Abstract
Enzymes are highly specific catalysts that accelerate reactions in biological systems. Carbonic anhydrase (CA) is an enzyme found in plants, microorganisms, and vertebrates. CA catalyses CO2 hydration/ dehydration. There are different families and isoenzymes of CAs. Fifteen α-CA isoenzymes have been reported in humans. The status of CO2 hydration and dehydration is important for a variety of biological processes. CAs play an important role in many physiological and pathological events in several tissue types. Their levels are increased in some diseases; therefore, CA inhibition has been applied as a therapeutic option. However, the high diversity of these isoenzymes is an important consideration. Isoenzyme- specific CA inhibitors can reduce the side effects of treatment. Some agents containing additional sulfonamides approved for other therapeutic applications, such as topiramate, celecoxib/valdecoxib, sulpiride, and famotidine, have inhibitory effects on CA isoenzymes. These bind to the zinc ion in the CA active site. Recently, research has been conducted on the use of a hybrid form of active ingredient and a CA inhibitor. CA inhibitor-NSAID hybrid compounds demonstrated more efficacy than NSAIDs in arthritis, which has attracted further attention of researchers in conducting research on CA-hybrid drugs.
Keywords: Hybrid compounds, Carbonic anhydrase, physiologic function, pathologic status, enzyme and inhibition.
Graphical Abstract
[2]
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]
[http://dx.doi.org/10.1021/cr200176r] [PMID: 22607219]
[3]
Escudero-Almanza, D.J.; Ojeda-Barrios, D.L.; Hernández-Rodríguez, O.A.; Sánchez Chávez, E.; Ruíz-Anchondo, T.; Sida-Arreola, J.P. Carbonic anhydrase and zinc in plant physiology. Chil. J. Agric. Res., 2012, 72(1), 140-146.
[http://dx.doi.org/10.4067/S0718-58392012000100022]
[http://dx.doi.org/10.4067/S0718-58392012000100022]
[4]
Boone, C.D.; Pinard, M.; McKenna, R.; Silverman, D. Catalytic mechanism of α-class carbonic anhydrases: CO2 hydration and proton transfer. Carbonic Anhydrase:Mechanism, Regulation, Links to Disease, and Industrial Applications;; Frost, S.C.; McKenna, R., Eds.; Springer: Dordrecht,, 2014, pp. 31-52.
[http://dx.doi.org/10.1007/978-94-007-7359-2_3]
[http://dx.doi.org/10.1007/978-94-007-7359-2_3]
[5]
Ozensoy Guler, O.; Supuran, C.T.; Capasso, C. Carbonic anhydrase IX as a novel candidate in liquid biopsy. J. Enzyme Inhib. Med. Chem., 2020, 35(1), 255-260.
[http://dx.doi.org/10.1080/14756366.2019.1697251] [PMID: 31790601]
[http://dx.doi.org/10.1080/14756366.2019.1697251] [PMID: 31790601]
[6]
McKenna, R.; Frost, S.C. Overview of the Carbonic Anhydrase Family.Carbonic anhydrase: Mechanism, regulation, links to disease, and industrial applications; Frost, S.C.; McKenna, R., Eds.; Springer: Dordrecht, 2014, pp. 3-5.
[http://dx.doi.org/10.1007/978-94-007-7359-2_1]
[http://dx.doi.org/10.1007/978-94-007-7359-2_1]
[8]
Bhat, F.A.; Ganai, B.A.; Uqab, B. Carbonic anhydrase: Mechanism, structure and importance in higher plants. Asian. J. Plant Sci. Res., 2017, 7(3), 17-23.
[9]
Agarwal, T.; Singla, R.K.; Garg, A. In: Carbonic anhydrases andtheir physiological roles, proceedings of the MOL2NET'19, conference on molecular, biomedical
&,computational sciences and engineering, 5th edition, USINEWS-03: US-IN-EU worldwide science workshop series, UMN, Duluth, USA, 20 March-20 December 2019 2019.
[http://dx.doi.org/10.3390/mol2net-05-06764]
[http://dx.doi.org/10.3390/mol2net-05-06764]
[10]
Imtaiyaz Hassan, M.; Shajee, B.; Waheed, A.; Ahmad, F.; Sly, W.S. Structure, function and applications of carbonic anhydrase isozymes. Bioorg. Med. Chem., 2013, 21(6), 1570-1582.
