Nrf2 deficiency potentiates methamphetamine-induced dopaminergic axonal damage and gliosis in the striatum

GLIA

Volumn 59, Issue 12, 2011, Pages 1850-1863

  Granado, Noelia ^a,b,c   Lastres Becker, Isabel ^b,d   Ares Santos, Sara ^a,b   Oliva, Idaira ^e   Martin, Eduardo ^e   Cuadrado, Antonio ^b,d   Moratalla, Rosario ^a,b  

^a INSTITUTO CAJAL   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^d AUTONOMOUS UNIVERSITY OF MADRID   (Spain)

^e UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

Author keywords

Amphetamine derivatives; Inflammation; Neurodegeneration; Nrf2

Indexed keywords

CD11B ANTIGEN; DOPAMINE TRANSPORTER; INTERLEUKIN 15; MESSENGER RNA; METHAMPHETAMINE; NEUROPROTECTIVE AGENT; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXONAL INJURY; CELL ACTIVATION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DRUG POTENTIATION; GLIOSIS; MACROGLIA; MALE; MICROGLIA; MOUSE; NERVE DEGENERATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECTUM TEMPERATURE; SUBSTANTIA NIGRA;

ADRENERGIC UPTAKE INHIBITORS; ANIMALS; AXONS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE; GLIOSIS; INFLAMMATION MEDIATORS; MALE; METHAMPHETAMINE; MICE; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; WALLERIAN DEGENERATION;

EID: 80053541907     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21229     Document Type: Article

References (51)

