and literature review (2005 - 2013). Expert Opin. Ther. Pat., 2013, 23(6), 681-691.
[http://dx.doi.org/10.1517/13543776.2013.780598] [PMID: 23488823]
[10]
Leiner, M. The ferment carbonic anhydrase in the animal body. Nat. Sci., 1940, 28, 316-317.
[http://dx.doi.org/10.1007/BF01734561]
[11]
Leiner, M.; Leiner, G. Activators of carbonic anhydrase. Nat. Sci., 1941, 29, 195-197.
[http://dx.doi.org/10.1007/BF01503749]
[12]
Leiner, M.; Leiner, G. The measuring methods for investigating the catalytic activity of carbonic anhydrase. Biochem. Z., 1941, 311, 119-145.
[13]
Main, R.E.; Locke, A. Activation of carbonic anhydrase by histamine. J. Biol. Chem., 1941, 140, LXXXI.
[14]
Kiese, M. The activation of carbonic anhydrase. Nat. Sci., 1941, 29, 116-117.
[http://dx.doi.org/10.1007/BF01486163]
[15]
Supuran, C.T. Carbonic anhydrase activators. Part 4. A general mechanism of action for activators of isozymes I, II and III. Rev. Roum. Chim., 1992, 37, 411-421.
[16]
Supuran, C.T.; Balaban, A.T. Carbonic anhydrase activators. Part 8. pKa - Activation relationship in a series of amino acid derivatives activators of isozyme II. Rev. Roum. Chim., 1994, 39, 107-113.
[17]
Tu, C.K.; Silverman, D.N.; Forsman, C.; Jonsson, B.H.; Lindskog, S. Role of histidine 64 in the catalytic mechanism of human carbonic anhydrase II studied with a site-specific mutant. Biochemistry, 1989, 28(19), 7913-7918.
[http://dx.doi.org/10.1021/bi00445a054] [PMID: 2514797]
[18]
Briganti, F.; Mangani, S.; Orioli, P.; Scozzafava, A.; Vernaglione, G.; Supuran, C.T. Carbonic anhydrase activators: X-ray crystallographic and spectroscopic investigations for the interaction of isozymes I and II with histamine. Biochemistry, 1997, 36(34), 10384-10392.
[http://dx.doi.org/10.1021/bi970760v] [PMID: 9265618]
[19]
Temperini, C.; Scozzafava, A.; Vullo, D.; Supuran, C.T. 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(27), 7057-7066.
[http://dx.doi.org/10.1002/chem.200600159] [PMID: 16807956]
[20]
Temperini, C.; Scozzafava, A.; Vullo, D.; Supuran, C.T. 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(10), 3019-3027.
[http://dx.doi.org/10.1021/jm0603320] [PMID: 16686544]
[21]
Temperini, C.; Innocenti, A.; Scozzafava, A.; Supuran, C.T. 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(18), 8373-8378.
[http://dx.doi.org/10.1016/j.bmc.2008.08.043] [PMID: 18774300]
[22]
Temperini, C.; Innocenti, A.; Scozzafava, A.; Mastrolorenzo, A.; Supuran, C.T. 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(3), 628-635.
[http://dx.doi.org/10.1016/j.bmcl.2006.11.027] [PMID: 17127057]
[23]
Temperini, C.; Scozzafava, A.; Puccetti, L.; Supuran, C.T. 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(23), 5136-5141.
[http://dx.doi.org/10.1016/j.bmcl.2005.08.069] [PMID: 16214338]
[24]
Sun, M.K.; Alkon, D.L. Carbonic anhydrase gating of attention: Memory therapy and enhancement. Trends Pharmacol. Sci., 2002, 23(2), 83-89.
[http://dx.doi.org/10.1016/S0165-6147(02)01899-0] [PMID: 11830265]
[25]
Sun, M.K.; Alkon, D.L. Pharmacological enhancement of synaptic efficacy, spatial learning, and memory through carbonic anhydrase activation in rats. J. Pharmacol. Exp. Ther., 2001, 297(3), 961-967.
