Abstract
Methamphetamine (METH) is one of the most commonly abused agents by illicit-drug users. Thioredoxin-1 (Trx-1) plays important biological roles both in intra- and extracellular compartments, including in regulation of various intracellular molecules via thiol redox control. In this study, we found that Trx-1 was induced by METH in rat pheochromocytoma PC12 cells. Furthermore, PI3K/Akt pathway was involved in METH-induced increase of Trx-1 expression. An increase in phosphorylated cAMP response element-binding protein (CREB) was also observed after exposure of PC12 cells to METH, which was inhibited by a PI3K inhibitor, LY294002. In addition, the siRNA targeted toTrx-1 reduced the level of phosphorylated CREB by METH, suggesting Trx-1 is necessary for increased activity of CREB by METH. The results obtained in this study showed that Trx-1 might play a role in the actions of METH.
Similar content being viewed by others
References
Bai J, Nakamura H, Kwon YW, Hattori I, Yamaguchi Y, Kim YC, Kondo N, Oka S, Ueda S, Masutani H, Yodoi J (2003) Critical roles of thioredoxin in nerve growth factor-mediated signal transduction and neurite outgrowth in PC12 cells. J Neurosci 23:503–509
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
Barrot M, Olivier JD, Perrotti LI, DiLeone RJ, Berton O, Eisch AJ, Impey S, Storm DR, Neve RL, Yin JC, Zachariou V, Nestler EJ (2002) CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci USA 99:11435–11440
Brunzell DH, Mineur YS, Neve RL, Picciotto MR (2009) Nucleus accumbens CREB activity is necessary for nicotine conditioned place preference. Neuropsychopharmacology 34:1993–2001
Cadet JL, Ordonez SV, Ordonez JV (1997) Methamphetamine induces apoptosis in immortalized neural cells: protection by the proto-oncogene, bcl-2. Synapse 25:176–184
Carlezon WA Jr, Thome J, Olson VG, Lane-Ladd SB, Brodkin ES, Hiroi N, Duman RS, Neve RL, Nestler EJ (1998) Regulation of cocaine reward by CREB. Science 282:2272–2275
Carlezon WA Jr, Duman RS, Nestler EJ (2005) The many faces of CREB. Trends Neurosci 28:436–445
Cheng HC, Shih HM, Chern Y (2002) Essential role of cAMP-response element-binding protein activation by A2A adenosine receptors in rescuing the nerve growth factor-induced neurite outgrowth impaired by blockage of the MAPK cascade. J Biol Chem 277:33930–33942
Davis S, Vanhoutte P, Pages C, Caboche J, Laroche S (2000) The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J Neurosci 20:4563–4572
Desole MS, Sciola L, Delogu MR, Sircana S, Migheli R, Miele E (1997) Role of oxidative stress in the manganese and 1-methyl-4-(2′-ethylphenyl)-1,2,3,6-tetrahydropyridine-induced apoptosis in PC12 cells. Neurochem Int 31:169–176
Di Chiara G, Acquas E, Tanda G, Cadoni C (1993) Drugs of abuse: biochemical surrogates of specific aspects of natural reward? Biochem Soc Symp 59:65–81
Dietz DM, Dietz KC, Nestler EJ, Russo SJ (2009) Molecular mechanisms of psychostimulant-induced structural plasticity. Pharmacopsychiatry 42(Suppl 1):S69–S78
DiRocco DP, Scheiner ZS, Sindreu CB, Chan GC, Storm DR (2009) A role for calmodulin-stimulated adenylyl cyclases in cocaine sensitization. J Neurosci 29:2393–2403
Du K, Montminy M (1998) CREB is a regulatory target for the protein kinase Akt/PKB. J Biol Chem 273:32377–32379
Han W, Takamatsu Y, Yamamoto H, Kasai S, Endo S, Shirao T, Kojima N, Ikeda K (2011) Inhibitory role of inducible cAMP early repressor (ICER) in methamphetamine-induced locomotor sensitization. PLoS One 6:e21637
Hartley A, Stone JM, Heron C, Cooper JM, Schapira AH (1994) Complex I inhibitors induce dose-dependent apoptosis in PC12 cells: relevance to Parkinson’s disease. J Neurochem 63:1987–1990
Hirota K, Matsui M, Murata M, Takashima Y, Cheng FS, Itoh T, Fukuda K, Yodoi J (2000) Nucleoredoxin, glutaredoxin, and thioredoxin differentially regulate NF-kappaB, AP-1, and CREB activation in HEK293 cells. Biochem Biophys Res Commun 274:177–182
Kondo N, Nakamura H, Masutani H, Yodoi J (2006) Redox regulation of human thioredoxin network. Antioxid Redox Signal 8:1881–1890
Kuczenski R, Segal DS, Cho AK, Melega W (1995) Hippocampus norepinephrine, caudate dopamine and serotonin, and behavioral responses to the stereoisomers of amphetamine and methamphetamine. J Neurosci 15:1308–1317