1. Albers DS, Sonsalla PK. 1995. Methamphetamine-induced hyperthermia and dopaminergic neurotoxicity in mice: pharmacological profile of protective and nonprotective agents. J Pharmacol Exp Ther 275: 1104-1114.
2. Cadet JL, Jayanthi S, Deng X. 2005. Methamphetamine-induced neuronal apoptosis involves the activation of multiple death pathways. Neurotox Res 8: 199-206.
3. Cadet JL, Krasnova IN, Jayanthi S, Lyles J. 2007. Neurotoxicity of substituted amphetamines: Molecular and cellular mechanisms. Neurotox Res 11: 183-202.
4. Calkins MJ, Jakel RJ, Johnson DA, Chan K, Kan YW, Johnson JA. 2005. Protection from mitochondrial complex II inhibition in vitro and in vivo by Nrf2-mediated transcription. Proc Natl Acad Sci USA 102: 244-249.
5. Chen PC, Vargas MR, Pani AK, Smeyne RJ, Johnson DA, Kan YW, Johnson JA. 2009. Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease: Critical role for the astrocyte. Proc Natl Acad Sci USA 106: 2933-2938.
6. Clark J, Simon DK. 2009. Transcribe to survive: Transcriptional control of antioxidant defense programs for neuroprotection in Parkinson's disease. Antioxid Redox Signal 3: 509-528.
7. Cullinan SB, Zhang D, Hannink M, Arvisais E, Kaufman RJ, Diehl JA. 2003. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol 23: 7198-7209.
8. Darmopil S, Martín AB, De Diego IR, Ares S, Moratalla R. 2009. Genetic inactivation of dopamine D1 but not D2 receptors inhibits L-DOPA-induced dyskinesia and histone activation. Biol Psychiatry 66: 603-613.
9. Darmopil S, Muñetón-Gómez VC, de Ceballos ML, Bernson M, Moratalla R. 2008. Tyrosine hydroxylase cells appearing in the mouse striatum after dopamine denervation are likely to be projection neurones regulated by L-DOPA. Eur J Neurosci 27: 580-592.
10. 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.
11. Fantegrossi WE, Ciullo JR, Wakabayashi KT, De La GR, 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.
12. Gómez-Nicola D, Valle-Argos B, Pita-Thomas DW, Nieto-Sampedro M. 2008. Interleukin 15 expression in the CNS: Blockade of its activity prevents glial activation after an inflammatory injury. Glia 56: 494-505.
13. Granado N, Ares-Santos S, O'shea E, Vicario-Abejón 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.
14. Granado N, Ares-Santos S, Oliva I, O Shea E, Martin ED, Colado MI, Moratalla R. 2011. Dopamine D2-receptor knockout mice are protected against dopaminergic neurotoxicity induced by methamphetamine or MDMA. Neurobiol Dis 42: 391-403.
15. Granado N, Escobedo I, O'shea E, Colado MI, Moratalla R. 2008a. Early loss of dopaminergic terminals in striosomes after MDMA administration to mice. Synapse 62: 80-84.
16. Granado N, Ortiz O, Suarez LM, Martin ED, Cena V, Solis JM, Moratalla R. 2008c. D1 but notD5 dopamine receptors are critical for LTP, spatial learning, and LTP-induced arc and zif268 expression in the hippocampus. Cereb Cortex 18: 1-12.
17. Granado N, O'shea E, Bove J, Vila M, Colado MI, Moratalla R. 2008b. Persistent MDMA-induced dopaminergic neurotoxicity in the striatum and substantia nigra of mice. J Neurochem 107: 1102-1112.
18. Innamorato NG, Rojo AI, Garcia-Yague AJ, Yamamoto M, de Ceballos ML, Cuadrado A. 2008. The transcription factor Nrf2 is a therapeutic target against brain inflammation. J Immunol 181: 680-689.
19. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, Yamamoto M, Nabeshima Y. 1997. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236: 313-322.
20. Jakel RJ, Townsend JA, Kraft AD, Johnson JA. 2007. Nrf2-mediated protection against 6-hydroxydopamine. Brain Res 1144: 192-201.
21. Jayanthi S, McCoy MT, Beauvais G, Ladenheim B, Gilmore K, Wood W3rd, Becker K, Cadet JL. 2009. Methamphetamine induces dopamine D1 receptor-dependent endoplasmic reticulum stress-related molecular events in the rat striatum. PLoS One 4: e6092
22. Johnson JA, Johnson DA, Kraft AD, Calkins MJ, Jakel RJ, Vargas MR, Chen PC. 2008. The Nrf2-ARE pathway: An indicator and modulator of oxidative stress in neurodegeneration. Ann NY Acad Sci 1147: 61-69.
23. Kang J, Jiang L, Goldman SA, Nedergaard M. 1998. Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1: 683-692.
24. Krasnova IN, Cadet JL. 2009. Methamphetamine toxicity and messengers of death. Brain Res Rev 60: 379-407. Review.
25. Lai YT, Tsai YP, Cherng CG, Ke JJ, Ho MC, Tsai CW, Yu L. 2009. Lipopolysaccharide mitagates methamphetamine-induced striatal dopamine depletion via modulating local TNF-alpha and dopamine transporter expression. J Neural Transm 116: 405-415.
