1,705
Views
31
CrossRef citations to date
0
Altmetric
Research Paper

Psychoactive substances belonging to the amphetamine class potently activate brain carbonic anhydrase isoforms VA, VB, VII, and XII

, , , &
Pages 1253-1259 | Received 28 Aug 2017, Accepted 31 Aug 2017, Published online: 22 Sep 2017

References

  • (a) European Drug report 2016: Trends and Developments. European Monitoring Centre for Drugs and drug Addicion (EMCDDA). Available from: http://www.emcdda.europa.eu/system/files/publications/2637/TDAT16001ENN.pdf.(b) European Drug report 2015: Trends and Developments. European Monitoring Centre for Drugs and drug Addicion (EMCDDA). Available from: http://www.emcdda.europa.eu/system/files/publications/974/TDAT15001ENN.pdf.
  • Bertol E, Pascali J, Palumbo D, et al. 3-MeO-PCP intoxication in two young men: first in vivo detection in Italy. Forensic Sci Int 2017;274:7–12.
  • Bertol E, Vaiano F, Mari F, et al. Advances in new psychoactive substances identification: the U.R.I.To.N. Consortium. J Enzyme Inhib Med Chem 2017;32:841–9.
  • 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.
  • 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.
  • Temperini C, Scozzafava A, Supuran CT. Carbonic anhydrase activation and the drug design. Curr Pharm Des 2008;14:708–15.
  • 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.
  • Supuran CT. Carbonic anhydrases: from biomedical applications of the inhibitors and activators to biotechnological use for CO(2) capture. J Enzyme Inhib Med Chem 2013;28:229–30.
  • Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov 2017;12:61–88.
  • Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32.
  • Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81.
  • Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60.
  • Leiner M, Leiner G. Die Aktivatoren der Kohlensäureanhydrase. Naturwiss 1941;29:195–7.
  • Leiner M, Leiner G. Die Messmethoden zur Untersuchung der katalytischen Wirksamkeit der Kohlensäureanhydrase. Biochem Z 1941;311:119–45.
  • Main RE, Locke A. Activation of carbonic anhydrase by histamine. J Biol Chem 1941;140:LXXXI.
  • Kiese M. Die Aktivierung der Kohlensäureanhydrase. Naturwiss 1941;29:116–17.
  • (a) 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. (b) 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • Scozzafava A, Supuran CT. Carbonic anhydrase activators: high affinity isozymes I, II, and IV activators, incorporating a beta-alanyl-histidine scaffold. J Med Chem 2002;45:284–91.
  • (a) Ilies M, Banciu MD, Ilies MA, et al. Carbonic anhydrase activators: design of high affinity isozymes I, II, and IV activators, incorporating tri-/tetrasubstituted-pyridinium-azole moieties. J Med Chem 2002;45:504–10.(b) Supuran CT, Scozzafava A. Carbonic anhydrase activators: amino acyl/dipeptidyl histamine derivatives bind with high affinity to isozymes I, II and IV and act as efficient activators. Bioorg Med Chem 1999;7:2915–23.
  • 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.
  • (a) 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.(b) 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.
  • Sun MK, Alkon DL. Carbonic anhydrase gating of attention: memory therapy and enhancement. Trends Pharmacol Sci 2002;23:83–9.
  • 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.
  • Khalifah RG. The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. J Biol Chem 1971;246:2561–73.
  • (a) Vullo D, Nishimori I, Scozzafava 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;18:4303–1. (b) 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.(c) 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.
  • (a) Nishimori I, Onishi S, Vullo D, et al. Carbonic anhydrase activators. The first activation study of the human secretory isoform VI. Bioorg Med Chem 2007;15:5351–7.(b) 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.(c) 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.
  • Le Duc Y, Licsandru E, Vullo D, et al. Carbonic anhydrases activation with 3-amino-1H-1,2,4-triazole-1-carboxamides: discovery of subnanomolar isoform II activators. Bioorg Med Chem 2017;25:1681–6.
  • Licsandru E, Tanc M, Kocsis I, et al. A class of carbonic anhydrase I – selective activators. J Enzyme Inhib Med Chem 2017;32:37–46.
