Neuronal nicotinic receptors as new targets for amphetamine-induced oxidative damage and neurotoxicity

Pharmaceuticals

Volumn 4, Issue 6, 2011, Pages 822-847

  Pubill, David ^a   Garcia Ratés, Sara ^a   Camarasa, Jordi ^a   Escubedo, Elena ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Calcium influx; Mdma; Methamphetamine; Neuroprotection; Nicotinic

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; AMPHETAMINE DERIVATIVE; BUNGAROTOXIN RECEPTOR; CALCIUM ION; CALPAIN; CASPASE 3; DOPAMINE TRANSPORTER; MEMANTINE; METHAMPHETAMINE; METHYLLYCACONITINE; NICOTINIC RECEPTOR; NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN METABOLITE; VESICULAR MONOAMINE TRANSPORTER;

BRAIN ELECTROPHYSIOLOGY; BRAIN SYNAPTOSOME; CALCIUM TRANSPORT; CELL MEMBRANE; COGNITIVE DEFECT; DRUG ABUSE; DRUG MECHANISM; ENZYME ACTIVATION; HUMAN; LIGAND BINDING; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; RECEPTOR BINDING; REVIEW; UPREGULATION;

EID: 79959294275     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph4060822     Document Type: Review

References (128)

1. Capela, J.P.; Carmo, H.; Remiao, F.; Bastos, M.L.; Meisel, A.; Carvalho, F. Molecular and cellular mechanisms of ecstasy-induced neurotoxicity: An overview. Mol. Neurobiol. 2009, 39, 210-271.
2. Krasnova, I.N.; Cadet, J.L. Methamphetamine toxicity and messengers of death. Brain Res. Rev. 2009, 60, 379-407.
3. Lyles, J.; Cadet, J.L. Methylenedioxymethamphetamine (MDMA, Ecstasy) neurotoxicity: Cellular and molecular mechanisms. Brain Res. Rev. 2003, 42, 155-168.
4. Thrash, B.; Karuppagounder, S.S.; Uthayathas, S.; Suppiramaniam, V.; Dhanasekaran, M. Neurotoxic effects of methamphetamine. Neurochem. Res. 2010, 35, 171-179.
5. Karlsen, S.N.; Spigset, O.; Slordal, L. The dark side of ecstasy: Neuropsychiatric symptoms after exposure to 3,4-methylenedioxymethamphetamine. Basic Clin. Pharmacol. Toxicol. 2008, 102, 15-24.
6. McCann, U.D.; Mertl, M.; Eligulashvili, V.; Ricaurte, G.A. Cognitive performance in (+/-) 3,4-methylenedioxymethamphetamine (MDMA, "ecstasy") users: A controlled study. Psychopharmacology 1999, 143, 417-425.
7. Parrott, A.C.; Lees, A.; Garnham, N.J.; Jones, M.; Wesnes, K. Cognitive performance in recreational users of MDMA of 'ecstasy': Evidence for memory deficits. J. Psychopharmacol. 1998, 12, 79-83.
8. Reneman, L.; Endert, E.; de Bruin, K.; Lavalaye, J.; Feenstra, M.G.; de Wolff, F.A.; Booij, J. The acute and chronic effects of MDMA ("ecstasy") on cortical 5-HT2A receptors in rat and human brain. Neuropsychopharmacology 2002, 26, 387-396.
9. Rogers, G.; Elston, J.; Garside, R.; Roome, C.; Taylor, R.; Younger, P.; Zawada, A.; Somerville, M. The harmful health effects of recreational ecstasy: A systematic review of observational evidence. Health Technol. Assess. 2009, 13, iii-iv, ix-xii, 1-315.
10. Volkow, N.D.; Chang, L.; Wang, G.J.; Fowler, J.S.; Ding, Y.S.; Sedler, M.; Logan, J.; Franceschi, D.; Gatley, J.; Hitzemann, R.; et al. Low level of brain dopamine D2 receptors in methamphetamine abusers: Association with metabolism in the orbitofrontal cortex. Am. J. Psychiatry 2001, 158, 2015-2021.
11. Nulsen, C.E.; Fox, A.M.; Hammond, G.R. Differential effects of ecstasy ecstasy on short-term and working memory: A meta-analysis. Neuropsychol. Rev. 2010, 20, 21-32.
