Abstract
Clinical and preclinical studies have indicated that chronic methamphetamine (MA) use is associated with extensive neurodegeneration, psychosis, and cognitive impairment. Evidence from animal models has suggested a considerable role of excess dopamine or glutamate, oxidative stress, neuroinflammation, and apoptosis in MA-induced neurotoxicity, and that protein kinase Cδ might mediate the interaction among these factors. In addition, the relatively long-lasting and recurrent nature of MA psychosis has been reproduced in animals treated with various dosing regimens of MA, which have shown behavioral sensitization, sociability deficits, and impaired prepulse inhibition. Genetic predisposition as well as dopaminergic and glutamatergic alterations might be important in the development of MA psychosis. Neuroimaging studies have identified functional and morphological changes related to the cognitive dysfunction shown in chronic MA users. Failure in the task-evoked phosphorylation of extracellular signal-related kinase likely underlies MA-induced memory impairment. Recent progress has suggested certain roles of oxidative stress and neuroinflammation in the psychosis and cognitive deficits induced by repeated low doses of MA. This review provides a comprehensive description of pertinent findings from human and animal studies, with an emphasis on the current understanding of the underlying mechanisms of MA neuropsychotoxicity and its relevance to Parkinson’s disease or schizophrenia.
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Abbreviations
- CaMKII:
-
Ca2+/calmodulin-dependent kinase II
- CBP:
-
CREB binding protein
- DAOA:
-
d-Amino acid oxidase activator
- DOPAC:
-
3,4-Dihydroxyphenylacetic acid
- DA:
-
Dopamine
- DARPP-32:
-
Dopamine and cAMP-regulated phosphoprotein-32
- DAT:
-
Dopamine transporter
- DTNBP1:
-
Dystrobrevin-binding protein 1
- ETC:
-
Electron transport chain
- ERK:
-
Extracellular signal-related kinase
- fMRI:
-
Functional magnetic resonance imaging
- GSH:
-
Glutathione
- GPx:
-
Glutathione peroxidase
- GLU:
-
Glutamate
- HVA:
-
Homovanillic acid
- HIV-1:
-
Human immunodeficiency virus type 1
- IFN-γ:
-
Interferon-γ
- IL-1β:
-
Interleukin-1β
- IL-6:
-
Interleukin-6
- LPS:
-
Lipopolysaccharide
- MRS:
-
Magnetic resonance spectroscopy
- mGluR5:
-
Metabotropic GLU receptor 5
- MA:
-
Methamphetamine
- 3-MT:
-
3-Methoxytyramine
- MPTP:
-
1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine
- MAPKs:
-
Mitogen-activated protein kinases
- MAO:
-
Monoamine oxidase
- NAC:
-
N-acetylcysteine
- PHOX:
-
NADPH oxidase
- NMDA:
-
N-methyl-d-aspartate
- NADPH:
-
Nicotinamide adenine dinucleotide phosphate
- NOS:
-
NO synthase
- NSAIDs:
-
Non-steroidal anti-inflammatory drugs
- NFκB:
-
Nuclear factor κB
- NAc:
-
Nucleus accumbens
- PD:
-
Parkinson’s disease
- PET:
-
Positron emission tomography
- PKC:
-
Protein kinase C
- ROS:
-
Reactive oxygen species
- SERT:
-
Serotonin transporter
- SOD:
-
Superoxide dismutase
- TUNEL:
-
Terminal deoxynucleotidyl transferase dUDP nick end labeling
- TNF-α:
-
Tumor necrosis factor-α
- TH:
-
Tyrosine hydroxylase
- TPH:
-
Tryptophan hydroxylase
- UPDRS:
-
Unified Parkinson’s Disease Rating Scale
- VMAT-2:
-
Vesicular monoamine transporter-2
References
Abekawa T, Ohmori T, Koyama T (1995) Effects of nitric oxide (NO) synthesis inhibition on the development of supersensitivity to stereotypy and locomotion stimulating effects of methamphetamine. Brain Res 679:200–204
Abekawa T, Ito K, Nakagawa S, Nakato Y, Koyama T (2008) Olanzapine and risperidone block a high dose of methamphetamine-induced schizophrenia-like behavioral abnormalities and accompanied apoptosis in the medial prefrontal cortex. Schizophr Res 101:84–94
Abekawa T, Ito K, Nakagawa S, Nakato Y, Koyama T (2011) Effects of aripiprazole and haloperidol on progression to schizophrenia-like behavioural abnormalities and apoptosis in rodents. Schizophr Res 125:77–87
Açikgöz O, Gönenç S, Kayatekin BM, Uysal N, Pekçetin C, Semin I, Güre A (1998) Methamphetamine causes lipid peroxidation and an increase in superoxide dismutase activity in the rat striatum. Brain Res 813:200–202
Adams JP, Roberson ED, English JD, Selcher JC, Sweatt JD (2000) MAPK regulation of gene expression in the central nervous system. Acta Neurobiol Exp (Wars) 60:377–394
Ajjimaporn A, Shavali S, Ebadi M, Govitrapong P (2008) Zinc rescues dopaminergic SK-N-SH cell lines from methamphetamine-induced toxicity. Brain Res Bull 77:361–366
Akiyama K (2006) Longitudinal clinical course following pharmacological treatment of methamphetamine psychosis which persists after long-term abstinence. Ann N Y Acad Sci 1074:125–134
Althobaiti YS, Almalki AH, Das SC, Alshehri FS, Sari Y (2016) Effects of repeated high-dose methamphetamine and ceftriaxone post-treatments on tissue content of dopamine and serotonin as well as glutamate and glutamine. Neurosci Lett 634:25–31
Anglin MD, Burke C, Perrochet B, Stamper E, Dawud-Noursi S (2000) History of the methamphetamine problem. J Psychoact Drugs 32:137–141
Ango F, Pin JP, Tu JC, Xiao B, Worley PF, Bockaert J, Fagni L (2000) Dendritic and axonal targeting of type 5 metabotropic glutamate receptor is regulated by homer1 proteins and neuronal excitation. J Neurosci 20:8710–8716
Arai S, Takuma K, Mizoguchi H, Ibi D, Nagai T, Takahashi K, Kamei H, Nabeshima T, Yamada K (2008) Involvement of pallidotegmental neurons in methamphetamine- and MK-801-induced impairment of prepulse inhibition of the acoustic startle reflex in mice: reversal by GABAB receptor agonist baclofen. Neuropsychopharmacology 33:3164–3175
Ares-Santos S, Granado N, Oliva I, O’Shea E, Martin ED, Colado MI, Moratalla R (2012) Dopamine D(1) receptor deletion strongly reduces neurotoxic effects of methamphetamine. Neurobiol Dis 45:810–820
Ares-Santos S, Granado N, Espadas I, Martinez-Murillo R, Moratalla R (2014) Methamphetamine causes degeneration of dopamine cell bodies and terminals of the nigrostriatal pathway evidenced by silver staining. Neuropsychopharmacology 39:1066–1080
Asanuma M, Miyazaki I, Higashi Y, Cadet JL, Ogawa N (2002) Methamphetamine-induced increase in striatal p53 DNA-binding activity is attenuated in Cu, Zn-superoxide dismutase transgenic mice. Neurosci Lett 325:191–194
Asanuma M, Tsuji T, Miyazaki I, Miyoshi K, Ogawa N (2003) Methamphetamine-induced neurotoxicity in mouse brain is attenuated by ketoprofen, a non-steroidal anti-inflammatory drug. Neurosci Lett 352:13–16
Bachmann RF, Wang Y, Yuan P, Zhou R, Li X, Alesci S, Du J, Manji HK (2009) Common effects of lithium and valproate on mitochondrial functions: protection against methamphetamine-induced mitochondrial damage. Int J Neuropsychopharmacol 12:805–822
Barbosa DJ, Capela JP, Feio-Azevedo R, Teixeira-Gomes A, Bastos Mde L, Carvalho F (2015) Mitochondria: key players in the neurotoxic effects of amphetamines. Arch Toxicol 89:1695–1725
Barr AM, Panenka WJ, MacEwan GW, Thornton AE, Lang DJ, Honer WG, Lecomte T (2006) The need for speed: an update on methamphetamine addiction. J Psychiatry Neurosci 31:301–313
Battaglia G, Fornai F, Busceti CL, Aloisi G, Cerrito F, De Blasi A, Melchiorri D, Nicoletti F (2002) Selective blockade of mGlu5 metabotropic glutamate receptors is protective against methamphetamine neurotoxicity. J Neurosci 22:2135–2141
Baucum AJ 2nd, Rau KS, Riddle EL, Hanson GR, Fleckenstein AE (2004) Methamphetamine increases dopamine transporter higher molecular weight complex formation via a dopamine- and hyperthermia-associated mechanism. J Neurosci 24:3436–3443
Baumann MH, Ayestas MA, Sharpe LG, Lewis DB, Rice KC, Rothman RB (2002) Persistent antagonism of methamphetamine-induced dopamine release in rats pretreated with GBR12909 decanoate. J Pharmacol Exp Ther 301:1190–1197
Beauvais G, Atwell K, Jayanthi S, Ladenheim B, Cadet JL (2011) Involvement of dopamine receptors in binge methamphetamine-induced activation of endoplasmic reticulum and mitochondrial stress pathways. PLoS ONE 6:e28946
Belcher AM, O’Dell SJ, Marshall JF (2005) Impaired object recognition memory following methamphetamine, but not p-chloroamphetamine- or d-amphetamine-induced neurotoxicity. Neuropsychopharmacology 30:2026–2034
Belcher AM, Feinstein EM, O’Dell SJ, Marshall JF (2008) Methamphetamine influences on recognition memory: comparison of escalating and single-day dosing regimens. Neuropsychopharmacology 33:1453–1463
Berg D, Seppi K, Behnke S, Liepelt I, Schweitzer K, Stockner H, Wollenweber F, Gaenslen A, Mahlknecht P, Spiegel J, Godau J, Huber H, Srulijes K, Kiechl S, Bentele M, Gasperi A, Schubert T, Hiry T, Probst M, Schneider V, Klenk J, Sawires M, Willeit J, Maetzler W, Fassbender K, Gasser T, Poewe W (2011) Enlarged substantia nigra hyperechogenicity and risk for Parkinson disease: a 37-month 3-center study of 1847 older persons. Arch Neurol 68(7):932–937
Bisagno V, Ferguson D, Luine VN (2002) Short toxic methamphetamine schedule impairs object recognition task in male rats. Brain Res 940:95–101
Boger HA, Middaugh LD, Granholm AC, McGinty JF (2009) Minocycline restores striatal tyrosine hydroxylase in GDNF heterozygous mice but not in methamphetamine-treated mice. Neurobiol Dis 33:459–466
Boileau I, Rusjan P, Houle S, Wilkins D, Tong J, Selby P, Guttman M, Saint-Cyr JA, Wilson AA, Kish SJ (2008) Increased vesicular monoamine transporter binding during early abstinence in human methamphetamine users: is VMAT2 a stable dopamine neuron biomarker? J Neurosci 28:9850–9856
Borgmann K, Ghorpade A (2015) HIV-1, methamphetamine and astrocytes at neuroinflammatory Crossroads. Front Microbiol 6:1143
