L-Ascorbate attenuates methamphetamine neurotoxicity through enhancing the induction of endogenous heme oxygenase-1

Toxicology and Applied Pharmacology

Volumn 265, Issue 2, 2012, Pages 241-252

  Huang, Ya Ni ^a   Wang, Jiz Yuh ^b   Lee, Ching Tien ^a   Lin, Chih Hung ^c   Lai, Chien Cheng ^d   Wang, Jia Yi ^c  

^a HSIN SHENG COLLEGE OF MEDICAL CARE AND MANAGEMENT   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d FAR EASTERN MEMORIAL HOSPITAL   (Taiwan)

Author keywords

Heme oxygenase 1; Methamphetamine; P38 MAPK; ROS; Vitamin C

Indexed keywords

ASCORBIC ACID; HEME OXYGENASE 1; METHAMPHETAMINE; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; CELL DAMAGE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME LOCALIZATION; IMMUNOFLUORESCENCE; NERVE CELL; NEUROTOXICITY; NONHUMAN; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; ASCORBIC ACID; BLOTTING, WESTERN; CELL SURVIVAL; CEREBRAL CORTEX; COCULTURE TECHNIQUES; DRUG INTERACTIONS; ENZYME INDUCTION; HEME OXYGENASE-1; IMMUNOHISTOCHEMISTRY; METHAMPHETAMINE; NEUROGLIA; NEURONS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SIGNAL TRANSDUCTION;

EID: 84868507153     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.08.036     Document Type: Article

References (82)

