429
Views
45
CrossRef citations to date
0
Altmetric
Review

Applications of carbonic anhydrases inhibitors in renal and central nervous system diseases

Pages 713-721 | Received 17 May 2018, Accepted 24 Aug 2018, Published online: 10 Sep 2018

References

  • Supuran CT. Structure and function of carbonic anhydrases. Biochem J. 2016;473:2023–2032.
  • 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;30:325–332.
  • Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nature Rev Drug Discov. 2008;7:168–181.
  • Scozzafava A, Mastrolorenzo A, Supuran CT. Carbonic anhydrase inhibitors and activators and their use in therapy. Expert Opinion on Therapeutic Patents. 2006;16:1627–1664.
  • Aggarwal M, McKenna R. Update on carbonic anhydrase inhibitors: a patent review (2008–2011). Expert Opin Ther Pat. 2012;22:903–915.
  • 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;112:4421–4468.
  • 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;31:345–360.
  • Carta F, Supuran CT. Diuretics with carbonic anhydrase inhibitory action: a patent and literature review (2005–2013). Expert Opin Ther Pat. 2013;23:681–691.
  • Masini E, Carta F, Scozzafava A, et al. Antiglaucoma carbonic anhydrase inhibitors: a patent review. Expert Opin Ther Pat. 2013;23:705–716.
  • Scozzafava A, Supuran CT, Carta F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin Ther Pat. 2013;23:725–735.
  • Supuran CT. Carbonic anhydrases and metabolism. Metabolites. 2018;8:E25.
  • Monti SM, Supuran CT, De Simone G. Anticancer carbonic anhydrase inhibitors: a patent review (2008–2013). Expert Opin Ther Pat. 2013;23:737–749.
  • Supuran CT, Scozzafava A. Carbonic anhydrase inhibitors and their therapeutic potential. Expert Opin Ther Pat. 2000;10:575–600.
  • Supuran CT. Structure-based drug discovery of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2012;27:759–772.
  • Maren TH. Carbonic anhydrase: chemistry, physiology and inhibition. Physiol Rev. 1967;47:595–781.
  • Parkkila S, Parkkila AK, Kivelä J. Role of carbonic anhydrase and its inhibitors in biological science related to gastroenterology, neurology and nephrology. In: Supuran CT, Scozzafava A, Conway J, editors. Carbonic anhydrase – its inhibitors and activators. Boca Raton (FL): CRC Press; 2004. p. 281–303.
  • Maren TH. Benzolamide. A renal carbonic anhydrase inhibitor. In: Fe A, editor. Orphan drugs. New York and Basel: Marcel Dekker; 1982. p. 89–115.
  • Nawata CM, Hung CC, Tsui TK, et al. Ammonia excretion in rainbow trout (Oncorhynchus mykiss): evidence for Rh glycoprotein and H+-ATPase involvement. Physiol Genomics. 2007;31:463–474.
  • Weiner ID, Verlander JW. Renal and hepatic expression of the ammonium transporter proteins, Rh B glycoprotein and Rh C glycoprotein. Acta Physiol Scans. 2003;179:331–338.
  • Carta F, Scozzafava A, Supuran CT. Sulfonamides (RSO2NH2): a patent review 2008–2012. Expert Opin Ther Pat. 2012;22:747–758.
  • Scozzafava A, Carta F, Supuran CT. Secondary and tertiary sulfonamides: a patent review (2008–2012). Expert Opin Ther Pat. 2013;23:203–213.
  • Carta F, Supuran CT, Scozzafava A. Novel therapies for glaucoma: a patent review 2007–2011. Expert Opin Ther Pat. 2012;22:79–88.
  • Supuran CT, Scozzafava A. Benzolamide is not a membrane-impermeant carbonic anhydrase inhibitor. J Enzyme Inhib Med Chem. 2004;19:269–273.
  • Zinke M, Hanff E, Böhmer A, et al. Discovery and microassay of a nitrite-dependent carbonic anhydrase activity by stable-isotope dilution gas chromatography-mass spectrometry. Amino Acids. 2016;48:245–255.
  • Hanff E, Zinke M, Böhmer A, et al. GC-MS determination of nitrous anhydrase activity of bovine and human carbonic anhydrase II and IV. Anal Biochem. 2018;550:132–136.
  • Chobanyan-Jürgens K, Schwarz A, Böhmer A, et al. Renal carbonic anhydrases are involved in the reabsorption of endogenous nitrite. Nitric Oxide. 2012;26:126–131.
  • Tsikas D, Hanff E, Bollenbach A, et al. Results, meta-analysis and a first evaluation of UNOxR, the urinary nitrate-to-nitrite molar ratio, as a measure of nitrite reabsorption in experimental and clinical settings. Amino Acids. 2018 May 4 Epub ahead of print] (in press). DOI:10.1007/s00726-018-2573-z
  • Van Berkel MA, Elefritz JL. Evaluating off-label uses of acetazolamide. Am J Health Syst Pharm. 2018;75:524–531.
