CYP2E1 induction leads to oxidative stress and cytotoxicity in glutathione-depleted cerebellar granule neurons

Toxicology in Vitro

Volumn 28, Issue 7, 2014, Pages 1206-1214

  Valencia Olvera, Ana Carolina ^a   Morán, Julio ^a   Camacho Carranza, Rafael ^a   Prospéro García, Oscar ^b   Espinosa Aguirre, Jesús Javier ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

8 oxo dG; Brain cytochrome P450 2E1; BSO; Cerebellar granule cells; Isoniazid; Oxidative stress

Indexed keywords

ALLYL SULFIDE; CYTOCHROME P450 2E1; GLUTATHIONE; REACTIVE OXYGEN METABOLITE; CYTOCHROME P450 2E1 INDUCER; DNA; ISONIAZID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATTENUATION; BRAIN CELL CULTURE; BRAIN NERVE CELL; CELL DEATH; CELL VIABILITY; CEREBELLAR GRANULE NEURON; CONTROLLED STUDY; CYTOTOXICITY; DNA METABOLISM; IMMUNOCYTOCHEMISTRY; INHIBITION KINETICS; LONG TERM EXPOSURE; NONHUMAN; OXIDATIVE STRESS; PRIMARY CELL CULTURE; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; ANIMAL; CELL CULTURE; CELL SURVIVAL; CEREBELLUM; CYTOLOGY; DRUG EFFECTS; METABOLISM; NERVE CELL; OXIDATION REDUCTION REACTION;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; CEREBELLUM; CYTOCHROME P-450 CYP2E1; CYTOCHROME P-450 CYP2E1 INDUCERS; DNA; GLUTATHIONE; ISONIAZID; NEURONS; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES;

EID: 84903887848     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2014.05.014     Document Type: Article

References (48)