1. Abekawa T., Ito K., Nakagawa S., Nakato Y., Koyama T. Olanzapine and risperidone block a high dose of methamphetamine-induced schizophrenia-like behavioral abnormalities and accompanied apoptosis in the medial prefrontal cortex. Schizophr. Res. 2008, 101:84-94.
2. Abraham N.G., Lavrovsky Y., Schwartzman M.L., Stoltz R.A., Levere R.D., Gerritsen M.E., Shibahara S., Kappas A. Transfection of the human heme oxygenase gene into rabbit coronary microvessel endothelial cells: protective effect against heme and hemoglobin toxicity. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:6798-6802.
3. Alam J., Cook J.L. Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr. Pharm. Des. 2003, 9:2499-2511.
4. Alam J., Wicks C., Stewart D., Gong P., Touchard C., Otterbein S., Choi A.M., Burow M.E., Tou J. Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells. Role of p38 kinase and Nrf2 transcription factor. J. Biol. Chem. 2000, 275:27694-27702.
5. Armstrong B.D., Noguchi K.K. The neurotoxic effects of 3,4-methylenedioxymethamphetamine (MDMA) and methamphetamine on serotonin, dopamine, and GABA-ergic terminals: an in-vitro autoradiographic study in rats. Neurotoxicology 2004, 25:905-914.
6. Asanuma M., Miyazaki I., Higashi Y., Diaz-Corrales F.J., Shimizu M., Miyoshi K., Ogawa N. Suppression of p53-activated gene, PAG608, attenuates methamphetamine-induced neurotoxicity. Neurosci. Lett. 2007, 414:263-267.
7. Barr A.M., Panenka W.J., MacEwan G.W., Thornton A.E., Lang D.J., Honer W.G., Lecomte T. The need for speed: an update on methamphetamine addiction. J. Psychiatry Neurosci. 2006, 31:301-313.
8. Becker J.C., Grosser N., Boknik P., Schroder H., Domschke W., Pohle T. Gastroprotection by vitamin C - a heme oxygenase-1-dependent mechanism?. Biochem. Biophys. Res. Commun. 2003, 312:507-512.
9. Bowie A.G., O'Neill L.A. Vitamin C inhibits NF-kappa B activation by TNF via the activation of p38 mitogen-activated protein kinase. J. Immunol. 2000, 165:7180-7188.
10. Brouard S., Otterbein L.E., Anrather J., Tobiasch E., Bach F.H., Choi A.M., Soares M.P. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J. Exp. Med. 2000, 192:1015-1026.
11. Cadet J.L., Krasnova I.N. Molecular bases of methamphetamine-induced neurodegeneration. Int. Rev. Neurobiol. 2009, 88:101-119.
12. Cadet J.L., Ordonez S.V., Ordonez J.V. Methamphetamine induces apoptosis in immortalized neural cells: protection by the proto-oncogene, bcl-2. Synapse 1997, 25:176-184.
13. Cadet J.L., Jayanthi S., Deng X. Speed kills: cellular and molecular bases of methamphetamine-induced nerve terminal degeneration and neuronal apoptosis. FASEB J. 2003, 17:1775-1788.
14. Cadet J.L., Krasnova I.N., Jayanthi S., Lyles J. Neurotoxicity of substituted amphetamines: molecular and cellular mechanisms. Neurotox. Res. 2007, 11:183-202.
15. Carcamo J.M., Borquez-Ojeda O., Golde D.W. Vitamin C inhibits granulocyte macrophage-colony-stimulating factor-induced signaling pathways. Blood 2002, 99:3205-3212.
16. Chen K., Maines M.D. Nitric oxide induces heme oxygenase-1 via mitogen-activated protein kinases ERK and p38. Cell Mol. Biol. (Noisy-le-grand) 2000, 46:609-617.
17. Chen K., Gunter K., Maines M.D. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J. Neurochem. 2000, 75:304-313.
18. Cuadrado A., Rojo A.I. Heme oxygenase-1 as a therapeutic target in neurodegenerative diseases and brain infections. Curr. Pharm. Des. 2008, 14:429-442.
19. Das S., Fraga C.G., Das D.K. Cardioprotective effect of resveratrol via HO-1 expression involves p38 map kinase and PI-3-kinase signaling, but does not involve NFkappaB. Free Radic. Res. 2006, 40:1066-1075.
20. Davidson C., Gow A.J., Lee T.H., Ellinwood E.H. Methamphetamine neurotoxicity: necrotic and apoptotic mechanisms and relevance to human abuse and treatment. Brain Res. Brain Res. Rev. 2001, 36:1-22.
21. De Vito M.J., Wagner G.C. Methamphetamine-induced neuronal damage: a possible role for free radicals. Neuropharmacology 1989, 28:1145-1150.
