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Lipopolysaccharide mitagates methamphetamine-induced striatal dopamine depletion via modulating local TNF-α and dopamine transporter expression

  • Basic Neurosciences, Genetics and Immunology - Original Article
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Abstract

Systemic lipopolysaccharide (LPS) treatment may affect methamphetamine (MA)-induced nigrostriatal dopamine (DA) depletion. This study was undertaken to determine the critical time window for the protective effects of LPS treatment and the underlying mechanisms. An LPS injection (1 mg/kg) 72 h before or 2 h after MA treatment [three consecutive, subcutaneous injections of MA (10 mg/kg each) at 2-h intervals] diminished the MA-induced DA depletion in mouse striatum. Such an LPS-associated effect was independent of MA-produced hyperthermia. TNF-α, IL-1β, IL-6 expressions were all elevated in striatal tissues following a systemic injection with LPS, indicating that peripheral LPS treatment affected striatal pro-inflammatory cytokine expression. Striatal TNF-α expression was dramatically increased at 72 and 96 h after the MA treatment, while such TNF-α elevation was abolished by the LPS pretreatment protocol. Moreover, MA-produced activation of nuclear NFκB, a transcription factor following TNF-α activation, in striatum was abolished by the LPS (1 mg/kg) pretreatment. Furthermore, thalidomide, a TNF-α antagonist, treatment abolished the LPS pretreatment-associated protective effects. Pretreatment with mouse recombinant TNF-α in striatum diminished the MA-produced DA depletion. Finally, single LPS treatment caused a rapid down-regulation of dopamine transporter (DAT) in striatum. Taken together, we conclude that peripheral LPS treatment protects nigrostriatal DA neurons against MA-induced toxicity, in part, by reversing elevated TNF-α expression and subsequent signaling cascade and causing a rapid DAT down-regulation in striatum.

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References

  • Arai H, Furuya T, Yasuda T, Miura M, Mizuno Y, Mochizuki H (2004) Neurotoxic effects of lipopolysaccharide on nigrostriatal dopaminergic neurons are mediated by microglial activation, interleukin-1B, and expression of caspase-11 in mice. J Biol Chem 279:51647–51653

    Article  PubMed  CAS  Google Scholar 

  • Asanuma M, Tsuji T, Miyazaki I, Miyoshi K, Ogawa N (2003) Methamphetamine-induced neurotoxicity in mouse brain is attenuated by ketoprofen, a non-steroid anti-inflammatory drug. Neurosci Lett 352:13–16

    Article  PubMed  CAS  Google Scholar 

  • Bannerman DD, Goldblum SE (1999) Direct effect of endotoxin on the endothelium: barrier function and injury. Lab Invest 79:1181–1191

    PubMed  CAS  Google Scholar 

  • Barcia C, Sanchez Bahillo A, Fernandez-Villalba E, Bautista V, Poza Y, Poza M, Fernandez-Barreiro A, Hirsch EC, Herrero MT (2004) Evidence of active microglia in substantia nigra pars compacta of parkinsonian monkeys 1 year after MPTP exposure. Glia 46:402–409

    Article  PubMed  Google Scholar 

  • Broening HW, Morford LL, Vorhees CV (2005) Interactions of dopamine D1 and D2 receptor antagonists with d-methamphetamine-induced hyperthermia and striatal dopamine and serotonin reductions. Synapse 56:84–93

    Article  PubMed  CAS  Google Scholar 

  • Burow ME, Weldom CB, Melnik LI, Duong BN, Collins-Burow BM, Beckman BS, McLachlan JA (2000) PI3-K/AKT regulation of NF-κB signaling events and suppression of TNF-induced apoptosis. Biochem Biophys Res Comm 271:342–345

    Article  PubMed  CAS  Google Scholar 

  • Cadet JL, Ali S, Epstein C (1994) Involvement of oxygen-based radicals in methamphetamine-induced neurotoxicity: evidence from the use of CuZnSOD transgenic mice. Ann N Y Acad Sci 738:388–391

    Article  PubMed  CAS  Google Scholar 

  • Cadet JL, Krasnova IN, Jayanthi S, Lyles J (2007) Neurotoxicity of substituted amphetamines: molecular and cellular mechanisms. Neurotoxic Res 11:183–202