12. Ricaurte, G.A.; Guillery, R.W.; Seiden, L.S.; Schuster, C.R.; Moore, R.Y. Dopamine nerve terminal degeneration produced by high doses of methylamphetamine in the rat brain. Brain Res. 1982, 235, 93-103.
13. Ellison, G.; Eison, M.S.; Huberman, H.S.; Daniel, F. Long-term changes in dopaminergic innervation of caudate nucleus after continuous amphetamine administration. Science 1978, 201, 276-278.
14. Hotchkiss, A.J.; Gibb, J.W. Long-term effects of multiple doses of methamphetamine on tryptophan hydroxylase and tyrosine hydroxylase activity in rat brain. J. Pharmacol. Exp. Ther. 1980, 214, 257-262.
15. Escubedo, E.; Guitart, L.; Sureda, F.X.; Jimenez, A.; Pubill, D.; Pallas, M.; Camins, A.; Camarasa, J. Microgliosis and down-regulation of adenosine transporter induced by methamphetamine in rats. Brain Res. 1998, 814, 120-126.
16. Ricaurte, G.A.; Seiden, L.S.; Schuster, C.R. Further evidence that amphetamines produce long-lasting dopamine neurochemical deficits by destroying dopamine nerve fibers. Brain Res. 1984, 303, 359-364.
17. Pubill, D.; Canudas, A.M.; Pallas, M.; Camins, A.; Camarasa, J.; Escubedo, E. Different glial response to methamphetamine- and methylenedioxymethamphetamine-induced neurotoxicity. Naunyn Schmiedebergs Arch. Pharmacol. 2003, 367, 490-499.
18. Quinton, M.S.; Yamamoto, B.K. Causes and consequences of methamphetamine and MDMA toxicity. AAPS J. 2006, 8, E337-E347.
19. Stone, D.M.; Hanson, G.R.; Gibb, J.W. Differences in the central serotonergic effects of methylenedioxymethamphetamine (MDMA) in mice and rats. Neuropharmacology 1987, 26, 1657-1661.
20. Riddle, E.L.; Fleckenstein, A.E.; Hanson, G.R. Mechanisms of methamphetamine-induced dopaminergic neurotoxicity. AAPS J. 2006, 8, E413-E418.
21. Gibb, J.W.; Stone, D.M.; Johnson, M.; Hanson, G.R. Role of dopamine in the neurotoxicity induced by amphetamines and related designer drugs. NIDA Res. Monogr. 1989, 94, 161-178.
22. Chiueh, C.C.; Miyake, H.; Peng, M.T. Role of dopamine autoxidation, hydroxyl radical generation, and calcium overload in underlying mechanisms involved in MPTP-induced parkinsonism. Adv. Neurol. 1993, 60, 251-258.
23. Garthwaite, J.; Boulton, C.L. Nitric oxide signaling in the central nervous system. Annu. Rev. Physiol. 1995, 57, 683-706.
24. Nash, J.F.; Yamamoto, B.K. Methamphetamine neurotoxicity and striatal glutamate release: Comparison to 3,4-methylenedioxymethamphetamine. Brain Res. 1992, 581, 237-243.
25. Wang, J.Q.; Lau, Y.S. Dose-related alteration in nitric oxide synthase mRNA expression induced by amphetamine and the full D1 dopamine receptor agonist SKF-82958 in mouse striatum. Neurosci. Lett. 2001, 311, 5-8.
26. Guilarte, T.R.; Nihei, M.K.; McGlothan, J.L.; Howard, A.S. Methamphetamine-induced deficits of brain monoaminergic neuronal markers: Distal axotomy or neuronal plasticity. Neuroscience 2003, 122, 499-513.
27. Thomas, D.M.; Walker, P.D.; Benjamins, J.A.; Geddes, T.J.; Kuhn, D.M. Methamphetamine neurotoxicity in dopamine nerve endings of the striatum is associated with microglial activation. J. Pharmacol. Exp. Ther. 2004, 311, 1-7.
28. Monks, T.J.; Jones, D.C.; Bai, F.; Lau, S.S. The role of metabolism in 3,4-(+)-methylenedioxyamphetamine and 3,4-(+)-methylenedioxymethamphetamine (ecstasy) toxicity. Ther. Drug Monit. 2004, 26, 132-136.
29. Pubill, D.; Chipana, C.; Camins, A.; Pallas, M.; Camarasa, J.; Escubedo, E. Free radical production induced by methamphetamine in rat striatal synaptosomes. Toxicol. Appl. Pharmacol. 2005, 204, 57-68.