Bosse KE, Charlton JL, Susick LL, Newman B, Eagle AL, Mathews TA, Perrine SA, Conti AC (2015) Deficits in behavioral sensitization and dopaminergic responses to methamphetamine in adenylyl cyclase 1/8-deficient mice. J Neurochem 135:1218–1231
Bowyer JF, Davies DL, Schmued L, Broening HW, Newport GD, Slikker W Jr, Holson RR (1994) Further studies of the role of hyperthermia in methamphetamine neurotoxicity. J Pharmacol Exp Ther 268:1571–1580
Bowyer JF, Holson RR, Miller DB, O’Callaghan JP (2001) Phenobarbital and dizocilpine can block methamphetamine-induced neurotoxicity in mice by mechanisms that are independent of thermoregulation. Brain Res 919:179–183
Braren SH, Drapala D, Tulloch IK, Serrano PA (2014) Methamphetamine-induced short-term increase and long-term decrease in spatial working memory affects protein Kinase M zeta (PKMζ), dopamine, and glutamate receptors. Front Behav Neurosci 8:438
Brodie C, Blumberg PM (2003) Regulation of cell apoptosis by protein kinase c delta. Apoptosis 8:19–27
Brown JM, Gouty S, Iyer V, Rosenberger J, Cox BM (2006) Differential protection against MPTP or methamphetamine toxicity in dopamine neurons by deletion of ppN/OFQ expression. J Neurochem 98:495–505
Burrows KB, Meshul CK (1997) Methamphetamine alters presynaptic glutamate immunoreactivity in the caudate nucleus and motor cortex. Synapse 27:133–144
Burrows KB, Nixdorf WL, Yamamoto BK (2000) Central administration of methamphetamine synergizes with metabolic inhibition to deplete striatal monoamines. J Pharmacol Exp Ther 292:853–860
Cadet JL, Sheng P, Ali S, Rothman R, Carlson E, Epstein C (1994) Attenuation of methamphetamine-induced neurotoxicity in copper/zinc superoxide dismutase transgenic mice. J Neurochem 62:380–383
Callaghan RC, Cunningham JK, Sajeev G, Kish SJ (2010) Incidence of Parkinson’s disease among hospital patients with methamphetamine-use disorders. Mov Disord 25:2333–2339
Callaghan RC, Cunningham JK, Sykes J, Kish SJ (2012a) Increased risk of Parkinson’s disease in individuals hospitalized with conditions related to the use of methamphetamine or other amphetamine-type drugs. Drug Alcohol Depend 120:35–40
Callaghan RC, Cunningham JK, Allebeck P, Arenovich T, Sajeev G, Remington G, Boileau I, Kish SJ (2012b) Methamphetamine use and schizophrenia: a population-based cohort study in California. Am J Psychiatry 169:389–396
Cass WA (1997) Decreases in evoked overflow of dopamine in rat striatum after neurotoxic doses of methamphetamine. J Pharmacol Exp Ther 280:105–113
Cass WA, Manning MW (1999) Recovery of presynaptic dopaminergic functioning in rats treated with neurotoxic doses of methamphetamine. J Neurosci 19:7653–7660
Cass WA, Harned ME, Peters LE, Nath A, Maragos WF (2003) HIV-1 protein Tat potentiation of methamphetamine-induced decreases in evoked overflow of dopamine in the striatum of the rat. Brain Res 984:133–142
Castino R, Lazzeri G, Lenzi P, Bellio N, Follo C, Ferrucci M, Fornai F, Isidoro C (2008) Suppression of autophagy precipitates neuronal cell death following low doses of methamphetamine. J Neurochem 106:1426–1439
Cen X, Nitta A, Ibi D, Zhao Y, Niwa M, Taguchi K, Hamada M, Ito Y, Ito Y, Wang L, Nabeshima T (2008) Identification of Piccolo as a regulator of behavioral plasticity and dopamine transporter internalization. Mol Psychiatry 13:451–463
Cervinski MA, Foster JD, Vaughan RA (2005) Psychoactive substrates stimulate dopamine transporter phosphorylation and down-regulation by cocaine-sensitive and protein kinase C-dependent mechanisms. J Biol Chem 280:40442–40449
Chanasong R, Thanoi S, Watiktinkorn P, Reynolds GP, Nudmamud-Thanoi S (2013) Genetic variation of GRIN1 confers vulnerability to methamphetamine-dependent psychosis in a Thai population. Neurosci Lett 551:58–61
Chao YL, Chen HH, Chen CH (2012) Effects of repeated electroconvulsive shock on methamphetamine-induced behavioral abnormalities in mice. Brain Stimul 5:393–401
Chen CK, Lin SK, Sham PC, Ball D, Loh EW, Hsiao CC, Chiang YL, Ree SC, Lee CH, Murray RM (2003) Pre-morbid characteristics and co-morbidity of methamphetamine users with and without psychosis. Psychol Med 33:1407–1414
Chen CK, Lin SK, Sham PC, Ball D, Loh EW, Murray RM (2005) Morbid risk for psychiatric disorder among the relatives of methamphetamine users with and without psychosis. Am J Med Genet B Neuropsychiatr Genet 136B:87–91
Chen H, Wu J, Zhang J, Fujita Y, Ishima T, Iyo M, Hashimoto K (2012a) Protective effects of the antioxidant sulforaphane on behavioral changes and neurotoxicity in mice after the administration of methamphetamine. Psychopharmacology 222:37–45
Chen YJ, Liu YL, Zhong Q, Yu YF, Su HL, Toque HA, Dang YH, Chen F, Xu M, Chen T (2012b) Tetrahydropalmatine protects against methamphetamine-induced spatial learning and memory impairment in mice. Neurosci Bull 28:222–232
Chipana C, Torres I, Camarasa J, Pubill D, Escubedo E (2008) Memantine protects against amphetamine derivatives-induced neurotoxic damage in rodents. Neuropharmacology 54:1254–1263
Chiu HY, Chan MH, Lee MY, Chen ST, Zhan ZY, Chen HH (2014) Long-lasting alterations in 5-HT2A receptor after a binge regimen of methamphetamine in mice. Int J Neuropsychopharmacol 17:1647–1658
Clemens KJ, Cornish JL, Hunt GE, McGregor IS (2007) Repeated weekly exposure to MDMA, methamphetamine or their combination: long-term behavioural and neurochemical effects in rats. Drug Alcohol Depend 86:183–190
Cruickshank CC, Dyer KR (2009) A review of the clinical pharmacology of methamphetamine. Addiction 104:1085–1099
Cubells JF, Rayport S, Rajendran G, Sulzer D (1994) Methamphetamine neurotoxicity involves vacuolation of endocytic organelles and dopamine-dependent intracellular oxidative stress. J Neurosci 14:2260–2271
Cunha-Oliveira T, Rego AC, Oliveira CR (2013) Oxidative stress and drugs of abuse: an update. Mini Rev Org Chem 10:321–334
Curtin K, Fleckenstein AE, Robison RJ, Crookston MJ, Smith KR, Hanson GR (2015) Methamphetamine/amphetamine abuse and risk of Parkinson’s disease in Utah: a population-based assessment. Drug Alcohol Depend 146:30–38
Dai H, Okuda H, Iwabuchi K, Sakurai E, Chen Z, Kato M, Iinuma K, Yanai K (2004) Social isolation stress significantly enhanced the disruption of prepulse inhibition in mice repeatedly treated with methamphetamine. Ann N Y Acad Sci 1025:257–266
Damghani F, Bigdeli I, Miladi-Gorji H, Fadaei A (2016) Swimming exercise attenuates psychological dependence and voluntary methamphetamine consumption in methamphetamine withdrawn rats. Iran J Basic Med Sci 19:594–600
Dang DK, Duong CX, Nam Y, Shin EJ, Lim YK, Jeong JH, Jang CG, Nah SY, Nabeshima T, Kim HC (2015) Inhibition of protein kinase (PK) Cδ attenuates methamphetamine-induced dopaminergic toxicity via upregulation of phosphorylation of tyrosine hydroxylase at Ser40 by modulation of protein phosphatase 2A and PKA. Clin Exp Pharmacol Physiol 42:192–201
Dang DK, Shin EJ, Nam Y, Ryoo S, Jeong JH, Jang CG, Nabeshima T, Hong JS, Kim HC (2016) Apocynin prevents mitochondrial burdens, microglial activation, and pro-apoptosis induced by a toxic dose of methamphetamine in the striatum of mice via inhibition of p47phox activation by ERK. J Neuroinflammation 13:12
Darke S, Kaye S, McKetin R, Duflou J (2008) Major physical and psychological harms of methamphetamine use. Drug Alcohol Rev 27:253–262
Davidson C, Gow AJ, Lee TH, Ellinwood EH (2001) Methamphetamine neurotoxicity: necrotic and apoptotic mechanisms and relevance to human abuse and treatment. Brain Res Brain Res Rev 36:1–22
De Vito MJ, Wagner GC (1989) Methamphetamine-induced neuronal damage: a possible role for free radicals. Neuropharmacology 28:1145–1150
Deng X, Cadet JL (2000) Methamphetamine-induced apoptosis is attenuated in the striata of copper-zinc superoxide dismutase transgenic mice. Brain Res Mol Brain Res 83:121–124
Deng X, Wang Y, Chou J, Cadet JL (2001) Methamphetamine causes widespread apoptosis in the mouse brain: evidence from using an improved TUNEL histochemical method. Brain Res Mol Brain Res 93:64–69
Di Giacomo V, Rapino M, Sancilio S, Patruno A, Zara S, Di Pietro R, Cataldi A (2010) PKC-δ signalling pathway is involved in H9c2 cells differentiation. Differentiation 80:204–212
Di Monte DA, Royland JE, Jakowec MW, Langston JW (1996) Role of nitric oxide in methamphetamine neurotoxicity: protection by 7-nitroindazole, an inhibitor of neuronal nitric oxide synthase. J Neurochem 67:2443–2450
Dluzen DE, McDermott JL, Bourque M, Di Paolo T, Darvesh AS, Buletko AB, Laping NJ (2011) Markers associated with sex differences in methamphetamine-induced striatal dopamine neurotoxicity. Curr Neuropharmacol 9:40–44
Eichenbaum H (2001) The hippocampus and declarative memory: cognitive mechanisms and neural codes. Behav Brain Res 127:199–207
Eisch AJ, Marshall JF (1998) Methamphetamine neurotoxicity: dissociation of striatal dopamine terminal damage from parietal cortical cell body injury. Synapse 30:433–445
Eisch AJ, Gaffney M, Weihmuller FB, O’Dell SJ, Marshall JF (1992) Striatal subregions are differentially vulnerable to the neurotoxic effects of methamphetamine. Brain Res 598:321–326
Eisch AJ, Schmued LC, Marshall JF (1998) Characterizing cortical neuron injury with Fluoro-Jade labeling after a neurotoxic regimen of methamphetamine. Synapse 30:329–333
Endo H, Kamada H, Nito C, Nishi T, Chan PH (2006) Mitochondrial translocation of p53 mediates release of cytochrome c and hippocampal CA1 neuronal death after transient global cerebral ischemia in rats. J Neurosci 26:7974–7983
Ernst T, Chang L, Leonido-Yee M, Speck O (2000) Evidence for long-term neurotoxicity associated with methamphetamine abuse: a 1H MRS study. Neurology 54:1344–1349
Fallgatter AJ, Ehlis AC, Herrmann MJ, Hohoff C, Reif A, Freitag CM, Deckert J (2010) DTNBP1 (dysbindin) gene variants modulate prefrontal brain function in schizophrenic patients-support for the glutamate hypothesis of schizophrenias. Genes Brain Behav 9:489–497