1. Anandatheerthavarada H.K., Shankar S.K., Bhamre S., Boyd M.R., Song B.J., Ravindranath V. Induction of brain cytochrome P-450IIE1 by chronic ethanol treatment. Brain Res. 1993, 601:279-285.
2. Bains J.S., Shaw C.A. Neurodegenerative disorders in humans: the role of glutathione in oxidative stress-mediated neuronal death. Brain Res. Brain Res. Rev. 1997, 25:335-358.
3. Baudry M., Etienne S., Bruce A., Palucki M., Jacobsen E., Malfroy B. Salen-manganese complexes are superoxide dismutase-mimics. Biochem. Biophys. Res. Commun. 1993, 192:964-968.
4. Bell L.C., Guengerich F.P. Oxidation kinetics of ethanol by human cytochrome P450 2E1. Rate-limiting product release accounts for effects of isotopic hydrogen substitution and cytochrome b5 on steady-state kinetics. J. Biol. Chem. 1997, 272:29643-29651.
5. Bhagwat S.V., Boyd M.R., Ravindranath V. Brain mitochondrial cytochromes P450: xenobiotic metabolism, presence of multiple forms and their selective inducibility. Arch. Biochem. Biophys. 1995, 320:73-83.
6. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
7. Brady J.F., Ishizaki H., Fukuto J.M., Lin M.C., Fadel A., Gapac J.M., Yang C.S. Inhibition of cytochrome P-450 2E1 by diallyl sulfide and its metabolites. Chem. Res. Toxicol. 1991, 4:642-647.
8. Cederbaum A.I., Wu D., Mari M., Bai J. CYP2E1-dependent toxicity and oxidative stress in HepG2 cells. Free Radical Biol. Med. 2001, 31:1539-1543.
9. Cohn J.A., Alvares A.P., Kappas A. On the occurrence of cytochrome P-450 and aryl hydrocarbon hydroxylase activity in rat brain. J. Exp. Med. 1977, 145:1607-1611.
10. Chen Q., Cederbaum A.I. Cytotoxicity and apoptosis produced by cytochrome P450 2E1 in Hep G2 cells. Mol. Pharmacol. 1998, 53:638-648.
11. Dai Y., Rashba-Step J., Cederbaum A.I. Stable expression of human cytochrome P4502E1 in HepG2 cells: characterization of catalytic activities and production of reactive oxygen intermediates. Biochemistry 1993, 32:6928-6937.
12. Das M., Seth P.K., Mukhtar H. Characterization of microsomal aryl hydrocarbon hydroxylase of rat brain. J. Pharmacol. Exp. Ther. 1981, 216:156-161.
13. Ding X., Kaminsky L.S. Human extrahepatic cytochromes P450: function in xenobiotic metabolism and tissue-selective chemical toxicity in the respiratory and gastrointestinal tracts. Annu. Rev. Pharmacol. Toxicol. 2003, 43:149-173.
14. Dutheil F., Beaune P., Loriot M.A. Xenobiotic metabolizing enzymes in the central nervous system: contribution of cytochrome P450 enzymes in normal and pathological human brain. Biochimie 2008, 90:426-436.
15. Ferguson C.S., Tyndale R.F. Cytochrome P450 enzymes in the brain: emerging evidence of biological significance. Trends Pharmacol. Sci. 2011, 32:708-714.
16. Gonzalez F.J. The 2006 Bernard B. Brodie Award Lecture. Cyp2e1. Drug Metab. Dispos.: Biolog. Fate Chem. 2007, 35:1-8.
17. Guengerich F.P., MacDonald J.S. Applying mechanisms of chemical toxicity to predict drug safety. Chem. Res. Toxicol. 2007, 20:344-369.
18. Gurumurthy P., Ramachandran R., Balasubramanian R., Rahman F., Victor L., Narayana A.S.L., Sarma G.R. Gastro-intestinal absorption of isoniazid and rifampicin in patients with intestinal tuberculosis. Indian J. Tuber. 1990, 37:5-10.
19. Hall A.G. Glutathione and the regulation of cell death. Adv. Exp. Med. Biol. 1999, 457:199-203.
20. Howard L.A., Miksys S., Hoffmann E., Mash D., Tyndale R.F. Brain CYP2E1 is induced by nicotine and ethanol in rat and is higher in smokers and alcoholics. Br. J. Pharmacol. 2003, 138:1376-1386.
21. Joshi M., Tyndale R.F. Induction and recovery time course of rat brain CYP2E1 after nicotine treatment. Drug Metab. Dispos.: Biolog. Fate Chem. 2006, 34:647-652.
22. Khokhar J.Y., Tyndale R.F. Drug metabolism within the brain changes drug response: selective manipulation of brain CYP2B alters propofol effects. Neuropsychopharmacology: official publication of the American College of. Neuropsychopharmacology 2011, 36:692-700.
23. Khokhar J.Y., Tyndale R.F. Rat brain CYP2B-enzymatic activation of chlorpyrifos to the oxon mediates cholinergic neurotoxicity. Toxicol. Sci. 2012, 126:325-335.
24. Lee S.S., Buters J.T., Pineau T., Fernandez-Salguero P., Gonzalez F.J. Role of CYP2E1 in the hepatotoxicity of acetaminophen. J. Biol. Chem. 1996, 271:12063-12067.
25. Lu Y., Cederbaum A.I. CYP2E1 and oxidative liver injury by alcohol. Free Radical Biol. Med. 2008, 44:723-738.
