Aroclor 1254 induced cytotoxicity and mitochondrial dysfunction in isolated rat hepatocytes

Toxicology

Volumn 262, Issue 3, 2009, Pages 175-183

  Aly, Hamdy A A ^a,b   Domènech, Òscar ^b  

^a Al Azhar University   (Egypt)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Aroclor 1254; Hepatocytes; Mitochondria; Oxidative stress

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; ACONITATE HYDRATASE; AROCLOR 1254; CARDIOLIPIN; CYTOCHROME P450 1A1; CYTOCHROME P450 2B; ETHOXYRESORUFIN DEETHYLASE; FATTY ACID; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; LACTATE DEHYDROGENASE; LIPID; PENTOXYRESORUFIN DEALKYLASE; POLYCHLORINATED BIPHENYL; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

ANIMAL CELL; ARTICLE; CELL ASSAY; CELL DAMAGE; CELL ISOLATION; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CULTURE MEDIUM; CYTOTOXICITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME INHIBITION; FATTY ACID OXIDATION; INCUBATION TIME; LIPID PEROXIDATION; LIVER CELL; LIVER MITOCHONDRION; LIVER TOXICITY; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR MECHANICS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FAMILY; RAT; TARGET CELL;

ANIMALS; CELL SURVIVAL; CHLORODIPHENYL (54% CHLORINE); DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX III; GLUTATHIONE; HEPATOCYTES; L-LACTATE DEHYDROGENASE; LIPID PEROXIDATION; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA, LIVER; OXIDATIVE STRESS; RATS; TOXICITY TESTS;

RATTUS;

EID: 67651051837     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2009.05.018     Document Type: Article

References (102)

