Endoplasmic reticulum stress responses differ in meninges and associated vasculature, striatum, and parietal cortex after a neurotoxic amphetamine exposure

Synapse

Volumn 64, Issue 8, 2010, Pages 579-593

  Thomas, Monzy ^a   George, Nysia I ^a   Saini, Upasana T ^a   Patterson, Tucker A ^a   Hanig, Joseph P ^b   Bowyer, John F ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

Amphetamines; Blood brain barrier; Endoplasmic reticulum stress; Gene expression; Hyperthermia; Meninges; Unfolded protein response; Vasculature

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; AMPHETAMINE; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; PROTEIN DISULFIDE ISOMERASE; PROTEIN IRE1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; BRAIN BLOOD VESSEL; CONTROLLED STUDY; CORPUS STRIATUM; DNA MICROARRAY; ENDOPLASMIC RETICULUM STRESS; GENE; GENE EXPRESSION; HEAT SHOCK RESPONSE; HYPERTHERMIA; MALE; MENINX; NEUROTOXICITY; NONHUMAN; PARIETAL LOBE; PERK GENE; PRIORITY JOURNAL; RAT;

AMPHETAMINE; ANIMALS; CEREBROVASCULAR CIRCULATION; CORPUS STRIATUM; ENDOPLASMIC RETICULUM; MALE; MENINGES; NEUROTOXINS; PARIETAL LOBE; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PHYSIOLOGICAL; TIME FACTORS;

EID: 77956463862     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20763     Document Type: Article

References (96)