Kuhar MJ, Jaworski JN, Hubert GW, Philpot KB, Dominguez G (2005) Cocaine- and amphetamine-regulated transcript peptides play a role in drug abuse and are potential therapeutic targets. AAPS J 7:E259–E265
Larson EB, Graham DL, Arzaga RR, Buzin N, Webb J, Green TA, Bass CE, Neve RL, Terwilliger EF, Nestler EJ, Self DW (2011) Overexpression of CREB in the nucleus accumbens shell increases cocaine reinforcement in self-administering rats. J Neurosci 31:16447–16457
Luo FC, Qi L, Lv T, Wang SD, Liu H, Nakamura H, Yodoi J, Bai J (2012) Geranylgeranylacetone protects mice against morphine-induced hyperlocomotion, rewarding effect, and withdrawal syndrome. Free Radic Biol Med 52:1218–1227
Maldonado R, Blendy JA, Tzavara E, Gass P, Roques BP, Hanoune J, Schutz G (1996) Reduction of morphine abstinence in mice with a mutation in the gene encoding CREB. Science 273:657–659
Martin F, Nunez C, Marin MT, Laorden ML, Kovacs KJ, Milanes MV (2012) Involvement of noradrenergic transmission in the PVN on CREB activation, TORC1 levels, and pituitary-adrenal axis activity during morphine withdrawal. PLoS One 7:e31119
Masutani H, Bai J, Kim YC, Yodoi J (2004) Thioredoxin as a neurotrophic cofactor and an important regulator of neuroprotection. Mol Neurobiol 29:229–242
McClung CA, Nestler EJ (2003) Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat Neurosci 6:1208–1215
McDaid J, Graham MP, Napier TC (2006) Methamphetamine-induced sensitization differentially alters pCREB and DeltaFosB throughout the limbic circuit of the mammalian brain. Mol Pharmacol 70:2064–2074
Moron JA, Gullapalli S, Taylor C, Gupta A, Gomes I, Devi LA (2010) Modulation of opiate-related signaling molecules in morphine-dependent conditioned behavior: conditioned place preference to morphine induces CREB phosphorylation. Neuropsychopharmacology 35:955–966
Pliakas AM, Carlson RR, Neve RL, Konradi C, Nestler EJ, Carlezon WA Jr (2001) Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J Neurosci 21:7397–7403
Rau TF, Kothiwal A, Zhang L, Ulatowski S, Jacobson S, Brooks DM, Cardozo-Pelaez F, Chopp M, Poulsen DJ (2011) Low dose methamphetamine mediates neuroprotection through a PI3K-AKT pathway. Neuropharmacology 61:677–686
Song W, Guan HJ, Zhu XZ, Chen ZL, Yin ML, Cheng XF (2000) Protective effect of bilobalide against nitric oxide-induced neurotoxicity in PC12 cells. Acta Pharmacol Sin 21:415–420
Svenningsson P, Tzavara ET, Carruthers R, Rachleff I, Wattler S, Nehls M, McKinzie DL, Fienberg AA, Nomikos GG, Greengard P (2003) Diverse psychotomimetics act through a common signaling pathway. Science 302:1412–1415
Vialou V, Feng J, Robison AJ, Ku SM, Ferguson D, Scobie KN, Mazei-Robison MS, Mouzon E, Nestler EJ (2012) Serum response factor and cAMP response element binding protein are both required for cocaine induction of {Delta}FosB. J Neurosci 32:7577–7584
Widnell KL, Russell DS, Nestler EJ (1994) Regulation of expression of cAMP response element-binding protein in the locus coeruleus in vivo and in a locus coeruleus-like cell line in vitro. Proc Natl Acad Sci USA 91:10947–10951
Yang HY, Pu XP (2009) Chronic morphine administration induces over-expression of aldolase C with reduction of CREB phosphorylation in the mouse hippocampus. Eur J Pharmacol 609:51–57
Zhou LF, Zhu YP (2006) Changes of CREB in rat hippocampus, prefrontal cortex and nucleus accumbens during three phases of morphine induced conditioned place preference in rats. J Zhejiang Univ Sci B 7:107–113
Acknowledgments
This study was supported by the National Natural Science Foundation of China (No. 81160162, U1202227), and a grant from the Key Laboratory of Medical Neurobiology, Kunming University of Science and Technology.
Conflict of interest
The authors declare that they have no competing financial interests.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lv, T., Wang, SD. & Bai, J. Thioredoxin-1 was Required for CREB Activity by Methamphetamine in Rat Pheochromocytoma Cells. Cell Mol Neurobiol 33, 319–325 (2013). https://doi.org/10.1007/s10571-012-9897-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10571-012-9897-0