[http://dx.doi.org/10.1016/j.bmc.2012.04.044] [PMID: 22607884]
[http://dx.doi.org/10.1016/j.bmc.2012.04.044] [PMID: 22607884]
[11]
Supuran, C.T.; Capasso, C. An overview of the bacterial carbonic anhydrases. Metabolites, 2017, 7(4), 56.
[http://dx.doi.org/10.3390/metabo7040056] [PMID: 29137134]
[http://dx.doi.org/10.3390/metabo7040056] [PMID: 29137134]
[12]
DiMario, R.J.; Machingura, M.C.; Waldrop, G.L.; Moroney, J.V. The many types of carbonic anhydrases in photosynthetic organisms. Plant Sci., 2018, 268, 11-17.
[http://dx.doi.org/10.1016/j.plantsci.2017.12.002] [PMID: 29362079]
[http://dx.doi.org/10.1016/j.plantsci.2017.12.002] [PMID: 29362079]
[13]
McKenna, R.; Supuran, C.T. Carbonic anhydrase inhibitors drug Design .Carbonic anhydrase: Mechanism, regulation, links to disease,and industrial applications; Frost, S.C.; McKenna, R., Eds.; Springer: Dordrecht, 2014, pp. 291-324.
[http://dx.doi.org/10.1007/978-94-007-7359-2_15]
[http://dx.doi.org/10.1007/978-94-007-7359-2_15]
[14]
Mboge, M.Y.; Mahon, B.P.; McKenna, R.; Frost, S.C. Carbonic anhydrases: Role in pH control and cancer. Metabolites, 2018, 8(1), 19.
[http://dx.doi.org/10.3390/metabo8010019] [PMID: 29495652]
[http://dx.doi.org/10.3390/metabo8010019] [PMID: 29495652]
[15]
Del Prete, S.; Nocentini, A.; Supuran, C.T.; 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(1), 1060-1068.
[http://dx.doi.org/10.1080/14756366.2020.1755852] [PMID: 32314608]
[http://dx.doi.org/10.1080/14756366.2020.1755852] [PMID: 32314608]
[16]
Nocentini, A.; Supuran, C.T. Carbonic anhydrase inhibitors for the treatment of neuropathic pain and arthritis. Carbonic Anhydrases; Supuran, C.T; Nocentini, A., Ed.; Academic Press, 2019, pp. 367-386.
[http://dx.doi.org/10.1016/B978-0-12-816476-1.00017-4]
[http://dx.doi.org/10.1016/B978-0-12-816476-1.00017-4]
[17]
Frost, S.C. Physiological functions of the alpha class of carbonic anhydrases.Carbonic anhydrase: Mechanism, regulation, links to disease, and industrial applications; Frost, S.C.; McKenna, R., Eds.; Springer: Dordrecht, 2014, pp. 9-30.
[http://dx.doi.org/10.1007/978-94-007-7359-2_2]
[http://dx.doi.org/10.1007/978-94-007-7359-2_2]
[18]
Nocentini, A.; Donald, W.A.; Supuran, C.T. Human carbonic anhydrases: Tissue distribution, physiological role, and druggability. , 2019; pp. 151-185.
[19]
Wistrand, P.J.; Carter, N.D.; Conroy, C.W.; Mahieu, I. Carbonic anhydrase IV activity is localized on the exterior surface of human erythrocytes. Acta Physiol. Scand., 1999, 165(2), 211-218.
[http://dx.doi.org/10.1046/j.1365-201x.1999.00478.x] [PMID: 10090333]
[http://dx.doi.org/10.1046/j.1365-201x.1999.00478.x] [PMID: 10090333]
[20]
Kumar, S.; Rulhania, S.; Jaswal, S.; Monga, V. Recent advances in the medicinal chemistry of carbonic anhydrase inhibitors. Eur. J. Med. Chem., 2021, 209112923.
[http://dx.doi.org/10.1016/j.ejmech.2020.112923] [PMID: 33121862]
[http://dx.doi.org/10.1016/j.ejmech.2020.112923] [PMID: 33121862]
[21]
Chiang, W.L.; Chu, S.C.; Lai, J.C.; Yang, S.F.; Chiou, H.L.; Hsieh, Y.S. Alternations in quantities and activities of erythrocyte cytosolic carbonic anhydrase isoenzymes in glucose-6-phosphate dehydrogenase-deficient individuals. Clin. Chim. Acta, 2001, 314(1-2), 195-201.
