Molecular Neurobiology

, Volume 55, Issue 5, pp 4136–4159 | Cite as

Protein Kinase Cδ Gene Depletion Protects Against Methamphetamine-Induced Impairments in Recognition Memory and ERK1/2 Signaling via Upregulation of Glutathione Peroxidase-1 Gene

  • The-Vinh Tran
  • Eun-Joo Shin
  • Lan Thuy Ty Nguyen
  • Youngho Lee
  • Dae-Joong Kim
  • Ji Hoon Jeong
  • Choon-Gon Jang
  • Seung-Yeol Nah
  • Kazuya Toriumi
  • Toshitaka Nabeshima
  • Kiyofumi Yamada
  • Hyoung-Chun Kim
Article

Abstract

Accumulating evidence has suggested that repeated treatment with methamphetamine (MA) resulted in cognitive impairments. Importantly, we show that selective upregulation of protein kinase Cδ (PKCδ) in the prefrontal cortex (PFC) of wild-type mice persisted for 28 days post withdrawal of MA. On day 28, the MA-induced increase in phospho-PKCδ expression and decrease in phospho-ERK1/2 expression were significantly attenuated by both the Src inhibitor PP2 and the dopamine D1 receptor antagonist SCH 23390. However, neither protein kinase A inhibitor H89 nor calmodulin-dependent protein kinase II inhibitor KN93 attenuated MA-induced alterations in phospho-PKCδ expression and phospho-ERK1/2 expression. Since PKCδ knockout (KO) significantly increased the expression of glutathione peroxidase (GPx)-1, we also utilized GPx-1 KO and GPx-1-overexpressing transgenic (GPx-1 TG) mice. Repeated MA treatment induced cognitive impairment, as assessed by the novel object recognition test. Moreover, the extent of cognitive impairment correlated with the extent of increased phospho-PKCδ expression and decreased GPx1 expression. In the absence of MA, exposure to novel objects increased phospho-ERK1/2 and GPx-1 expression in the PFC; however, these expression levels were decreased in the presence of MA. PKCδ KO and GPx-1 TG mice each exhibited significantly attenuated MA-induced decreases in phospho-ERK1/2 and GPx-1 expression. Consistently, PKCδ inhibition induces GPx/GSH-dependent antioxidant systems. More importantly, the antipsychotic drug clozapine significantly protected against cognitive impairment and was associated with alterations in phospho-ERK1/2 and phospho-PKCδ expression. However, GPx-1 KO potentiated MA-induced cognitive deficits and alterations in phospho-ERK1/2 and phospho-PKCδ expression. These results suggest that MA induces cognitive impairment by inhibiting ERK1/2 signaling, activating PKCδ, and inactivating GPx-1 by upregulating Src kinase or the D1 receptor. They also suggest that clozapine requires activation of ERK1/2 signaling via positive modulation between the phospho-PKCδ and GPx-1 genes to restore cognitive function.

Keywords

Methamphetamine-induced cognitive impairment Prefrontal cortex Novel object recognition test Protein kinase Cδ Glutathione peroxidasex-1 ERK1/2 signaling Antipsychotic clozapine 