Fantegrossi WE, Ciullo JR, Wakabayashi KT, De La Garza R 2nd, Traynor JR, Woods JH (2008) A comparison of the physiological, behavioral, neurochemical and microglial effects of methamphetamine and 3,4-methylenedioxymethamphetamine in the mouse. Neuroscience 151:533–543
Fischer JF, Cho AK (1979) Chemical release of dopamine from striatal homogenates: evidence for an exchange diffusion model. J Pharmacol Exp Ther 208:203–209
Fitzmaurice PS, Tong J, Yazdanpanah M, Liu PP, Kalasinsky KS, Kish SJ (2006) Levels of 4-hydroxynonenal and malondialdehyde are increased in brain of human chronic users of methamphetamine. J Pharmacol Exp Ther 319:703–709
Flora G, Lee YW, Nath A, Maragos W, Hennig B, Toborek M (2002) Methamphetamine-induced TNF-alpha gene expression and activation of AP-1 in discrete regions of mouse brain: potential role of reactive oxygen intermediates and lipid peroxidation. Neuromolecular Med 2:71–85
Fornai F, Lenzi P, Ferrucci M, Lazzeri G, di Poggio AB, Natale G, Busceti CL, Biagioni F, Giusiani M, Ruggieri S, Paparelli A (2005) Occurrence of neuronal inclusions combined with increased nigral expression of alpha-synuclein within dopaminergic neurons following treatment with amphetamine derivatives in mice. Brain Res Bull 65:405–413
Frey K, Kilbourn M, Robinson T (1997) Reduced striatal vesicular monoamine transporters after neurotoxic but not after behaviorally-sensitizing doses of methamphetamine. Eur J Pharmacol 334:273–279
Friend DM, Fricks-Gleason AN, Keefe KA (2014) Is there a role for nitric oxide in methamphetamine-induced dopamine terminal degeneration? Neurotox Res 25:153–160
Fukami G, Hashimoto K, Koike K, Okamura N, Shimizu E, Iyo M (2004) Effect of antioxidant N-acetyl-l-cysteine on behavioral changes and neurotoxicity in rats after administration of methamphetamine. Brain Res 1016:90–95
Fumagalli F, Gainetdinov RR, Valenzano KJ, Caron MG (1998) Role of dopamine transporter in methamphetamine-induced neurotoxicity: evidence from mice lacking the transporter. J Neurosci 18:4861–4869
Fumagalli F, Gainetdinov RR, Wang YM, Valenzano KJ, Miller GW, Caron MG (1999) Increased METH neurotoxicity in heterozygous vesicular monoamine transporter 2 knock-out mice. J Neurosci 19:2424–2431
Futamura T, Akiyama S, Sugino H, Forbes A, McQuade RD, Kikuchi T (2010) Aripiprazole attenuates established behavioral sensitization induced by methamphetamine. Prog Neuropsychopharmacol Biol Psychiatry 34:1115–1119
Gao HM, Liu B, Zhang W, Hong JS (2003) Critical role of microglial NADPH oxidase-derived free radicals in the in vitro MPTP model of Parkinson’s disease. FASEB J 17:1954–1956
Gao HM, Zhou H, Hong JS (2012) NADPH oxidases: novel therapeutic targets for neurodegenerative diseases. Trends Pharmacol Sci 33:295–303
Glasner-Edwards S, Mooney LJ (2014) Methamphetamine psychosis: epidemiology and management. CNS Drugs 28:1115–1126
Golembiowska K, Konieczny J, Wolfarth S, Ossowska K (2003) Neuroprotective action of MPEP, a selective mGluR5 antagonist, in methamphetamine-induced dopaminergic neurotoxicity is associated with a decrease in dopamine outflow and inhibition of hyperthermia in rats. Neuropharmacology 45:484–492
Gonçalves J, Martins T, Ferreira R, Milhazes N, Borges F, Ribeiro CF, Malva JO, Macedo TR, Silva AP (2008) Methamphetamine-induced early increase of IL-6 and TNF-alpha mRNA expression in the mouse brain. Ann N Y Acad Sci 1139:103–111
González B, Raineri M, Cadet JL, García-Rill E, Urbano FJ, Bisagno V (2014) Modafinil improves methamphetamine-induced object recognition deficits and restores prefrontal cortex ERK signaling in mice. Neuropharmacology 87:188–197
Goodwin JS, Larson GA, Swant J, Sen N, Javitch JA, Zahniser NR, De Felice LJ, Khoshbouei H (2009) Amphetamine and methamphetamine differentially affect dopamine transporters in vitro and in vivo. J Biol Chem 284:2978–2989
Gordon R, Singh N, Lawana V, Ghosh A, Harischandra DS, Jin H, Hogan C, Sarkar S, Rokad D, Panicker N, Anantharam V, Kanthasamy AG, Kanthasamy A (2016) Protein kinase Cδ upregulation in microglia drives neuroinflammatory responses and dopaminergic neurodegeneration in experimental models of Parkinson’s disease. Neurobiol Dis 93:96–114
Grace AA (1991) Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 41:1–24
Grace CE, Schaefer TL, Herring NR, Graham DL, Skelton MR, Gudelsky GA, Williams MT, Vorhees CV (2010) Effect of a neurotoxic dose regimen of (+)-methamphetamine on behavior, plasma corticosterone, and brain monoamines in adult C57BL/6 mice. Neurotoxicol Teratol 32:346–355
Granado N, Ares-Santos S, O’Shea E, Vicario-Abejon C, Colado MI, Moratalla R (2010) Selective vulnerability in striosomes and in the nigrostriatal dopaminergic pathway after methamphetamine administration: early loss of TH in striosomes after methamphetamine. Neurotox Res 18:48–58
Granado N, Ares-Santos S, Oliva I, O’Shea E, Martin ED, Colado MI, Moratalla R (2011a) Dopamine D2-receptor knockout mice are protected against dopaminergic neurotoxicity induced by methamphetamine or MDMA. Neurobiol Dis 42:391–403
Granado N, Lastres-Becker I, Ares-Santos S, Oliva I, Martin E, Cuadrado A, Moratalla R (2011b) Nrf2 deficiency potentiates methamphetamine-induced dopaminergic axonal damage and gliosis in the striatum. Glia 59:1850–1863
Grant KM, LeVan TD, Wells SM, Li M, Stoltenberg SF, Gendelman HE, Carlo G, Bevins RA (2012) Methamphetamine-associated psychosis. J Neuroimmune Pharmacol 7:113–139
Gross NB, Duncker PC, Marshall JF (2011) Striatal dopamine D1 and D2 receptors: widespread influences on methamphetamine-induced dopamine and serotonin neurotoxicity. Synapse 65:1144–1155
Guilarte TR, Nihei MK, McGlothan JL, Howard AS (2003) Methamphetamine-induced deficits of brain monoaminergic neuronal markers: distal axotomy or neuronal plasticity. Neuroscience 122:499–513
Guillot TS, Shepherd KR, Richardson JR, Wang MZ, Li Y, Emson PC, Miller GW (2008) Reduced vesicular storage of dopamine exacerbates methamphetamine-induced neurodegeneration and astrogliosis. J Neurochem 106:2205–2217
Hadamitzky M, Markou A, Kuczenski R (2011) Extended access to methamphetamine self-administration affects sensorimotor gating in rats. Behav Brain Res 217:386–390
Harris AC, LeSage MG, Shelley D, Perry JL, Pentel PR, Owens SM (2015) The anti-(+)-methamphetamine monoclonal antibody mAb7F9 attenuates acute (+)-methamphetamine effects on intracranial self-stimulation in rats. PLoS ONE 10:e0118787
Harvey DC, Lacan G, Tanious SP, Melega WP (2000) Recovery from methamphetamine induced long-term nigrostriatal dopaminergicdeficits without substantia nigra cell loss. Brain Res 871:259–270
Hashimoto K, Tsukada H, Nishiyama S, Fukumoto D, Kakiuchi T, Shimizu E (2004) Protective effects on N-acetyl-l-cysteine on the reduction of dopamine transporters in the striatum of monkeys treated with methamphetamine. Neuropsychopharmacology 29:2018–2023
Hashimoto K, Nakahara T, Yamada H, Hirano M, Kuroki T, Kanba S (2007a) A neurotoxic dose of methamphetamine induces gene expression of Homer 1a, but not Homer 1b or 1c, in the striatum and nucleus accumbens. Neurochem Int 51:227–232
Hashimoto K, Tsukada H, Nishiyama S, Fukumoto D, Kakiuchi T, Iyo M (2007b) Protective effects of minocycline on the reduction of dopamine transporters in the striatum after administration of methamphetamine: a positron emission tomography study in conscious monkeys. Biol Psychiatry 61:577–581
Hastrup H, Sen N, Javitch JA (2003) The human dopamine transporter forms a tetramer in the plasma membrane: cross-linking of a cysteine in the fourth transmembrane segment is sensitive to cocaine analogs. J Biol Chem 278:45045–45048
Hayashi T, Hirata H, Asanuma M, Ladenheim B, Tsao LI, Cadet JL, Su TP (2001) Delta opioid peptide [d-Ala2, d-Leu5]enkephalin causes a near complete blockade of the neuronal damage caused by a single high dose of methamphetamine: examining the role of p53. Synapse 39:305–312
Henry BL, Geyer MA, Buell MR, Perry W, Young JW, Minassian A, Translational Methamphetamine AIDS Research Center (TMARC) Group (2014) Prepulse inhibition in HIV-1 gp120 transgenic mice after withdrawal from chronic methamphetamine. Behav Pharmacol 25:12–22
Hermida-Ameijeiras A, Méndez-Alvarez E, Sánchez-Iglesias S, Sanmartín-Suárez C, Soto-Otero R (2004) Autoxidation and MAO-mediated metabolism of dopamine as a potential cause of oxidative stress: role of ferrous and ferric ions. Neurochem Int 45:103–116
Herring NR, Schaefer TL, Gudelsky GA, Vorhees CV, Williams MT (2008) Effect of (+)-methamphetamine on path integration learning, novel object recognition, and neurotoxicity in rats. Psychopharmacology 199:637–650
Heysieattalab S, Naghdi N, Zarrindast MR, Haghparast A, Mehr SE, Khoshbouei H (2016) The effects of GABAA and NMDA receptors in the shell-accumbens on spatial memory of METH-treated rats. Pharmacol Biochem Behav 142:23–35
Hirata H, Cadet JL (1997a) p53-knockout mice are protected against the long-term effects of methamphetamine on dopaminergic terminals and cell bodies. J Neurochem 69:780–790
Hirata H, Cadet JL (1997b) Methamphetamine-induced serotonin neurotoxicity is attenuated in p53-knockout mice. Brain Res 768:345–348
Hirata H, Ladenheim B, Carlson E, Epstein C, Cadet JL (1996) Autoradiographic evidence for methamphetamine-induced striatal dopaminergic loss in mouse brain: attenuation in CuZn-superoxide dismutase transgenic mice. Brain Res 714:95–103
Hirata H, Asanuma M, Cadet JL (1998) Melatonin attenuates methamphetamine-induced toxic effects on dopamine and serotonin terminals in mouse brain. Synapse 30:150–155