[http://dx.doi.org/10.1016/S0009-8981(01)00682-9] [PMID: 11718695]
[http://dx.doi.org/10.1016/S0009-8981(01)00682-9] [PMID: 11718695]
[22]
Lehtonen, J.; Shen, B.; Vihinen, M.; Casini, A.; Scozzafava, A.; Supuran, C.T.; Parkkila, A.K.; Saarnio, J.; Kivelä, A.J.; Waheed, A.; Sly, W.S.; Parkkila, S. Characterization of CA XIII, a novel member of the carbonic anhydrase isozyme family. J. Biol. Chem., 2004, 279(4), 2719-2727.
[http://dx.doi.org/10.1074/jbc.M308984200] [PMID: 14600151]
[http://dx.doi.org/10.1074/jbc.M308984200] [PMID: 14600151]
[23]
Gao, B.B.; Clermont, A.; Rook, S.; Fonda, S.J.; Srinivasan, V.J.; Wojtkowski, M.; Fujimoto, J.G.; Avery, R.L.; Arrigg, P.G.; Bursell, S.E.; Aiello, L.P.; Feener, E.P. Extracellular carbonic anhydrase mediates hemorrhagic retinal and cerebral vascular permeability through prekallikrein activation. Nat. Med., 2007, 13(2), 181-188.
[http://dx.doi.org/10.1038/nm1534] [PMID: 17259996]
[http://dx.doi.org/10.1038/nm1534] [PMID: 17259996]
[24]
Forrester, J.V.; Dick, A.D.; McMenamin, P.G.; Roberts, F.; Pearlman, E. General and ocular pharmacology. In: The eye: Basic sciences in practice; Saunders Ltd, 2016; pp. 338-369.
[http://dx.doi.org/10.1016/B978-0-7020-5554-6.00006-X]
[http://dx.doi.org/10.1016/B978-0-7020-5554-6.00006-X]
[25]
Hageman, G.S.; Zhu, X.L.; Waheed, A.; Sly, W.S. Localization of carbonic anhydrase IV in a specific capillary bed of the human eye. Proc. Natl. Acad. Sci. USA, 1991, 88(7), 2716-2720.
[http://dx.doi.org/10.1073/pnas.88.7.2716] [PMID: 1901414]
[http://dx.doi.org/10.1073/pnas.88.7.2716] [PMID: 1901414]
[26]
Karjalainen, S.L.; Haapasalo, H.K.; Aspatwar, A.; Barker, H.; Parkkila, S.; Haapasalo, J.A. Carbonic anhydrase related protein expression in astrocytomas and oligodendroglial tumors. BMC Cancer, 2018, 18(1), 584.
[http://dx.doi.org/10.1186/s12885-018-4493-4] [PMID: 29792187]
[http://dx.doi.org/10.1186/s12885-018-4493-4] [PMID: 29792187]
[27]
Ochrietor, J.D.; Clamp, M.F.; Moroz, T.P.; Grubb, J.H.; Shah, G.N.; Waheed, A.; Sly, W.S.; Linser, P.J. Carbonic anhydrase XIV identified as the membrane CA in mouse retina: Strong expression in Müller cells and the RPE. Exp. Eye Res., 2005, 81(4), 492-500.
[http://dx.doi.org/10.1016/j.exer.2005.03.010] [PMID: 16126196]
[http://dx.doi.org/10.1016/j.exer.2005.03.010] [PMID: 16126196]
[28]
Schwartz, G.J. Physiology and molecular biology of renal carbonic anhydrase. J. Nephrol., 2002, 15(5)(Suppl. 5), S61-S74.
[PMID: 12027223]
[PMID: 12027223]
[29]
Pala, N.; Cadoni, R.; Sechi, M. Carbonic anhydrase I. In: Carbonic anhydrases as biocatalysts; Supuran, C.T.; De Simone, G., Eds.; Elsevier: Amsterdam, 2015; pp. 31-49.
[http://dx.doi.org/10.1016/B978-0-444-63258-6.00003-2]
[http://dx.doi.org/10.1016/B978-0-444-63258-6.00003-2]
[30]
Zamanova, S.; Shabana, A.M.; Mondal, U.K.; Ilies, M.A. Carbonic anhydrases as disease markers. Expert Opin. Ther. Pat., 2019, 29(7), 509-533.