Abbreviations

AChE

Acetylcholine esterase

c-Abl

Abelson tyrosine kinase

CaMKII

Ca2+/calmodulin-dependent protein kinase II

ChAT

Choline acetyl transferase

CREB

cAMP response binding protein

DMSO

Dimethyl sulfoxide

DNA-PK

DNA-dependent protein kinase

Elk-1

ETS-like gene-1

ERK1/2

Extracellular signal-regulated kinases 1/2

GFAP

Glial fibrillary acidic protein

GPx-1

Glutathione peroxidase-1

GSH

Glutathione

GSSG

Glutathione disulfide

hRad9

Human checkpoint protein Rad9

Iba-1

Ionized calcium-binding adapter molecule 1

KO

Knockout

MA

Methamphetamine

MAPK

Mitogen-activated protein kinase

Neu-N

Neuronal nuclei

NFκB

Nuclear factor kappa B

NORT

Novel object recognition test

Nrf2

Nuclear factor (erythroid-derived 2)-like 2

PFC

Prefrontal cortex

PKA

Protein kinase A

PKCδ

Protein kinase C delta

PLS3

Phospholipid scramblase 3

SHPTP1

Src homology 2-containing tyrosine phosphatase 1

Src kinase

Proto-oncogene tyrosine-protein kinase Src

STAT1

Signal transducer and activator of transcription 1

TAAR1

Trace amine associated receptor 1

TG

Overexpressing transgenic

WT

Wild type

Notes

Acknowledgements

This study was supported by a grant (14182MFDS979) from the Korea Food and Drug Administration, Republic of Korea, and in part by JSPS KAKENHI Grants (No. 26460240, 16K10195) from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and a grant-in-aid of SRF. The-Vinh Tran and Lan Thuy Ty Nguyen were supported by the BK21 PLUS program.

Compliance with Ethical Standards

All the mice were treated in strict accordance with the NIH Guide for the Humane Care and Use of Laboratory Animals.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Supplementary material

12035_2017_638_MOESM1_ESM.pdf (373 kb)
Supplementary Fig. S1 (PDF 372 kb)
12035_2017_638_MOESM2_ESM.pdf (292 kb)
Supplementary Fig. S2 (PDF 292 kb)
12035_2017_638_MOESM3_ESM.pdf (103 kb)
Supplementary Fig. S3 (PDF 103 kb)
12035_2017_638_MOESM4_ESM.pdf (132 kb)
Supplementary Fig. S4 (PDF 131 kb)
12035_2017_638_MOESM5_ESM.pdf (105 kb)
Supplementary Fig. S5 (PDF 104 kb)
12035_2017_638_MOESM6_ESM.pdf (161 kb)
Supplementary Fig. S6 (PDF 160 kb)
12035_2017_638_MOESM7_ESM.pdf (173 kb)
Supplementary Fig. S7 (PDF 172 kb)
12035_2017_638_MOESM8_ESM.pdf (1.1 mb)
Supplementary Fig. S8 (PDF 1170 kb)
12035_2017_638_MOESM9_ESM.pdf (261 kb)
Supplementary Fig. S9 (PDF 260 kb)
12035_2017_638_MOESM10_ESM.pdf (125 kb)
Supplementary Fig. S10 (PDF 125 kb)
12035_2017_638_MOESM11_ESM.docx (38 kb)
ESM 1 (DOCX 37 kb)