Hirsch E, Graybiel AM, Agid YA (1988) Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson’s disease. Nature 334:345–348
Hodges AB, Ladenheim B, McCoy MT, Beauvais G, Cai N, Krasnova IN, Cadet JL (2011) Long-term protective effects of methamphetamine preconditioning against single-day methamphetamine toxic challenges. Curr Neuropharmacol 9:35–39
Hogan KA, Staal RG, Sonsalla PK (2000) Analysis of VMAT2 binding after methamphetamine or MPTP treatment: disparity between homogenates and vesicle preparations. J Neurochem 74:2217–2220
Hotchkiss AJ, Gibb JW (1980) Long term effects of multiple doses of methamphetamine on tryptophan hydroxylase and tyrosine hydroxylase activity in rat brain. J Pharmacol Exp Ther 214:257–262
Hozumi H, Asanuma M, Miyazaki I, Fukuoka S, Kikkawa Y, Kimoto N, Kitamura Y, Sendo T, Kita T, Gomita Y (2008) Protective effects of interferon-gamma against methamphetamine-induced neurotoxicity. Toxicol Lett 177:123–129
Hsieh JH, Stein DJ, Howells FM (2014) The neurobiology of methamphetamine induced psychosis. Front Hum Neurosci 8:537
Huang CL, Huang NK, Shyue SK, Chern Y (2003) Hydrogen peroxide induces loss of dopamine transporter activity: a calcium-dependent oxidative mechanism. J Neurochem 86:1247–1259
Huang MC, Lin SK, Chen CH, Pan CH, Lee CH, Liu HC (2013) Oxidative stress status in recently abstinent methamphetamine abusers. Psychiatry Clin Neurosci 67:92–100
Iijima M, Koike H, Chaki S (2013) Effect of an mGlu2/3 receptor antagonist on depressive behavior induced by withdrawal from chronic treatment with methamphetamine. Behav Brain Res 246:24–28
Imam SZ, Ali SF (2000) Selenium, an antioxidant, attenuates methamphetamine-induced dopaminergic toxicity and peroxynitrite generation. Brain Res 855:186–191
Imam SZ, Newport GD, Islam F, Slikker W Jr, Ali SF (1999) Selenium, an antioxidant, protects against methamphetamine-induced dopaminergic neurotoxicity. Brain Res 818:575–578
Imam SZ, Newport GD, Itzhak Y, Cadet JL, Islam F, Slikker W Jr, Ali SF (2001a) Peroxynitrite plays a role in methamphetamine-induced dopaminergic neurotoxicity: evidence from mice lacking neuronal nitric oxide synthase gene or overexpressing copper-zinc superoxide dismutase. J Neurochem 76:745–749
Imam SZ, Itzhak Y, Cadet JL, Islam F, Slikker W Jr, Ali SF (2001b) Methamphetamine-induced alteration in striatal p53 and bcl-2 expressions in mice. Brain Res Mol Brain Res 91:174–178
Imam SZ, Newport GD, Duhart HM, Islam F, Slikker W Jr, Ali SF (2002) Methamphetamine-induced dopaminergic neurotoxicity and production of peroxynitrite are potentiated in nerve growth factor differentiated pheochromocytoma 12 cells. Ann N Y Acad Sci 965:204–213
Itzhak Y, Ali SF (1996) The neuronal nitric oxide synthase inhibitor, 7-nitroindazole, protects against methamphetamine-induced neurotoxicity in vivo. J Neurochem 67:1770–1773
Itzhak Y, Martin JL, Black MD, Ali SF (1998) Effect of melatonin on methamphetamine-and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced dopaminergic neurotoxicity and methamphetamine-induced behavioral sensitization. Neuropharmacology 37:781–791
Itzhak Y, Martin JL, Ali SF (2000) Comparison between the role of the neuronal and inducible nitric oxide synthase in methamphetamine-induced neurotoxicity and sensitization. Ann N Y Acad Sci 914:104–111
Itzhak Y, Anderson KL, Ali SF (2004) Differential response of nNOS knockout mice to MDMA (“ecstasy”)- and methamphetamine-induced psychomotor sensitization and neurotoxicity. Ann N Y Acad Sci 1025:119–128
Jayanthi S, Deng X, Bordelon M, McCoy MT, Cadet JL (2001) Methamphetamine causes differential regulation of pro-death and anti-death Bcl-2 genes in the mouse neocortex. FASEB J 15:1745–1752
Jayanthi S, Deng X, Noailles PA, Ladenheim B, Cadet JL (2004) Methamphetamine induces neuronal apoptosis via cross-talks between endoplasmic reticulum and mitochondria-dependent death cascades. FASEB J 18:238–251
Jiang J, Wang M, Liang B, Shi Y, Su Q, Chen H, Huang J, Su J, Pan P, Li Y, Wang H, Chen R, Liu J, Zhao F, Ye L, Liang H (2016) In vivo effects of methamphetamine on HIV-1 replication: a population-based study. Drug Alcohol Depend 159:246–254
Jin H, Kanthasamy A, Anantharam V, Rana A, Kanthasamy AG (2011a) Transcriptional regulation of pro-apoptotic protein kinase Cdelta: implications for oxidative stress-induced neuronal cell death. J Biol Chem 286:19840–19859
Jin H, Kanthasamy A, Ghosh A, Yang Y, Anantharam V, Kanthasamy AG (2011b) α-Synuclein negatively regulates protein kinase Cδ expression to suppress apoptosis in dopaminergic neurons by reducing p300 histone acetyltransferase activity. J Neurosci 31:2035–2051
Johanson CE, Frey KA, Lundahl LH, Keenan P, Lockhart N, Roll J, Galloway GP, Koeppe RA, Kilbourn MR, Robbins T, Schuster CR (2006) Cognitive function and nigrostriatal markers in abstinent methamphetamine abusers. Psychopharmacology 185:327–338
Johnson-Davis KL, Fleckenstein AE, Wilkins DG (2003) The role of hyperthermia and metabolism as mechanisms of tolerance to methamphetamine neurotoxicity. Eur J Pharmacol 482:151–154
Jung BD, Shin EJ, Nguyen XK, Jin CH, Bach JH, Park SJ, Nah SY, Wie MB, Bing G, Kim HC (2010) Potentiation of methamphetamine neurotoxicity by intrastriatal lipopolysaccharide administration. Neurochem Int 56:229–244
Kai N, Nishizawa K, Tsutsui Y, Ueda S, Kobayashi K (2015) Differential roles of dopamine D1 and D2 receptor-containing neurons of the nucleus accumbens shell in behavioral sensitization. J Neurochem 135:1232–1241
Kalayasiri R, Verachai V, Gelernter J, Mutirangura A, Malison RT (2014) Clinical features of methamphetamine-induced paranoia and preliminary genetic association with DBH-1021C→T in a Thai treatment cohort. Addiction 109:965–976
Kalechstein AD, Newton TF, Green M (2003) Methamphetamine dependence is associated with neurocognitive impairment in the initial phases of abstinence. J Neuropsychiatry Clin Neurosci 15:215–220
Kamei H, Nagai T, Nakano H, Togan Y, Takayanagi M, Takahashi K, Kobayashi K, Yoshida S, Maeda K, Takuma K, Nabeshima T, Yamada K (2006) Repeated methamphetamine treatment impairs recognition memory through a failure of novelty-induced ERK1/2 activation in the prefrontal cortex of mice. Biol Psychiatry 59:75–84
Kaneko Y, Kashiwa A, Ito T, Ishii S, Umino A, Nishikawa T (2007) Selective serotonin reuptake inhibitors, fluoxetine and paroxetine, attenuate the expression of the established behavioral sensitization induced by methamphetamine. Neuropsychopharmacology 32:658–664
Kanthasamy AG, Kitazawa M, Kanthasamy A, Anantharam V (2003) Role of proteolytic activation of protein kinase Cdelta in oxidative stress-induced apoptosis. Antioxid Redox Signal 5:609–620
Kanthasamy K, Gordon R, Jin H, Anantharam V, Ali S, Kanthasamy AG, Kanthasamy A (2011) Neuroprotective effect of resveratrol against methamphetamine-induced dopaminergic apoptotic cell death in a cell culture model of neurotoxicity. Curr Neuropharmacol 9:49–53
Kaul S, Kanthasamy A, Kitazawa M, Anantharam V, Kanthasamy AG (2003) Caspase-3 dependent proteolytic activation of protein kinase C delta mediates and regulates 1-methyl-4-phenylpyridinium (MPP+)-induced apoptotic cell death in dopaminergic cells: relevance to oxidative stress in dopaminergic degeneration. Eur J Neurosci 18:1387–1401
Kaul S, Anantharam V, Yang Y, Choi CJ, Kanthasamy A, Kanthasamy AG (2005) Tyrosine phosphorylation regulates the proteolytic activation of protein kinase Cdelta in dopaminergic neuronal cells. J Biol Chem 280:28721–28730
Khoshbouei H, Sen N, Guptaroy B, Johnson L, Lund D, Gnegy ME, Galli A, Javitch JA (2004) N-terminal phosphorylation of the dopamine transporter is required for amphetamine-induced efflux. PLoS Biol 2:E78
Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG (2009) Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 29:13435–13444
Kim HC, Jhoo WK, Choi DY, Im DH, Shin EJ, Suh JH, Floyd RA, Bing G (1999) Protection of methamphetamine nigrostriatal toxicity by dietary selenium. Brain Res 851:76–86
Kim HC, Jhoo WK, Shin EJ, Bing G (2000) Selenium deficiency potentiates methamphetamine-induced nigral neuronal loss; comparison with MPTP model. Brain Res 862:247–252
Kim HC, Shin EJ, Jang CG, Lee MK, Eun JS, Hong JT, Oh KW (2005) Pharmacological action of Panax ginseng on the behavioral toxicities induced by psychotropic agents. Arch Pharm Res 28:995–1001
Kim YH, Lim JH, Lee TJ, Park JW, Kwon TK (2007) Expression of cyclin D3 through Sp1 sites by histone deacetylase inhibitors is mediated with protein kinase C-delta (PKC-delta) signal pathway. J Cell Biochem 101:987–995
Kish SJ, Fitzmaurice PS, Boileau I, Schmunk GA, Ang LC, Furukawa Y, Chang LJ, Wickham DJ, Sherwin A, Tong J (2009) Brain serotonin transporter in human methamphetamine users. Psychopharmacology 202:649–661
Kita T, Wagner GC, Nakashima T (2003) Current research on methamphetamine-induced neurotoxicity: animal models of monoamine disruption. J Pharmacol Sci 92:178–195
Koriem KM, Abdelhamid AZ, Younes HF (2013) Caffeic acid protects tissue antioxidants and DNA content in methamphetamine induced tissue toxicity in Sprague Dawley rats. Toxicol Mech Methods 23:134–143
Kousik SM, Carvey PM, Napier TC (2014) Methamphetamine self-administration results in persistent dopaminergic pathology: implications for Parkinson’s disease risk and reward-seeking. Eur J Neurosci 40:2707–2714
Krasnova IN, Justinova Z, Ladenheim B, Jayanthi S, McCoy MT, Barnes C, Warner JE, Goldberg SR, Cadet JL (2010) Methamphetamine self-administration is associated with persistent biochemical alterations in striatal and cortical dopaminergic terminals in the rat. PLoS ONE 5:e8790