[http://dx.doi.org/10.1080/13543776.2019.1629419] [PMID: 31172829]
[http://dx.doi.org/10.1080/13543776.2019.1629419] [PMID: 31172829]
[31]
Benej, M.; Pastorekova, S.; Pastorek, J. Carbonic Anhydrase IX: Regulation and role in cancer. In: Carbonic anhydrase: Mechanism, regulation, links to disease, and industrial applications; Frost, S.C.; McKenna, R., Eds.; Springer: Dordrecht, 2014; pp. 199-220.
[http://dx.doi.org/10.1007/978-94-007-7359-2_11]
[http://dx.doi.org/10.1007/978-94-007-7359-2_11]
[32]
Türeci, O.; Sahin, U.; Vollmar, E.; Siemer, S.; Göttert, E.; Seitz, G.; Parkkila, A.K.; Shah, G.N.; Grubb, J.H.; Pfreundschuh, M.; Sly, W.S. Human carbonic anhydrase XII: cDNA cloning, expression, and chromosomal localization of a carbonic anhydrase gene that is overexpressed in some renal cell cancers. Proc. Natl. Acad. Sci. USA, 1998, 95(13), 7608-7613.
[http://dx.doi.org/10.1073/pnas.95.13.7608] [PMID: 9636197]
[http://dx.doi.org/10.1073/pnas.95.13.7608] [PMID: 9636197]
[33]
Kaunisto, K.; Parkkila, S.; Rajaniemi, H.; Waheed, A.; Grubb, J.; Sly, W.S. Carbonic anhydrase XIV: Luminal expression suggests key role in renal acidification. Kidney Int., 2002, 61(6), 2111-2118.
[http://dx.doi.org/10.1046/j.1523-1755.2002.00371.x] [PMID: 12028451]
[http://dx.doi.org/10.1046/j.1523-1755.2002.00371.x] [PMID: 12028451]
[34]
Aspatwar, A.; Tolvanen, M.E.; Ortutay, C.; Parkkila, S. Carbonic anhydrase related protein VIII and its role in neurodegeneration and cancer. Curr. Pharm. Des., 2010, 16(29), 3264-3276.
[http://dx.doi.org/10.2174/138161210793429823] [PMID: 20819067]
[http://dx.doi.org/10.2174/138161210793429823] [PMID: 20819067]
[35]
Morimoto, K.; Nishimori, I.; Takeuchi, T.; Kohsaki, T.; Okamoto, N.; Taguchi, T.; Yunoki, S.; Watanabe, R.; Ohtsuki, Y.; Onishi, S. Overexpression of carbonic anhydrase-related protein XI promotes proliferation and invasion of gastrointestinal stromal tumors. Virchows Arch., 2005, 447(1), 66-73.
[http://dx.doi.org/10.1007/s00428-005-1225-3] [PMID: 15942747]
[http://dx.doi.org/10.1007/s00428-005-1225-3] [PMID: 15942747]
[36]
Supuran, C.T. Acetazolamide for the treatment of idiopathic intracranial hypertension. Expert Rev. Neurother., 2015, 15(8), 851-856.
[http://dx.doi.org/10.1586/14737175.2015.1066675] [PMID: 26154918]
[http://dx.doi.org/10.1586/14737175.2015.1066675] [PMID: 26154918]
[37]
Liu, X.; Lu, D.; Bowser, R.; Liu, J. Expression of carbonic anhydrase I in motor neurons and alterations in ALS. Int. J. Mol. Sci., 2016, 17(11), 1820.
[http://dx.doi.org/10.3390/ijms17111820] [PMID: 27809276]
[http://dx.doi.org/10.3390/ijms17111820] [PMID: 27809276]
[38]
Waheed, A.; Sly, W.S. Membrane associated carbonic anhydrase IV (CA IV): A personal and historical perspective. Carbonic anhydrase: Mechanism, regulation, links to disease, and industrial applications; Frost, S.C.; McKenna, R., Eds.; Springer: Dordrecht, , 2014; pp. 157-180.
[http://dx.doi.org/10.1007/978-94-007-7359-2_9]
[http://dx.doi.org/10.1007/978-94-007-7359-2_9]
[39]
Brion, L.P.; Suarez, C.; Zhang, H.; Cammer, W. Up-regulation of carbonic anhydrase isozyme IV in CNS myelin of mice genetically deficient in carbonic anhydrase II. J. Neurochem., 1994, 63(1), 360-366.