22. Deng X., Wang Y., Chou J., Cadet J.L. Methamphetamine causes widespread apoptosis in the mouse brain: evidence from using an improved TUNEL histochemical method. Brain Res. Mol. Brain Res. 2001, 93:64-69.
23. Dennery P.A., Wong H.E., Sridhar K.J., Rodgers P.A., Sim J.E., Spitz D.R. Differences in basal and hyperoxia-associated HO expression in oxidant-resistant hamster fibroblasts. Am. J. Physiol. 1996, 271:L672-L679.
24. Elbekai R.H., Duke J., El-Kadi A.O. Ascorbic acid differentially modulates the induction of heme oxygenase-1, NAD(P)H:quinone oxidoreductase 1 and glutathione S-transferase Ya by As(3+), Cd(2+) and Cr(6+). Cancer Lett. 2007, 246:54-62.
25. Elbirt K.K., Whitmarsh A.J., Davis R.J., Bonkovsky H.L. Mechanism of sodium arsenite-mediated induction of heme oxygenase-1 in hepatoma cells. Role of mitogen-activated protein kinases. J. Biol. Chem. 1998, 273:8922-8931.
26. Ferrandiz M.L., Devesa I. Inducers of heme oxygenase-1. Curr. Pharm. Des. 2008, 14:473-486.
27. Harrison F.E., May J.M. Vitamin C function in the brain: vital role of the ascorbate transporter SVCT2. Free Radic. Biol. Med. 2009, 46:719-730.
28. Huang J., Agus D.B., Winfree C.J., Kiss S., Mack W.J., McTaggart R.A., Choudhri T.F., Kim L.J., Mocco J., Pinsky D.J., Fox W.D., Israel R.J., Boyd T.A., Golde D.W., Connolly E.S. Dehydroascorbic acid, a blood-brain barrier transportable form of vitamin C, mediates potent cerebroprotection in experimental stroke. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:11720-11724.
29. Huang Y.N., Wu C.H., Lin T.C., Wang J.Y. Methamphetamine induces heme oxygenase-1 expression in cortical neurons and glia to prevent its toxicity. Toxicol. Appl. Pharmacol. 2009, 240:315-326.
30. Immenschuh S., Ramadori G. Gene regulation of heme oxygenase-1 as a therapeutic target. Biochem. Pharmacol. 2000, 60:1121-1128.
31. Itzhak Y., Achat-Mendes C. Methamphetamine and MDMA (ecstasy) neurotoxicity: 'of mice and men'. IUBMB Life 2004, 56:249-255.
32. King G., Alicata D., Cloak C., Chang L. Neuropsychological deficits in adolescent methamphetamine abusers. Psychopharmacology (Berl.) 2010, 212:243-249.
33. Kita T., Wagner G.C., Nakashima T. Current research on methamphetamine-induced neurotoxicity: animal models of monoamine disruption. J. Pharmacol. Sci. 2003, 92:178-195.
34. Kiyatkin E.A. Brain hyperthermia during physiological and pathological conditions: causes, mechanisms, and functional implications. Curr. Neurovasc. Res. 2004, 1:77-90.
35. Kiyatkin E.A., Sharma H.S. Acute methamphetamine intoxication: brain hyperthermia, blood-brain barrier, brain edema, and morphological cell abnormalities. Int. Rev. Neurobiol. 2009, 88:65-100.
36. Kiyatkin E.A., Brown P.L., Sharma H.S. Brain edema and breakdown of the blood-brain barrier during methamphetamine intoxication: critical role of brain hyperthermia. Eur. J. Neurosci. 2007, 26:1242-1253.
37. Klongpanichapak S., Govitrapong P., Sharma S.K., Ebadi M. Attenuation of cocaine and methamphetamine neurotoxicity by coenzyme Q10. Neurochem. Res. 2006, 31:303-311.
38. Ku B.M., Joo Y., Mun J., Roh G.S., Kang S.S., Cho G.J., Choi W.S., Kim H.J. Heme oxygenase protects hippocampal neurons from ethanol-induced neurotoxicity. Neurosci. Lett. 2006, 405:168-171.
39. Lee D.W., Gelein R.M., Opanashuk L.A. Heme-oxygenase-1 promotes polychlorinated biphenyl mixture aroclor 1254-induced oxidative stress and dopaminergic cell injury. Toxicol. Sci. 2006, 90:159-167.
40. Leon A., Le Foll I., Charriault-Marlangue C., Leprince J., Vaudry H., Gabriel C., Duval D. Level of haem oxygenase does not obligatorily reflect the sensitivity of PC12 cells to an oxidative shock induced by glutathione depletion. J. Neurochem. 2003, 84:459-470.
41. Levine M., Conry-Cantilena C., Wang Y., Welch R.W., Washko P.W., Dhariwal K.R., Park J.B., Lazarev A., Graumlich J.F., King J., Cantilena L.R. Vitamin C pharmacokinetics in healthy volunteers: evidence for a recommended dietary allowance. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:3704-3709.