Krasnova IN, Chiflikyan M, Justinova Z, McCoy MT, Ladenheim B, Jayanthi S, Quintero C, Brannock C, Barnes C, Adair JE, Lehrmann E, Kobeissy FH, Gold MS, Becker KG, Goldberg SR, Cadet JL (2013) CREB phosphorylation regulates striatal transcriptional responses in the self-administration model of methamphetamine addiction in the rat. Neurobiol Dis 58:132–143
Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312–318
Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99–163
Kuczenski R, Everall IP, Crews L, Adame A, Grant I, Masliah E (2007) Escalating dose-multiple binge methamphetamine exposure results in degeneration of the neocortex and limbic system in the rat. Exp Neurol 207:42–51
Kuhn DM, Francescutti-Verbeem DM, Thomas DM (2006) Dopamine quinones activate microglia and induce a neurotoxic gene expression profile: relationship to methamphetamine-induced nerve ending damage. Ann N Y Acad Sci 1074:31–41
Kuribara H (1995) Dopamine D1 receptor antagonist SCH 23390 retards methamphetamine sensitization in both combined administration and early posttreatment schedules in mice. Pharmacol Biochem Behav 52:759–763
Kuribara H, Uchihashi Y (1994) Effects of dopamine antagonism on methamphetamine sensitization: evaluation by ambulatory activity in mice. Pharmacol Biochem Behav 47:101–106
Ladenheim B, Krasnova IN, Deng X, Oyler JM, Polettini A, Moran TH, Huestis MA, Cadet JL (2000) Methamphetamine-induced neurotoxicity is attenuated in transgenic mice with a null mutation for interleukin-6. Mol Pharmacol 58:1247–1256
Latchoumycandane C, Anantharam V, Jin H, Kanthasamy A, Kanthasamy A (2011) Dopaminergic neurotoxicant 6-OHDA induces oxidative damage through proteolytic activation of PKCδ in cell culture and animal models of Parkinson’s disease. Toxicol Appl Pharmacol 256:314–323
Lau JWS, Senok S, Stadlin A (2000) Methamphetamine-induced oxidative stress in cultured mouse astrocytes. Ann N Y Acad Sci 914:146–156
LaVoie MJ, Hastings TG (1999) Dopamine quinone formation and protein modification associated with the striatal neurotoxicity of methamphetamine: evidence against a role for extracellular dopamine. J Neurosci 19:1484–1491
Lecomte T, Mueser KT, Macewan GW, Laferriere-Simard M, Thornton AE, Buchanan T, Goldner E, Brink J, Ehmann TS, Lang DJ, Kang S, Barr AM, Honer WG (2010) Profiles of individuals seeking psychiatric help for psychotic symptoms linked to methamphetamine abuse—baseline results from the MAPS (methamphetamine and psychosis study). Mental Health Subst Use 3:168–181
Lee KW, Kim HC, Lee SY, Jang CG (2011) Methamphetamine-sensitized mice are accompanied by memory impairment and reduction of N-methyl-d-aspartate receptor ligand binding in the prefrontal cortex and hippocampus. Neuroscience 178:101–107
Liang H, Wang X, Chen H, Song L, Ye L, Wang SH, Wang YJ, Zhou L, Ho WZ (2008) Methamphetamine enhances HIV infection of macrophages. Am J Pathol 172:1617–1624
Lieberman JA, Kane JM, Alvir J (1987) Provocative tests with psychostimulant drugs in schizophrenia. Psychopharmacology 91:415–433
Lieberman JA, Alvir J, Geisler S, Ramos-Lorenzi J, Woerner M, Novacenko H, Cooper T, Kane JM (1994) Methylphenidate response, psychopathology and tardive dyskinesia as predictors of relapse in schizophrenia. Neuropsychopharmacology 11:107–118
Lin M, Chandramani-Shivalingappa P, Jin H, Ghosh A, Anantharam V, Ali S, Kanthasamy AG, Kanthasamy A (2012) Methamphetamine-induced neurotoxicity linked to ubiquitin-proteasome system dysfunction and autophagy-related changes that can be modulated by protein kinase C delta in dopaminergic neuronal cells. Neuroscience 210:308–332
Lominac KD, Quadir SG, Barrett HM, McKenna CL, Schwartz LM, Ruiz PN, Wroten MG, Campbell RR, Miller BW, Holloway JJ, Travis KO, Rajasekar G, Maliniak D, Thompson AB, Urman LE, Kippin TE, Phillips TJ, Szumlinski KK (2016) Prefrontal glutamate correlates of methamphetamine sensitization and preference. Eur J Neurosci 43:689–702
Lu P, Mamiya T, Lu L, Mouri A, Niwa M, Kim HC, Zou LB, Nagai T, Yamada K, Ikejima T, Nabeshima T (2010) Silibinin attenuates cognitive deficits and decreases of dopamine and serotonin induced by repeated methamphetamine treatment. Behav Brain Res 207:387–393
Maehara S, Hikichi H, Satow A, Okuda S, Ohta H (2008) Antipsychotic property of a muscarinic receptor agonist in animal models for schizophrenia. Pharmacol Biochem Behav 91:140–149
Mahajan SD, Aalinkeel R, Sykes DE, Reynolds JL, Bindukumar B, Adal A, Qi M, Toh J, Xu G, Prasad PN, Schwartz SA (2008) Methamphetamine alters blood brain barrier permeability via the modulation of tight junction expression: implication for HIV-1 neuropathogenesis in the context of drug abuse. Brain Res 1203:133–148
Manning EE, van den Buuse M (2013) BDNF deficiency and young-adult methamphetamine induce sex-specific effects on prepulse inhibition regulation. Front Cell Neurosci 7:92
Maragos WF, Jakel R, Chesnut D, Pocernich CB, Butterfield DA, St Clair D, Cass WA (2000) Methamphetamine toxicity is attenuated in mice that overexpress human manganese superoxide dismutase. Brain Res 878:218–222
Maragos WF, Young KL, Turchan JT, Guseva M, Pauly JR, Nath A, Cass WA (2002) Human immunodeficiency virus-1 Tat protein and methamphetamine interact synergistically to impair striatal dopaminergic function. J Neurochem 83:955–963
Mark KA, Soghomonian JJ, Yamamoto BK (2004) High-dose methamphetamine acutely activates the striatonigral pathway to increase striatal glutamate and mediate long-term dopamine toxicity. J Neurosci 24:11449–11456
Marshall JF, O’Dell SJ (2012) Methamphetamine influences on brain and behavior: unsafe at any speed? Trends Neurosci 35:536–545
McCann UD, Wong DF, Yokoi F, Villemagne V, Dannals RF, Ricaurte GA (1998) Reduced striatal dopamine transporter density in abstinent methamphetamine and methcathinone users: evidence from positron emission tomography studies with [11C]WIN-35,428. J Neurosci 18:8417–8422
McCann UD, Kuwabara H, Kumar A, Palermo M, Abbey R, Brasic J, Ye W, Alexander M, Dannals RF, Wong DF, Ricaurte GA (2008) Persistent cognitive and dopamine transporter deficits in abstinent methamphetamine users. Synapse 62:91–100
McConnell SE, O’Banion MK, Cory-Slechta DA, Olschowka JA, Opanashuk LA (2015) Characterization of binge-dosed methamphetamine-induced neurotoxicity and neuroinflammation. Neurotoxicology 50:131–141
McFadden LM, Hadlock GC, Allen SC, Vieira-Brock PL, Stout KA, Ellis JD, Hoonakker AJ, Andrenyak DM, Nielsen SM, Wilkins DG, Hanson GR, Fleckenstein AE (2012) Methamphetamine selfadministration causes persistent striatal dopaminergic alterations and mitigates the deficits caused by a subsequent methamphetamine exposure. J Pharmacol Exp Ther 340:295–303
Melega WP, Raleigh MJ, Stout DB, Lacan G, Huang SC, Phelps ME (1997) Recovery of striatal dopamine function after acute amphetamine-and METH-induced neurotoxicity in the vervet monkey. Brain Res 766:113–120
Melega WP, Jorgensen MJ, Laćan G, Way BM, Pham J, Morton G, Cho AK, Fairbanks LA (2008) Long-term methamphetamine administration in the vervet monkey models aspects of a human exposure: brain neurotoxicity and behavioral profiles. Neuropsychopharmacology 33:1441–1452
Metzger RR, Haughey HM, Wilkins DG, Gibb JW, Hanson GR, Fleckenstein AE (2000) Methamphetamine-induced rapid decrease in dopamine transporter function: role of dopamine and hyperthermia. J Pharmacol Exp Ther 295:1077–1085
Mirecki A, Fitzmaurice P, Ang L, Kalasinsky KS, Peretti FJ, Aiken SS, Wickham DJ, Sherwin A, Nobrega JN, Forman HJ, Kish SJ (2004) Brain antioxidant systems in human methamphetamine users. J Neurochem 8:1396–1408
Miyamoto Y, Iida A, Sato K, Muramatsu S, Nitta A (2014) Knockdown of dopamine D2 receptors in the nucleus accumbens core suppresses methamphetamine-induced behaviors and signal transduction in mice. Int J Neuropsychopharmacol 18:pyu038
Mizoguchi H, Takuma K, Fukakusa A, Ito Y, Nakatani A, Ibi D, Kim HC, Yamada K (2008) Improvement by minocycline of methamphetamine-induced impairment of recognition memory in mice. Psychopharmacology 196:233–241
Mizoguchi H, Ibi D, Takase F, Nagai T, Kamei H, Toth E, Sato J, Takuma K, Yamada K (2011) Nicotine ameliorates impairment of working memory in methamphetamine-treated rats. Behav Brain Res 220:159–163
Mizuno M, Malta RS Jr, Nagano T, Nawa H (2004) Conditioned place preference and locomotor sensitization after repeated administration of cocaine or methamphetamine in rats treated with epidermal growth factor during the neonatal period. Ann N Y Acad Sci 1025:612–618
Moratalla R, Khairnar A, Simola N, Granado N, Garcia-Montes JR, Porceddu PF, Tizabi Y, Costa G, Morelli M (2015) Amphetamine-related drugs neurotoxicity in humans and in experimental animals: main mechanisms. Prog Neurobiol. doi:10.1016/j.pneurobio.2015.09.011
Morgan ME, Gibb JW (1980) Short-term and long-term effects of methamphetamine on biogenic amine metabolism in extra-striatal dopaminergic nuclei. Neuropharmacology 19:989–995
Moszczynska A, Fitzmaurice P, Ang L, Kalasinsky KS, Schmunk GA, Peretti FJ, Aiken SS, Wickham DJ, Kish SJ (2004) Why is Parkinsonism not a feature of human methamphetamine users? Brain 127:363–370
Motbey CP, Clemens KJ, Apetz N, Winstock AR, Ramsey J, Li KM, Wyatt N, Callaghan PD, Bowen MT, Cornish JL, McGregor IS (2013) High levels of intravenous mephedrone (4-methylmethcathinone) self-administration in rats: neural consequences and comparison with methamphetamine. J Psychopharmacol 27:823–836
Nagai T, Takuma K, Dohniwa M, Ibi D, Mizoguchi H, Kamei H, Nabeshima T, Yamada K (2007) Repeated methamphetamine treatment impairs spatial working memory in rats: reversal by clozapine but not haloperidol. Psychopharmacology 194:21–32