[http://dx.doi.org/10.1046/j.1471-4159.1994.63010360.x] [PMID: 8207439]
[http://dx.doi.org/10.1046/j.1471-4159.1994.63010360.x] [PMID: 8207439]
[40]
Halmi, P.; Parkkila, S.; Honkaniemi, J. Expression of carbonic anhydrases II, IV, VII, VIII and XII in rat brain after kainic acid induced status epilepticus. Neurochem. Int., 2006, 48(1), 24-30.
[http://dx.doi.org/10.1016/j.neuint.2005.08.007] [PMID: 16271802]
[http://dx.doi.org/10.1016/j.neuint.2005.08.007] [PMID: 16271802]
[41]
Blandina, P.; Provensi, G.; Passsani, M.B.; Capasso, C.; Supuran, C.T. Carbonic anhydrase modulation of emotional memory. Implications for the treatment of cognitive disorders. J. Enzyme Inhib. Med. Chem., 2020, 35(1), 1206-1214.
[http://dx.doi.org/10.1080/14756366.2020.1766455] [PMID: 32401069]
[http://dx.doi.org/10.1080/14756366.2020.1766455] [PMID: 32401069]
[42]
Ghandour, M.S.; Langley, O.K.; Zhu, X.L.; Waheed, A.; Sly, W.S. Carbonic anhydrase IV on brain capillary endothelial cells: A marker associated with the blood-brain barrier. Proc. Natl. Acad. Sci. USA, 1992, 89(15), 6823-6827.
[http://dx.doi.org/10.1073/pnas.89.15.6823] [PMID: 1495971]
[http://dx.doi.org/10.1073/pnas.89.15.6823] [PMID: 1495971]
[43]
Ghandour, M.S.; Parkkila, A.K.; Parkkila, S.; Waheed, A.; Sly, W.S. Mitochondrial carbonic anhydrase in the nervous system: Expression in neuronal and glial cells. J. Neurochem., 2000, 75(5), 2212-2220.
[http://dx.doi.org/10.1046/j.1471-4159.2000.0752212.x] [PMID: 11032910]
[http://dx.doi.org/10.1046/j.1471-4159.2000.0752212.x] [PMID: 11032910]
[44]
Price, T.O.; Sheibani, N.; Shah, G.N. Regulation of high glucose-induced apoptosis of brain pericytes by mitochondrial CA VA: A specific target for prevention of diabetic cerebrovascular pathology. Biochim. Biophys. Acta Mol. Basis Dis., 2017, 1863(4), 929-935.
[http://dx.doi.org/10.1016/j.bbadis.2017.01.025] [PMID: 28131914]
[http://dx.doi.org/10.1016/j.bbadis.2017.01.025] [PMID: 28131914]
[45]
Lomelino, C.L.; Andring, J.T.; McKenna, R. Crystallography and its impact on carbonic anhydrase research. Int. J. Med. Chem., 2018, 20189419521.
[http://dx.doi.org/10.1155/2018/9419521] [PMID: 30302289]
[http://dx.doi.org/10.1155/2018/9419521] [PMID: 30302289]
[46]
Thiry, A.; Dogné, J.M.; Supuran, C.T.; Masereel, B. Carbonic anhydrase inhibitors as anticonvulsant agents. Curr. Top. Med. Chem., 2007, 7(9), 855-864.
[http://dx.doi.org/10.2174/156802607780636726] [PMID: 17504130]
[http://dx.doi.org/10.2174/156802607780636726] [PMID: 17504130]
[47]
Haapasalo, J.; Nordfors, K.; Haapasalo, H.; Parkkila, S. The expression of carbonic anhydrases II, IX and XII in brain tumors. Cancers (Basel), 2020, 12(7), 1723.
[http://dx.doi.org/10.3390/cancers12071723] [PMID: 32610540]
[http://dx.doi.org/10.3390/cancers12071723] [PMID: 32610540]
[48]
Nocentini, A.; Supuran, C.T. Carbonic anhydrase inhibitors as antitumor/antimetastatic agents: A patent review (2008-2018). Expert Opin. Ther. Pat., 2018, 28(10), 729-740.
[http://dx.doi.org/10.1080/13543776.2018.1508453] [PMID: 30074415]
[http://dx.doi.org/10.1080/13543776.2018.1508453] [PMID: 30074415]
[49]
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]
[http://dx.doi.org/10.1038/nrd2467] [PMID: 18167490]
[50]
Hilvo, M.; Supuran, C.T.; Parkkila, S. Characterization and inhibition of the recently discovered carbonic anhydrase isoforms CA XIII, XIV and XV. Curr. Top. Med. Chem., 2007, 7(9), 893-899.