30. Gotti, C.; Moretti, M.; Gaimarri, A.; Zanardi, A.; Clementi, F.; Zoli, M. Heterogeneity and complexity of native brain nicotinic receptors. Biochem. Pharmacol. 2007, 74, 1102-1111.
31. Hogg, R.C.; Raggenbass, M.; Bertrand, D. Nicotinic acetylcholine receptors: From structure to brain function. Rev. Physiol. Biochem. Pharmacol. 2003, 147, 1-46.
32. Taly, A.; Corringer, P.J.; Guedin, D.; Lestage, P.; Changeux, J.P. Nicotinic receptors: Allosteric transitions and therapeutic targets in the nervous system. Nat. Rev. Drug Discov. 2009, 8, 733-750.
33. Le, N.N.; Corringer, P.J.; Changeux, J.P. The diversity of subunit composition in nAChRs: Evolutionary origins, physiologic and pharmacologic consequences. J. Neurobiol. 2002, 53, 447-456.
34. Gotti, C.; Clementi, F. Neuronal nicotinic receptors: From structure to pathology. Prog. Neurobiol. 2004, 74, 363-396.
35. 2+ permeability of nicotinic acetylcholine receptors. Cell Calcium 2004, 35, 1-8.
36. Jatzke, C.; Watanabe, J.; Wollmuth, L.P. Voltage and concentration dependence of Ca(2+) permeability in recombinant glutamate receptor subtypes. J. Physiol. 2002, 538, 25-39.
37. Dajas-Bailador, F.; Wonnacott, S. Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends Pharmacol. Sci. 2004, 25, 317-324.
38. Deng, X.; Cadet, J.L. Methamphetamine administration causes overexpression of nNOS in the mouse striatum. Brain Res. 1999, 851, 254-257.
39. Kramer, H.K.; Poblete, J.C.; Azmitia, E.C. Activation of protein kinase C (PKC) by 3,4-methylenedioxymethamphetamine (MDMA) occurs through the stimulation of serotonin receptors and transporter. Neuropsychopharmacology 1997, 17, 117-129.
40. Jensen, A.A.; Frolund, B.; Liljefors, T.; Krogsgaard-Larsen, P. Neuronal nicotinic acetylcholine receptors: Structural revelations, target identifications, and therapeutic inspirations. J. Med. Chem. 2005, 48, 4705-4745.
41. Champtiaux, N.; Changeux, J.P. Knock-out and knock-in mice to investigate the role of nicotinic receptors in the central nervous system. Curr. Drug Targets CNS Neurol. Disord. 2002, 1, 319-330.
42. Drago, J.; McColl, C.D.; Horne, M.K.; Finkelstein, D.I.; Ross, S.A. Neuronal nicotinic receptors: Insights gained from gene knockout and knockin mutant mice. Cell Mol. Life Sci. 2003, 60, 1267-1280.
43. Picciotto, M.R.; Caldarone, B.J.; King, S.L.; Zachariou, V. Nicotinic receptors in the brain. Links between molecular biology and behavior. Neuropsychopharmacology 2000, 22, 451-465.
44. Picciotto, M.R.; Caldarone, B.J.; Brunzell, D.H.; Zachariou, V.; Stevens, T.R.; King, S.L. Neuronal nicotinic acetylcholine receptor subunit knockout mice: Physiological and behavioral phenotypes and possible clinical implications. Pharmacol. Ther. 2001, 92, 89-108.
45. Dani, J.A.; Harris, R.A. Nicotine addiction and comorbidity with alcohol abuse and mental illness. Nat. Neurosci. 2005, 8, 1465-1470.
46. Hom, D.G.; Jiang, D.; Hong, E.J.; Mo, J.Q.; Andersen, J.K. Elevated expression of glutathione peroxidase in PC12 cells results in protection against methamphetamine but not MPTP toxicity. Brain Res. Mol. Brain Res. 1997, 46, 154-160.
47. Jayanthi, S.; Ladenheim, B.; Andrews, A.M.; Cadet, J.L. Overexpression of human copper/zinc superoxide dismutase in transgenic mice attenuates oxidative stress caused by methylenedioxymethamphetamine (Ecstasy). Neuroscience 1999, 91, 1379-1387.