    Article  CAS  Google Scholar 

  • Camandola S, Mattson MP (2000) Pro-apoptotic action of PAR-4 involves inhibition of NF-κB activity and suppression of BCL-2 expression. J Neurosci Res 61:134–139

    Article  PubMed  CAS  Google Scholar 

  • Cardenas H, Bolin LM (2003) Compromised reactive microgliosis in MPTP-lesioned IL-6 KO mice. Brain Res 985:89–97

    Article  PubMed  CAS  Google Scholar 

  • De Vito MJ, Wagner GC (1989) Methamphetamine-induced neuronal damage: a possible role for free radicals. Neuropharmacol 28:1145–1150

    Article  Google Scholar 

  • Ding Y, Li L (2008) Lipopolysaccharide preconditioning induces protection against lipopolysaccharide-induced neurotoxicity in organotypic midbrain slice culture. Neurosci Bull 24:209–218

    Article  PubMed  CAS  Google Scholar 

  • Escubedo E, Chipana C, Perez-Sanchez M, Camarasa J, Pubill D (2005) Methyllycaconitine prevents methamphetamine-induced effects in mouse striatum: involvement of α7 nicotinic receptors. J Pharmacol Exp Ther 315:658–667

    Article  PubMed  CAS  Google Scholar 

  • Fernyhough P, Smith DR, Schapansky J, van der Ploeg R, Gardiner NJ, Tweed CW, Kontos A, Freeman L, Purves-Tyson TD, Glazner GW (2005) Activation of nuclear factor-κB via endogenous tumor necrosis factor α regulates survival of axotomized adult sensory neurons. J Neurosci 25:1682–1690

    Article  PubMed  CAS  Google Scholar 

  • Fukumura M, Cappon GD, Pu C, Broening HW, Vorhees CV (1998) A single dose model of methamphetamine-induced neurotoxicity in rats: effects on neostriatal monoamines and glial fibrillary acidic protein. Brain Res 806:1–7

    Article  PubMed  CAS  Google Scholar 

  • Gao HM, Liu B, Zhang W, Hong JS (2003) Synergistic dopaminergic neurotoxicity of MPTP and inflammogen lipopolysaccharide: relevance to the etiology of Parkinson’s disease. FASEB J 17:1957–1959

    PubMed  CAS  Google Scholar 

  • Gayle DA, Ling Z, Tong C, Landers T, Lipton JW, Carvey PM (2002) Lipopolysaccharide (LPS)-induced dopamine cell loss in culture: roles of tumor necrosis factor-alpha, interleukin-1beta, and nitric oxide. Brain Res Dev Brain Res 133:27–35

    Article  PubMed  CAS  Google Scholar 

  • Glazner GW, Camamdola S, Mattson MP (2000) Nuclear factor κB mediates the cell survival-promoting action of activity-dependent neurotrophic factor peptide-9. J Neurochem 75:101–108

    Article  PubMed  CAS  Google Scholar 

  • Hirsch EC, Hunot S, Hartmann A (2005) Neuroinflammatory processes in Parkinson’s disease. Parkinsonism Relat Disord Suppl 1:S9–S15

    Article  Google Scholar 

  • Hom DG, Jiang D, Hong EJ, Mo JQ, Andersen JK (1997) Elevated expression of glutathione peroxidase in PC12 cells results in protection against methamphetamine but not MPTP toxicity. Brain Res Mol Brain Res 46:154–160

    Article  PubMed  CAS  Google Scholar 

  • Itzhak Y, Gandia C, Huang PL, Ali SF (1998) Resistance of neuronal nitric oxide synthase-deficient mice to methamphetamine-induced dopaminergic neurotoxicity. J Pharmacol Exp Ther 284:1040–1047

    PubMed  CAS  Google Scholar 

  • Kato H, Kurosaki R, Oki C, Araki T (2004) Arundic acid, an astrocyte-modulating agent, protects dopaminergic neurons against MPTP neurotoxicity in mice. Brain Res 1030:66–73

    Article  PubMed  CAS  Google Scholar 

  • Kita T, Saraya T, Konishi N, Matsunari Y, Shimada K, Nakamura M, O’Hara K, Wagner GC, Nakashima T (2003) 1-Methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine pretreatment attenuates methamphetamine-induced dopamine toxicity. Pharmacol Toxicol 92:71–80