[PMID: 11356917]
[26]
Canto de Souza, L.; Provensi, G.; Vullo, D.; Carta, F.; Scozzafava, A.; Costa, A.; Schmidt, S.D.; Passani, M.B.; Supuran, C.T.; Blandina, P. 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, 148-156.
[http://dx.doi.org/10.1016/j.neuropharm.2017.03.009] [PMID: 28286213]
[27]
Abdo, M.R.; Vullo, D.; Saada, M.C.; Montero, J.L.; Scozzafava, A.; Winum, J.Y.; Supuran, C.T. Carbonic anhydrase activators: activation of human isozymes I, II and IX with phenylsulfonylhydrazido l-histidine derivatives. Bioorg. Med. Chem. Lett., 2009, 19(9), 2440-2443.
[http://dx.doi.org/10.1016/j.bmcl.2009.03.050] [PMID: 19345095]
[28]
Saada, M.C.; Vullo, D.; Montero, J.L.; Scozzafava, A.; Supuran, C.T.; Winum, J.Y. Mono- and di-halogenated histamine, histidine and carnosine derivatives are potent carbonic anhydrase I, II, VII, XII and XIV activators. Bioorg. Med. Chem., 2014, 22(17), 4752-4758.
[http://dx.doi.org/10.1016/j.bmc.2014.07.005] [PMID: 25082511]
[29]
Dave, K.; Ilies, M.A.; Scozzafava, A.; Temperini, C.; Vullo, D.; Supuran, C.T. An inhibitor-like binding mode of a carbonic anhydrase activator within the active site of isoform II. Bioorg. Med. Chem. Lett., 2011, 21(9), 2764-2768.
[http://dx.doi.org/10.1016/j.bmcl.2010.10.045] [PMID: 21036610]
[30]
Abdülkadir Coban, T.; Beydemir, S.; Gülcin, I.; Ekinci, D.; Innocenti, A.; Vullo, D.; Supuran, C.T. Sildenafil is a strong activator of mammalian carbonic anhydrase isoforms I-XIV. Bioorg. Med. Chem., 2009, 17(16), 5791-5795.
[http://dx.doi.org/10.1016/j.bmc.2009.07.019] [PMID: 19635671]
[31]
Supuran, C.T. Structure-based drug discovery of carbonic anhydrase inhibitors. J. Enzyme Inhib. Med. Chem., 2012, 27(6), 759-772.
[http://dx.doi.org/10.3109/14756366.2012.672983] [PMID: 22468747]
[32]
Lou, Y.; McDonald, P.C.; Oloumi, A.; Chia, S.; Ostlund, C.; Ahmadi, A.; Kyle, A.; Auf dem Keller, U.; Leung, S.; Huntsman, D.; Clarke, B.; Sutherland, B.W.; Waterhouse, D.; Bally, M.; Roskelley, C.; Overall, C.M.; Minchinton, A.; Pacchiano, F.; Carta, F.; Scozzafava, A.; Touisni, N.; Winum, J.Y.; Supuran, C.T.; Dedhar, S. Targeting tumor hypoxia: Suppression of breast tumor growth and metastasis by novel carbonic anhydrase IX inhibitors. Cancer Res., 2011, 71(9), 3364-3376.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-4261] [PMID: 21415165]
[33]
Carta, F.; Di Cesare Mannelli, L.; Pinard, M.; Ghelardini, C.; Scozzafava, A.; McKenna, R.; Supuran, C.T. A class of sulfonamide carbonic anhydrase inhibitors with neuropathic pain modulating effects. Bioorg. Med. Chem., 2015, 23(8), 1828-1840.
[http://dx.doi.org/10.1016/j.bmc.2015.02.027] [PMID: 25766630]
[34]
Di Cesare Mannelli, L.; Micheli, L.; Carta, F.; Cozzi, A.; Ghelardini, C.; Supuran, C.T. Carbonic anhydrase inhibition for the management of cerebral ischemia: In vivo evaluation of sulfonamide and coumarin inhibitors. J. Enzyme Inhib. Med. Chem., 2016, 31(6), 894-899.