1. Adebusoye S.A., Ilori M.O., Picardal F.W., and Amund O.O. Extensive biodegradation of polychlorinated biphenyls in Aroclor 1242 and electrical transformer fluid (Askarel) by natural strains of microorganisms indigenous to contaminated African systems. Chemosphere 73 (2008) 126-132
2. Aly, H.A.A., Domenech, O., Abdel-Naim, A.B., 2009. Aroclor 1254 impairs spermatogenesis and induces oxidative stress in rat testicular mitochondria. Food Chem. Toxicol., Mar 21.
3. Andric N.L., Andric S.A., Zoric S.N., Kostic T.S., Stojilkovic S.S., and Kovacevic R.Z. Parallelism and dissociation in the actions of an Aroclor 1260-based transformer fluid on testicular androgenesis and antioxidant enzymes. Toxicology 194 (2003) 65-75
4. Baird L. Toxic organic chemicals. Environmental Chemistry (1995), WH Freeman and Company, New York pp. 252-274
5. Banudevi S., Arunkumar A., Sharmila M., Senthilkumar J., Balasubramanian K., Srinivasan N., Aruldhas M.M., and Arunakaran J. Diallyl disulfide-induced modulation of a few phase I and II drug metabolizing enzymes on Aroclor 1254 toxicity in Rattus norvegicus liver and ventral prostate. J. Clin. Biochem. Nutr. 36 (2005) 59-65
6. Banudevi S., Krishnamoorthy G., Venkataraman P., Vignesh C., Aruldhas M.M., and Arunakaran J. Role of alpha-tocopherol on antioxidant status in liver, lung and kidney of PCB exposed male albino rats. Food Chem. Toxicol. 44 (2006) 2040-2046
7. Bonfanti P., Colombo A., Villa S., Comelli F., Costa B., and Santagostino A. The effects of accumulation of an environmentally relevant polychlorinated biphenyl mixture on cytochrome P450 and P-glycoprotein expressions in fetuses and pregnant rats. Chemosphere 75 (2009) 572-579
8. Bray T.M., and Taylor C.G. Tissue glutathione, nutrition, and oxidative stress. Can. J. Physiol. Pharmacol. 71 (1993) 746-751
9. Bruggisser R., von Daeniken K., Jundt G., Schaffner W., and Tullberg-Reinert H. Interference of plant extracts, phytoestrogens and antioxidants with the MTT tetrazolium assay. Planta Med. 68 (2002) 445-448
10. Burke M.D., Thompson S., Elcombe C.R., Halpert J., Haaparanta T., and Mayer R.T. Ethoxy-, pentoxy- and benzyloxyphenoxazones and homologues: a series of substrates to distinguish between different induced cytochromes P-450. Biochem. Pharmacol. 34 (1985) 3337-3345
11. Burke M.D., Thompson S., Weaver R.J., Wolf C.R., and Mayer R.T. Cytochrome P450 specificities of alkoxyresorufin O-dealkylation in human and rat liver. Biochem. Pharmacol. 48 (1994) 923-936
12. Burqin D.E., Diliberto J.J., Derr-Yellin E.C., Kannan N., Kodavanti P.R., and Birnbaum L.S. Differential effects of two lots of aroclor 1254 on enzyme induction, thyroid hormones, and oxidative stress. Environ. Health Perspect. 109 (2001) 1163-1168
13. Castell J.V., Gomez-Lechon M.J., Ponsoda X., and Bort R. In vitro investigation of the molecular mechanisms of hepatotoxicity. In: Castell J.V., and Gomez-Lechon M.J. (Eds). In Vitro Methods in Pharmaceutical Research (1997), Academic Press, London 375-410
14. Choy C.S., Cheah K.P., Chiou H.Y., Li J.S., Liu Y.H., Yong S.F., Chiu W.T., Liao J.W., and Hu C.M. Induction of hepatotoxicity by sanguinarine is associated with oxidation of protein thiols and disturbance of mitochondrial respiration. J. Appl. Toxicol. 28 (2008) 945-956
15. Chu I., Bowers W.J., Caldwell D., Nakai J., Wade M.G., Yagminas A., Li N., Moir D., El Abbas L., Håkansson H., Gill S., Mueller R., and Pulido O. Toxicological effects of in utero and lactational exposure of rats to a mixture of environmental contaminants detected in Canadian Arctic human populations. J. Toxicol. Environ. Health A 71 (2008) 93-108
16. Chung H.C., Kim S.H., Lee M.G., Cho C.K., Kim T.H., Lee D.H., and Kim S.G. Mitochondrial dysfunction by gamma-irradiation accompanies the induction of cytochrome P450 2E1 (CYP2E1) in rat liver. Toxicology 161 (2001) 79-91