48. Maragos, W.F.; Jakel, R.; Chesnut, D.; Pocernich, C.B.; Butterfield, D.A.; St. Clair, D.; Cass, W.A. Methamphetamine toxicity is attenuated in mice that overexpress human manganese superoxide dismutase. Brain Res. 2000, 878, 218-222.
49. Imam, S.Z.; Ali, S.F. Selenium, an antioxidant, attenuates methamphetamine-induced dopaminergic toxicity and peroxynitrite generation. Brain Res. 2000, 855, 186-191.
50. Imam, S.Z.; El-Yazal, J.; Newport, G.D.; Itzhak, Y.; Cadet, J.L.; Slikker, W., Jr.; Ali, S.F. Methamphetamine-induced dopaminergic neurotoxicity: Role of peroxynitrite and neuroprotective role of antioxidants and peroxynitrite decomposition catalysts. Ann. N.Y. Acad. Sci. 2001, 939, 366-380.
51. Virmani, A.; Gaetani, F.; Imam, S.; Binienda, Z.; Ali, S. The protective role of L-carnitine against neurotoxicity evoked by drug of abuse, methamphetamine, could be related to mitochondrial dysfunction. Ann. N.Y. Acad. Sci. 2002, 965, 225-232.
52. Fukami, G.; Hashimoto, K.; Koike, K.; Okamura, N.; Shimizu, E.; Iyo, M. Effect of antioxidant N-acetyl-L-cysteine on behavioral changes and neurotoxicity in rats after administration of methamphetamine. Brain Res. 2004, 1016, 90-95.
53. Pubill, D.; Verdaguer, E.; Sureda, F.X.; Camins, A.; Pallas, M.; Camarasa, J.; Escubedo, E. Carnosine prevents methamphetamine-induced gliosis but not dopamine terminal loss in rats. Eur. J. Pharmacol. 2002, 448, 165-168.
54. Seiden, L.S.; Lew, R.; Malberg, J.E. Neurotoxicity of methamphetamine and methylenedioxymethamphetamine. Neurotox. Res. 2001, 3, 101-116.
55. Tata, D.A.; Raudensky, J.; Yamamoto, B.K. Augmentation of methamphetamine-induced toxicity in the rat striatum by unpredictable stress: Contribution of enhanced hyperthermia. Eur. J. Neurosci. 2007, 26, 739-748.
56. Bowyer, J.F.; Davies, D.L.; Schmued, L.; Broening, H.W.; Newport, G.D.; Slikker, W., Jr.; Holson, R.R. Further studies of the role of hyperthermia in methamphetamine neurotoxicity. J. Pharmacol. Exp. Ther. 1994, 268, 1571-1580.
57. Ali, S.F.; Newport, G.D.; Slikker, W., Jr. Methamphetamine-induced dopaminergic toxicity in mice. Role of environmental temperature and pharmacological agents. Ann. N.Y. Acad. Sci. 1996, 801, 187-198.
58. O'Callaghan, J.P.; Miller, D.B. Neurotoxicity profiles of substituted amphetamines in the C57BL/6J mouse. J. Pharmacol. Exp. Ther. 1994, 270, 741-751.
59. Kim, S.; Westphalen, R.; Callahan, B.; Hatzidimitriou, G.; Yuan, J.; Ricaurte, G.A. Toward development of an in vitro model of methamphetamine-induced dopamine nerve terminal toxicity. J. Pharmacol. Exp. Ther. 2000, 293, 625-633.
60. Hastings, T.G.; Lewis, D.A.; Zigmond, M.J. Role of oxidation in the neurotoxic effects of intrastriatal dopamine injections. Proc. Natl. Acad. Sci. USA 1996, 93, 1956-1961.
61. Stephans, S.E.; Yamamoto, B.K. Methamphetamine-induced neurotoxicity: Roles for glutamate and dopamine efflux. Synapse 1994, 17, 203-209.
62. Sulzer, D.; Rayport, S. Amphetamine and other psychostimulants reduce pH gradients in midbrain dopaminergic neurons and chromaffin granules: A mechanism of action. Neuron 1990, 5, 797-808.
63. Vatassery, G.T. Oxidation of vitamin E, vitamin C, and thiols in rat brain synaptosomes by peroxynitrite. Biochem. Pharmacol. 1996, 52, 579-586.
64. Vatassery, G.T.; Lai, J.C.; DeMaster, E.G.; Smith, W.E.; Quach, H.T. Oxidation of vitamin E and vitamin C and inhibition of brain mitochondrial oxidative phosphorylation by peroxynitrite. J. Neurosci. Res. 2004, 75, 845-853.