References

  1. 1.
    Srisurapanont M, Ali R, Marsden J, Sunga A, Wada K, Monteiro M (2003) Psychotic symptoms in methamphetamine psychotic in-patients. Int J Neuropsychopharmacol 6:347–352CrossRefPubMedGoogle Scholar
  2. 2.
    Simon SL, Domier C, Carnell J, Brethen P, Rawson R, Ling W (2000) Cognitive impairment in individuals currently using methamphetamine. Am J Addict 9:222–231CrossRefPubMedGoogle Scholar
  3. 3.
    Nordahl TE, Salo R, Leamon M (2003) Neuropsychological effects of chronic methamphetamine use on neurotransmitters and cognition: a review. J Neuropsychiatry Clin Neurosci 15:317–325CrossRefPubMedGoogle Scholar
  4. 4.
    Arai S, Takuma K, Mizoguchi H, Ibi D, Nagai T, Kamei H, Kim HC, Yamada K (2009) GABAB receptor agonist baclofen improves methamphetamine-induced cognitive deficit in mice. Eur J Pharmacol 602:101–104CrossRefPubMedGoogle Scholar
  5. 5.
    Kamei H, Nagai T, Nakano H, Togan Y, Takayanagi M, Takahashi K, Kobayashi K, Yoshida S et al (2006) Repeated methamphetamine treatment impairs recognition memory through a failure of novelty-induced ERK1/2 activation in the prefrontal cortex of mice. Biol Psychiatry 59:75–84CrossRefPubMedGoogle Scholar
  6. 6.
    Loftis JM, Choi D, Hoffman W, Huckans MS (2011) Methamphetamine causes persistent immune dysregulation: a cross-species, translational report. Neurotox Res 20:59–68CrossRefPubMedGoogle Scholar
  7. 7.
    Loftis JM, Huckans M (2013) Substance use disorders: Psychoneuroimmunological mechanisms and new targets for therapy. Pharmacol Ther 139:289–300CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Beardsley PM, Hauser KF (2014) Glial modulators as potential treatments of psychostimulant abuse. Adv Pharmacol 69:1–69CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Ramesh G, MacLean AG, Philipp MT (2013) Cytokines and chemokines at the crossroads of neuroinflammation, neurodegeneration, and neuropathic pain. Mediat Inflamm 2013:480739Google Scholar
  10. 10.
    Borgmann K, Ghorpade A (2015) HIV-1, methamphetamine and astrocytes at neuroinflammatory crossroads. Front Microbiol 6:1143CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Cadet JL, Bisagno V (2014) Glial-neuronal ensembles: partners in drug addiction-associated synaptic plasticity. Front Pharmacol 5:204CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Panicker N, Saminathan H, Jin H, Neal M, Harischandra DS, Gordon R, Kanthasamy K, Lawana V et al (2015) Fyn kinase regulates microglial neuroinflammatory responses in cell culture and animal models of Parkinson’s disease. J Neurosci 35:10058–10077CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Gordon R, Singh N, Lawana V, Ghosh A, Harischandra DS, Jin H, Hogan C, Sarkar S et al (2016) Protein kinase Cδ upregulation in microglia drives neuroinflammatory responses and dopaminergic neurodegeneration in experimental models of Parkinson’s disease. Neurobiol Dis 93:96–114CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Nguyen XK, Lee J, Shin EJ, Dang DK, Jeong JH, Nguyen TT, Nam Y, Cho HJ et al (2015) Liposomal melatonin rescues methamphetamine-elicited mitochondrial burdens, pro-apoptosis, and dopaminergic degeneration through the inhibition PKCδ gene. J Pineal Res 58:86–106CrossRefPubMedGoogle Scholar
  15. 15.
    Nam Y, Wie MB, Shin EJ, Nguyen TT, Nah SY, Ko SK, Jeong JH, Jang CG et al (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 35:927–944CrossRefPubMedGoogle Scholar
  16. 16.
    Dang DK, Duong CX, Nam Y, Shin EJ, Lim YK, Jeong JH, Jang CG, Nah SY et al (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 42:192–201CrossRefPubMedGoogle Scholar
  17. 17.