Nair MP, Saiyed ZM, Nair N, Gandhi NH, Rodriguez JW, Boukli N, Provencio-Vasquez E, Malow RM, Miguez-Burbano MJ (2009) Methamphetamine enhances HIV-1 infectivity in monocyte derived dendritic cells. J Neuroimmune Pharmacol 4:129–139
Nakagawa Y, Chiba K (2015) Diversity and plasticity of microglial cells in psychiatric and neurological disorders. Pharmacol Ther 154:21–35
Nakajima A, Yamada K, Nagai T, Uchiyama T, Miyamoto Y, Mamiya T, He J, Nitta A, Mizuno M, Tran MH, Seto A, Yoshimura M, Kitaichi K, Hasegawa T, Saito K, Yamada Y, Seishima M, Sekikawa K, Kim HC, Nabeshima T (2004) Role of tumor necrosis factor-alpha in methamphetamine-induced drug dependence and neurotoxicity. J Neurosci 24:2212–2225
Nakamura K, Chen CK, Sekine Y, Iwata Y, Anitha A, Loh EW, Takei N, Suzuki A, Kawai M, Takebayashi K, Suzuki K, Minabe Y, Tsuchiya K, Yamada K, Iyo M, Ozaki N, Inada T, Iwata N, Harano M, Komiyama T, Yamada M, Sora I, Ujike H, Ball DM, Yoshikawa T, Lin SK, Mori N (2006) Association analysis of SOD2 variants with methamphetamine psychosis in Japanese and Taiwanese populations. Hum Genet 120:243–252
Nakato Y, Abekawa T, Ito K, Inoue T, Koyama T (2010) Lamotrigine blocks the initiation and expression of repeated high-dose methamphetamine-induced prepulse inhibition deficit in rats. Neurosci Lett 481:183–187
Nam Y, Wie MB, Shin EJ, Nguyen TT, Nah SY, Ko SK, Jeong JH, Jang CG, Kim HC (2015) Ginsenoside Re protects methamphetamine-induced mitochondrial burdens and proapoptosis via genetic inhibition of protein kinase C δ in human neuroblastoma dopaminergic SH-SY5Y cell lines. J Appl Toxicol 35:927–944
Newton TF, Kalechstein AD, Hardy DJ, Cook IA, Nestor L, Ling W, Leuchter AF (2004) Association between quantitative EEG and neurocognition in methamphetamine-dependent volunteers. Clin Neurophysiol 115:194–198
Nguyen XK, Lee J, Shin EJ, Dang DK, Jeong JH, Nguyen TT, Nam Y, Cho HJ, Lee JC, Park DH, Jang CG, Hong JS, Nabeshima T, Kim HC (2015) Liposomal melatonin rescues methamphetamine-elicited mitochondrial burdens, pro-apoptosis, and dopaminergic degeneration through the inhibition PKCδ gene. J Pineal Res 58:86–106
Noda Y, Mouri A, Ando Y, Waki Y, Yamada SN, Yoshimi A, Yamada K, Ozaki N, Wang D, Nabeshima T (2010) Galantamine ameliorates the impairment of recognition memory in mice repeatedly treated with methamphetamine: involvement of allosteric potentiation of nicotinic acetylcholine receptors and dopaminergic-ERK1/2 systems. Int J Neuropsychopharmacol 13:1343–1354
Nordahl TE, Salo R, Leamon M (2003) Neuropsychological effects of chronic methamphetamine use on neurotransmitters and cognition: a review. J Neuropsychiatry Clin Neurosci 15:317–325
North A, Swant J, Salvatore MF, Gamble-George J, Prins P, Butler B, Mittal MK, Heltsley R, Clark JT, Khoshbouei H (2013) Chronic methamphetamine exposure produces a delayed, long-lasting memory deficit. Synapse 67:245–257
O’Callaghan JP, Miller DB (1994) Neurotoxicity profiles of substituted amphetamines in the C57BL/6J mouse. J Pharmacol Exp Ther 270:741–751
O’Dell SJ, Marshall JF (2000) Repeated administration of methamphetamine damages cells in the somatosensory cortex: overlap with cytochrome oxidase-rich barrels. Synapse 37:32–37
Ohno M, Watanabe S (1995) Nitric oxide synthase inhibitors block behavioral sensitization to methamphetamine in mice. Eur J Pharmacol 275:39–44
Okochi T, Kishi T, Ikeda M, Kitajima T, Kinoshita Y, Kawashima K, Okumura T, Tsunoka T, Fukuo Y, Inada T, Yamada M, Uchimura N, Iyo M, Sora I, Ozaki N, Ujike H, Iwata N (2011) Genetic association analysis of NOS3 and methamphetamine-induced psychosis among Japanese. Curr Neuropharmacol 9:151–154
Okumura T, Okochi T, Kishi T, Ikeda M, Kitajima T, Kinoshita Y, Kawashima K, Tsunoka T, Fukuo Y, Inada T, Yamada M, Uchimura N, Iyo M, Sora I, Ozaki N, Ujike H, Iwata N (2011) Genetic association analysis of NOS1 and methamphetamine-induced psychosis among Japanese. Curr Neuropharmacol 9:155–159
Pakkenberg B, Moller A, Gundersen HJ, Mouritzen Dam A, Pakkenberg H (1991) The absolute number of nerve cells in substantia nigra in normal subjects and in patients with Parkinson’s disease estimated with an unbiased stereological method. J Neurol Neurosurg Psychiatry 54:30–33
Panenka WJ, Procyshyn RM, Lecomte T, MacEwan GW, Flynn SW, Honer WG, Barr AM (2013) Methamphetamine use: a comprehensive review of molecular, preclinical and clinical findings. Drug Alcohol Depend 129:167–179
Panicker N, Saminathan H, Jin H, Neal M, Harischandra DS, Gordon R, Kanthasamy K, Lawana V, Sarkar S, Luo J, Anantharam V, Kanthasamy AG, Kanthasamy A (2015) Fyn kinase regulates microglial neuroinflammatory responses in cell culture and animal models of Parkinson’s Disease. J Neurosci 35:10058–10077
Park SU, Ferrer JV, Javitch JA, Kuhn DM (2002) Peroxynitrite inactivates the human dopamine transporter by modification of cysteine 342: potential mechanism of neurotoxicity in dopamine neurons. J Neurosci 22:4399–4405
Park MJ, Lee SK, Lim MA, Chung HS, Cho SI, Jang CG, Lee SM (2006) Effect of alpha-tocopherol and deferoxamine on methamphetamine-induced neurotoxicity. Brain Res 1109:176–182
Paulus MP, Hozack NE, Zauscher BE, Frank L, Brown GG, Braff DL, Schuckit MA (2002) Behavioral and functional neuroimaging evidence for prefrontal dysfunction in methamphetamine-dependent subjects. Neuropsychopharmacology 26:53–63
Peter D, Jimenez J, Liu Y, Kim J, Edwards RH (1994) The chromaffin granule and synaptic vesicle amine transporters differ in substrate recognition and sensitivity to inhibitors. J Biol Chem 269:7231–7237
Pirompul N, Govitrapong P, Chetsawang B (2013) Farnesyltransferase inhibitor attenuates methamphetamine toxicity-induced Ras proteins activation and cell death in neuroblastoma SH-SY5Y cells. Neurosci Lett 545:138–143
Pu C, Broening HW, Vorhees CV (1996) Effect of methamphetamine on glutamate-positive neurons in the adult and developing rat somatosensory cortex. Synapse 23:328–334
Pucilowska J, Puzerey PA, Karlo JC, Galán RF, Landreth GE (2012) Disrupted ERK signaling during cortical development leads to abnormal progenitor proliferation, neuronal and network excitability and behavior, modeling human neuro-cardio-facial-cutaneous and related syndromes. J Neurosci 32:8663–8677
Qin L, Liu Y, Wang T, Wei SJ, Block ML, Wilson B, Liu B, Hong JS (2004) NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. J Biol Chem 279:1415–1421
Qin L, Liu Y, Hong JS, Crews FT (2013) NADPH oxidase and aging drive microglial activaton, oxidative stress, and dopaminergic neurodegeneration following systemic LPS administration. Glia 61:855–868
Racay P, Tatarkova Z, Drgova A, Kaplan P, Dobrota D (2007) Effect of ischemic preconditioning on mitochondrial dysfunction and mitochondrial p53 translocation after transient global cerebral ischemia in rats. Neurochem Res 32:1823–1832
Raineri M, Gonzalez B, Goitia B, Garcia-Rill E, Krasnova IN, Cadet JL, Urbano FJ, Bisagno V (2012) Modafinil abrogates methamphetamine-induced neuroinflammation and apoptotic effects in the mouse striatum. PLoS ONE 7:e46599
Reichel CM, Schwendt M, McGinty JF, Olive MF, See RE (2011) Loss of object recognition memory produced by extended access to methamphetamine self-administration is reversed by positive allosteric modulation of metabotropic glutamate receptor 5. Neuropsychopharmacology 36:782–792
Reichel CM, Ramsey LA, Schwendt M, McGinty JF, See RE (2012a) Methamphetamine-induced changes in the object recognition memory circuit. Neuropharmacology 62:1119–1126
Reichel CM, Chan CH, Ghee SM, See RE (2012b) Sex differences in escalation of methamphetamine self-administration: cognitive and motivational consequences in rats. Psychopharmacology 223:371–380
Remington G, Foussias G, Agid O, Fervaha G, Takeuchi H, Hahn M (2014) The neurobiology of relapse in schizophrenia. Schizophr Res 152:381–390
Ren Q, Zhang JC, Ma M, Fujita Y, Wu J, Hashimoto K (2014) 7,8-Dihydroxyflavone, a TrkB agonist, attenuates behavioral abnormalities and neurotoxicity in mice after administration of methamphetamine. Psychopharmacology 231:159–166
Ren Q, Ma M, Yang C, Zhang JC, Yao W, Hashimoto K (2015) BDNF-TrkB signaling in the nucleus accumbens shell of mice has key role in methamphetamine withdrawal symptoms. Transl Psychiatry 5:e666
Rendell PG, Mazur M, Henry JD (2009) Prospective memory impairment in former users of methamphetamine. Psychopharmacology 203:609–616
Riddle EL, Fleckenstein AE, Hanson GR (2006) Mechanisms of methamphetamine-induced dopaminergic neurotoxicity. AAPS J 8:E413–E418
Roberts AC, De Salvia MA, Wilkinson LS, Collins P, Muir JL, Everitt BJ, Robbins TW (1994) 6-Hydroxydopamine lesions of the prefrontal cortex in monkeys enhance performance on an analog of the Wisconsin Card Sort Test: possible interactions with subcortical dopamine. J Neurosci 14:2531–2544
Rogers JL, De Santis S, See RE (2008) Extended methamphetamine self-administration enhances reinstatement of drug seeking and impairs novel object recognition in rats. Psychopharmacology 199:615–624
Rusyniak DE (2013) Neurologic manifestations of chronic methamphetamine abuse. Psychiatr Clin North Am 36:261–275
Saha K, Sambo D, Richardson BD, Lin LM, Butler B, Villarroel L, Khoshbouei H (2014) Intracellular methamphetamine prevents the dopamine-induced enhancement of neuronal firing. J Biol Chem 289:22246–22257
Salamanca SA, Sorrentino EE, Nosanchuk JD, Martinez LR (2015) Impact of methamphetamine on infection and immunity. Front Neurosci 8:445
Saminathan H, Asaithambi A, Anantharam V, Kanthasamy AG, Kanthasamy A (2011) Environmental neurotoxic pesticide dieldrin activates a non receptor tyrosine kinase to promote PKCδ-mediated dopaminergic apoptosis in a dopaminergic neuronal cell model. Neurotoxicology 32:567–577