42. Levine M., Padayatty S.J., Espey M.G. Vitamin C: a concentration-function approach yields pharmacology and therapeutic discoveries. Adv. Nutr. 2011, 2:78-88.
43. Lin C.H., Kuo S.C., Huang L.J., Gean P.W. Neuroprotective effect of N-acetylcysteine on neuronal apoptosis induced by a synthetic gingerdione compound: involvement of ERK and p38 phosphorylation. J. Neurosci. Res. 2006, 84:1485-1494.
44. London E.D., Simon S.L., Berman S.M., Mandelkern M.A., Lichtman A.M., Bramen J., Shinn A.K., Miotto K., Learn J., Dong Y., Matochik J.A., Kurian V., Newton T., Woods R., Rawson R., Ling W. Mood disturbances and regional cerebral metabolic abnormalities in recently abstinent methamphetamine abusers. Arch. Gen. Psychiatry 2004, 61:73-84.
45. Mancuso C. Heme oxygenase and its products in the nervous system. Antioxid. Redox Signal 2004, 6:878-887.
46. Marshall J.F., Belcher A.M., Feinstein E.M., O'Dell S.J. Methamphetamine-induced neural and cognitive changes in rodents. Addiction 2007, 102(Suppl. 1):61-69.
47. Matsuda L.A., Schmidt C.J., Gibb J.W., Hanson G.R. Ascorbic acid-deficient condition alters central effects of methamphetamine. Brain Res. 1987, 400:176-180.
48. Matsuda L.A., Schmidt C.J., Gibb J.W., Hanson G.R. Effects of methamphetamine on central monoaminergic systems in normal and ascorbic acid-deficient guinea pigs. Biochem. Pharmacol. 1988, 37:3477-3484.
49. McDonagh A.F. Is bilirubin good for you?. Clin. Perinatol. 1990, 17:359-369.
50. Melega W.P., Williams A.E., Schmitz D.A., DiStefano E.W., Cho A.K. Pharmacokinetic and pharmacodynamic analysis of the actions of D-amphetamine and D-methamphetamine on the dopamine terminal. J. Pharmacol. Exp. Ther. 1995, 274:90-96.
51. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65:55-63.
52. Padayatty S.J., Sun H., Wang Y., Riordan H.D., Hewitt S.M., Katz A., Wesley R.A., Levine M. Vitamin C pharmacokinetics: implications for oral and intravenous use. Ann. Intern. Med. 2004, 140:533-537.
53. Pu C., Broening H.W., Vorhees C.V. Effect of methamphetamine on glutamate-positive neurons in the adult and developing rat somatosensory cortex. Synapse 1996, 23:328-334.
54. Quinton M.S., Yamamoto B.K. Causes and consequences of methamphetamine and MDMA toxicity. AAPS J. 2006, 8:E337-E347.
55. Ranjan A., Theodore D., Haran R.P., Chandy M.J. Ascorbic acid and focal cerebral ischaemia in a primate model. Acta Neurochir. (Wien) 1993, 123:87-91.
56. Reiber H., Ruff M., Uhr M. Ascorbate concentration in human cerebrospinal fluid (CSF) and serum. Intrathecal accumulation and CSF flow rate. Clin. Chim. Acta 1993, 217:163-173.
57. Rice M.E. Ascorbate regulation and its neuroprotective role in the brain. Trends Neurosci. 2000, 23:209-216.
58. Riddle E.L., Fleckenstein A.E., Hanson G.R. Mechanisms of methamphetamine-induced dopaminergic neurotoxicity. AAPS J. 2006, 8:E413-E418.
59. Rosales-Corral S., Tan D.X., Reiter R.J., Valdivia-Velazquez M., Martinez-Barboza G., Acosta-Martinez J.P., Ortiz G.G. Orally administered melatonin reduces oxidative stress and proinflammatory cytokines induced by amyloid-beta peptide in rat brain: a comparative, in vivo study versus vitamin C and E. J. Pineal Res. 2003, 35:80-84.
60. Rosenkranz A.R., Schmaldienst S., Stuhlmeier K.M., Chen W., Knapp W., Zlabinger G.J. A microplate assay for the detection of oxidative products using 2',7'-dichlorofluorescin-diacetate. J. Immunol. Methods 1992, 156:39-45.
61. Ryter S.W., Otterbein L.E., Morse D., Choi A.M. Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol. Cell. Biochem. 2002, 234-235:249-263.
62. Ryu R., Shin Y., Choi J.W., Min W., Ryu H., Choi C.R., Ko H. Depletion of intracellular glutathione mediates zinc-induced cell death in rat primary astrocytes. Exp. Brain Res. 2002, 143:257-263.
63. Sagara J., Bannai S., Shikano N., Makino N. Conflicting effects of N-acetylcysteine on purified neurons derived from rat cortical culture. Neuroreport 2010, 21:416-421.