[http://dx.doi.org/10.3109/14756366.2015.1113407] [PMID: 26607399]
[35]
Margheri, F.; Ceruso, M.; Carta, F.; Laurenzana, A.; Maggi, L.; Lazzeri, S.; Simonini, G.; Annunziato, F.; Del Rosso, M.; Supuran, C.T.; Cimaz, R. Overexpression of the transmembrane carbonic anhydrase isoforms IX and XII in the inflamed synovium. J. Enzyme Inhib. Med. Chem, 2016. (sup4), 60-63.
[http://dx.doi.org/10.1080/14756366.2016.1217857]
[36]
Bua, S.; Di Cesare Mannelli, L.; Vullo, D.; Ghelardini, C.; Bartolucci, G.; Scozzafava, A.; Supuran, C.T.; Carta, F. 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(3), 1159-1170.
[http://dx.doi.org/10.1021/acs.jmedchem.6b01607] [PMID: 28075587]
[37]
Alterio, V.; Di Fiore, A.; D’Ambrosio, K.; Supuran, C.T.; De Simone, G. Multiple binding modes of inhibitors to carbonic anhydrases: How to design specific drugs targeting 15 different isoforms? Chem. Rev., 2012, 112(8), 4421-4468.
[http://dx.doi.org/10.1021/cr200176r] [PMID: 22607219]
[38]
Carta, F.; Supuran, C.T.; Scozzafava, A. Sulfonamides and their isosters as carbonic anhydrase inhibitors. Future Med. Chem., 2014, 6(10), 1149-1165.
[http://dx.doi.org/10.4155/fmc.14.68] [PMID: 25078135]
[39]
Scott, A.D.; Phillips, C.; Alex, A.; Flocco, M.; Bent, A.; Randall, A.; O’Brien, R.; Damian, L.; Jones, L.H. Thermodynamic optimisation in drug discovery: A case study using carbonic anhydrase inhibitors. ChemMedChem, 2009, 4(12), 1985-1989.
[http://dx.doi.org/10.1002/cmdc.200900386] [PMID: 19882701]
[40]
Pacchiano, F.; Aggarwal, M.; Avvaru, B.S.; Robbins, A.H.; Scozzafava, A.; McKenna, R.; Supuran, C.T. 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., 2010, 46(44), 8371-8373.
[41]
Pacchiano, F.; Carta, F.; McDonald, P.C.; Lou, Y.; Vullo, D.; Scozzafava, A.; Dedhar, S.; Supuran, C.T. Ureido-substituted benzenesulfonamides potently inhibit carbonic anhydrase IX and show antimetastatic activity in a model of breast cancer metastasis. J. Med. Chem., 2011, 54(6), 1896-1902.
[http://dx.doi.org/10.1021/jm101541x] [PMID: 21361354]
[42]
Safety study of slc-0111 in subjects with advanced solid tumours. https://clinicaltrials.gov/ct2/show/NCT02215850
[43]
Nishimori, I.; Vullo, D.; Innocenti, A.; Scozzafava, A.; Mastrolorenzo, A.; Supuran, C.T. Carbonic anhydrase inhibitors. The mitochondrial isozyme VB as a new target for sulfonamide and sulfamate inhibitors. J. Med. Chem., 2005, 48(24), 7860-7866.
[http://dx.doi.org/10.1021/jm050483n] [PMID: 16302824]
[44]
Dodgson, S.J.; Shank, R.P.; Maryanoff, B.E. Topiramate as an inhibitor of carbonic anhydrase isoenzymes. Epilepsia, 2000, 41(Suppl. 1), S35-S39.
[http://dx.doi.org/10.1111/j.1528-1157.2000.tb06047.x] [PMID: 10768298]
[45]
Dodgson, S.J.; Cherian, K. Mitochondrial carbonic anhydrase is involved in rat renal glucose synthesis. Am. J. Physiol., 1989, 257(6 Pt 1), E791-E796.
[PMID: 2514597]
[46]
Spencer, I.M.; Hargreaves, I.; Chegwidden, W.R. Effects of the carbonic anhydrase inhibitor acetazolamide on lipid synthesis in the locust. Biochem. Soc. Trans., 1988, 16, 973-974.