Sams-Dodd F (1998) Effects of continuous d-amphetamine and phencyclidine administration on social behaviour, stereotyped behaviour, and locomotor activity in rats. Neuropsychopharmacology 19:18–25
Sato M (1992) A lasting vulnerability to psychosis in patients with previous methamphetamine psychosis. Ann N Y Acad Sci 654:160–170
Sato M, Chen CC, Akiyama K, Otsuki S (1983) Acute exacerbation of paranoid psychotic state after long-term abstinence in patients with previous methamphetamine psychosis. Biol Psychiatry 18:429–440
Schröder N, O’Dell SJ, Marshall JF (2003) Neurotoxic methamphetamine regimen severely impairs recognition memory in rats. Synapse 49:89–96
Schultz CC, Nenadic I, Koch K, Wagner G, Roebel M, Schachtzabel C, Mühleisen TW, Nöthen MM, Cichon S, Deufel T, Kiehntopf M, Rietschel M, Reichenbach JR, Sauer H, Schlösser RG (2011) Reduced cortical thickness is associated with the glutamatergic regulatory gene risk variant DAOA Arg30Lys in schizophrenia. Neuropsychopharmacology 36:1747–1753
Schwendt M, Rocha A, See RE, Pacchioni AM, McGinty JF, Kalivas PW (2009) Extended methamphetamine self-administration in rats results in a selective reduction of dopamine transporter levels in the prefrontal cortex and dorsal striatum not accompanied by marked monoaminergic depletion. J Pharmacol Exp Ther 331:555–562
Scofield MD, Trantham-Davidson H, Schwendt M, Leong KC, Peters J, See RE, Reichel CM (2015) Failure to recognize novelty after extended methamphetamine self-administration results from loss of long-term depression in the perirhinal cortex. Neuropsychopharmacology 40:2526–2535
Seddigh R, Keshavarz-Akhlaghi AA, Shariati B (2014) Treating methamphetamine-induced resistant psychosis with clozapine. Case Rep Psychiatry 2014:845145
Seemann S, Hainaut P (2005) Roles of thioredoxin reductase 1 and APE/Ref-1 in the control of basal p53 stability and activity. Oncogene 24:3853–3863
Segal DS, Kuczenski R, O’Neil ML, Melega WP, Cho AK (2003) Escalating dose methamphetamine pretreatment alters the behavioral and neurochemical profiles associated with exposure to a high-dose methamphetamine binge. Neuropsychopharmacology 28:1730–1740
Segal DS, Kuczenski R, O’Neil ML, Melega WP, Cho AK (2005) Prolonged exposure of rats to intravenous methamphetamine: behavioral and neurochemical characterization. Psychopharmacology 180:501–512
Seiden LS, Commins DL, Vosmer G, Axt K, Marek G (1988) Neurotoxicity in dopamine and 5-hydroxytryptamine terminal fields: a regional analysis in nigrostriatal and mesolimbic projections. Ann NY Acad Sci 537:161–172
Sekine Y, Iyo M, Ouchi Y, Matsunaga T, Tsukada H, Okada H, Yoshikawa E, Futatsubashi M, Takei N, Mori N (2001) Methamphetamine-related psychiatric symptoms and reduced brain dopamine transporters studied with PET. Am J Psychiatry 158:1206–1214
Sekine Y, Ouchi Y, Takei N, Yoshikawa E, Nakamura K, Futatsubashi M, Okada H, Minabe Y, Suzuki K, Iwata Y, Tsuchiya KJ, Tsukada H, Iyo M, Mori N (2006) Brain serotonin transporter density and aggression in abstinent methamphetamine abusers. Arch Gen Psychiatry 63:90–100
Sekine Y, Ouchi Y, Sugihara G, Takei N, Yoshikawa E, Nakamura K, Iwata Y, Tsuchiya KJ, Suda S, Suzuki K, Kawai M, Takebayashi K, Yamamoto S, Matsuzaki H, Ueki T, Mori N, Gold MS, Cadet JL (2008) Methamphetamine causes microglial activation in the brains of human abusers. J Neurosci 28:5756–5761
Shiba T, Yamato M, Kudo W, Watanabe T, Utsumi H, Yamada K (2011) In vivo imaging of mitochondrial function in methamphetamine-treated rats. Neuroimage 57:866–872
Shimazoe T, Yoshimatsu A, Kawashimo A, Watanabe S (2000) Roles of adenosine A(1) and A(2A) receptors in the expression and development of methamphetamine-induced sensitization. Eur J Pharmacol 388:249–254
Shin EJ, Nabeshima T, Suh HW, Jhoo WK, Oh KW, Lim YK, Kim DS, Choi KH, Kim HC (2005) Ginsenosides attenuate methamphetamine-induced behavioral side effects in mice via activation of adenosine A2A receptors: possible involvements of the striatal reduction in AP-1 DNA binding activity and proenkephalin gene expression. Behav Brain Res 158:143–157
Shin EJ, Bing G, Chae JS, Kim TW, Bach JH, Park DH, Yamada K, Nabeshima T, Kim HC (2009) Role of microsomal epoxide hydrolase in methamphetamine-induced drug dependence in mice. J Neurosci Res 87:3679–3686
Shin EJ, Duong CX, Nguyen TX, Bing G, Bach JH, Park DH, Nakayama K, Ali SF, Kanthasamy AG, Cadet JL, Nabeshima T, Kim HC (2011) PKCδ inhibition enhances tyrosine hydroxylase phosphorylation in mice after methamphetamine treatment. Neurochem Int 59:39–50
Shin EJ, Duong CX, Nguyen XK, Li Z, Bing G, Bach JH, Park DH, Nakayama K, Ali SF, Kanthasamy AG, Cadet JL, Nabeshima T, Kim HC (2012) Role of oxidative stress in methamphetamine-induced dopaminergic toxicity mediated by protein kinase Cδ. Behav Brain Res 232:98–113
Shin EJ, Shin SW, Nguyen TT, Park DH, Wie MB, Jang CG, Nah SY, Yang BW, Ko SK, Nabeshima T, Kim HC (2014) Ginsenoside Re rescues methamphetamine-induced oxidative damage, mitochondrial dysfunction, microglial activation, and dopaminergic degeneration by inhibiting the protein kinase Cδ gene. Mol Neurobiol 49:1400–1421
Shin EJ, Nam Y, Lee JW, Nguyen PT, Yoo JE, Tran TV, Jeong JH, Jang CG, Oh YJ, Youdim MB, Lee PH, Nabeshima T, Kim HC (2016) N-methyl, N-propynyl-2-phenylethylamine (MPPE), a selegiline analog, attenuates MPTP-induced dopaminergic toxicity with guaranteed behavioral safety: involvement of inhibitions of mitochondrial oxidative burdens and p53 gene-elicited pro-apoptotic change. Mol Neurobiol 53:6251–6269
Silva CD, Neves AF, Dias AI, Freitas HJ, Mendes SM, Pita I, Viana SD, de Oliveira PA, Cunha RA, Fontes Ribeiro CA, Prediger RD, Pereira FC (2014) A single neurotoxic dose of methamphetamine induces a long-lasting depressive-like behaviour in mice. Neurotox Res 25:295–304
Simon SL, Domier C, Carnell J, Brethen P, Rawson R, Ling W (2000) Cognitive impairment in individuals currently using methamphetamine. Am J Addict 9:222–231
Simon SL, Domier CP, Sim T, Richardson K, Rawson RA, Ling W (2002) Cognitive performance of current methamphetamine and cocaine abusers. J Addict Dis 21:61–74
Simon SL, Dacey J, Glynn S, Rawson R, Ling W (2004) The effect of relapse on cognition in abstinent methamphetamine abusers. J Subst Abuse Treat 27:59–66
Simon SL, Dean AC, Cordova X, Monterosso JR, London ED (2010) Methamphetamine dependence and neuropsychological functioning: evaluating change during early abstinence. J Stud Alcohol Drugs 71:335–344
Solhi H, Malekirad A, Kazemifar AM, Sharifi F (2014) Oxidative stress and lipid peroxidation in prolonged users of methamphetamine. Drug Metab Lett 7:79–82
Son JH, Kuhn J, Keefe KA (2013) Perseverative behavior in rats with methamphetamine-induced neurotoxicity. Neuropharmacology 67:95–103
Sonsalla PK, Gibb JW, Hanson GR (1986) Roles of D1 and D2 dopamine receptor subtypes in mediating the methamphetamine-induced changes in monoamine systems. J Pharmacol Exp Ther 238:932–937
Sonsalla PK, Riordan DE, Heikkila RE (1991) Competitive and noncompetitive antagonists at N-methyl-d-aspartate receptors protect against methamphetamine-induced dopaminergic damage in mice. J Pharmacol Exp Ther 256:506–512
Sonsalla PK, Jochnowitz ND, Zeevalk GD, Oostveen JA, Hall ED (1996) Treatment of mice with methamphetamine produces cell loss in the substantia nigra. Brain Res 738:172–175
Speidel D (2010) Transcription-independent p53 apoptosis: an alternative route to death. Trends Cell Biol 20:14–24
Sriram K, Miller DB, O’Callaghan JP (2006) Minocycline attenuates microglial activation but fails to mitigate striatal dopaminergic neurotoxicity: role of tumor necrosis factor-alpha. J Neurochem 96:706–718
Srisurapanont M, Ali R, Marsden J, Sunga A, Wada K, Monteiro M (2003) Psychotic symptoms in methamphetamine psychotic in-patients. Int J Neuropsychopharmacol 6:347–352
Stephans SE, Whittingham TS, Douglas AJ, Lust WD, Yamamoto BK (1998) Substrates of energy metabolism attenuate methamphetamine-induced neurotoxicity in striatum. J Neurochem 71:613–621
Sucic S, Dallinger S, Zdrazil B, Weissensteiner R, Jørgensen TN, Holy M, Kudlacek O, Seidel S, Cha JH, Gether U, Newman AH, Ecker GF, Freissmuth M, Sitte HH (2010) The N terminus of monoamine transporters is a lever required for the action of amphetamines. J Biol Chem 285:10924–10938
Sulzer D, Sonders MS, Poulsen NW, Galli A (2005) Mechanisms of neurotransmitter release by amphetamines: a review. Prog Neurobiol 75:406–433
Takigawa M, Maeda H, Ueyama K, Tominaga H, Matsumoto K (1993) A dual approach to self-stimulation and locomotor trace affected by chronic methamphetamine treatment for an animal model of schizophrenia. Can J Physiol Pharmacol 71:321–325
Tata DA, Yamamoto BK (2008) Chronic stress enhances methamphetamine-induced extracellular glutamate and excitotoxicity in the rat striatum. Synapse 62:325–336
Theodore S, Stolberg S, Cass WA, Maragos WF (2006) Human immunodeficiency virus-1 protein tat and methamphetamine interactions. Ann N Y Acad Sci 1074:178–190
Thomas DM, Kuhn DM (2005) MK-801 and dextromethorphan block microglial activation and protect against methamphetamine-induced neurotoxicity. Brain Res 1050:190–198
Thomas DM, Walker PD, Benjamins JA, Geddes TJ, Kuhn DM (2004) Methamphetamine neurotoxicity in dopamine nerve endings of the striatum is associated with microglial activation. J Pharmacol Exp Ther 311:1–7
Thompson PM, Hayashi KM, Simon SL, Geaga JA, Hong MS, Sui Y, Lee JY, Toga AW, Ling W, London ED (2004) Structural abnormalities in the brains of human subjects who use methamphetamine. J Neurosci 24:6028–6036
Thrash B, Karuppagounder SS, Uthayathas S, Suppiramaniam V, Dhanasekaran M (2010) Neurotoxic effects of methamphetamine. Neurochem Res 35:171–179