17. Czarna M., and Jarmuszkiewicz W. Role of mitochondria in reactive oxygen species generation and removal, relevance to signaling and programmed cell death. Postepy. Biochem. 52 (2006) 145-156
18. Denomme M.A., Bandiera S., Lambert I., Copp L., Safe L., and Safe S. Polychlorinated biphenyls as phenobarbitone-type inducers of microsomal enzymes. Structure-activity relationships for a series of 2,4-dichloro-substituted congeners. Biochem. Pharmacol. 32 (1983) 2955-2963
19. Droge W. Free radicals in the physiological control of cell function. Physiol. Rev. 82 (2002) 47-95
20. Duranteau J., Chandel N.S., Kulisz A., Shao Z., and Schumacker P.T. Intracellular signaling by reactive oxygen species during hypoxia in cardiomyocytes. J. Biol. Chem. 273 (1998) 11619-11624
21. Fadhel Z.A., Lu Z., Robertson L.W., and Glauert H.P. Role of cytochrome P450 induction and lipid peroxidation in 3,3′,4,4′-tetrachlorobiphenyl (PCB-77) and 2,2′,4,4′,5,5′-hexachlorobiphenyl (PCB-153)-induced toxicity in liver of male rats. Toxicol. Sci. 54 (2000) 78
22. Fadhel Z., Lu Z., Robertson L.W., and Glauert H.P. Effect of 3,3′,4,4′-tetrachlorobiphenyl and 2,2′,4,4′,5,5′-hexachlorobiphenyl on the induction of hepatic lipid peroxidation and cytochrome P-450 associated enzyme activities in rats. Toxicology 175 (2002) 15-25
23. Farber J.L., and Young E.E. Accelerated phospholipid degradation in anoxic rat hepatocytes. Arch. Biochem. Biophys. 211 (1981) 312-320
24. Fariss M.W., Chan C.B., Patel M., and Van Houten B. Role of mitochondria in toxic oxidative stress. Mol. Interv. 5 (2005) 94-111
25. Fréneaux E., Labbe G., Letteron P., The Le Dinh, Degott C., Genève J., Larrey D., and Pessayre D. Inhibition of the mitochondrial oxidation of fatty acids by tetracycline in mice and in man: possible role in microvesicular steatosis induced by this antibiotic. Hepatology 8 (1988) 1056-1062
26. Gallet P.F., Maftah A., Petit J.M., Denis-Gay M., and Julien R. Direct cardiolipin assay in yeast using the red fluorescence emission of 10-N-nonyl acridine orange. Eur. J. Biochem. 15 (1995) 113-119
27. Gardner P.R. Aconitase: sensitive target and measure of superoxide. Methods Enzymol. 349 (2002) 9-23
28. Giesy J.P., and Kannan K. Dioxin-like and non-dioxin-like toxic effects of polychlorinated biphenyls (PCBs): implications for risk assessment. Crit. Rev. Toxicol. 28 (1998) 511-569
29. Halliwell B., and Gutteridge J.M.C. Role of free radicals and catalytic metal ions in human disease: an overview. Meth. Enzymol. 186 (1990) 1-85
30. Hauff K.D., and Hatch G.M. Cardiolipin metabolism and Barth syndrome. Prog. Lipid Res. 45 (2006) 91-101
31. Hausladen A., and Fridovich I. Superoxide and peroxynitrite inactivate aconitases, but nitric oxide does not. J. Biol. Chem. 269 (1994) 29405-29408
32. Hausladen A., and Fridovich I. Measuring nitric oxide and superoxide: rate constants for aconitase reactivity. Methods Enzymol. 269 (1996) 37-41
33. Hissin P.J., and Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 74 (1976) 214-226
34. Hoek J.B., Farber J.L., Thomas A.P., and Wang X. Calcium ion-dependent signalling and mitochondrial dysfunction: mitochondrial calcium uptake during hormonal stimulation in intact liver cells and its implication for the mitochondrial permeability transition. Biochim. Biophys. Acta 1272 (1995) 93-102
35. Hsiao G., Lin Y.H., Lin C.H., Chou D.S., Lin W.C., and Sheu J.R. The protective effects of PMC against chronic carbon tetrachloride-induced hepatotoxicity in vivo. Biol. Pharm. Bull. 4 (2001) 1271-1276
36. Ikegwuonu F.I., Ganen L.G., Larsen M.C., Shen X., and Jefcoate C.R. The regulation by gender, strain, dose, and feeding status of the induction of multiple forms of cytochrome P450 isozymes in rat hepatic microsomes by 2,4,5,29,49,59-hexachlorobiphenyl. Toxicol. Appl. Pharmacol. 139 (1996) 33-41