[http://dx.doi.org/10.1042/bst0160973]
[47]
Lynch, C.J.; Fox, H.; Hazen, S.A.; Stanley, B.A.; Dodgson, S.; Lanoue, K.F. Role of hepatic carbonic anhydrase in de novo lipogenesis. Biochem. J., 1995, 310(Pt 1), 197-202.
[http://dx.doi.org/10.1042/bj3100197] [PMID: 7646445]
[48]
Picard, F.; Deshaies, Y.; Lalonde, J.; Samson, P.; Richard, D. Topiramate reduces energy and fat gains in lean (Fa/?) and obese (fa/fa) Zucker rats. Obes. Res., 2000, 8(9), 656-663.
[http://dx.doi.org/10.1038/oby.2000.84] [PMID: 11225714]
[49]
Supuran, C.T. Carbonic anhydrase inhibitors as emerging drugs for the treatment of obesity. Expert Opin. Emerg. Drugs, •••, 17, 11-15.
[50]
Supuran, C.T.; Di Fiore, A.; De Simone, G. Carbonic anhydrase inhibitors as emerging drugs for the treatment of obesity. Expert Opin. Emerg. Drugs, 2008, 13(2), 383-392.
[http://dx.doi.org/10.1517/14728214.13.2.383] [PMID: 18537527]
[51]
Heal, D.J.; Gosden, J.; Smith, S.L. What is the prognosis for new centrally-acting anti-obesity drugs? Neuropharmacology, 2012, 63(1), 132-161.
[http://dx.doi.org/10.1016/j.neuropharm.2012.01.017] [PMID: 22313529]
[52]
Najarian, T. Combination therapy for effecting weight loss and treating obesity. US0002462; 2004.
[53]
Najarian, T. Combination therapy for effecting weight loss and treating obesity. US0234950, 2006.
[54]
Najarian, T. Combination therapy for effecting weight loss and treating obesity. US0234951, 2006.
[55]
Najarian, T; Tam, P.Y.; Wilson, L.F. Compositions and methods for treating obesity and related disorders. WO153632, 2008.
[56]
Vitale, R.M.; Pedone, C.; Amodeo, P.; Antel, J.; Wurl, M.; Scozzafava, A.; Supuran, C.T.; De Simone, G. Molecular modeling study for the binding of zonisamide and topiramate to the human mitochondrial carbonic anhydrase isoform VA. Bioorg. Med. Chem., 2007, 15(12), 4152-4158.
[http://dx.doi.org/10.1016/j.bmc.2007.03.070] [PMID: 17420132]
[57]
De Simone, G.; Di Fiore, A.; Menchise, V.; Pedone, C.; Antel, J.; Casini, A.; Scozzafava, A.; Wurl, M.; Supuran, C.T. Carbonic anhydrase inhibitors. Zonisamide is an effective inhibitor of the cytosolic isozyme II and mitochondrial isozyme V: Solution and X-ray crystallographic studies. Bioorg. Med. Chem. Lett., 2005, 15(9), 2315-2320.
[http://dx.doi.org/10.1016/j.bmcl.2005.03.032] [PMID: 15837316]
[58]
Vullo, D.; Franchi, M.; Gallori, E.; Pastorek, J.; Scozzafava, A.; Pastorekova, S.; Supuran, C.T. Carbonic anhydrase inhibitors. Inhibition of cytosolic isozymes I and II and transmembrane, cancer-associated isozyme IX with anions. J. Enzyme Inhib. Med. Chem., 2003, 18(5), 403-406.
[http://dx.doi.org/10.1080/1475636031000138732] [PMID: 14692506]
[59]
Innocenti, A.; Scozzafava, A.; Supuran, C.T. Carbonic anhydrase inhibitors. Inhibition of cytosolic isoforms I, II, III, VII and XIII with less investigated inorganic anions. Bioorg. Med. Chem. Lett., 2009, 19(7), 1855-1857.