  • Deen PMT, de Groot AIM. Methods for treating renal disorders. WO. 2015. 2015/101609.
  • Alsady M, de Groot T, Kortenoeven MLA, et al. Lithium induces aerobic glycolysis and glutaminolysis in collecting duct principal cells. Am J Physiol Renal Physiol. 2018;314:F230–F239.
  • Anderberg J, Gray J, McPherson P, et al. Method and composition for diagnosis and prognosis of renal injury and renal failure. JP2016029379. 2016.
  • Granier C, Molina F, Salvetat N, et al. Early prediction markers of diabetic nephropathy. CN106796240. 2017.
  • Geyer RR, Zhao P, Parker MD, et al. Assay and method for quantitating carbonic anhydrase activity and assessing red blood hemolysis. US2016/0355867. 2016.
  • Scozzafava A, Briganti F, Mincione G, et al. Carbonic anhydrase inhibitors: synthesis of water-soluble, aminoacyl/dipeptidyl sulfonamides possessing long-lasting intraocular pressure-lowering properties via the topical route. J Med Chem. 1999;42:3690–3700.
  • Borras J, Scozzafava A, Menabuoni L, et al. Carbonic anhydrase inhibitors: synthesis of water-soluble, topically effective intraocular pressure lowering aromatic/heterocyclic sulfonamides containing 8-quinoline-sulfonyl moieties: is the tail more important than the ring? Bioorg Med Chem. 1999;7:2397–2406.
  • Supuran C, Dedhar S, McDonald P, et al. Novel sulfonamide compounds for inhibition of metastatic tumor growth. WO021963. 2012.
  • Dorogov MV, Krasavin MY. Aromatic derivatives of sulfanilamides carbonic anhydrase II (CA II) inhibitors. Methods for production and use thereof. RU2607630. 2017.
  • Choudhary MI, Saleem M, Bhatti AS, et al. Potent inhibitors of human carbonic anhydrase II and bovine carbonic anhydrase II and their mechanism of action. US2017/0073306. 2017.
  • Snyder JP, Shi Q, Kaiser TM, et al. Carbonic anhydrase inhibitors and uses thereto. WO2016/154524. 2016.
  • Zhang Z. Arylsulfonamide compounds as carbonic anhydrase inhibitors and their therapeutic use. WO2017/004543.
  • Supuran C, Dedhar S, Carta F, et al. Carbonic anhydrase inhibitors with antimetastatic activity. WO070024. 2012.
  • Supuran CT, Parkkila S. Treatment of mammalian disorders mediated by alpha-carbonic anhydrase isoforms. JP20160203758. 2016.
  • Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov. 2011;10:767–777.
  • Thiry A, Dognè JM, Masereel B, et al. Carbonic anhydrase inhibitors as anticonvulsant agents. Curr Top Med Chem. 2007;7:855–864.
  • 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;48:24–30.
  • Supuran CT. Acetazolamide for the treatment of idiopathic intracranial hypertension. Expert Rev Neurother. 2015;15:851–856.
  • Supuran CT. Carbonic anhydrase inhibition and the management of neuropathic pain. Expert Rev Neurother. 2016;16:961–968.
  • Aggarwal M, Kondeti B, McKenna R. Anticonvulsant/antiepileptic carbonic anhydrase inhibitors: a patent review. Expert Opin Ther Pat. 2013;23:717–724.
  • Hamidi S, Avoli M. Carbonic anhydrase inhibition by acetazolamide reduces in vitro epileptiform synchronization. Neuropharmacology. 2015;95:377–387.
  • Casini A, Antel J, Abbate F, et al. Carbonic anhydrase inhibitors: SAR and X-ray crystallographic study for the interaction of sugar sulfamates/sulfamides with isozymes I, II and IV. Bioorg Med Chem Lett. 2003;13:841–845.
  • De Simone G, Di Fiore A, Menchise V, et al. 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;15:2315–2320.
  • Supuran CT. Drug interaction considerations in the therapeutic use of carbonic anhydrase inhibitors. Expert Opin Drug Metab Toxicol. 2016;12:423–431.
  • Wei H, Chang X, Wang X, et al. Medicine composition for treating epilepsy. CN103301124. 2013.
  • Bowden C. Treatment of sleep apnea with combination of carbonic anhydrase inhibitor and aldosterone antagonist. US2016/0045527.
  • Wilson L, Tam P, Najarian T, et al. Treatment of obstructive sleep apnea syndrome with a combination of carbonic anhydrase inhibitor and an additional agent. IN66116DEN2012. 2015.
  • Stadelmann K, Latshang TD, Nussbaumer-Ochsner Y, et al. Impact of acetazolamide and CPAP on cortical activity in obstructive sleep apnea patients. PLoS One. 2014;9:e93931.