37. Iqbal M., and Athar M. Attenuation of iron-nitrilotriacetate mediated renal oxidative stress, toxicity and hyperproliferative response by the prophylactic treatment of rats with garlic oil. Food Chem. Toxicol. 36 (1998) 485-495
38. James A.M., Cochemé H.M., Smith R.A., and Murphy M.P. Interactions of mitochondria-targeted and untargeted ubiquinones with the mitochondrial respiratory chain and reactive oxygen species. Implications for the use of exogenous ubiquinines as therapies and experimental tools. J. Biol. Chem. 280 (2005) 21295-212312
39. Kaufmann P., Török M., Hänni A., Roberts P., Gasser R., and Krähenbühl S. Mechanisms of benzarone and benzbromarone-induced hepatic toxicity. Hepatology 41 (2005) 925-935
40. Kimbrough R.D. Polychlorinated biphenyls (PCBs) and human health: an update. Crit. Rev. Toxicol. 25 (1995) 133-163
41. Kirkland R.A., and Franklin J.L. Bax, reactive oxygen, and cytochrome c release in neuronal apoptosis. Antioxid. Redox. Signal. 5 (2003) 589-596
42. Kowaltowski A.J., and Vercesi A.E. Mitochondrial damage induced by conditions of oxidative stress. Free Radical Bio. med. 26 (1999) 463-471
43. Lambert C., Apel K., Biesalski H.K., and Frank J. 2-Methoxyestradiol induces caspase-independent, mitochondria-centered apoptosis in DS-sarcoma cells. Int. J. Cancer 108 (2004) 493-501
44. Larsen J.C. Risk assessments of polychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans, and dioxin-like polychlorinated biphenyls in food. Mol. Nutr. Food Res. 50 (2006) 885-896
45. Latipää P.M., Kärki T.T., Hiltunen J.K., and Hassinen I.E. Regulation of palmitoylcarnitine oxidation in isolated rat liver mitochondria. Role of the redox state of NAD(H). Biochim. Biophys. Acta 875 (1986) 293-300
46. Liu M.J., Wang Z., Li H.X., Wu R.C., Liu Y.Z., and Wu Q.Y. Mitochondrial dysfunction as an early event in the process of apoptosis induced by woodfordin I in human leukemia K562 cells. Toxicol. Appl. Pharmacol. 194 (2004) 141-155
47. Lu, C.F., Wang, Y.M., Peng, S.Q., Zou, L.B., Tan, D.H., Liu, G., Fu, Z., Wang, Q.X., Zhao, J., 2009. Combined Effects of Repeated Administration of 2,3,7,8-Tetrachlorodibenzo-p-dioxin and Polychlorinated Biphenyls on Kidneys of Male Rats. Arch Environ Contam Toxicol., Apr 17.
48. Mariussen E., Myhre O., Reistad T., and Fonnum F. The polychlorinated biphenyl mixture Aroclor 1254 induces death of rat cerebellar granule cells: the involvement of the N-methyl-d-aspartate receptor and reactive oxygen species. Toxicol. Appl. Pharmacol. 179 (2002) 137-144
49. Martins N.M., Santos N.A.G., Curti C., Bianchi M.L.P., and Santos A.C. Cisplatin induces mitochondrial oxidative stress with resultant energetic metabolism impairment, membrane rigidification and apoptosis in rat liver. J. Appl. Toxicol. 28 (2008) 337-344
50. McLean M.R., Twaroski T.P., and Robertson L.W. Redox cycling of 2-(x'-mono,-di,-trichlorophenyl)-1, 4-benzoquinones, oxidation products of polychlorinated biphenyls. Arch. Biochem. Biophys. 376 (2000) 449-455
51. Moriarty-Craige S.E., and Jones D.P. Extracellular thiols and thiol/disulfide redox in metabolism. Annu. Rev. Nutr. 24 (2004) 481-509
52. Morse R.M., Valenzuela G.A., Greenwald T.P., Eulie P.J., Wesley R.C., and McCallum R.W. Amiodarone-induced liver toxicity. Ann. Intern. Med. 109 (1988) 838-840
53. Myhre O., Vestad T.A., Sagstuen E., Aarnes H., and Fonnum F. The effects of aliphatic (n-nonane), naphtenic (1,2,4-trimethylcyclohexane) and aromatic (1,2,4-trimethylbenzene) hydrocarbons on respiratory burst in human neutrophil granulocytes. Toxicol. Appl. Pharmacol. 167 (2000) 222-230
54. Ngui J.S., and Bandiera S.M. Induction of hepatic CYP2B is a more sensitive indicator of exposure to aroclor 1260 than CYP1A in male rats. Toxicol. Appl. Pharmacol. 161 (1999) 160-167