64. Sagrista M.L., Garcia A.E., Africa De Madariaga M., Mora M. Antioxidant and pro-oxidant effect of the thiolic compounds N-acetyl-L-cysteine and glutathione against free radical-induced lipid peroxidation. Free Radic. Res. 2002, 36:329-340.
65. Salo R., Ravizza S., Fassbender C. Overlapping cognitive patterns in schizophrenia and methamphetamine dependence. Cogn. Behav. Neurol. 2011, 24:187-193.
66. Santos L.F., Freitas R.L., Xavier S.M., Saldanha G.B., Freitas R.M. Neuroprotective actions of vitamin C related to decreased lipid peroxidation and increased catalase activity in adult rats after pilocarpine-induced seizures. Pharmacol. Biochem. Behav. 2008, 89:1-5.
67. Schipper H.M., Liberman A., Stopa E.G. Neural heme oxygenase-1 expression in idiopathic Parkinson's disease. Exp. Neurol. 1998, 150:60-68.
68. Shin E.J., Suh S.K., Lim Y.K., Jhoo W.K., Hjelle O.P., Ottersen O.P., Shin C.Y., Ko K.H., Kim W.K., Kim D.S., Chun W., Ali S., Kim H.C. Ascorbate attenuates trimethyltin-induced oxidative burden and neuronal degeneration in the rat hippocampus by maintaining glutathione homeostasis. Neuroscience 2005, 133:715-727.
69. Solov'eva M.E., Solov'ev V.V., Faskhutdinova A.A., Kudriavtsev A.A., Akatov V.S. Prooxidant and cytotoxic action of N-acetylcysteine and glutathione combined with vitamin Bl2b. Tsitologiia 2007, 49:70-78.
70. Suttner D.M., Dennery P.A. Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J. 1999, 13:1800-1809.
71. Takizawa S., Hirabayashi H., Matsushima K., Tokuoka K., Shinohara Y. Induction of heme oxygenase protein protects neurons in cortex and striatum, but not in hippocampus, against transient forebrain ischemia. J. Cereb. Blood Flow Metab. 1998, 18:559-569.
72. Thompson P.M., Hayashi K.M., Simon S.L., Geaga J.A., Hong M.S., Sui Y., Lee J.Y., Toga A.W., Ling W., London E.D. Structural abnormalities in the brains of human subjects who use methamphetamine. J. Neurosci. 2004, 24:6028-6036.
73. Ulrich-Merzenich G., Zeitler H., Panek D., Bokemeyer D., Vetter H. Vitamin C promotes human endothelial cell growth via the ERK-signaling pathway. Eur. J. Nutr. 2007, 46:87-94.
74. Valko M., Morris H., Cronin M.T. Metals, toxicity and oxidative stress. Curr. Med. Chem. 2005, 12:1161-1208.
75. Volkow N.D., Chang L., Wang G.J., Fowler J.S., Franceschi D., Sedler M.J., Gatley S.J., Hitzemann R., Ding Y.S., Wong C., Logan J. Higher cortical and lower subcortical metabolism in detoxified methamphetamine abusers. Am. J. Psychiatry 2001, 158:383-389.
76. Wagner G.C., Carelli R.M., Jarvis M.F. Pretreatment with ascorbic acid attenuates the neurotoxic effects of methamphetamine in rats. Res. Commun. Chem. Pathol. Pharmacol. 1985, 47:221-228.
77. Wang J.Y., Shum A.Y., Ho Y.J. Oxidative neurotoxicity in rat cerebral cortex neurons: synergistic effects of H2O2 and NO on apoptosis involving activation of p38 mitogen-activated protein kinase and caspase-3. J. Neurosci. Res. 2003, 72:508-519.
78. Wu C.C., Hsu M.C., Hsieh C.W., Lin J.B., Lai P.H., Wung B.S. Upregulation of heme oxygenase-1 by Epigallocatechin-3-gallate via the phosphatidylinositol 3-kinase/Akt and ERK pathways. Life Sci. 2006, 78:2889-2897.
79. Wu P.H., Shen Y.C., Wang Y.H., Chi C.W., Yen J.C. Baicalein attenuates methamphetamine-induced loss of dopamine transporter in mouse striatum. Toxicology 2006, 226:238-245.
80. Yao P., Nussler A., Liu L., Hao L., Song F., Schirmeier A., Nussler N. Quercetin protects human hepatocytes from ethanol-derived oxidative stress by inducing heme oxygenase-1 via the MAPK/Nrf2 pathways. J. Hepatol. 2007, 47:253-261.
81. Yi J.H., Hazell A.S. N-acetylcysteine attenuates early induction of heme oxygenase-1 following traumatic brain injury. Brain Res. 2005, 1033:13-19.
82. Zhu J.P., Xu W., Angulo J.A. Methamphetamine-induced cell death: selective vulnerability in neuronal subpopulations of the striatum in mice. Neuroscience 2006, 140:607-622.