Shotgun proteomics analysis of protein responding to methamphetamine addiction in rat cerebellum

Authors

  • Oranee Ritsayong Faculty of Medical Science, Naresuan University
  • Sri-arun Iamjan Faculty of Medical Science, Naresuan University
  • Sittiruk Roytrakul National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency
  • Samur Thanoi Faculty of Medical Science, Naresuan University
  • Sutisa Nudmamud-Thanoi Faculty of Medical Science, Naresuan University

Keywords:

Methamphetamine, drug addiction, cerebellum, proteomics

Abstract

Background : Methamphetamine (METH) is an addictive psychostimulant drug that induces damages several regions of the brain, including the cerebellum. METH can induce some proteins changes in synaptic neurotransmission and signal transduction underlying the mechanism of drug addiction in several brain regions such as the striatum, hippocampus and nucleus accumbens. Nevertheless, few studies have examined the effects of METH in the cerebellum.

Objective : The aim of the current study was to investigate changes in the synaptic neurotransmission and signal transduction protein expression in rat cerebellum following METH exposure using proteomics technique.

Methods : Male Sprague-Dawley rats were treated with an escalating dose-METH binge and saline in control group for 15 days. Three samples from each group were pooled and proteins were extracted from the cerebellar tissues. The proteomics, liquid chromatography-tandem mass spectrometry (LC-MS/ MS) was then performed to identify the protein associated with the METHinduced drug addiction.

Results : In the cerebellar samples, it was found that nine proteins were altered and mapped to synaptic transmission and signal transduction. In METH group, seven proteins were identified, including excitatory amino acid transporter 1, synaptotagmin-7, shisa-6, thioredoxin-related transmembrane protein 4, serine/ threonine-protein kinase SIK1, plexin-B3, calbindin, were found upregulation while two down-regulated proteins including cAMP-specific 3',5'-cyclic phosphodiesterase 4D and neuronal acetylcholine receptor subunit alpha-10 were observed.

Conclusion : The alteration of synaptic transmission and signal transduction proteins was found in the cerebellum following METH exposure. The results of this study provide evidence to support disturbance of protein expression in cerebellum in METH addiction.

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References

Srisurapanont M, Ali R, Marsden J, Sunga A, Wada K, Monteiro M. Psychotic symptoms in methamphetamine psychotic in-patients. Int J Neuropsychopharmacol 2003;6:347-52.

https://doi.org/10.1017/S1461145703003675

Mansouri MT, Naghizadeh B, Ghorbanzadeh B, Alboghobeish S, Houshmand G, Amirgholami N. Venlafaxine attenuates the development of morphine tolerance and dependence: role of L-arginine/nitric oxide/cGMP pathway. Endocr Metab Immune Disord Drug Targets 2017;18:1-9.

https://doi.org/10.2174/1871530318666171213153920

Simon SL, Domier C, Carnell J, Brethen P, Rawson R, Ling W. Cognitive impairment in individuals currently using methamphetamine. Am J Addict 2000;9:222-31.

https://doi.org/10.1080/10550490050148053

Koob GF, Volkow ND. Neurocircuitry of addiction. Neuropsychopharmacology 2010; 35:217-38.

https://doi.org/10.1038/npp.2009.110

Belujon P, Grace AA. Hippocampus, amygdala, and stress: interacting systems that affect susceptibility to addiction. Ann N Y Acad Sci 2011;1216:114-21. https://doi.org/10.1111/j.1749-6632.2010.05896.x

Wearne TA, Mirzaei M, Franklin JL, Goodchild AK, Haynes PA, Cornish JL. Methamphetamineinduced sensitization is associated with alterations to the proteome of the prefrontal cortex: implications for the maintenance of psychotic disorders. J Proteome Res 2015; 14:397-410.

https://doi.org/10.1021/pr500719f

Anderson CM, Maas LC, Frederick B, Bendor JT, Spencer TJ, Livni E, et al. Cerebellar vermis involvement in cocaine-related behaviors. Neuropsychopharmacology 2006;31:1318-26.

https://doi.org/10.1038/sj.npp.1300937

Vazquez-Sanroman D, Carbo-Gas M, Leto K, Cerezo-Garcia M, Gil-Miravet I, SanchisSegura C, et al. Cocaine-induced plasticity in the cerebellum of sensitised mice. Psychopharmacology (Berl) 2015;232:4455-67. https://doi.org/10.1007/s00213-015-4072-1

Moulton EA, Elman I, Becerra LR, Goldstein RZ, Borsook D. The cerebellum and addiction: insights gained from neuroimaging research. Addict Biol 2014;19:317-31.