65. Jekabsone, A.; Ivanoviene, L.; Brown, G.C.; Borutaite, V. Nitric oxide and calcium together inactivate mitochondrial complex I and induce cytochrome c release. J. Mol. Cell Cardiol. 2003, 35, 803-809.
66. Demiryurek, A.T.; Cakici, I.; Kanzik, I. Peroxynitrite: A putative cytotoxin. Pharmacol. Toxicol. 1998, 82, 113-117.
67. Park, S.U.; Ferrer, J.V.; Javitch, J.A.; Kuhn, D.M. Peroxynitrite inactivates the human dopamine transporter by modification of cysteine 342: Potential mechanism of neurotoxicity in dopamine neurons. J. Neurosci. 2002, 22, 4399-4405.
68. Itzhak, Y.; Gandia, C.; Huang, P.L.; Ali, S.F. Resistance of neuronal nitric oxide synthase-deficient mice to methamphetamine-induced dopaminergic neurotoxicity. J. Pharmacol. Exp. Ther. 1998, 284, 1040-1047.
69. Ali, S.F.; Itzhak, Y. Effects of 7-nitroindazole, an NOS inhibitor on methamphetamine-induced dopaminergic and serotonergic neurotoxicity in mice. Ann. N.Y. Acad. Sci. 1998, 844, 122-130.
70. Colado, M.I.; Camarero, J.; Mechan, A.O.; Sanchez, V.; Esteban, B.; Elliott, J.M.; Green, A.R. A study of the mechanisms involved in the neurotoxic action of 3,4-methylenedioxymethamphetamine (MDMA, ecstasy) on dopamine neurones in mouse brain. Br. J. Pharmacol. 2001, 134, 1711-1723.
71. Darvesh, A.S.; Yamamoto, B.K.; Gudelsky, G.A. Evidence for the involvement of nitric oxide in 3,4-methylenedioxymethamphetamine-induced serotonin depletion in the rat brain. J. Pharmacol. Exp. Ther. 2005, 312, 694-701.
72. Itzhak, Y.; Martin, J.L.; Ali, S.F. nNOS inhibitors attenuate methamphetamine-induced dopaminergic neurotoxicity but not hyperthermia in mice. Neuroreport 2000, 11, 2943-2946.
73. Sanchez, V.; Zeini, M.; Camarero, J.; O'Shea, E.; Bosca, L.; Green, A.R.; Colado, M.I. The nNOS inhibitor, AR-R17477AR, prevents the loss of NF68 immunoreactivity induced by methamphetamine in the mouse striatum. J. Neurochem. 2003, 85, 515-524.
74. Imam, S.Z.; Crow, J.P.; Newport, G.D.; Islam, F.; Slikker, W., Jr.; Ali, S.F. Methamphetamine generates peroxynitrite and produces dopaminergic neurotoxicity in mice: Protective effects of peroxynitrite decomposition catalyst. Brain Res. 1999, 837, 15-21.
75. Foster, J.D.; Pananusorn, B.; Vaughan, R.A. Dopamine transporters are phosphorylated on N-terminal serines in rat striatum. J. Biol. Chem. 2002, 277, 25178-25186.
76. Giambalvo, C.T. Differential effects of amphetamine transport vs. dopamine reverse transport on particulate PKC activity in striatal synaptoneurosomes. Synapse 2003, 49, 125-133.
77. Sandoval, V.; Riddle, E.L.; Ugarte, Y.V.; Hanson, G.R.; Fleckenstein, A.E. Methamphetamine-induced rapid and reversible changes in dopamine transporter function: An in vitro model. J. Neurosci. 2001, 21, 1413-1419.
78. Zhang, L.; Coffey, L.L.; Reith, M.E. Regulation of the functional activity of the human dopamine transporter by protein kinase C. Biochem. Pharmacol. 1997, 53, 677-688.
79. Chipana, C.; Camarasa, J.; Pubill, D.; Escubedo, E. Protection against MDMA-induced dopaminergic neurotoxicity in mice by methyllycaconitine: Involvement of nicotinic receptors. Neuropharmacology 2006, 51, 885-895.
80. Escubedo, E.; Chipana, C.; Perez-Sanchez, M.; Camarasa, J.; Pubill, D. Methyllycaconitine prevents methamphetamine-induced effects in mouse striatum: Involvement of alpha7 nicotinic receptors. J. Pharmacol. Exp. Ther. 2005, 315, 658-667.