[http://dx.doi.org/10.2174/156802607780636672] [PMID: 17504134]
[http://dx.doi.org/10.2174/156802607780636672] [PMID: 17504134]
[51]
Kim, Y.T.; Hitchcock, R.W.; Bridge, M.J.; Tresco, P.A. Chronic response of adult rat brain tissue to implants anchored to the skull. Biomaterials, 2004, 25(12), 2229-2237.
[http://dx.doi.org/10.1016/j.biomaterials.2003.09.010] [PMID: 14741588]
[http://dx.doi.org/10.1016/j.biomaterials.2003.09.010] [PMID: 14741588]
[52]
Lynch, C.J.; Hazen, S.A.; Horetsky, R.L.; Carter, N.D.; Dodgson, S.J. Differentiation-dependent expression of carbonic anhydrase II and III in 3T3 adipocytes. Am. J. Physiol., 1993, 265(1 Pt 1), C234-C243.
[http://dx.doi.org/10.1152/ajpcell.1993.265.1.C234] [PMID: 8338133]
[http://dx.doi.org/10.1152/ajpcell.1993.265.1.C234] [PMID: 8338133]
[53]
Parkkila, S.; Parkkila, A.K.; Rajaniemi, H. Circadian periodicity in salivary carbonic anhydrase VI concentration. Acta Physiol. Scand., 1995, 154(2), 205-211.
[http://dx.doi.org/10.1111/j.1748-1716.1995.tb09902.x] [PMID: 7572216]
[http://dx.doi.org/10.1111/j.1748-1716.1995.tb09902.x] [PMID: 7572216]
[54]
Karhumaa, P.; Leinonen, J.; Parkkila, S.; Kaunisto, K.; Tapanainen, J.; Rajaniemi, H. The identification of secreted carbonic anhydrase VI as a constitutive glycoprotein of human and rat milk. Proc. Natl. Acad. Sci. USA, 2001, 98(20), 11604-11608.
[http://dx.doi.org/10.1073/pnas.121172598] [PMID: 11553764]
[http://dx.doi.org/10.1073/pnas.121172598] [PMID: 11553764]
[55]
Ogawa, Y.; Matsumoto, K.; Maeda, T.; Tamai, R.; Suzuki, T.; Sasano, H.; Fernley, R.T. Characterization of lacrimal gland carbonic anhydrase VI. J. Histochem. Cytochem., 2002, 50(6), 821-827.
[http://dx.doi.org/10.1177/002215540205000608] [PMID: 12019298]
[http://dx.doi.org/10.1177/002215540205000608] [PMID: 12019298]
[56]
Kaseda, M.; Ichihara, N.; Nishita, T.; Amasaki, H.; Asari, M. Immunohistochemistry of the bovine secretory carbonic anhydrase isozyme (CA-VI) in bovine alimentary canal and major salivary glands. J. Vet. Med. Sci., 2006, 68(2), 131-135.
[http://dx.doi.org/10.1292/jvms.68.131] [PMID: 16520534]
[http://dx.doi.org/10.1292/jvms.68.131] [PMID: 16520534]
[57]
Leinonen, J.S.; Saari, K.A.; Seppänen, J.M.; Myllylä, H.M.; Rajaniemi, H.J. Immunohistochemical demonstration of carbonic anhydrase isoenzyme VI (CA VI) expression in rat lower airways and lung. J. Histochem. Cytochem., 2004, 52(8), 1107-1112.
[http://dx.doi.org/10.1369/jhc.4A6282.2004] [PMID: 15258187]
[http://dx.doi.org/10.1369/jhc.4A6282.2004] [PMID: 15258187]
[58]
Smith, C.E.; Nanci, A.; Moffatt, P. Evidence by signal peptide trap technology for the expression of carbonic anhydrase 6 in rat incisor enamel organs. Eur. J. Oral Sci., 2006, 114(s1)(Suppl. 1), 147-153.
[http://dx.doi.org/10.1111/j.1600-0722.2006.00273.x] [PMID: 16674677]
[http://dx.doi.org/10.1111/j.1600-0722.2006.00273.x] [PMID: 16674677]
[59]
Kivelä, J.; Parkkila, S.; Waheed, A.; Parkkila, A.K.; Sly, W.S.; Rajaniemi, H. Secretory carbonic anhydrase isoenzyme (CA VI) in human serum. Clin. Chem., 1997, 43(12), 2318-2322.