    Shin EJ, Duong CX, Nguyen TX, Bing G, Bach JH, Park DH, Nakayama K, Ali SF et al (2011) PKCδ inhibition enhances tyrosine hydroxylase phosphorylation in mice after methamphetamine treatment. Neurochem Int 59:39–50CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Shin EJ, Duong CX, Nguyen XK, Li Z, Bing G, Bach JH, Park DH, Nakayama K et al (2012) Role of oxidative stress in methamphetamine-induced dopaminergic toxicity mediated by protein kinase C delta. Behav Brain Res 232:98–113CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Shin EJ, Nam Y, Tu TT, Lim YK, Wie MB, Kim DJ, Jeong JH, Kim HC (2016) Protein kinase Cδ mediates trimethyltin-induced neurotoxicity in mice in vivo via inhibition of glutathione defense mechanism. Arch Toxicol 90:937–953CrossRefPubMedGoogle Scholar
  20. 20.
    Lei XG, Cheng WH, McClung JP (2007) Metabolic regulation and function of glutathione peroxidase-1. Annu Rev Nutr 27:41–61CrossRefPubMedGoogle Scholar
  21. 21.
    Barayuga SM, Pang X, Andres MA, Panee J, Bellinger FP (2013) Methamphetamine decreases levels of glutathione peroxidases 1 and 4 in SH-SY5Y neuronal cells: protective effects of selenium. Neurotoxicology 37:240–246CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    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 851:76–86CrossRefPubMedGoogle Scholar
  23. 23.
    Shin EJ, Shin SW, Nguyen TT, Park DH, Wie MB, Jang CG, Nah SY, Yang BW et al (2014) Ginsenoside re rescues methamphetamine-induced oxidative damage, mitochondrial dysfunction, microglial activation, and dopaminergic degeneration by inhibiting the protein kinase Cδ gene. Mol Neurobiol 49:1400–1421CrossRefPubMedGoogle Scholar
  24. 24.
    Dias R, Robbins TW, Roberts AC (1996) Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380:69–72CrossRefPubMedGoogle Scholar
  25. 25.
    Nagai T, Takuma K, Kamei H, Ito Y, Nakamichi N, Ibi D, Nakanishi Y, Murai M et al (2007) Dopamine D1 receptors regulate protein synthesis-dependent long-term recognition memory via extracellular signal-regulated kinase 1/2 in the prefrontal cortex. Learn Mem 14:117–125CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Schafe GE, Atkins CM, Swank MW, Bauer EP, Sweatt JD, LeDoux JE (2000) Activation of ERK/MAP kinase in the amygdale is required for memory consolidation of pavlovian fear conditioning. J Neurosci 20:8177–8187PubMedGoogle Scholar
  27. 27.
    Miyamoto A, Nakayama K, Imaki H, Hirose S, Jiang Y, Abe M, Tsukiyama T, Nagahama H et al (2002) Increased proliferation of B cells and auto-immunity in mice lacking protein kinase C delta. Nature 416:865–869CrossRefPubMedGoogle Scholar
  28. 28.
    Ho YS, Magnenat JL, Bronson RT, Cao J, Gargano M, Sugawara M, Funk CD (1997) Mice deficient in cellular glutathione peroxidase develop normally and show no increased sensitivity to hyperoxia. J Biol Chem 272:16644–16651CrossRefPubMedGoogle Scholar
  29. 29.
    Cheng WH, Ho YS, Ross DA, Valentine BA, Combs GF, Lei XG (1997) Cellular glutathione peroxidase knockout mice express normal levels of selenium-dependent plasma and phospholipid hydroperoxide glutathione peroxidases in various tissues. J Nutr 127:1445–1450CrossRefPubMedGoogle Scholar
  30. 30.
    Cheng WH, Ho YS, Valentine BA, Ross DA, Combs GF Jr, Lei XG (1998) Cellular glutathione peroxidase is the mediator of body selenium to protect against paraquat lethality in transgenic mice. J Nutr 128:1070–1076CrossRefPubMedGoogle Scholar
  31. 31.
    Kim SD, Yang SI, Kim HC, Shin CY, Ko KH (2007) Inhibition of GSK-3beta mediates expression of MMP-9 through ERK1/2 activation and translocation of NF-kappaB in rat primary astrocyte. Brain Res 1186:12–20CrossRefPubMedGoogle Scholar
  32. 32.
    Shin EJ, Nabeshima T, Suh HW, Jhoo WK, Oh KW, Lim YK, Kim DS, Choi KH et al (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 158:143–157CrossRefPubMedGoogle Scholar
  33. 33.