[http://dx.doi.org/10.1016/j.bmcl.2009.02.088] [PMID: 19269822]
[60]
Temperini, C.; Scozzafava, A.; Supuran, C.T. Carbonic anhydrase inhibitors. X-ray crystal studies of the carbonic anhydrase II-trithiocarbonate adduct--an inhibitor mimicking the sulfonamide and urea binding to the enzyme. Bioorg. Med. Chem. Lett., 2010, 20(2), 474-478.
[http://dx.doi.org/10.1016/j.bmcl.2009.11.124] [PMID: 20005709]
[61]
Carta, F.; Aggarwal, M.; Maresca, A.; Scozzafava, A.; McKenna, R.; Supuran, C.T. Dithiocarbamates: A new class of carbonic anhydrase inhibitors. Crystallographic and kinetic investigations. Chem. Commun. (Camb.), 2012, 48(13), 1868-1870.
[http://dx.doi.org/10.1039/c2cc16395k] [PMID: 22218610]
[62]
Carta, F.; Aggarwal, M.; Maresca, A.; Scozzafava, A.; McKenna, R.; Masini, E.; Supuran, C.T. Dithiocarbamates strongly inhibit carbonic anhydrases and show antiglaucoma action in vivo. J. Med. Chem., 2012, 55(4), 1721-1730.
[http://dx.doi.org/10.1021/jm300031j] [PMID: 22276570]
[63]
Carta, F.; Akdemir, A.; Scozzafava, A.; Masini, E.; Supuran, C.T. Xanthates and trithiocarbonates strongly inhibit carbonic anhydrases and show antiglaucoma effects in vivo. J. Med. Chem., 2013, 56(11), 4691-4700.
[http://dx.doi.org/10.1021/jm400414j] [PMID: 23647428]
[64]
Vullo, D.; Durante, M.; Di Leva, F.S.; Cosconati, S.; Masini, E.; Scozzafava, A.; Novellino, E.; Supuran, C.T.; Carta, F. Monothiocarbamates strongly inhibit carbonic anhydrases in vitro and possess intraocular pressure lowering activity in an animal model of glaucoma. J. Med. Chem., 2016, 59(12), 5857-5867.
[http://dx.doi.org/10.1021/acs.jmedchem.6b00462] [PMID: 27253845]
[65]
Woster, P.M. Polyamine structure and synthetic analogs; Polyamine Cell Sign, 2006, pp. 3-24.
[http://dx.doi.org/10.1007/978-1-59745-145-1_1]
[66]
Fleidervish, I.A.; Libman, L.; Katz, E.; Gutnick, M.J. Endogenous polyamines regulate cortical neuronal excitability by blocking voltage-gated Na channels. Proc. Natl. Acad. Sci. USA, 2008, 105, 18994-18999.
[http://dx.doi.org/10.1073/pnas.0803464105] [PMID: 19020082]
[67]
Wallace, H.M.; Niiranen, K.; Katz, E.; Gutnick, M.J. Polyamine analogues - an update. Amino Acids, 2007, 33(2), 261-265.
[http://dx.doi.org/10.1007/s00726-007-0534-z] [PMID: 17443267]
[68]
Casero, R.A., Jr; Marton, L.J. Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases. Nat. Rev. Drug Discov., 2007, 6(5), 373-390.
[http://dx.doi.org/10.1038/nrd2243] [PMID: 17464296]
[69]
Soda, K.; Dobashi, Y.; Kano, Y.; Tsujinaka, S.; Konishi, F. Polyamine-rich food decreases age-associated pathology and mortality in aged mice. Exp. Gerontol., 2009, 44(11), 727-732.
[http://dx.doi.org/10.1016/j.exger.2009.08.013] [PMID: 19735716]
[70]
Casero, R.A.; Pegg, A.E. Polyamine catabolism and disease. Biochem. J., 2009, 421(3), 323-338.
[http://dx.doi.org/10.1042/BJ20090598] [PMID: 19589128]
[71]
Li, J.; Doyle, K.M.; Tatlisumak, T. Polyamines in the brain: Distribution, biological interactions, and their potential therapeutic role in brain ischaemia. Curr. Med. Chem., 2007, 14(17), 1807-1813.