https://doi.org/10.1111/adb.12101

Ferrucci M, Busceti CL, Falleni A, Giorgi FS, Ruggieri S, Fornai F. Effects of methamphetamine on the cerebellar cortex: a preliminary study. Ann N Y Acad Sci 2006;1074:149-53.

https://doi.org/10.1196/annals.1369.014

Hamamura M, Ozawa H, Kimuro Y, Okouchi J, Higasa K, Iwaki A, et al. Differential decreases in c-fos and aldolase C mRNA expression in the rat cerebellum after repeated administration of methamphetamine. Brain Res Mol Brain Res 1999;64:119-31.

https://doi.org/10.1016/S0169-328X(98)00306-4

Howell LL, Kimmel HL. Monoamine transporters and psychostimulant addiction. Biochem Pharmacol 2008;75:196-217. https://doi.org/10.1016/j.bcp.2007.08.003

Mark KA, Soghomonian JJ, Yamamoto BK. High-dose methamphetamine acutely activates the striatonigral pathway to increase striatal glutamate and mediate long-term dopamine toxicity. J Neurosci 2004;24: 11449-56. https://doi.org/10.1523/JNEUROSCI.3597-04.2004

Kuczenski R, Everall IP, Crews L, Adame A, Grant I, Masliah E. Escalating dose-multiple binge methamphetamine exposure results in degeneration of the neocortex and limbic system in the rat. Exp Neurol 2007;207: 42-51. https://doi.org/10.1016/j.expneurol.2007.05.023

Kerdsan W, Thanoi S, Nudmamud-Thanoi S. Changes in glutamate/NMDA receptor subunit 1 expression in rat brain after acute and subacute exposure to methamphetamine. J Biomed Biotechnol 2009;2009:329631. https://doi.org/10.1155/2009/329631

Yu MF, Lin TY, Ho WH, Yin HS. Amphetamine induces differential changes in the gene expression of metabotropic glutamate receptor 5 in cultured cortical and hippocampal neurons. J Mol Neurosci 2001;17:13-24. https://doi.org/10.1385/JMN:17:1:13

Kumari R, Lakhan R, Kalita J, Misra UK, Mittal B. Association of alpha subunit of GABAA receptor subtype gene polymorphisms with epilepsy susceptibility and drug resistance in north Indian population. Seizure 2010;19: 237-41. https://doi.org/10.1016/j.seizure.2010.02.009

Veerasakul S, Thanoi S, Reynolds GP, NudmamudThanoi S. Effect of Methamphetamine Exposure on Expression of Calcium Binding Proteins in Rat Frontal Cortex and Hippocampus. Neurotox Res 2016;30:427-33. https://doi.org/10.1007/s12640-016-9628-2

Wang L, Wu N, Zhao TY, Li J. The potential biomarkers of drug addiction: proteomic and metabolomics challenges. Biomarkers 2016; 1-8. https://doi.org/10.1080/1354750X.2016.1201530

Kobeissy FH, Warren MW, Ottens AK, Sadasivan S, Zhang Z, Gold MS, et al. Psychoproteomic analysis of rat cortex following acute methamphetamine exposure. J Proteome Res 2008;7:1971-83.

https://doi.org/10.1021/pr800029h

Segal DS, Kuczenski R, O'Neil ML, Melega WP, Cho AK. Escalating dose methamphetamine pretreatment alters the behavioral and neurochemical profiles associated with exposure to a high-dose methamphetamine binge. Neuropsychopharmacology 2003;28: 1730-40.

https://doi.org/10.1038/sj.npp.1300247

Kerdsan W, Thanoi S, Nudmamud-Thanoi S. Changes in the neuronal glutamate transporter EAAT3 in rat brain after exposure to methamphetamine. Basic Clin Pharmacol Toxicol 2012;111:275-8.

https://doi.org/10.1111/j.1742-7843.2012.00899.x

Shirai Y, Shirakawa O, Nishino N, Saito N, Nakai H. Increased striatal glutamate transporter by repeated intermittent administration of methamphetamine. Psychiatry Clin Neurosci 1996;50:161-4.

https://doi.org/10.1111/j.1440-1819.1996.tb01682.x

Raudensky J, Yamamoto BK. Effects of chronic unpredictable stress and methamphetamine on hippocampal glutamate function. Brain Res 2007;1135:129-35.