    Tran TV, Shin EJ, Jeong JH, Lee JW, Lee Y, Jang CG, Nah SY, Lei XG et al (2016) Protective potential of the glutathione peroxidase-1 gene in abnormal behaviors induced by phencyclidine in mice. Mol Neurobiol. doi: 10.1007/s12035-016-0239-y
  34. 34.
    Kim HJ, Shin EJ, Lee BH, Choi SH, Jung SW, Cho IH, Hwang SH, Kim JY et al (2015) Oral Administration of gintonin attenuates cholinergic impairments by scopolamine, amyloid-β protein, and mouse model of Alzheimer’s disease. Mol Cells 38:796–805CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Shin EJ, Ko KH, Kim WK, Chae JS, Yen TP, Kim HJ, Wie MB, Kim HC (2008) Role of glutathione peroxidase in the ontogeny of hippocampal oxidative stress and kainate seizure sensitivity in the genetically epilepsy-prone rats. Neurochem Int 52:1134–1147CrossRefPubMedGoogle Scholar
  36. 36.
    Tran HY, Shin EJ, Saito K, Nguyen XK, Chung YH, Jeong JH, Bach JH, Park DH et al (2012) Protective potential of IL-6 against trimethyltin-induced neurotoxicity in vivo. Free Radic Biol Med 52:1159–1174CrossRefPubMedGoogle Scholar
  37. 37.
    Janknecht R, Ernst WH, Pingoud V, Nordheim A (1993) Activation of ternary complex factor Elk-1 by MAP kinases. EMBO J 12:5097–5104PubMedPubMedCentralGoogle Scholar
  38. 38.
    Mayr BM, Canettieri G, Montminy MR (2001) Distinct effects of cAMP and mitogenic signals on CREB-binding protein recruitment impact specificity to target gene activation via CREB. Proc Natl Acd Sci USA 98:10936–10941CrossRefGoogle Scholar
  39. 39.
    Treisman R (1996) Regulation of transcription by MAP kinase cascades. Curr Opin Cell Biol 8:205–215CrossRefPubMedGoogle Scholar
  40. 40.
    McAllister AK, Katz LC, Lo DC (1999) Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22:295–318CrossRefPubMedGoogle Scholar
  41. 41.
    West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM, Shaywitz AJ, Takasu MA, Tao X et al (2001) Calcium regulation of neuronal gene expression. Proc Natl Acad Sci U S A 98:11024–11031CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602–609CrossRefPubMedGoogle Scholar
  43. 43.
    Kelleher RJ III, Govindarajan A, Jung HY, Kang H, Tonegawa S (2004) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116:467–479CrossRefPubMedGoogle Scholar
  44. 44.
    Narita M, Akai H, Nagumo Y, Sunagawa N, Hasebe K, Nagase H, Kita T, Hara C et al (2004) Implications of protein kinase C in the nucleus accumbens in the development of sensitization to methamphetamine in rats. Neuroscience 127:941–948CrossRefPubMedGoogle Scholar
  45. 45.
    Altuntas I, Aksoy H, Coskun I, Cayköylü A, Akçay F (2000) Erythrocyte superoxide dismutase and glutathione peroxidase activities, and malondialdehyde and reduced glutathione levels in schizophrenic patients. Clin Chem Lab Med 38:1277–1281CrossRefPubMedGoogle Scholar
  46. 46.
    Yao JK, Reddy RD, van Kammen DP (1999) Human plasma glutathione peroxidase and symptom severity in schizophrenia. Biol Psychiatry 45:1512–1515CrossRefPubMedGoogle Scholar
  47. 47.
    Gawryluk JW, Wang JF, Andreazza AC, Shao L, Young LT (2011) Decreased levels of glutathione, the major brain antioxidant, in post-mortem prefrontal cortex from patients with psychiatric disorders. Int J Neuropsychopharmacol 14:123–130CrossRefPubMedGoogle Scholar
  48. 48.
    Radonjić NV, Knezević ID, Vilimanovich U, Kravić-Stevović T, Marina LV, Nikolić T, Todorović V, Bumbasirević V et al (2010) Decreased glutathione levels and altered antioxidant defense in an animal model of schizophrenia: long-term effects of perinatal phencyclidine administration. Neuropharmacology 58:739–745CrossRefPubMedGoogle Scholar
  49. 49.
    Ward NE, Pierce DS, Chung SE, Gravitt KR, O'Brian CA (1998) Irreversible inactivation of protein kinase C by glutathione. J Biol Chem 273:12558–12566CrossRefPubMedGoogle Scholar
  50. 50.