    Article  PubMed  CAS  Google Scholar 

  • Kiyatkin EA (2005) Brain hyperthermia as physiological and pathological phenomena. Brain Res Brain Res Rev 50:27–56

    Article  PubMed  Google Scholar 

  • Kozak W, Conn CA, Kluger MJ (1994) Lipopolysaccharide induces fever and depresses locomotor activity in unrestrained mice. Am J Physiol 266:R125–R135

    PubMed  CAS  Google Scholar 

  • Kuo YM, Chen HH, Shieh CC, Chuang KP, Cherng CG, Yu L (2003) 4-Hydroxytamoxifen attenuates methamphetamine-induced nigrostriatal dopaminergic toxicity in intact and gonadetomized mice. J Neurochem 87:1436–1443

    PubMed  CAS  Google Scholar 

  • LaVoie MJ, Card JP, Hastings TG (2004) Microglial activation precedes dopamine terminal pathology in methamphetamine-induced neurotoxicity. Exp Neurol 187:47–57

    Article  PubMed  CAS  Google Scholar 

  • Liao P-C, Kuo Y-M, Hsu H-C, Cherng CG, Yu L (2005) Local proteins associated with methamphetamine-induced nigrostriatal dopaminergic neurotoxicity. J Neurochem 95:160–168

    Article  PubMed  CAS  Google Scholar 

  • Lin YC, Kuo Y-M, Liao P-C, Cherng CG, Su S-W, Yu L (2007) Attenuation of methamphetamine-induced nigrostriatal dopaminergic neurotoxicity in mice by lipopolysaccharide pretreatment. Chin J Physiol 50:51–56

    PubMed  CAS  Google Scholar 

  • Ling ZD, Chang Q, Lipton JW, Tong CW, Landers TM, Carvey PM (2004) Combined toxicity of prenatal bacterial endotoxin exposure and postnatal 6-hydroxydopamine in the adult rat midbrain. Neuroscience 124:619–628

    Article  PubMed  CAS  Google Scholar 

  • Lipsky RH, Xu K, Zhu D, Kelly C, Terhakopian A, Movelli A, Marimi AM (2001) Nuclear factor κB is a critical determinant in N-methyl-d-asparatate receptor- mediated neuroprotection. J Neurochem 78:254–264

    Article  PubMed  CAS  Google Scholar 

  • Marek GJ, Vosmer G, Seiden LS (1990) Dopamine uptake inhibitors block long-term neurotoxic effects of methamphetamine upon dopaminergic neurons. Brain Res 513:274–279

    Article  PubMed  CAS  Google Scholar 

  • 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 H-C, Nabeshima T (2004) Role of tumor necrosis factor-α in methamphetamine-induced drug dependence and neurotoxicity. J Neurosci 24:2212–2225

    Article  PubMed  CAS  Google Scholar 

  • O’Callaghan JP, Miller DB (1994) Neurotoxicity profiles of substituted amphetamines in the C57BL/6J mouse. J Pharm Exp Ther 270:741–751

    Google Scholar 

  • Pu C, Fisher JE, Cappon GD, Vorhees CV (1994) The effects of amfonelic acid, a dopamine uptake inhibitor, on methamphetamine-induced dopaminergic terminal degeneration and astrocyclic response in rat striatum. Brain Res 649:217–224

    Article  PubMed  CAS  Google Scholar 

  • Quan N, He L, Lai W (2002) Endothelial activation is an intermediate step for peripheral lipopolysaccharide-induced activation of paraventricular nucleus. Brain Res Bull 59:447–452

    Article  Google Scholar 

  • Rocha AC, Fernandes ES, Quintao NL, Campos MM, Calixto JB (2006) Relevance of tumour necrosis factor-alpha for the inflammatory and nociceptive responses evoked by carrageenan in the mouse paw. Brit J Pharmacol 148:688–695

    Article  CAS  Google Scholar 

  • Romashkova JA, Makarov SS (1999) NF-κB is a target of AKT in anti-apoptotic PDGF signaling. Nature 401:86–90

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Alavez M, Gombart LM, Huitron-Resendiz S, Carr JR, Wills DN, Berg G, Campbell IL, Gauvin DV, Henriksen SJ, Criado JR (2004) Physiological and behavioral effects of methamphetamine in a mouse model of endotoxemia: a preliminary study. Pharmacol Biochem Behav 77:365–370