1. Bartzokis G, Beckson M, Lu PH, Edwards N, Rapoport R, Wiseman E, Bridge P. 2000. Age-related brain volume reductions in amphetamine and cocaine addicts and normal controls: Implications for addiction research. Psychiatry Res 98:93-102. (Pubitemid 30179661)
2. Bowyer JF, Ali S. 2006. High doses of methamphetamine that cause disruption of the blood-brain barrier in limbic regions produce extensive neuronal degeneration in mouse hippocampus. Synapse 60:521-532.
3. Bowyer JF, Holson RR. 1995.Methamphetamine and amphetamine neurotoxicity: Characteristics, interactions with body temperature and possible mechanisms. In: Chang LW, Dyer RS, editors. Handbook of neurotoxicology. New York: Marcel Dekker. p 845-870.
4. Bowyer JF, Schmued LC. 2006. Fluoro-Ruby labeling prior to an amphetamine neurotoxic insult shows a definitive massive loss of dopaminergic terminals and axons in the caudate-putamen. Brain Res 1075:236-239.
5. Bowyer JF, Tank AW, Newport GD, Slikker W Jr, Ali SF, Holson RR. 1992. The influence of environmental temperature on the transient effects of methamphetamine on dopamine levels and dopamine release in rat striatum. J Pharmacol Exp Ther 260:817-824.
6. Bowyer JF, Davies DL, Schmued L, Broening HW, Newport GD, Slikker W Jr, Holson RR. 1994. Further studies of the role of hyperthermia in methamphetamine neurotoxicity. J Pharmacol Exp Ther 268:1571-1580. (Pubitemid 24100380)
7. Bowyer JF, Peterson SL, Rountree RL, Tor-Agbidye J, Wang GJ. 1998. Neuronal degeneration in rat forebrain resulting from D-amphetamine- induced convulsions is dependent on seizure severity and age. Brain Res 809:77-90.
8. Bowyer JF, Harris AJ, Delongchamp RR, Jakab RL, Miller DB, Little AR, O'Callaghan JP. 2004. Selective changes in gene expression in cortical regions sensitive to amphetamine during the neurodegenerative process. Neurotoxicology 25:555-572.
9. Bowyer JF, Pogge AR, Delongchamp RR, O'Callaghan JP, Patel KM, Vrana KE, Freeman WM. 2007. A threshold neurotoxic ampheta- mine exposure inhibits parietal cortex expression of synaptic plasticity- related genes. Neuroscience 144:66-76.
10. Bowyer JF, Robinson B, Ali S, Schmued LC. 2008a. Neurotoxic-related changes in tyrosine hydroxylase, microglia, myelin, and the blood-brain barrier in the caudate-putamen from acute methamphetamine exposure. Synapse 62:193-204.
11. Bowyer JF, Thomas MT, Schmued LC, Ali SF. 2008b. Brain regionspecific neurodegenerative profiles showing the relative importance of amphetamine dose, hyperthermia, seizures and the blood-brain barrier. Ann N Y Acad Sci 1139:127-139.
12. Burnstock G. 1985. Neurogenic control of cerebral circulation. Cephalalgia 5Suppl 2:25-33.
13. Cadet JL, Jayanthi S, Deng X. 2005. Methamphetamine-induced neuronal apoptosis involves the activation of multiple death pathways. Review. Neurotox Res 8(3/4):199-206.
14. Cadet JL, Krasnova IN, Jayanthi S, Lyles J. 2007. Neurotoxicity of substituted amphetamines: Molecular and cellular mechanisms. Neurotox Res 11(3/4):183-202.
15. Chomczynski P, Mackey K. 1995. Short technical reports. Modification of the TRI reagent procedure for isolation of RNA from polysaccharide- and proteoglycan-rich sources. Biotechniques 19:942-945.
16. Ciechanover A, Brundin P. 2003. The ubiquitin proteasome system in neurodegenerative diseases: Sometimes the chicken, sometimes the egg. Neuron 40:427-446. (Pubitemid 37244106)
17. Commins DL, Seiden LS. 1986. Alpha-methyltyrosine blocks methylamphetamine- induced degeneration in the rat somatosensory cortex. Brain Res 365:15-20.
18. Conci F, D'Angelo V, Tampieri D, Vecchi G. 1988. Intracerebral hemorrhage and angiographic beading following amphetamine abuse. Ital J Neurol Sci 9:77-81.
19. Davidson C, Gow AJ, Lee TH, Ellinwood EH. 2001. Methamphetamine neurotoxicity: Necrotic and apoptotic mechanisms and relevance to human abuse and treatment. Brain Res Brain Res Rev 36:1-22.
20. Deng X, Wang Y, Chou J, Cadet JL. 2001. Methamphetamine causes widespread apoptosis in the mouse brain: Evidence from using an improved TUNEL histochemical method. Brain Res Mol Brain Res 93:64-69.
21. Dono R, Texido G, Dussel R, Ehmke H, Zeller R. 1998. Impaired cerebral cortex development and blood pressure regulation in FGF-2- deficient mice. EMBO J 17:4213-4225. (Pubitemid 28362612)