https://doi.org/10.1016/j.brainres.2006.12.002

Xue CJ, Ng JP, Li Y, Wolf ME. Acute and repeated systemic amphetamine administration:effects on extracellular glutamate, aspartate, and serine levels in rat ventral tegmental area and nucleus accumbens. J Neurochem 1996; 67:352-63. https://doi.org/10.1046/j.1471-4159.1996.67010352.x

Mark KA, Quinton MS, Russek SJ, Yamamoto BK. Dynamic changes in vesicular glutamate transporter 1 function and expression related to methamphetamine-induced glutamate release. J Neurosci 2007;27:6823-31. https://doi.org/10.1523/JNEUROSCI.0013-07.2007

Stephans SE, Yamamoto BY. Effect of repeated methamphetamine administrations on dopamine and glutamate efflux in rat prefrontal cortex. Brain Res 1995;700:99-106.

https://doi.org/10.1016/0006-8993(95)00938-M

Klaassen RV, Stroeder J, Coussen F, Hafner AS, Petersen JD, Renancio C, et al. Shisa6 traps AMPA receptors at postsynaptic sites and prevents their desensitization during synaptic activity. Nat Commun 2016;7:10682. https://doi.org/10.1038/ncomms10682

Wearne TA, Parker LM, Franklin JL, Goodchild AK, Cornish JL. Behavioral sensitization to methamphetamine induces specific interneuronal mRNA pathology across the prelimbic and orbitofrontal cortices. Prog Neuropsychopharmacol Biol Psychiatry 2017; 77:42-8.

https://doi.org/10.1016/j.pnpbp.2017.03.018

Isao T, Akiyama K. Effect of acute and chronic treatment with methamphetamine on mRNA expression of synaptotagmin IV and 25 KDa-synaptic-associated protein in the rat brain. Psychiatry Clin Neurosci 2004;58: 410-9. https://doi.org/10.1111/j.1440-1819.2004.01276.x

Dietrich JB, Takemori H, Grosch-Dirrig S, Bertorello A, Zwiller J. Cocaine induces the expression of MEF2C transcription factor in rat striatum through activation of SIK1 and phosphorylation of the histone deacetylase HDAC5. Synapse 2012;66:61-70. https://doi.org/10.1002/syn.20988

Fox J, Lu Z, Barrows L. Thiol-disulfide oxidoreductases TRX1 and TMX3 decrease neuronal atrophy in a lentiviral mouse model of Huntington's disease. PLoS Curr 2015;7 pii: ecurrents.hd.b966ec2eca8e2d89d2bb4d0 20be4351e.

Runker AE, O'Tuathaigh C, Dunleavy M, Morris DW, Little GE, Corvin AP, et al. Mutation of Semaphorin-6A disrupts limbic and cortical connectivity and models neurodevelopmental psychopathology. PLoS One 2011;6:e26488. https://doi.org/10.1371/journal.pone.0026488

Taslim N, Soderstrom K, Dar MS. Role of mouse cerebellar nicotinic acetylcholine receptor (nAChR) alpha(4)beta(2)- and alpha(7) subtypes in the behavioral cross-tolerance between nicotine and ethanol-induced ataxia. Behav Brain Res 2011;217:282-92. https://doi.org/10.1016/j.bbr.2010.10.026

Liu L, Yu J, Li L, Zhang B, Liu L, Wu CH, et al. Alpha7 nicotinic acetylcholine receptor is required for amyloid pathology in brain endothelial cells induced by Glycoprotein 120, methamphetamine and nicotine. Sci Rep 2017;7:40467. https://doi.org/10.1038/srep40467

Logrip ML. Phosphodiesterase regulation of alcohol drinking in rodents. Alcohol 2015;49: 795-802.

https://doi.org/10.1016/j.alcohol.2015.03.007

Schaefer TL, Braun AA, Amos-Kroohs RM, Williams MT, Ostertag E, Vorhees CV. A new model of Pde4d deficiency: genetic knockdown of PDE4D enzyme in rats produces an antidepressant phenotype without spatial cognitive effects. Genes Brain Behav 2012; 11:614-22. https://doi.org/10.1111/j.1601-183X.2012.00796.x

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Published

2023-08-16

How to Cite

1.
Ritsayong O, Iamjan S- arun, Roytrakul S, Thanoi S, Nudmamud-Thanoi S. Shotgun proteomics analysis of protein responding to methamphetamine addiction in rat cerebellum. Chula Med J [Internet]. 2023 Aug. 16 [cited 2024 Dec. 23];62(3). Available from: https://he05.tci-thaijo.org/index.php/CMJ/article/view/343

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Vol. 62 No. 3 (2018): Chulalongkorn Medical Journal

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Original Articles

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