    Domenicotti C, Marengo B, Nitti M, Verzola D, Garibotto G, Cottalasso D, Poli G, Melloni E et al (2003) A novel role of protein kinase C-delta in cell signaling triggered by glutathione depletion. Biochem Pharmacol 66:1521–1526CrossRefPubMedGoogle Scholar
  51. 51.
    Domenicotti C, Marengo B, Verzola D, Garibotto G, Traverso N, Patriarca S, Maloberti G, Cottalasso D et al (2003) Role of PKC-delta activity in glutathione-depleted neuroblastoma cells. Free Radic Biol Med 35:504–516CrossRefPubMedGoogle Scholar
  52. 52.
    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 210:308–332CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Corcoran A, Cotter TG (2013) Redox regulation of protein kinases. FEBS J 280:1944–1965CrossRefPubMedGoogle Scholar
  54. 54.
    Ito Y, Takuma K, Mizoguchi H, Nagai T, Yamada K (2007) A novel azaindolizinone derivative ZSET1446 (Spiro[imidazo[1,2-a]pyridine-3,2-indan]-2(3H)-one) improves methamphetamine-induced impairment of recognition memory in mice by activating extracellular signal-regulated kinase 1/2. J Pharmacol Exp Ther 320:819–827CrossRefPubMedGoogle Scholar
  55. 55.
    Noda Y, Mouri A, Ando Y, Waki Y, Yamada SN, Yoshimi A, Yamada K, Ozaki N et al (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 13:1343–1354CrossRefPubMedGoogle Scholar
  56. 56.
    Hida H, Mouri A, Mori K, Matsumoto Y, Seki T, Taniguchi M, Yamada K, Iwamoto K et al (2015) Blonanserin ameliorates phencyclidine-induced visual-recognition memory deficits: the complex mechanism of blonanserin action involving D3-5-HT2A and D1-NMDA receptors in the mPFC. Neuropsychopharmacology 40:601–613CrossRefPubMedGoogle Scholar
  57. 57.
    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 26:53–63CrossRefPubMedGoogle Scholar
  58. 58.
    Volkow ND, Chang L, Wang GJ, Fowler JS, Leonido-Yee M, Franceschi D (2001) Association of dopamine transporter reduction with psychomotor impairment in methamphetamine abusers. Am J Psychiatry 158:377–382CrossRefPubMedGoogle Scholar
  59. 59.
    Réus GZ, Fries GR, Stertz L, Badawy M, Passos IC, Barichello T, Kapczinski F, Quevedo J (2015) The role of inflammation and microglial activation in the pathophysiology of psychiatric disorders. Neuroscience 300:141–154CrossRefPubMedGoogle Scholar
  60. 60.
    Pereira M, Siba IP, Chioca LR, Correia D, Vital MA, Pizzolatti MG, Santos AR, Andreatini R (2011) Myricitrin, a nitric oxide and protein kinase C inhibitor, exerts antipsychotic-like effects in animal models. Prog Neuro-Psychopharmacol Biol Psychiatry 35:1636–1644CrossRefGoogle Scholar
  61. 61.
    Abrial E, Lucas G, Scarna H, Haddjeri N, Lambás-Señas L (2011) A role for the PKC signaling system in the pathophysiology and treatment of mood disorders: involvement of a functional imbalance? Mol Neurobiol 44:407–419CrossRefPubMedGoogle Scholar
  62. 62.
    Sugino H, Futamura T, Mitsumoto Y, Maeda K, Marunaka Y (2009) Atypical antipsychotics suppress production of proinflammatory cytokines and up-regulate interleukin-10 in lipopolysaccharide-treated mice. Prog Neuro-Psychopharmacol Biol Psychiatry 33:303–307CrossRefGoogle Scholar
  63. 63.
    Möller M, Du Preez JL, Emsley R, Harvey BH (2011) Isolation rearing-induced deficits in sensorimotor gating and social interaction in rats are related to cortico-striatal oxidative stress, and reversed by sub-chronic clozapine administration. Eur Neuropsychopharmacol 21:471–483CrossRefPubMedGoogle Scholar
  64. 64.
    Aoyama Y, Mouri A, Toriumi K, Koseki T, Narusawa S, Ikawa N, Mamiya T, Nagai T et al (2014) Clozapine ameliorates epigenetic and behavioral abnormalities induced by phencyclidine through activation of dopamine D1 receptor. Int J Neuropsychopharmacol 17:723–737CrossRefPubMedGoogle Scholar
  65. 65.