22. Eisch AJ, Schmued LC, Marshall JF. 1998. Characterizing cortical neuron injury with Fluoro-Jade labeling after a neurotoxic regimen of methamphetamine. Synapse 30:329-333.
23. Ellinwood EH Jr, Escalante O. 1970. Behavior and histopathological findings during chronic methedrine intoxication. Biol Psychiatry 2:27-39.
24. Ermak G, Davies KJ. 2002. Calcium and oxidative stress: From cell signaling to cell death. Mol Immunol 38:713-721.
25. Ernst T, Chang L, Leonido-Yee M, Speck O. 2000. Evidence for long-term neurotoxicity associated with methamphetamine abuse: A 1H MRS study. Neurology 54:1344-1349. (Pubitemid 30174057)
26. Ersche KD, Fletcher PC, Lewis SJ, Clark L, Stocks-Gee G, London M, Deakin JB, Robbins TW, Sahakian BJ. 2005. Abnormal frontal activations related to decision-making in current and former amphetamine and opiate dependent individuals. Psychopharmacology (Berl) 180:612-623.
27. Ferri KF, Kroemer G. 2001. Organelle-specific initiation of cell death pathways. Nat Cell Biol 3:E255-E263.
28. Fleckenstein AE, Volz TJ, Riddle EL, Gibb JW, Hanson GR. 2007. New insights into the mechanism of action of amphetamines. Annu Rev Pharmacol Toxicol 47:681-698. (Pubitemid 46272143)
29. Hamel E. 2006. Perivascular nerves and the regulation of cerebrovascular tone. J Appl Physiol 100:1059-1064.
30. Haze K, Yoshida H, Yanagi H, Yura T, Mori K. 1999. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 10:3787-3799.
31. Hess A, Desiderio C, McAuliffe WG. 1990. Acute neuropathological changes in the caudate nucleus caused by MPTP and methamphetamine: Immunohistochemical studies. J Neurocytol 19:338-342. (Pubitemid 20222709)
32. Hotchkiss AJ, Morgan ME, Gibb JW. 1979. The long-term effects of multiple doses of methamphetamine on neostriatal tryptophan hydroxylase, tyrosine hydroxylase, choline acetyltransferase and glutamate decarboxylase activities. Life Sci 25:1373-1378.
33. Hurtley SM, Helenius A. 1989. Protein oligomerization in the endoplasmic reticulum. Annu Rev Cell Biol 5:277-307.
34. Imai Y, Soda M, Inoue H, Hattori N, Mizuno Y, Takahashi R. 2001. An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell 105:891-902.
35. Jayanthi S, Deng X, Bordelon M, McCoy MT, Cadet JL. 2001. Methamphetamine causes differential regulation of pro-death and antideath Bcl-2 genes in the mouse neocortex. FASEB J 15:1745-1752.
36. Jayanthi S, Deng X, Noailles PA, Ladenheim B, Cadet JL. 2004. Methamphetamine induces neuronal apoptosis via cross-talks between endoplasmic reticulum and mitochondria-dependent death cascades. FASEB J 18:238-251. (Pubitemid 38186243)
37. Kalant H, Kalant OJ. 1975. Death in amphetamine users: Causes and rates. Can Med Assoc J 112:299-304.
38. Kassed CA, Butler TL, Patton GW, Demesquita DD, Navidomskis MT, Memet S, Israel A, Pennypacker KR. 2004. Injury-induced NF-kappaB activation in the hippocampus: Implications for neuronal survival. FASEB J 18:723-724.
39. Kaufman RJ. 1999. Stress signaling from the lumen of the endoplasmic reticulum: Coordination of gene transcriptional and translational controls. Genes Dev 13:1211-1233.
40. Kaufman RJ. 2002. Orchestrating the unfolded protein response in health and disease. J Clin Invest 110:1389-1398.
41. Krasnova IN, Ladenheim B, Jayanthi S, Oyler J, Moran TH, Huestis MA, Cadet JL. 2001. Amphetamine-induced toxicity in dopamine terminals in CD-1 and C57BL/6J mice: Complex roles for oxygen- based species and temperature regulation. Neuroscience 107:265-274.
42. Kudo T, Kanemoto S, Hara H, Morimoto N, Morihara T, Kimura R, Tabira T, Imaizumi K, Takeda M. 2008. A molecular chaperone inducer protects neurons from ER stress. Cell Death Differ 15:364-375.
43. Kulik T, Kusano Y, Aronhime S, Sandler AL, Winn HR. 2008. Regulation of cerebral vasculature in normal and ischemic brain. Neuropharmacology 55:281-288.
44. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(2Delta Delta C(T)) Method. Methods 25:402-408. (Pubitemid 34164012)
45. Lu PD, Harding HP, Ron D. 2004. Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J Cell Biol 167:27-33.
46. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ. 2001. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21:1249-1259.