Thrash-Williams B, Karuppagounder SS, Bhattacharya D, Ahuja M, Suppiramaniam V, Dhanasekaran M (2016) Methamphetamine-induced dopaminergic toxicity prevented owing to the neuroprotective effects of salicylic acid. Life Sci 154:24–29
Todd G, Pearson-Dennett V, Wilcox RA, Chau MT, Thoirs K, Thewlis D, Vogel AP, White JM (2016) Adults with a history of illicit amphetamine use exhibit abnormal substantia nigra morphology and parkinsonism. Parkinsonism Relat Disord 25:27–32
Tomiyama G (1990) Chronic schizophrenia-like states in methamphetamine psychosis. Jpn J Psychiatry Neurol 44:531–539
Torres B, Ruoho AE (2014) N-terminus regulation of VMAT2 mediates methamphetamine-stimulated efflux. Neuroscience 259:194–202
Tran TV, Tran HQ, Tu TTH, Shin EJ, Jang CG, Yamada K, Nabeshima T, Kim HC (2016) PKCδ gene facilitates cognitive impairment induced by low doses of methamphetamine (MA) in mice. Int J Neuropsychopharmacol 19(Suppl 1):50. doi:10.1093/ijnp/pyw044.688
Truong JG, Wilkins DG, Baudys J, Crouch DJ, Johnson-Davis KL, Gibb JW, Hanson GR, Fleckenstein AE (2005) Age-dependent methamphetamine-induced alterations in vesicular monoamine transporter-2 function: implications for neurotoxicity. J Pharmacol Exp Ther 314:1087–1092
Tsuji T, Asanuma M, Miyazaki I, Miyoshi K, Ogawa N (2009) Reduction of nuclear peroxisome proliferator-activated receptor gamma expression in methamphetamine-induced neurotoxicity and neuroprotective effects of ibuprofen. Neurochem Res 34:764–774
Ujike H (2002) Stimulant-induced psychosis and schizophrenia: the role of sensitization. Curr Psychiatry Rep 4:177–184
Ujike H, Sato M (2004) Clinical features of sensitization to methamphetamine observed in patients with methamphetamine dependence and psychosis. Ann N Y Acad Sci 1025:279–287
United Nations Office on Drugs and Crime (2015) World Drug Report 2015. United Nations. https://www.unodc.org/documents/wdr2015/World_Drug_Report_2015.pdf. Accessed 28 June 2016
Villemagne V, Yuan J, Wong DF, Dannals RF, Hatzidimitriou G, Mathews WB, Ravert HT, Musachio J, McCann UD, Ricaurte GA (1998) Brain dopamine neurotoxicity in baboons treated with doses of methamphetamine comparable to those recreationally abused by humans: evidence from [11C]WIN-35,428 positron emission tomography studies and direct in vitro determinations. J Neurosci 18:419–427
Volkow ND, Chang L, Wang GJ, Fowler JS, Franceschi D, Sedler M, Gatley SJ, Miller E, Hitzemann R, Ding YS, Logan J (2001a) Loss of dopamine transporters in methamphetamine abusers recovers with protracted abstinence. J Neurosci 21:9414–9418
Volkow ND, Chang L, Wang GJ, Fowler JS, Leonido-Yee M, Franceschi D, Sedler MJ, Gatley SJ, Hitzemann R, Ding YS, Logan J, Wong C, Miller EN (2001b) Association of dopamine transporter reduction with psychomotor impairment in methamphetamine abusers. Am J Psychiatry 158:377–382
Volkow ND, Chang L, Wang GJ, Fowler JS, Ding YS, Sedler M, Logan J, Franceschi D, Gatley J, Hitzemann R, Gifford A, Wong C, Pappas N (2001c) Low level of brain dopamine D2 receptors in methamphetamine abusers: association with metabolism in the orbitofrontal cortex. Am J Psychiatry 158:2015–2021
Wagner GC, Lucot JB, Schuster CR, Seiden LS (1983) Alpha-methyltyrosine attenuates and reserpine increases METH-induced neuronal changes. Brain Res 270:285–288
Walker J, Winhusen T, Storkson JM, Lewis D, Pariza MW, Somoza E, Somoza V (2014) Total antioxidant capacity is significantly lower in cocaine-dependent and methamphetamine-dependent patients relative to normal controls: results from a preliminary study. Hum Psychopharmacol 29:537–543
Wang Q, Shin EJ, Nguyen XK, Li Q, Bach JH, Bing G, Kim WK, Kim HC, Hong JS (2012) Endogenous dynorphin protects against neurotoxin-elicited nigrostriatal dopaminergic neuron damage and motor deficits in mice. J Neuroinflammation 9:124
Wang Q, Chu CH, Oyarzabal E, Jiang L, Chen SH, Wilson B, Qian L, Hong JS (2014) Subpicomolar diphenyleneiodonium inhibits microglial NADPH oxidase with high specificity and shows great potential as a therapeutic agent for neurodegenerative diseases. Glia 62:2034–2043
Wang Q, Qian L, Chen SH, Chu CH, Wilson B, Oyarzabal E, Ali S, Robinson B, Rao D, Hong JS (2015) Post-treatment with ultra-low dose of NADPH oxidase inhibitor diphenyleneiodonium attenuates disease progression in multiple Parkinson’s disease models. Brain 138:1247–1262
Whitehead RE, Ferrer JV, Javitch JA, Justice JB (2001) Reaction of oxidized dopamine with endogenous cysteine residues in the human dopamine transporter. J Neurochem 76:1242–1251
Wilson JM, Kalasinsky KS, Levey AI, Bergeron C, Reiber G, Anthony RM, Schmunk GA, Shannak K, Haycock JW, Kish SJ (1996) Striatal dopamine nerve terminal markers in human, chronic methamphetamine users. Nat Med 2:699–703
Winyard PG, Moody CJ, Jacob C (2005) Oxidative activation of antioxidant defence. Trends Biochem Sci 30:453–461
Wu CF, Liu YL, Song M, Liu W, Wang JH, Li X, Yang JY (2003) Protective effects of pseudoginsenoside-F11 on methamphetamine-induced neurotoxicity in mice. Pharmacol Biochem Behav 76:103–109
Wu PH, Shen YC, Wang YH, Chi CW, Yen JC (2006) Baicalein attenuates methamphetamine-induced loss of dopamine transporter in mouse striatum. Toxicology 226:238–245
Wu CW, Ping YH, Yen JC, Chang CY, Wang SF, Yeh CL, Chi CW, Lee HC (2007) Enhanced oxidative stress and aberrant mitochondrial biogenesis in human neuroblastoma SHSY5Y cells during methamphetamine induced apoptosis. Toxicol Appl Pharmacol 220:243–251
Wu XF, Wang AF, Chen L, Huang EP, Xie WB, Liu C, Huang WY, Chen CX, Qiu PM, Wang HJ (2014) S-Nitrosylating protein disulphide isomerase mediates α-synuclein aggregation caused by methamphetamine exposure in PC12 cells. Toxicol Lett 230:19–27
Wu J, Zhu D, Zhang J, Li G, Liu Z, Sun J (2016) Melatonin treatment during the incubation of sensitization attenuates methamphetamine-induced locomotor sensitization and MeCP2 expression. Prog Neuropsychopharmacol Biol Psychiatry 65:145–152
Xie Z, Miller GM (2009) A receptor mechanism for methamphetamine action in dopamine transporter regulation in brain. J Pharmacol Exp Ther 330:316–325
Xu W, Zhu JP, Angulo JA (2005) Induction of striatal pre- and postsynaptic damage by methamphetamine requires the dopamine receptors. Synapse 58:110–121
Yamada H, Kuroki T, Nakahara T, Hashimoto K, Tsutsumi T, Hirano M, Maeda H (2007) The dopamine D1 receptor agonist, but not the D2 receptor agonist, induces gene expression of Homer 1a in rat striatum and nucleus accumbens. Brain Res 1131:88–96
Yoshida K (2007) PKCdelta signaling: mechanisms of DNA damage response and apoptosis. Cell Signal 19:892–901
Yoshimatsu A, Shimazoe T, Kawashimo A, Shuto T, Doi Y, Fukumoto T, Watanabe S (2001) Effects of adenosine A1- and A2A-receptor agonists on enhancement of dopamine release from the striatum in methamphetamine-sensitized rats. Jpn J Pharmacol 86:254–257
Yui K, Goto K, Ikemoto S, Ishiguro T, Angrist B, Duncan GE, Sheitman BB, Lieberman JA, Bracha SH, Ali SF (1999) Neurobiological basis of relapse prediction in stimulant-induced psychosis and schizophrenia: the role of sensitization. Mol Psychiatry 4:512–523
Yui K, Ikemoto S, Ishiguro T, Goto K (2000a) Studies of amphetamine or methamphetamine psychosis in Japan: relation of methamphetamine psychosis to schizophrenia. Ann N Y Acad Sci 914:1–12
Yui K, Ishiguro T, Goto K, Ikemoto S (2000b) Susceptibility to subsequent episodes in spontaneous recurrence of methamphetamine psychosis. Ann N Y Acad Sci 914:292–302
Yui K, Goto K, Ikemoto S, Ishiguro T (2000c) Stress induced spontaneous recurrence of methamphetamine psychosis: the relation between stressful experiences and sensitivity to stress. Drug Alcohol Depend 58:67–75
Zarrabi H, Khalkhali M, Hamidi A, Ahmadi R, Zavarmousavi M (2016) Clinical features, course and treatment of methamphetamine-induced psychosis in psychiatric inpatients. BMC Psychiatry 16:44
Zhang L, Kitaichi K, Fujimoto Y, Nakayama H, Shimizu E, Iyo M, Hashimoto K (2006) Protective effects of minocycline on behavioral changes and neurotoxicity in mice after administration of methamphetamine. Prog Neuropsychopharmacol Biol Psychiatry 30:1381–1393
Zhang W, Dallas S, Zhang D, Guo JP, Pang H, Wilson B, Miller DS, Chen B, Zhang W, McGeer PL, Hong JS, Zhang J (2007) Microglial PHOX and Mac-1 are essential to the enhanced dopaminergic neurodegeneration elicited by A30P and A53T mutant alpha synuclein. Glia 55:1178–1188
Zhang X, Tobwala S, Ercal N (2012) N-acetylcysteine amide protects against methamphetamine-induced tissue damage in CD-1 mice. Hum Exp Toxicol 31:931–944
Zhu JP, Xu W, Angulo JA (2006) Methamphetamine-induced cell death: selective vulnerability in neuronal subpopulations of the striatum in mice. Neuroscience 140:607–622
Acknowledgements
This study was supported by a Grant (#14182MFDS979) from the Korea Food and Drug Administration and, in part, by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT & Future Planning (#NRF-2016R1A1A1A05005201), Republic of Korea. Duy-Khanh Dang, The-Vinh Tran, and Hai-Quyen Tran were supported by the BK21 PLUS program, NRF, Republic of Korea. The English in this document has been checked by at least two professional editors, both native speakers of English (e-World Editing, Inc. Eugene, OR 97401, USA).
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Shin, EJ., Dang, DK., Tran, TV. et al. Current understanding of methamphetamine-associated dopaminergic neurodegeneration and psychotoxic behaviors. Arch. Pharm. Res. 40, 403–428 (2017). https://doi.org/10.1007/s12272-017-0897-y
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DOI: https://doi.org/10.1007/s12272-017-0897-y