[http://dx.doi.org/10.2174/092986707781058841] [PMID: 17627518]
[72]
Carta, F.; Temperini, C.; Innocenti, A.; Scozzafava, A.; Kaila, K.; Supuran, C.T. Polyamines inhibit carbonic anhydrases by anchoring to the zinc-coordinated water molecule. J. Med. Chem., 2010, 53(15), 5511-5522.
[http://dx.doi.org/10.1021/jm1003667] [PMID: 20590092]
[73]
Maresca, A.; Temperini, C.; Vu, H.; Pham, N.B.; Poulsen, S.A.; Scozzafava, A.; Quinn, R.J.; Supuran, C.T. Non-zinc mediated inhibition of carbonic anhydrases: coumarins are a new class of suicide inhibitors. J. Am. Chem. Soc., 2009, 131(8), 3057-3062.
[http://dx.doi.org/10.1021/ja809683v] [PMID: 19206230]
[74]
Tars, K.; Vullo, D.; Kazaks, A.; Leitans, J.; Lends, A.; Grandane, A.; Zalubovskis, R.; Scozzafava, A.; Supuran, C.T. 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(1), 293-300.
[http://dx.doi.org/10.1021/jm301625s] [PMID: 23241068]
[75]
Maresca, A.; Temperini, C.; Pochet, L.; Masereel, B.; Scozzafava, A.; Supuran, C.T. Deciphering the mechanism of carbonic anhydrase inhibition with coumarins and thiocoumarins. J. Med. Chem., 2010, 53(1), 335-344.
[http://dx.doi.org/10.1021/jm901287j] [PMID: 19911821]
[76]
Carta, F.; Maresca, A.; Scozzafava, A.; Supuran, C.T. Novel coumarins and 2-thioxo-coumarins as inhibitors of the tumor-associated carbonic anhydrases IX and XII. Bioorg. Med. Chem., 2012, 20(7), 2266-2273.
[http://dx.doi.org/10.1016/j.bmc.2012.02.014] [PMID: 22377674]
[77]
Davis, R.A.; Vullo, D.; Maresca, A.; Supuran, C.T.; Poulsen, S.A. Natural product coumarins that inhibit human carbonic anhydrases. Bioorg. Med. Chem., 2013, 21(6), 1539-1543.
[http://dx.doi.org/10.1016/j.bmc.2012.07.021] [PMID: 22892213]
[78]
Ferraroni, M.; Carta, F.; Scozzafava, A.; Supuran, C.T. Thioxocoumarins show an alternative carbonic anhydrase inhibition mechanism compared to coumarins. J. Med. Chem., 2016, 59(1), 462-473.
[http://dx.doi.org/10.1021/acs.jmedchem.5b01720] [PMID: 26688270]
[79]
Carta, F.; Maresca, A.; Scozzafava, A.; Supuran, C.T. 5- and 6-membered (thio)lactones are prodrug type carbonic anhydrase inhibitors. Bioorg. Med. Chem. Lett., 2012, 22(1), 267-270.
[http://dx.doi.org/10.1016/j.bmcl.2011.11.018] [PMID: 22137345]
[80]
Margheri, F.; Ceruso, M.; Carta, F.; Laurenzana, A.; Maggi, L.; Lazzeri, S.; Simonini, G.; Annunziato, F.; Del Rosso, M.; Supuran, C.T.; Cimaz, R. Overexpression of the transmembrane carbonic anhydrase isoforms IX and XII in the inflamed synovium. J. Enzyme Inhib. Med. Chem, 2016. 31(sup4), 60-63.
[81]
Chang, X.; Han, J.; Zhao, Y.; Yan, X.; Sun, S.; Cui, Y. Increased expression of carbonic anhydrase I in the synovium of patients with ankylosing spondylitis. BMC Musculoskelet. Disord., 2010, 11, 279-290.