47. McGee SM, McGee DN, McGee MB. 2004. Spontaneous intracerebral hemorrhage related to methamphetamine abuse: Autopsy findings and clinical correlation. Am J Forensic Med Pathol 25:334-337.
48. Miller DB, O'Callaghan JP. 1994. Environment-, drug- and stressinduced alterations in body temperature affect the neurotoxicity of substituted amphetamines in the C57BL/6J mouse. J Pharmacol Exp Ther 270:752-760.
49. Miller MA, Coon TP. 2006. Re: Delayed ischemic stroke associated with methamphetamine use. J Emerg Med 31:305-306; author reply306.
50. Mori K. 2000. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 101:451-454.
51. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. 2000. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403:98-103.
52. Nash JF, Yamamoto BK. 1992. Methamphetamine neurotoxicity and striatal glutamate release: Comparison to 3,4-methylenedioxymethamphetamine. Brain Res 581:237-243.
53. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K, Hori S, Kakizuka A, Ichijo H. 2002. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 16:1345-1355.
54. O'Callaghan JP, Miller DB. 1994. Neurotoxicity profiles of substituted amphetamines in the C57BL/6J mouse. J Pharmacol Exp Ther 270:741-751.
55. O'Callaghan JP, Miller DB. 2001. Neurotoxic effects of substituted amphetamines in rats and mice. In: Massaro EJ, editor. Handbook of neurotoxicology. Totowa, NJ: Humana. p 269-301.
56. Paschen W. 2004. Endoplasmic reticulum dysfunction in brain pathology: Critical role of protein synthesis. Curr Neurovasc Res 1:173-181.
57. Paschen W, Frandsen A. 2001. Endoplasmic reticulum dysfunction - a common denominator for cell injury in acute and degenerative diseases of the brain? J Neurochem 79:719-725.
58. Pennypacker KR, Kassed CA, Eidizadeh S, Saporta S, Sanberg PR, Willing AE. 2001. NF-kappaB p50 is increased in neurons surviving hippocampal injury. Exp Neurol 172:307-319. (Pubitemid 34075080)
59. Ricaurte GA, McCann UD. 2005. Recognition and management of complications of new recreational drug use. Lancet 365:2137-2145.
60. Ricaurte GA, Schuster CR, Seiden LS. 1980. Long-term effects of repeated methylamphetamine administration on dopamine and serotonin neurons in the rat brain: A regional study. Brain Res 193:153-163.
61. Ron D. 2002. Translational control in the endoplasmic reticulum stress response. J Clin Invest 110:1383-1388. (Pubitemid 35396906)
62. Rothrock JF, Rubenstein R, Lyden PD. 1988. Ischemic stroke associated with methamphetamine inhalation. Neurology 38:589-592.
63. Salanova V, Taubner R. 1984. Intracerebral haemorrhage and vasculitis secondary to amphetamine use. Postgrad Med J 60:429-430.
64. Schmued LC, Bowyer JF. 1997. Methamphetamine exposure can produce neuronal degeneration in mouse hippocampal remnants. Brain Res 759:135-140.
65. Schroder M, Kaufman RJ. 2005. ER stress and the unfolded protein response. Mutat Res 569(1/2):29-63.
66. Seiden LS, Sabol KE. 1995. Neurotoxicity of methamphetamine-related drugs and cocaine. In: Chang LW, Dyer RS, editors. Handbook of neurotoxicology. New York: Marcel Dekker. p 824-844.
67. Seiden LS, Fischman MW, Schuster CR. 1976. Long-term methamphetamine induced changes in brain catecholamines in tolerant rhesus monkeys. Drug Alcohol Depend 1:215-219.
68. Sharma HS, Ali SF. 2006. Alterations in blood-brain barrier function by morphine and methamphetamine. Ann N Y Acad Sci 1074:198-224. (Pubitemid 44532825)
69. Sharma HS, Westman J, Nyberg F. 1998. Pathophysiology of brain edema and cell changes following hyperthermic brain injury. Prog Brain Res 115:351-412.
70. Sharma HS, Sjoquist PO, Ali SF. 2007. Drugs of abuse-induced hyperthermia, blood - brain barrier dysfunction and neurotoxicity: Neuroprotective effects of a new antioxidant compound H-290/51. Curr Pharm Des 13:1903-1923.
71. Sherman MY, Goldberg AL. 2001. Cellular defenses against unfolded proteins: A cell biologist thinks about neurodegenerative diseases. Neuron 29:15-32.
72. Sonsalla PK, Nicklas WJ, Heikkila RE. 1989. Role for excitatory amino acids in methamphetamine-induced nigrostriatal dopaminergic toxicity. Science 243:398-400.
73. Soto C. 2008. Endoplasmic reticulum stress, PrP trafficking, and neurodegeneration. Dev Cell 15:339-341.
74. Soto C, Estrada LD. 2008. Protein misfolding and neurodegeneration. Arch Neurol 65:184-189.