    McMillian MK, Vainio PJ, Tuominen RK (1997) Role of protein kinase C in microglia-induced neurotoxicity in mesencephalic cultures. J Neuropathol Exp Neurol 56:301–307CrossRefPubMedGoogle Scholar
  66. 66.
    Dvoriantchikova G, Santos AR, Saeed AM, Dvoriantchikova X, Ivanov D (2014) Putative role of protein kinase C in neurotoxic inflammation mediated by extracellular heat shock protein 70 after ischemia-reperfusion. J Neuroinflammation 11:81CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Jeohn GH, Cooper CL, Jang KJ, Liu B, Lee DS, Kim HC, Hong JS (2002) Gö6976 inhibits LPS-induced microglial TNFalpha release by suppressing p38 MAP kinase activation. Neuroscience 114:689–697CrossRefPubMedGoogle Scholar
  68. 68.
    Salonen T, Sareila O, Jalonen U, Kankaanranta H, Tuominen R, Moilanen E (2006) Inhibition of classical PKC isoenzymes downregulates STAT1 activation and iNOS expression in LPS-treated murine J774 macrophages. Br J Pharmacol 147:790–799CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Suh KS, Tatunchak TT, Crutchley JM, Edwards LE, Marin KG, Yuspa SH (2003) Genomic structure and promoter analysis of PKC-δ. Genomics 82:57–67CrossRefPubMedGoogle Scholar
  70. 70.
    Jarvis CI, Staels B, Brugg B, Lemaigre-Dubreuil Y, Tedgui A, Mariani J (2002) Age-related phenotypes in the staggerer mouse expand the ROR-alpha nuclear receptor’s role beyond the cerebellu. Mol Cell Endocrinol 186:1–5CrossRefPubMedGoogle Scholar
  71. 71.
    Lo K, Landau NR, Smale ST (1991) LyF-1, a transcriptional regulator that interacts with a novel class of promoters for lymphocyte-specific gene. Mol Cell Biol 11:5229–5243CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Venugopal R, Jaiswal AK (1998) Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 17:3145–3156CrossRefPubMedGoogle Scholar
  73. 73.
    Steinberg S (2004) Disctinctive activation mechanisms and functions for protein kinase Cδ. Biochem J 384:449–459CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Borowsky B, Adham N, Jones KA, Raddatz R, Artymyshyn R, Ogozalek KL, Durkin MM, Lakhlani PP et al (2001) Trace amines: identification of a family of mammalian G protein-coupled receptors. Proc Natl Acad Sci U S A 98:8966–8971CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Xie Z, Miller GM (2007) Trace amine-associated receptor 1 is a modulator of the dopamine transporter. J Pharmacol Exp Ther 321:128–136CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • The-Vinh Tran
    • 1
  • Eun-Joo Shin
    • 1
  • Lan Thuy Ty Nguyen
    • 1
  • Youngho Lee
    • 1
  • Dae-Joong Kim
    • 2
  • Ji Hoon Jeong
    • 3
  • Choon-Gon Jang
    • 4
  • Seung-Yeol Nah
    • 5
  • Kazuya Toriumi
    • 6
  • Toshitaka Nabeshima
    • 7
  • Kiyofumi Yamada
    • 8
  • Hyoung-Chun Kim
    • 1
  1. 1.Neuropsychopharmacology and Toxicology Program, College of PharmacyKangwon National UniversityChunchonRepublic of Korea
  2. 2.Department of Anatomy and Cell Biology, Medical SchoolKangwon National UniversityChunchonRepublic of Korea
  3. 3.Department of Pharmacology, College of MedicineChung-Ang UniversitySeoulRepublic of Korea
  4. 4.Department of Pharmacology, School of PharmacySungkyunkwan UniversitySuwonSouth Korea
  5. 5.Ginsentology Research Laboratory and Department of Physiology, College of Veterinary Medicine and Bio/Molecular Informatics CenterKonkuk UniversitySeoulRepublic of Korea
  6. 6.Project for Schizophrenia Research, Department of Psychiatry and Behavioral SciencesTokyo Metropolitan Institute of Medical ScienceTokyoJapan
  7. 7.Advanced Diagnostic System Research LaboratoryFujita Health University Graduate School of Health SciencesToyoakeJapan
  8. 8.Department of Neuropsychopharmacology and Hospital PharmacyNagoya University Graduate School of MedicineNagoyaJapan

Personalised recommendations