81. Chipana, C.; Garcia-Rates, S.; Camarasa, J.; Pubill, D.; Escubedo, E. Different oxidative profile and nicotinic receptor interaction of amphetamine and 3,4-methylenedioxy-methamphetamine. Neurochem. Int. 2008, 52, 401-410.
82. 2+ entry and catecholamine release via nicotinic receptor activation in bovine adrenal chromaffin cells. Eur. J. Pharmacol. 2003, 460, 9-17.
83. Skau, K.A.; Gerald, M.C. Inhibition of alpha-bungarotoxin binding to rat and mouse diaphragms by amphetamine and related nonquaternary compounds. J. Pharmacol. Exp. Ther. 1978, 205, 69-76.
84. Klingler, W.; Heffron, J.J.; Jurkat-Rott, K.; O'sullivan, G.; Alt, A.; Schlesinger, F.; Bufler, J.; Lehmann-Horn, F. 3,4-Methylenedioxymethamphetamine (ecstasy) activates skeletal muscle nicotinic acetylcholine receptors. J. Pharmacol. Exp. Ther. 2005, 314, 1267-1273.
85. Garthwaite, J. Neuronal nitric oxide synthase and the serotonin transporter get harmonious. Proc. Natl. Acad. Sci. USA 2007, 104, 7739-7740.
86. Cao, B.J.; Reith, M.E. Nitric oxide inhibits uptake of dopamine and N-methyl-4- phenylpyridinium (MPP+) but not release of MPP+ in rat C6 glioma cells expressing human dopamine transporter. Br. J. Pharmacol. 2002, 137, 1155-1162.
87. Aznar, S.; Kostova, V.; Christiansen, S.H.; Knudsen, G.M. Alpha 7 nicotinic receptor subunit is present on serotonin neurons projecting to hippocampus and septum. Synapse 2005, 55, 196-200.
88. Chipana, C.; Torres, I.; Camarasa, J.; Pubill, D.; Escubedo, E. Memantine protects against amphetamine derivatives-induced neurotoxic damage in rodents. Neuropharmacology 2008, 54, 1254-1263.
89. Chipana, C.; Camarasa, J.; Pubill, D.; Escubedo, E. Memantine prevents MDMA-induced neurotoxicity. Neurotoxicology 2008, 29, 179-183.
90. Northrop, N.A.; Smith, L.P.; Yamamoto, B.K.; Eyerman, D.J. Regulation of glutamate release by alpha7 nicotinic receptors: Differential role in methamphetamine-induced damage to dopaminergic and serotonergic terminals. J. Pharmacol. Exp. Ther. 2011, 336, 900-907.
91. Aracava, Y.; Pereira, E.F.; Maelicke, A.; Albuquerque, E.X. Memantine blocks alpha7 * nicotinic acetylcholine receptors more potently than n-methyl-D-aspartate receptors in rat hippocampal neurons. J. Pharmacol. Exp. Ther. 2005, 312, 1195-1205.
92. Unger, C.; Svedberg, M.M.; Schutte, M.; Bednar, I.; Nordberg, A. Effect of memantine on the alpha 7 neuronal nicotinic receptors, synaptophysin- and low molecular weight MAP-2 levels in the brain of transgenic mice over-expressing human acetylcholinesterase. J. Neural Transm. 2005, 112, 255-268.
93. Green, B.T.; Welch, K.D.; Gardner, D.R.; Stegelmeier, B.L.; Pfister, J.A.; Cook, D.; Davis, T.Z. A toxicokinetic comparison of norditerpenoid alkaloids from Delphinium barbeyi and D. glaucescens in cattle. J. Appl. Toxicol. 2011, 31, 20-26.
94. Pfister, J.A.; Panter, K.E.; Manners, G.D. Effective dose in cattle of toxic alkaloids from tall larkspur (Delphinium barbeyi). Vet. Hum. Toxicol. 1994, 36, 10-11.
95. Simon, N.G.; Mattick, R.P. The impact of regular ecstasy use on memory function. Addiction 2002, 97, 1523-1529.
96. Simon, S.L.; Dacey, J.; Glynn, S.; Rawson, R.; Ling, W. The effect of relapse on cognition in abstinent methamphetamine abusers. J. Subst. Abuse Treat. 2004, 27, 59-66.