[http://dx.doi.org/10.1093/clinchem/43.12.2318] [PMID: 9439449]
[http://dx.doi.org/10.1093/clinchem/43.12.2318] [PMID: 9439449]
[60]
Mishra, C.B.; Tiwari, M.; Supuran, C.T. Progress in the development of human carbonic anhydrase inhibitors and their pharmacological applications: Where are we today? Med. Res. Rev., 2020, 40(6), 2485-2565.
[http://dx.doi.org/10.1002/med.21713] [PMID: 32691504]
[http://dx.doi.org/10.1002/med.21713] [PMID: 32691504]
[61]
Rahman, S.; Bibi, S.; Javed, T.; Alam, F.; Ali, A.; Qureshi, Z.R.; Ali, S.; Ullah, M.; Asad, M.H.B.; Hasan, S.M.F.; Sabatier, J.M.; Rizvanov, A.A. Review: Therapeutic potential of carbonic anhydrase inhibitors. Pak. J. Pharm. Sci., 2019, 32(2), 709-720.
[PMID: 31081787]
[PMID: 31081787]
[62]
Akocak, S.; Supuran, C.T. 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(1), 1652-1659.
[http://dx.doi.org/10.1080/14756366.2019.1664501] [PMID: 31530034]
[http://dx.doi.org/10.1080/14756366.2019.1664501] [PMID: 31530034]
[63]
Nocentini, A.; Supuran, C.T. Advances in the structural annotation of human carbonic anhydrases and impact on future drug discovery. Expert Opin. Drug Discov., 2019, 14(11), 1175-1197.
[http://dx.doi.org/ 10.1080/17460441.2019.1651289] [PMID: 31436118]
[http://dx.doi.org/ 10.1080/17460441.2019.1651289] [PMID: 31436118]
[64]
Akgul, O.; Di Cesare Mannelli, L.; Vullo, D.; Angeli, A.; Ghelardini, C.; Bartolucci, G.; Alfawaz Altamimi, A.S.; Scozzafava, A.; Supuran, C.T.; Carta, F. 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(11), 4961-4977.
[http://dx.doi.org/10.1021/acs.jmedchem.8b00420] [PMID: 29746127]
[http://dx.doi.org/10.1021/acs.jmedchem.8b00420] [PMID: 29746127]
[65]
Bua, S.; Lucarini, L.; Micheli, L.; Menicatti, M.; Bartolucci, G.; Selleri, S.; Di Cesare Mannelli, L.; Ghelardini, C.; Masini, E.; Carta, F.; Gratteri, P.; Nocentini, A.; Supuran, C.T. Bioisosteric development of multitarget nonsteroidal anti-inflammatory drug-carbonic anhydrases inhibitor hybrids for the management of rheumatoid arthritis. J. Med. Chem., 2020, 63(5), 2325-2342.
[http://dx.doi.org/10.1021/acs.jmedchem.9b01130] [PMID: 31689108]
[http://dx.doi.org/10.1021/acs.jmedchem.9b01130] [PMID: 31689108]
[66]
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]
[http://dx.doi.org/10.1517/13543776.2013.794788] [PMID: 23627893]
[67]
Supuran, C.T. Inhibition of carbonic anhydrase IX as a novel anticancer mechanism. World J. Clin. Oncol., 2012, 3(7), 98-103.
[http://dx.doi.org/10.5306/wjco.v3.i7.98] [PMID: 22787577]
[http://dx.doi.org/10.5306/wjco.v3.i7.98] [PMID: 22787577]
[68]
Supuran, C.T. Exploring the multiple binding modes of inhibitors to carbonic anhydrases for novel drug discovery. Expert Opin. Drug Discov., 2020, 15(6), 671-686.
[http://dx.doi.org/10.1080/17460441.2020.1743676] [PMID: 32208982]
[http://dx.doi.org/10.1080/17460441.2020.1743676] [PMID: 32208982]
[69]
van Kuijk, S.J.; Gieling, R.G.; Niemans, R.; Lieuwes, N.G.; Biemans, R.; Telfer, B.A.; Haenen, G.R.; Yaromina, A.; Lambin, P.; Dubois, L.J.; Williams, K.J. The sulfamate small molecule CAIX inhibitor S4 modulates doxorubicin efficacy. PLoS One, 2016, 11(8), e0161040.