26. Madan A., Graham R.A., Carroll K.M., Mudra D.R., Burton L.A., Krueger L.A., Downey A.D., Czerwinski M., Forster J., Ribadeneira M.D., Gan L.S., LeCluyse E.L., Zech K., Robertson P., Koch P., Antonian L., Wagner G., Yu L., Parkinson A. Effects of prototypical microsomal enzyme inducers on cytochrome P450 expression in cultured human hepatocytes. Drug Metab. Dispos. 2003, 31:421-431.
27. Mann A., Tyndale R.F. Cytochrome P450 2D6 enzyme neuroprotects against 1-methyl-4-phenylpyridinium toxicity in SH-SY5Y neuronal cells. Eur. J. Neurosci. 2010, 31:1185-1193.
28. Miller K.J., Anderholm D.C., Ames M.M. Metabolic activation of the serotonergic neurotoxin para-chloroamphetamine to chemically reactive intermediates by hepatic and brain microsomal preparations. Biochem. Pharmacol. 1986, 35:1737-1742.
29. Montoliu C., Sancho-Tello M., Azorin I., Burgal M., Valles S., Renau-Piqueras J., Guerri C. Ethanol increases cytochrome P4502E1 and induces oxidative stress in astrocytes. J. Neurochem. 1995, 65:2561-2570.
30. Moran J., Patel A.J. Effect of potassium depolarization on phosphate-activated glutaminase activity in primary cultures of cerebellar granule neurons and astroglial cells during development. Brain Res. Dev. Brain Res. 1989, 46:97-105.
31. Morgan E.T., Koop D.R., Coon M.J. Catalytic activity of cytochrome P-450 isozyme 3a isolated from liver microsomes of ethanol-treated rabbits. Oxidation of alcohols. J. Biol. Chem. 1982, 257:13951-13957.
32. Park K.S., Sohn D.H., Veech R.L., Song B.J. Translational activation of ethanol-inducible cytochrome P450 (CYP2E1) by isoniazid. Eur. J. Pharmacol. 1993, 248:7-14.
33. Rahman I., Kode A., Biswas S.K. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat. Protoc. 2006, 1:3159-3165.
34. Sanchez-Martin F.J., Fernandez-Salguero P.M., Merino J.M. Aryl hydrocarbon receptor-dependent induction of apoptosis by 2,3,7,8-tetrachlorodibenzo-p-dioxin in cerebellar granule cells from mouse. J. Neurochem. 2011, 118:153-162.
35. Seliskar M., Rozman D. Mammalian cytochromes P450-importance of tissue specificity. Biochim. Biophys. Acta 2007, 1770:458-466.
36. Shen C., Zhang H., Zhang G., Meng Q. Isoniazid-induced hepatotoxicity in rat hepatocytes of gel entrapment culture. Toxicol. Lett. 2006, 167:66-74.
37. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 1969, 27:502-522.
38. Trafalis D.T., Panteli E.S., Grivas A., Tsigris C., Karamanakos P.N. CYP2E1 and risk of chemically mediated cancers. Expert Opin. Drug Metab. Toxicol. 2010, 6:307-319.
39. Upadhya S.C., Boyd M.R., Ravindranath V. Characterization and localization of cytochrome P450 mediated metabolism of MPTP to nor-MPTP in mouse brain: relevance to Parkinson's disease. Neurotoxicity Res. 2001, 3:369-380.
40. Upadhya S.C., Tirumalai P.S., Boyd M.R., Mori T., Ravindranath V. Cytochrome P4502E (CYP2E) in brain: constitutive expression, induction by ethanol and localization by fluorescence in situ hybridization. Arch Biochem. Biophys. 2000, 373:23-34.
41. Weissman L., de Souza-Pinto N.C., Stevnsner T., Bohr V.A. DNA repair, mitochondria, and neurodegeneration. Neuroscience 2007, 145:1318-1329.
42. Wu D., Cederbaum A.I. Removal of glutathione produces apoptosis and necrosis in HepG2 cells overexpressing CYP2E1. Alcohol. Clin. Exp. Res. 2001, 25:619-628.
43. Wüllner U., Seyfried J., Groscurth P., Beinroth S., Winter S., Gleichmann M., Heneka M., Loschmann P., Schulz J.B., Weller M., Klockgether T. Glutathione depletion and neuronal cell death: the role of reactive oxygen intermediates and mitochondrial function. Brain Res. 1999, 826:53-62.
44. Yadav S., Dhawan A., Singh R.L., Seth P.K., Parmar D. Expression of constitutive and inducible cytochrome P450 2E1 in rat brain. Mol. Cell Biochem. 2006, 286:171-180.
45. Yue J., Dong G., He C., Chen J., Liu Y., Peng R. Protective effects of thiopronin against isoniazid-induced hepatotoxicity in rats. Toxicology 2009, 264:185-191.
46. Zand R., Nelson S.D., Slattery J.T., Thummel K.E., Kalhorn T.F., Adams S.P., Wright J.M. Inhibition and induction of cytochrome P4502E1-catalyzed oxidation by isoniazid in humans. Clin. Pharmacol. Ther. 1993, 54:142-149.
47. Zhong Y., Dong G., Luo H., Cao J., Wang C., Wu J., Feng Y.Q., Yue J. Induction of brain CYP2E1 by chronic ethanol treatment and related oxidative stress in hippocampus, cerebellum, and brainstem. Toxicology 2012, 302:275-284.
48. Zhou K., Khokhar J.Y., Zhao B., Tyndale R.F. First demonstration that brain CYP2D-mediated opiate metabolic activation alters analgesia in vivo. Biochem. Pharmacol. 2013, 85:1848-1855.