97. Kovacs, G.G.; Ando, R.D.; Adori, C.; Kirilly, E.; Benedek, A.; Palkovits, M.; Bagdy, G. Single dose of MDMA causes extensive decrement of serotoninergic fibre density without blockage of the fast axonal transport in Dark Agouti rat brain and spinal cord. Neuropathol. Appl. Neurobiol. 2007, 33, 193-203.
98. Battaglia, G.; Yeh, S.Y.; de Souza, E.B. MDMA-induced neurotoxicity: Parameters of degeneration and recovery of brain serotonin neurons. Pharmacol. Biochem. Behav. 1988, 29, 269-274.
99. Jimenez, A.; Jorda, E.G.; Verdaguer, E.; Pubill, D.; Sureda, F.X.; Canudas, A.M.; Escubedo, E.; Camarasa, J.; Camins, A.; Pallas, M. Neurotoxicity of amphetamine derivatives is mediated by caspase pathway activation in rat cerebellar granule cells. Toxicol. Appl. Pharmacol 2004, 196, 223-234.
100. Sprague, J.E.; Everman, S.L.; Nichols, D.E. An integrated hypothesis for the serotonergic axonal loss induced by 3,4-methylenedioxymethamphetamine. Neurotoxicology 1998, 19, 427-441.
101. Camarasa, J.; Marimon, J.M.; Rodrigo, T.; Escubedo, E.; Pubill, D. Memantine prevents the cognitive impairment induced by 3,4-methylenedioxymethamphetamine in rats. Eur. J. Pharmacol. 2008, 589, 132-139.
102. Camarasa, J.; Rodrigo, T.; Pubill, D.; Escubedo, E. Memantine is a useful drug to prevent the spatial and non-spatial memory deficits induced by methamphetamine in rats. Pharmacol. Res. 2010, 62, 450-456.
103. Garcia-Rates, S.; Camarasa, J.; Escubedo, E.; Pubill, D. Methamphetamine and 3,4-methylenedioxymethamphetamine interact with central nicotinic receptors and induce their up-regulation. Toxicol. Appl. Pharmacol 2007, 223, 195-205.
104. Flores, C.M.; Rogers, S.W.; Pabreza, L.A.; Wolfe, B.B.; Kellar, K.J. A subtype of nicotinic cholinergic receptor in rat brain is composed of alpha 4 and beta 2 subunits and is up-regulated by chronic nicotine treatment. Mol. Pharmacol. 1992, 41, 31-37.
105. Marks, M.J.; Burch, J.B.; Collins, A.C. Effects of chronic nicotine infusion on tolerance development and nicotinic receptors. J. Pharmacol. Exp. Ther. 1983, 226, 817-825.
106. Gaimarri, A.; Moretti, M.; Riganti, L.; Zanardi, A.; Clementi, F.; Gotti, C. Regulation of neuronal nicotinic receptor traffic and expression. Brain Res. Rev. 2007, 55, 134-143.
107. Picciotto, M.R. Nicotine as a modulator of behavior: Beyond the inverted U. Trends Pharmacol. Sci. 2003, 24, 493-499.
108. Pauly, J.R.; Marks, M.J.; Robinson, S.F.; van de Kamp, J.L.; Collins, A.C. Chronic nicotine and mecamylamine treatment increase brain nicotinic receptor binding without changing alpha 4 or beta 2 mRNA levels. J. Pharmacol. Exp. Ther. 1996, 278, 361-369.
109. Peng, X.; Gerzanich, V.; Anand, R.; Wang, F.; Lindstrom, J. Chronic nicotine treatment up-regulates alpha3 and alpha7 acetylcholine receptor subtypes expressed by the human neuroblastoma cell line SH-SY5Y. Mol. Pharmacol. 1997, 51, 776-784.
110. Blumenthal, E.M.; Conroy, W.G.; Romano, S.J.; Kassner, P.D.; Berg, D.K. Detection of functional nicotinic receptors blocked by alpha-bungarotoxin on PC12 cells and dependence of their expression on post-translational events. J. Neurosci. 1997, 17, 6094-6104.
111. Peng, X.; Gerzanich, V.; Anand, R.; Whiting, P.J.; Lindstrom, J. Nicotine-induced increase in neuronal nicotinic receptors results from a decrease in the rate of receptor turnover. Mol. Pharmacol. 1994, 46, 523-530.