75. Sriram K, Miller DB, O'Callaghan JP. 2006. Minocycline attenuates microglial activation but fails to mitigate striatal dopaminergic neurotoxicity: Role of tumor necrosis factor-alpha. J Neurochem 96:706-718.
76. Tanaka S, Uehara T, Nomura Y. 2000. Up-regulation of protein-disulfide isomerase in response to hypoxia/brain ischemia and its protective effect against apoptotic cell death. J Biol Chem 275:10388-10393. (Pubitemid 30202098)
77. Tata DA, Yamamoto BK. 2007. Interactions between methamphetamine and environmental stress: Role of oxidative stress, glutamate and mitochondrial dysfunction. Addiction 102Suppl 1:49-60.
78. Thomas DM, Francescutti-Verbeem DM, Liu X, Kuhn DM. 2004a. Identification of differentially regulated transcripts in mouse striatum following methamphetamine treatment - An oligonucleotide microarray approach. J Neurochem 88:380-393.
79. Thomas DM, Walker PD, Benjamins JA, Geddes TJ, Kuhn DM. 2004b. Methamphetamine neurotoxicity in dopamine nerve endings of the striatum is associated with microglial activation. J Pharmacol Exp Ther 311:1-7.
80. Thomas M, Yu Z, Dadgar N, Varambally S, Yu J, Chinnaiyan AM, Lieberman AP. 2005. The unfolded protein response modulates toxicity of the expanded glutamine androgen receptor. J. Biol. Chem. 280:21264-21271.
81. Thomas M, Harrell JM, Morishima Y, Peng HM, Pratt WB, Lieberman AP. 2006. Pharmacologic and genetic inhibition of hsp90-dependent trafficking reduces aggregation and promotes degradation of the expanded glutamine androgen receptor without stress protein induction. Hum Mol Genet 15:1876-1883.
82. Thomas M, George NI, Patterson TA, Bowyer JF. 2009. Amphetamine and environmentally induced hyperthermia differentially alter the expression of genes regulating vascular tone and angiogenesis in the meninges and associated vasculature. Synapse 63:881-894.
83. Tirasophon W, Welihinda AA, Kaufman RJ. 1998. A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev 12:1812-1824. (Pubitemid 28304334)
84. Tirasophon W, Lee K, Callaghan B, Welihinda A, Kaufman RJ. 2000. The endoribonuclease activity of mammalian IRE1 autoregulates its mRNA and is required for the unfolded protein response. Genes Dev 14:2725-2736.
85. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D. 2000. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664-666.
86. Van Antwerp DJ, Martin SJ, Kafri T, Green DR, Verma IM. 1996. Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 274:787-789.
87. van Kollenburg B, van Dijk J, Garbern J, Thomas AA, Scheper GC, Powers JM, van der Knaap MS. 2006. Glia-specific activation of all pathways of the unfolded protein response in vanishing white matter disease. J Neuropathol Exp Neurol 65:707-715.
88. Volkow ND, Chang L, Wang GJ, Fowler JS, Franceschi D, Sedler MJ, Gatley SJ, Hitzemann R, Ding YS, Wong C, Logan J. 2001a. Higher cortical and lower subcortical metabolism in detoxified methamphetamine abusers. Am J Psychiatry 158:383-389.
89. Volkow ND, Chang L, Wang GJ, Fowler JS, Leonido-Yee M, Franceschi D, Sedler MJ, Gatley SJ, Hitzemann R, Ding YS, Logan J, Wong C, Miller EN. 2001b. Association of dopamine transporter reduction with psychomotor impairment in methamphetamine abusers. Am J Psychiatry 158:377-382.
90. Wang CY, Mayo MW, Baldwin AS Jr. 1996. TNF- and cancer therapy- induced apoptosis: Potentiation by inhibition of NF-kappaB. Science 274:784-787.
91. Wilkinson B, Gilbert HF. 2004. Protein disulfide isomerase. Biochim Biophys Acta 1699(1/2):35-44.
92. Winslow BT, Voorhees KI, Pehl KA. 2007. Methamphetamine abuse. Am Fam Physician 76:1169-1174.
93. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R, Brown MS, Goldstein JL. 2000. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6:1355-1364.
94. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K. 2001. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881-891. (Pubitemid 34084979)
95. Yuan J, Hatzidimitriou G, Suthar P, Mueller M, McCann U, Ricaurte G. 2006. Relationship between temperature, dopaminergic neurotoxicity, and plasma drug concentrations in methamphetamine- treated squirrel monkeys. J Pharmacol Exp Ther 316: 1210-1218.
96. Zhang K, Kaufman RJ. 2006. The unfolded protein response: A stress signaling pathway critical for health and disease. Neurology 66(2Suppl 1):S102-S109.