    Article  PubMed  CAS  Google Scholar 

  • Singh AK, Jiang Y (2004) How does peripheral lipopolysaccharide induce gene expression in the brain of rats? Toxicology 201:197–207

    Article  PubMed  CAS  Google Scholar 

  • Thomas DM, Kuhn DM (2005) MK-801 and dextromethorphan block microglial activation and protect against methamphetamine-induced neurotoxicity. Brain Res 1050:190–198

    Article  PubMed  CAS  Google Scholar 

  • Thomas DM, Dowgiert J, Geddes TJ, Francescutti-Verbeem D, Liu X, Kuhn DM (2004) Microglial activation is a pharmacologically specific marker for the neurotoxic amphetamines. Neurosci Lett 367:349–354

    Article  PubMed  CAS  Google Scholar 

  • Valente P, Arzani D, Cesario A, Margaritora S, Carbone E, Russo P (2003) TNF increases camptothecin-induced apoptosis by inhibition of NF-κB. Eur J Cancer 39:1468–1477

    Article  PubMed  CAS  Google Scholar 

  • Veszelka S, Urbanyi Z, Pazmany T, Nemeth L, Obal I, Dung NTK, Abraham CS, Szabo G, Deli MA (2003) Human serum amyloid P component attenuates the bacterial lipopolysaccharide-induced increase in blood–brain barrier permeability in mice. Neurosci Lett 352:57–60

    Article  PubMed  CAS  Google Scholar 

  • Volz TJ, Fleckenstein AE, Hanson GR (2007) Methamphetamine-induced alterations in monoamine transport: implications for neurotoxicity, neuroprotection and treatment. Addict 102(Suppl 1):44–48

    Article  Google Scholar 

  • Wagner GC, Ricaurte GA, Seiden LS, Schuster CR, Miller JM, Westly J (1980) Long-lasting depletion of striatal DA and loss of DA uptake sites following the repeated administration of methamphetamine. Brain Res 171:151–160

    Article  Google Scholar 

  • Xu W, Zhu JP, Angulo JA (2005) Induction of striatal pre- and postsynaptic damage by methamphetamine requires the dopamine receptors. Synapse 58:110–121

    Article  PubMed  CAS  Google Scholar 

  • Yabe T, Wilson D, Schwartz JP (2001) NFκB activation is required for the neuroprotective effects of pigment epithelium-derived factor (PEDF) on cerebellar granule neurons. J Biol Chem 276:43313–43319

    Article  PubMed  CAS  Google Scholar 

  • Yu L, Liao PC (2000a) Estrogen and progesterone distinctively modulate methamphetamine-induced dopamine and serotonin depletions in C57BL/6J mice. J Neural Transm 107:1139–1147

    Article  PubMed  CAS  Google Scholar 

  • Yu L, Liao PC (2000b) Sexual differences and estrous cycle in methamphetamine-induced dopamine and serotonin depletions in the striatum of mice. J Neural Transm 107:419–427

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research is, in part, supported by ROC National Science Council grants No. 952413H006003MY2, 952320B006042 and to L.Y.

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Authors and Affiliations

  1. Behavioral Neuropharmacology Laboratory, Institute of Behavioral Medicine, National Cheng Kung University College of Medicine, 1 University Rd., Tainan, 70101, Taiwan, ROC

    Yu-Ting Lai, Yen-Ping N. Tsai, Ming-Che Ho, Chia-Wen Tsai & Lung Yu

  2. Department of Health Psychology, Chang Jung Christian University, Tainan, 71101, Taiwan, ROC

    Chianfang G. Cherng

  3. Department of Physiology, National Cheng Kung University College of Medicine, Tainan, 70101, Taiwan, ROC

    Jing-Jer Ke & Lung Yu

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  1. Yu-Ting Lai
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Correspondence to Lung Yu.

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Lai, YT., Tsai, YP.N., Cherng, C.G. et al. Lipopolysaccharide mitagates methamphetamine-induced striatal dopamine depletion via modulating local TNF-α and dopamine transporter expression. J Neural Transm 116, 405–415 (2009). https://doi.org/10.1007/s00702-009-0204-2

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  • DOI: https://doi.org/10.1007/s00702-009-0204-2

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