112. Sallette, J.; Pons, S.; Devillers-Thiery, A.; Soudant, M.; Prado, D.C.; Changeux, J.P.; Corringer, P.J. Nicotine upregulates its own receptors through enhanced intracellular maturation. Neuron 2005, 46, 595-607.
113. Vallejo, Y.F.; Buisson, B.; Bertrand, D.; Green, W.N. Chronic nicotine exposure upregulates nicotinic receptors by a novel mechanism. J. Neurosci. 2005, 25, 5563-5572.
114. Gopalakrishnan, M.; Molinari, E.J.; Sullivan, J.P. Regulation of human alpha4beta2 neuronal nicotinic acetylcholine receptors by cholinergic channel ligands and second messenger pathways. Mol. Pharmacol. 1997, 52, 524-534.
115. Nashmi, R.; Lester, H. Cell autonomy, receptor autonomy, and thermodynamics in nicotine receptor up-regulation. Biochem. Pharmacol. 2007, 74, 1145-1154.
116. Hansen, J.P.; Riddle, E.L.; Sandoval, V.; Brown, J.M.; Gibb, J.W.; Hanson, G.R.; Fleckenstein, A.E. Methylenedioxymethamphetamine decreases plasmalemmal and vesicular dopamine transport: Mechanisms and implications for neurotoxicity. J. Pharmacol. Exp. Ther. 2002, 300, 1093-1100.
117. Metzger, R.R.; Hanson, G.R.; Gibb, J.W.; Fleckenstein, A.E. 3-4-Methylenedioxymethamphetamineinduced acute changes in dopamine transporter function. Eur. J. Pharmacol. 1998, 349, 205-210.
118. Dickinson, J.A.; Hanrott, K.E.; Mok, M.H.; Kew, J.N.; Wonnacott, S. Differential coupling of alpha7 and non-alpha7 nicotinic acetylcholine receptors to calcium-induced calcium release and voltage-operated calcium channels in PC12 cells. J. Neurochem. 2007, 100, 1089-1096.
119. Garcia-Rates, S.; Camarasa, J.; Sanchez-Garcia, A.I.; Gandia, L.; Escubedo, E.; Pubill, D. The effects of 3,4-methylenedioxymethamphetamine (MDMA) on nicotinic receptors: Intracellular calcium increase, calpain/caspase 3 activation, and functional upregulation. Toxicol. Appl. Pharmacol. 2010, 244, 344-353.
120. Buki, A.; Koizumi, H.; Povlishock, J.T. Moderate posttraumatic hypothermia decreases early calpain-mediated proteolysis and concomitant cytoskeletal compromise in traumatic axonal injury. Exp. Neurol. 1999, 159, 319-328.
121. Pike, B.R.; Zhao, X.; Newcomb, J.K.; Posmantur, R.M.; Wang, K.K.; Hayes, R.L. Regional calpain and caspase-3 proteolysis of alpha-spectrin after traumatic brain injury. Neuroreport 1998, 9, 2437-2442.
122. Harris, A.S.; Morrow, J.S. Proteolytic processing of human brain alpha spectrin (fodrin): Identification of a hypersensitive site. J. Neurosci. 1988, 8, 2640-2651.
123. Wang, K.K. Calpain and caspase: Can you tell the difference? Trends Neurosci. 2000, 23, 20-26.
124. Zhang, Z.; Larner, S.F.; Liu, M.C.; Zheng, W.; Hayes, R.L.; Wang, K.K. Multiple alphaII-spectrin breakdown products distinguish calpain and caspase dominated necrotic and apoptotic cell death pathways. Apoptosis 2009, 14, 1289-1298.
125. Degenhardt, L.; Bruno, R.; Topp, L. Is ecstasy a drug of dependence? Drug Alcohol Depend. 2010, 107, 1-10.
126. Levi, M.S.; Borne, R.F. A review of chemical agents in the pharmacotherapy of addiction. Curr. Med. Chem. 2002, 9, 1807-1818.
127. Upreti, V.V.; Eddington, N.D. Fluoxetine pretreatment effects pharmacokinetics of 3,4-methylenedioxymethamphetamine (MDMA, ECSTASY) in rat. J. Pharm. Sci. 2008, 97, 1593-1605.
128. Johansen, P.O.; Krebs, T.S. How could MDMA (ecstasy) help anxiety disorders? A neurobiological rationale. J. Psychopharmacol. 2009, 23, 389-391.