26. Lo SC, Li X, Henzl MT, Beamer LJ, Hannink M. 2006. Structure of the Keap1:Nrf2 interface provides mechanistic insight into Nrf2 signaling. EMBO J 25: 3605-3617.
27. Martín AB, Fernández-Espejo E, Ferrer B, Gorriti MA, Navarro M, Rodríguez de Fonseca F, Moratalla R. 2008. Expression and function of CB1 receptor in the rat striatum: Localization and effects on D1 and D2 dopamine receptor-mediated motor behaviors. Neuropsychopharmacol 33: 1667-1679.
28. Martín ED, Buño W. 2005. Stabilizing effects of extracellular ATP on synaptic efficacy and plasticity in hippocampal pyramidal neurons. Eur J Neurosc 21: 936-944.
29. Martín ED, Fernández M, Perea G, Pascual O, Haydon PG, Araque A, Ceña V. 2007. Adenosine released by astrocytes contributes to hypoxia-induced modulation of synaptic transmission. Glia 55: 36-45.
30. 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.
31. O'Callaghan JP, Miller DB. 1994. Neurotoxicity profiles of substituted amphetamines in the C57BL/6J mouse. J Pharmacol Exp Ther 270: 741-751.
32. -/- mice and in hippocampal siRNA silenced Drd1a mice. J Neurosci 30: 12288-12300.
33. Pacchioni AM, Vallone J, Melendez RI, Shih A, Murphy TH, Kalivas PW. 2007. Nrf2 gene deletion fails to alter psychostimulant-induced behavior or neurotoxicity. Brain Res 1127: 26-35.
34. Pavón N, Martín AB, Mendialdua A, Moratalla R. 2006. ERK phosphorylation and FosB expression are associated with L-DOPA-induced dyskinesia in hemiparkinsonian mice. Biol Psychiatry 59: 64-74.
35. Perea G, Araque A. 2007. Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317: 1083-1086.
36. Rangasamy T, Cho CY, Thimmulappa RK, Zhen L, Srisuma SS, Kensler TW, Yamamoto M, Petrache I, Tuder RM, Biswal S. 2004. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest 114: 1248-1259.
37. Rangasamy T, Guo J, Mitzner WA, Roman J, Singh A, Fryer AD, Yamamoto M, Kensler TW, Tuder RM, Georas SN, Biswal S. 2005. Disruption of Nrf2 enhances susceptibility to severe airway inflammation and asthma in mice. J Exp Med 202: 47-59.
38. Ricaurte GA, Guillery RW, Seiden LS, Schuster CR, Moore RY. 1982. Dopamine nerve terminal degeneration produced by high doses of methylamphetamine in the rat brain. Brain Res 235: 93-103.
39. Rodrigues TB, Granado N, Ortiz O, Cerdan S, Moratalla R. 2007. Metabolic interactions between glutamatergic and dopaminergic neurotransmitter systems are mediated through D(1) dopamine receptors. J. Neurosci Res 85: 3284-3293.
40. Rojo AI, Innamorato NG, Martin-Moreno AM, De Ceballos ML, Yamamoto M, Cuadrado A. 2010. Nrf2 regulates microglial dynamics and neuroinflammation in experimental Parkinson's disease. Glia 58: 588-598.
41. Schmued LC, Albertson C, Slikker WJr. 1997. Fluoro-Jade: A novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res 751: 37-46.
42. Shih AY, Imbeault S, Barakauskas V, Erb H, Jiang L, Li P, Murphy TH. 2005. Induction of the Nrf2-driven antioxidant response confers neuroprotection during mitochondrial stress in vivo. J Biol Chem 280: 22925-22936.
43. 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.
44. 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.
45. Thomas DM, Francescutti-Verbeem DM, Kuhn DM. 2008. The newly synthesized pool of dopamine determines the severity of methamphetamine-induced neurotoxicity. J Neurochem 105: 605-616.
46. Thimmulappa RK, Lee H, Rangasamy T, Reddy SP, Yamamoto M, Kensler TW, Biswal S. 2006a. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J Clin Invest 116: 984-995.
47. Thimmulappa RK, Scollick C, Traore K, Yates M, Trush MA, Liby KT, Sporn MB, Yamamoto M, Kensler TW, Biswal S. 2006b. Nrf2-dependent protection from LPS induced inflammatory response and mortality by CDDO-imidazolide. Biochem Biophys Res Commun 351: 883-889.
48. Volkow ND, Chang L, Wang GJ, Fowler JS, Franceschi D, Sedler M, Gatley SJ, Miller E, Hitzemann R, Ding YS, Logan J. 2001. Loss of dopamine transporters in methamphetamine abusers recovers with protracted abstinence. J Neurosci 21: 9414-9418.
49. Xu W, Zhu JP, Angulo JA. 2005. Induction of striatal pre- and postsynaptic damage by methamphetamine requires the dopamine receptors. Synapse 58: 110-121.
50. Yamamoto BK, Zhu W. 1998. The effects of methamphetamine on the production of free radicals and oxidative stress. J. Pharmacol Exp Ther 287: 107-114.
51. Zhu JP, Xu W, Angulo JA. 2005. Disparity in the temporal appearance of methamphetamine-induced apoptosis and depletion of dopamine terminal markers in the striatum of mice. Brain Res 1049: 171-181.