[http://dx.doi.org/10.1186/1471-2474-11-279] [PMID: 21143847]
[82]
Zheng, Y.; Wang, L.; Zhang, W.; Xu, H.; Chang, X. Transgenic mice over-expressing carbonic anhydrase I showed aggravated joint inflammation and tissue destruction. BMC Musculoskelet. Disord., 2012, 13, 256-265.
[http://dx.doi.org/10.1186/1471-2474-13-256] [PMID: 23256642]
[83]
Deutsch, O.; Krief, G.; Konttinen, Y.T.; Zaks, B.; Wong, D.T.; Aframian, D.J.; Palmon, A. Identification of Sjögren’s syndrome oral fluid biomarker candidates following high-abundance protein depletion. Rheumatology (Oxford), 2015, 54(5), 884-890.
[http://dx.doi.org/10.1093/rheumatology/keu405] [PMID: 25339641]
[84]
Grandane, A.; Tanc, M.; Di Cesare Mannelli, L.; Carta, F.; Ghelardini, C.; Žalubovskis, R.; Supuran, C.T. 6-Substituted sulfocoumarins are selective carbonic anhdydrase IX and XII inhibitors with significant cytotoxicity against colorectal cancer cells. J. Med. Chem., 2015, 58(9), 3975-3983.
[http://dx.doi.org/10.1021/acs.jmedchem.5b00523] [PMID: 25875209]
[85]
Tanc, M.; Carta, F.; Scozzafava, A.; Supuran, C.T. 6-Substituted 1,2-benzoxathiine-2,2-dioxides are isoform-selective inhibitors of human carbonic anhydrases IX, XII and VA. Org. Biomol. Chem., 2015, 13(1), 77-80.
[http://dx.doi.org/10.1039/C4OB02155J] [PMID: 25373598]
[86]
Tanc, M.; Carta, F.; Bozdag, M.; Scozzafava, A.; Supuran, C.T. 7-Substituted-sulfocoumarins are isoform-selective, potent carbonic anhydrase II inhibitors. Bioorg. Med. Chem., 2013, 21(15), 4502-4510.
[http://dx.doi.org/10.1016/j.bmc.2013.05.032] [PMID: 23769167]
[87]
Karioti, A.; Carta, F.; Supuran, C.T. Phenols and polyphenols as carbonic anhydrase inhibitors. Molecules, 2016, 21(12)E1649
[http://dx.doi.org/10.3390/molecules21121649] [PMID: 27918439]
[88]
Karioti, A.; Carta, F.; Supuran, C.T. An update on natural products with carbonic anhydrase inhibitory activity. Curr. Pharm. Des., 2016, 22(12), 1570-1591.
[http://dx.doi.org/10.2174/1381612822666151211094235] [PMID: 26654592]
[89]
Busardò, F.P.; Bertol, E.; Vaiano, F.; Baglio, G.; Montana, A.; Barbera, N.; Zaami, S.; Romano, G. Post mortem concentrations of endogenous Gamma Hydroxybutyric Acid (GHB) and in vitro formation in stored blood and urine samples. Forensic Sci. Int., 2014, 243, 144-148.
[http://dx.doi.org/10.1016/j.forsciint.2014.07.019] [PMID: 25123534]
[90]
Bertol, E.; Vaiano, F.; Di Milia, M.G.; Mari, F. In vivo detection of the new psychoactive substance AM-694 and its metabolites. Forensic Sci. Int., 2015, 256, 21-27.
[http://dx.doi.org/10.1016/j.forsciint.2015.07.018] [PMID: 26295909]
[91]
Bertol, E.; Argo, A.; Procaccianti, P.; Vaiano, F.; Di Milia, M.G.; Furlanetto, S.; Mari, F. Detection of gamma-hydroxybutyrate in hair: Validation of GC-MS and LC-MS/MS methods and application to a real case. J. Pharm. Biomed. Anal., 2012, 70, 518-522.
[http://dx.doi.org/10.1016/j.jpba.2012.07.009] [PMID: 22884787]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 26
ISSUE: 15
Year: 2019
Page: [2558 - 2573]
Pages: 16
DOI: 10.2174/0929867325666180622120625
Price: $58

Article Metrics

PDF: 30
HTML: 3
EPUB: 1