[http://dx.doi.org/10.1371/journal.pone.0161040] [PMID: 27513947]
[http://dx.doi.org/10.1371/journal.pone.0161040] [PMID: 27513947]
[70]
Dik, B.; Coskun, D.; Bahcivan, E.; Er, A. Doxycycline and meloxicam can treat neuroinflammation by increasing activity of antioxidant enzymes in rat brain. Pak. J. Pharm. Sci., 2019, 32(1(Special)), 391-396.
[PMID: 30852475]
[PMID: 30852475]
[71]
Er, A.; Coskun, D.; Bahcivan, E.; Dik, B. Effect of doxycycline and meloxicam on cytokines, brain-derived neurotrophic factor, matrix metalloproteinase-3, tissue inhibitor of metalloproteinase-3 and cyclooxygenase-2 in brain. Iran. J. Basic Med. Sci., 2020, 23(10), 1328-1334.
[PMID: 33149866]
[PMID: 33149866]
[72]
Faki, Y.; Er, A. Different chemical structures and physiological/pathological roles of cyclooxygenases. Rambam Maimonides Med. J., 2021, 12(1), e0003.
[http://dx.doi.org/10.5041/RMMJ.10426] [PMID: 33245277]
[http://dx.doi.org/10.5041/RMMJ.10426] [PMID: 33245277]
[73]
Grösch, S.; Maier, T.J.; Schiffmann, S.; Geisslinger, G. Cyclooxygenase-2 (COX-2)-independent anticarcinogenic effects of selective COX-2 inhibitors. J. Natl. Cancer Inst., 2006, 98(11), 736-747.
[http://dx.doi.org/10.1093/jnci/djj206] [PMID: 16757698]
[http://dx.doi.org/10.1093/jnci/djj206] [PMID: 16757698]
[74]
Viegas-Junior, C.; Danuello, A.; da Silva Bolzani, V.; Barreiro, E.J.; Fraga, C.A.M. Molecular hybridization: A useful tool in the design of new drug prototypes. Curr. Med. Chem., 2007, 14(17), 1829-1852.
[http://dx.doi.org/10.2174/092986707781058805] [PMID: 17627520]
[http://dx.doi.org/10.2174/092986707781058805] [PMID: 17627520]
[75]
Micheli, L.; Bozdag, M.; Akgul, O.; Carta, F.; Guccione, C.; Bergonzi, M.C.; Bilia, A.R.; Cinci, L.; Lucarini, E.; Parisio, C.; Supuran, C.T.; Ghelardini, C.; Di Cesare Mannelli, L. Pain relieving effect of-NSAIDs-CAIs hybrid molecules: Systemic and intra-articular treatments against rheumatoid arthritis. Int. J. Mol. Sci., 2019, 20(8), 1923.
[http://dx.doi.org/10.3390/ijms20081923] [PMID: 31003542]
[http://dx.doi.org/10.3390/ijms20081923] [PMID: 31003542]
[76]
Aspatwar, A.; Berrino, E.; Bua, S.; Carta, F.; Capasso, C.; Parkkila, S.; Supuran, C.T. Toxicity evaluation of sulfamides and coumarins that efficiently inhibit human carbonic anhydrases. J. Enzyme Inhib. Med. Chem., 2020, 35(1), 1765-1772.
[http://dx.doi.org/10.1080/14756366.2020.1822829] [PMID: 32942905]
[http://dx.doi.org/10.1080/14756366.2020.1822829] [PMID: 32942905]
[77]
Türkan, F.; Huyut, Z.; Taslimi, P. Gülçin, İ The in vivo effects of cefazolin, cefuroxime, and cefoperazon on the carbonic anhydrase in different rat tissues. J. Biochem. Mol. Toxicol., 2018, 32(3), e22041.
[http://dx.doi.org/10.1002/jbt.22041] [PMID: 29457666]
[http://dx.doi.org/10.1002/jbt.22041] [PMID: 29457666]
[78]
Ničković V.P.; Mitić N.R.; Krdžić B.D.; Krdžić J.D.; Nikolić G.R.; Vasić M.Z.; Ranković G.; Babović P.; Sokolović D.; Veselinović A.M. Design and development of novel therapeutics for brucellosis treatment based on carbonic anhydrase inhibition. J. Biomol. Struct. Dyn., 2020, 38(6), 1848-1857.
[PMID: 31096856]
[PMID: 31096856]
Article Metrics
1