  • Zhang Y, Legrand YM, Petit E, et al. Dynamic encapsulation and activation of carbonic anhydrase in multivalent dynameric host matrices. Chem Commun (Camb) 2016;52:4053–5.
  • Abdelrahim MY, Tanc M, Winum JY, et al. Dominant behaviours in the expression of human carbonic anhydrase hCA I activity. Chem Commun (Camb) 2014;50:8043–6.
  • (a) Heal DJ, Smith SL, Gosden J, Nutt DJ. Amphetamine, past and present – a pharmacological and clinical perspective. J Psychopharmacol 2013;27:479–96.(b) Bidwell LC, McClernon FJ, Kollins SH. Cognitive enhancers for the treatment of ADHD. Pharmacol Biochem Behav 2011;99:262–74.
  • (a) Brams M, Mao AR, Doyle RL. Onset of efficacy of long-acting psychostimulants in pediatric attention-deficit/hyperactivity disorder. Postgrad Med 2008;120:69–88.(b) Forray A, Sofuoglu M. Future pharmacological treatments for substance use disorders. Br J Clin Pharmacol 2014;77:382–400.(c) Wilens TE, Adler LA, Adams J, et al. Misuse and diversion of stimulants prescribed for ADHD: a systematic review of the literature. J Am Acad Child Adolesc Psychiatry 2008;47:21–31.
  • Rogge G, Jones D, Hubert GW, et al. CART peptides: regulators of body weight, reward and other functions. Nat Rev Neurosci 2008;9:747–58.
  • (a) Jing L, Li JX. Trace amine-associated receptor 1: a promising target for the treatment of psychostimulant addiction. Eur J Pharmacol 2015;761:345–52.(b) Miller GM. The emerging role of trace amine-associated receptor 1 in the functional regulation of monoamine transporters and dopaminergic activity. J Neurochem 2011;116:164–76.(c) Borowsky B, Adham N, Jones KA, et al. Trace amines: identification of a family of mammalian G protein-coupled receptors. Proc Natl Acad Sci USA 2001;98:8966–71.
  • Malenka RC, Nestler EJ, Hyman SE. Higher cognitive function and behavioral control. In: Sydor A, Brown RY, eds. Molecular neuropharmacology: a foundation for clinical neuroscience. 2nd ed. New York (NY): McGraw-Hill Medical; 2009:318–21.
  • Spencer RC, Devilbiss DM, Berridge CW. The cognition-enhancing effects of psychostimulants involve direct action in the prefrontal cortex. Biol Psychiatry 2015;77:940–50.
  • Carvalho M, Carmo H, Costa VM, et al. Toxicity of amphetamines: an update. Arch Toxicol 2012;86:1167–231.
  • (a) Pan PW, Parkkila AK, Autio S, et al. Brain phenotype of carbonic anhydrase IX-deficient mice. Transgenic Res 2012;21:163–76.(b) Hilvo M, Supuran CT, Parkkila S. Characterization and inhibition of the recently discovered carbonic anhydrase isoforms CA XIII, XIV and XV. Curr Top Med Chem 2007;7:893–9.
  • (a) 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.(b) Parkkila S, Parkkila AK, Rajaniemi H, et al. Expression of membrane-associated carbonic anhydrase XIV on neurons and axons in mouse and human brain. Proc Natl Acad Sci USA 2001;98:1918–23.(c) Ghandour MS, Parkkila AK, Parkkila S, et al. Mitochondrial carbonic anhydrase in the nervous system: expression in neuronal and glial cells. J Neurochem 2000;75:2212–20.
  • (a) Thiry A, Dognè JM, Masereel B, Supuran CT. Carbonic anhydrase inhibitors as anticonvulsant agents. Curr Top Med Chem 2007;7:855–64.(b) Supuran CT. Acetazolamide for the treatment of idiopathic intracranial hypertension. Expert Rev Neurother 2015;15:851–6.
  • (a) Carta F, Di Cesare ML, Pinard M, et al. A class of sulfonamide carbonic anhydrase inhibitors with neuropathic pain modulating effects. Bioorg Med Chem 2015;23:1828–40.(b) Supuran CT. Carbonic anhydrase inhibition and the management of neuropathic pain. Expert Rev Neurother 2016;16:961–8.