  • Wang K, Smith ZM, Buxton RB, et al. Acetazolamide during acute hypoxia improves tissue oxygenation in the human brain. J Appl Physiol. 2015;119:1494–1500.
  • Okazawa H, Yamauchi H, Sugimoto K, et al. Effects of acetazolamide on cerebral blood flow, blood volume, and oxygen metabolism: a positron emission tomography study with healthy volunteers. J Cereb Blood Flow Metab. 2001;21:1472–1479.
  • Li S, An L, Duan Q, et al. Determining the rate of carbonic anhydrase reaction in the human brain. Sci Rep. 2018;8:2328.
  • 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. Enzyme Inhib Med Chem. 2016;31:894–899.
  • 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;23:1828–1840.
  • Uldall M, Botfield H, Jansen-Olesen I, et al. Acetazolamide lowers intracranial pressure and modulates the cerebrospinal fluid secretion pathway in healthy rats. Neurosci Lett. 2017;645:33–39.
  • 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. [Epub ahead of print] in press. DOI:10.1002/med.21497
  • Asiedu M, Ossipov MH, Kaila K, et al. Acetazolamide and midazolam act synergistically to inhibit neuropathic pain. Pain. 2010;148:302–308.
  • Silberstein SD. Topiramate in migraine prevention: a 2016 perspective. Headache. 2017;57:165–178.
  • 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;49:7024–7031.
  • Salameh TS, Shah GN, Price TO, et al. Blood-brain barrier disruption and neurovascular unit dysfunction in diabetic mice: protection with the mitochondrial carbonic anhydrase inhibitor topiramate. J Pharmacol Exp Ther. 2016;359:452–459.
  • Price TO, Sheibani N, Shah GN. 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. 2017;1863:929–935.
  • Patrick P, Price TO, Diogo AL, et al. Topiramate protects pericytes from glucotoxicity: role for mitochondrial CA VA in cerebromicrovascular disease in diabetes. J Endocrinol Diabetes. 2015;2. pii:. http://www.symbiosisonlinepublishing.com/endocrinology-diabetes/endocrinology-diabetes23.php
  • Li M, Wang W, Mai H, et al. Methazolamide improves neurological behavior by inhibition of neuron apoptosis in subarachnoid hemorrhage mice. Sci Rep. 2016;6:35055.
  • 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.
  • Kim CW, Kim NH, Park SAH, et al. Proteinic markers for diagnosing Alzheimer’s disease. KR20120041821. 2012.
  • Leiner M, Leiner G. Die Aktivatoren der Kohlensäureanhydrase. Naturwiss. 1941;29:195–197.
  • Clark AM, Perrin DD. A re-investigation of the question of activators of carbonic anhydrase. Biochem J. 1951;48:495–503.
  • 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;36:10384–10392.
  • Supuran CT. Carbonic anhydrase activators. Future Med Chem. 2018;10:561–573.
  • Temperini C, Scozzafava A, Vullo D, et al. 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;12:7057–7066.
  • Temperini C, Scozzafava A, Puccetti L, et al. 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;15:5136–5141.
  • 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;16:5152–5156.
  • Temperini C, Scozzafava A, Vullo D, et al. 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;49:3019–3027.
  • Temperini C, Innocenti A, Scozzafava A, et al. 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;16:8373–8378.
  • 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;17:628–635.
  • Casini A, Caccia S, Scozzafava A, et al. Carbonic anhydrase activators. The selective serotonin reuptake inhibitors fluoxetine, sertraline and citalopram are strong activators of isozymes I and II. Bioorg Med Chem Lett. 2003;13:2765–2768.
  • Abdülkadir Coban T, Beydemir S, Gülcin I, et al. Sildenafil is a strong activator of mammalian carbonic anhydrase isoforms I-XIV. Bioorg Med Chem. 2009;17:5791–5795.
  • Sugimoto A, Ikeda H, Tsukamoto H, et al. Timolol activates the enzyme activities of human carbonic anhydrase I and II. Biol Pharm Bull. 2010;33:301–306.
  • 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;32:1253–1259.
  • Sun MK, Alkon DL. Carbonic anhydrase gating of attention: memory therapy and enhancement. Trends Pharmacol Sci. 2002;23:83–89.
  • Sun MK, Alkon DL. Pharmacological enhancement of synaptic efficacy, spatial learning, and memory through carbonic anhydrase activation in rats. J Pharmacol Exp Ther. 2001;297:961–967.
  • de Souza LC, 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;118:148–156.
  • Hipkiss AR. Could carnosine or related structures suppress Alzheimer’s disease? J Alzheimers Dis. 2007;11:229–240.
  • 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;60:1159–1170.
  • Supuran CT. Carbon- versus sulphur-based zinc binding groups for carbonic anhydrase inhibitors? J Enzyme Inhib Med Chem. 2018;33:485–495.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.