  • (a) Ruusuvuori E, Li H, Huttu K, et al. Carbonic anhydrase isoform VII acts as a molecular switch in the development of synchronous gamma-frequency firing of hippocampal CA1 pyramidal cells. J Neurosci 2004;24:2699–707.(b) Ruusuvuori E, Huebner AK, Kirilkin I, et al. Neuronal carbonic anhydrase VII provides GABAergic excitatory drive to exacerbate febrile seizures. EMBO J 2013;32:2275–86.
  • (a) Scozzafava A, Supuran CT, Carta F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin Ther Pat 2013;23:725–35.(b) Supuran CT. Carbonic anhydrase inhibitors as emerging drugs for the treatment of obesity. Expert Opin Emerg Drugs 2012;17:11–15.
  • Briganti F, Pierattelli R, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. Part 37. Novel classes of isozyme I and II inhibitors and their mechanism of action. Kinetic and spectroscopic investigations on native and cobalt-substituted enzymes. Eur J Med Chem 1996;31:1001–10.
  • Supuran CT, Clare BW. Carbonic anhydrase inhibitors–Part 57: quantum chemical QSAR of a group of 1,3,4-thiadiazole-and 1,3,4-thiadiazoline disulfonamides with carbonic anhydrase inhibitory properties. Eur J Med Chem 1999;34:41–50.
  • 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.
  • Masini E, Carta F, Scozzafava A, Supuran CT. Antiglaucoma carbonic anhydrase inhibitors: a patent review. Expert Opin Ther Pat 2013;23:705–16.
  • Puccetti L, Fasolis G, Vullo D, et al. Carbonic anhydrase inhibitors. Inhibition of cytosolic/tumor-associated carbonic anhydrase isozymes I, II, IX, and XII with Schiff’s bases incorporating chromone and aromatic sulfonamide moieties, and their zinc complexes. Bioorg Med Chem Lett 2005;15:3096–101.
  • Monti SM, Supuran CT, De Simone G. Anticancer carbonic anhydrase inhibitors: a patent review (2008–2013). Expert Opin Ther Pat 2013;23:737–49.
  • Scozzafava A, Menabuoni L, Mincione F, Supuran CT. Carbonic anhydrase inhibitors. A general approach for the preparation of water-soluble sulfonamides incorporating polyamino–polycarboxylate tails and of their metal complexes possessing long-lasting, topical intraocular pressure-lowering properties. J Med Chem 2002;45:1466–76.
  • Garaj V, Puccetti L, Fasolis G, et al. Carbonic anhydrase inhibitors: novel sulfonamides incorporating 1,3,5-triazine moieties as inhibitors of the cytosolic and tumour-associated carbonic anhydrase isozymes I, II and IX. Bioorg Med Chem Lett 2005;15:3102–8.
  • Carta F, Supuran CT. Diuretics with carbonic anhydrase inhibitory action: a patent and literature review (2005–2013)). Expert Opin Ther Pat 2013;23:681–91.
  • Supuran CT, Nicolae A, Popescu A. Carbonic anhydrase inhibitors. Part 35. Synthesis of Schiff bases derived from sulfanilamide and aromatic aldehydes: the first inhibitors with equally high affinity towards cytosolic and membrane-bound isozymes. Eur J Med Chem 1996;31:431–8.
  • Fabrizi F, Mincione F, Somma T, et al. A new approach to antiglaucoma drugs: carbonic anhydrase inhibitors with or without NO donating moieties. Mechanism of action and preliminary pharmacology. J Enzyme Inhib Med Chem 2015;27:138–47.
  • 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.
  • Dubois L, Peeters S, Lieuwes NG, et al. Specific inhibition of carbonic anhydrase IX activity enhances the in vivo therapeutic effect of tumor irradiation. Radiother Oncol 2011;99:424–31.
  • Carta F, Scozzafava A, Supuran CT. Sulfonamides: a patent review (2008–2012)). Expert Opin Ther Pat 2012;22:747–58.