55. Paglia D.E., and Valentine W.N. Studies on quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 70 (1967) 158-169
56. Parkinson A., Safe S.H., Robertson L.W., Thomas P.E., Ryan D.E., Reik L.M., and Levin W. Immunochemical quantitation of cytochrome P-450 isozymes and epoxide hydrolase in liver microsomes from polychlorinated or polybrominated biphenyl-treated rats. A study of structure-activity relationships. J. Biol. Chem. 258 (1983) 5967-5976
57. Perez-Carreras M., Del Hoyo P., Martin M.A., Rubio J.C., Martin A., Castellano G., Colina F., Arenas J., and Solis-Herruzo J.A. Defective hepatic mitochondrial respiratory chain in patients with nonalcoholic steatohepatitis. Hepatology 38 (2003) 999-1007
58. 2+ channel complex type 1 (RyR1). Chem. Res. Toxicol. 19 (2006) 92-101
59. Pessah I.N., Lehmler H.-J., Robertson L.W., Perez C.F., Cabrales E., Bose D.D., et al. Enantiomeric specificity of (-)-2,2′,3,3′,6,6′-hexachlorobiphenyl toward ryanodine receptor types 1 and 2. Chem. Res. Toxicol. 22 (2009) 201-207
60. Petit J.M., Maftah A., Ratinaud M.H., and Julien R. 10-N-nonyl acridine orange interacts with cardiolipin and allows the quantification of this phospholipid in isolated mitochondria. Eur. J. Biochem. 209 (1992) 267-273
61. Petrosillo G., Portincasa P., Grattagliano I., Casanova G., Matera M., Ruggiero F.M., Ferri D., and Paradies G. Mitochondrial dysfunction in rat with nonalcoholic fatty liver involvement of complex I, reactive oxygen species and cardiolipin. Biochim. Biophys. Acta 1767 (2007) 1260-1267
62. Poland A., and Knutson J.C. 2,3,7,8-Tetrachlorodibenzo-p-dioxin and related halogenated aromatic hydrocarbons: examination of the mechanism of toxicity. Annu. Rev. Pharmacol. Toxicol. 22 (1982) 517-554
63. Poulos T.L., and Raag R. Cytochrome P450cam: crystallography, oxygen activation, and electron transfer. FASEB J. 6 (1992) 674-679
64. Risebrough R.W., Rieche P., Peakall D.B., Herman S.G., and Kirven M.N. Polychlorinated biphenyls in the global ecosystem. Nature 220 (1968) 1098-1102
65. Roue G., Bitton N., Yuste V.J., Montange T., Rubio M., Dessauge F., Delettre C., Merle-Beral H., Sarfati M., and Susin S.A. Mitochondrial dysfunction in CD47-mediated caspase-independent cell death: ROS production in the absence of cytochrome c and AIF release. Biochimie 85 (2003) 741-746
66. Sadeghi-Aliabadi H., Chan K., Lehmler H.J., Robertson L.W., and O'Brien P.J. Molecular cytotoxic mechanisms of catecholic polychlorinated biphenyl metabolites in isolated rat hepatocytes. Chem. Biol. Interact. 167 (2007) 184-192
67. Safe S.H. Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit. Rev. Toxicol. 24 (1994) 87-149
68. Sakac V., and Sakac M. Free oxygen radicals and kidney diseases-part I. Med. Pregl. 53 (2000) 463-474
69. Salvi M., and Toninello A. Aroclor 1254 inhibits the mitochondrial permeability transition and release of cytochrome c: a possible mechanism for its in vivo toxicity. Toxicol. Appl. Pharmacol. 176 (2001) 92-100
70. Schilderman P.A., Mass L.M., Pachen D.M., Dekok T.M., Kleinjans J.C., and Vanschooten F.S. Induction of DNA adducts by several polychlorinated biphenyls. Environ. Mol. Mutagen. 36 (2000) 79-86
71. Schlezinger J.J., White R.D., and Stegeman J.J. Oxidative inactivation of cytochrome p-4501A (CYP1A) stimulated by 3,3′,4,4′-tetrachlorobiphenyl: production of reactive oxygen by vertebrate CYP1As. Mol. Pharmacol. 56 (1999) 588-597
72. Schuetz E.G., Brimer C., and Schuetz J.D. Environmental xenobiotics and the antihormones cyproterone acetate and spironolactone use the nuclear hormone pregnenolone X receptor to activate the CYP3A23 hormone response element. Mol. Pharmacol. 54 (1998) 1113-1117
73. Seglen P.O. Preparation of isolated rat liver cells. Methods Cell Biol. 13 (1976) 29-83
74. Senft A.P., Dalton T.P., Nebert D.W., Genter M.B., Puga A., Hutchinson R.J., Kerzee J.K., Uno S., and Shertzer H.G. Mitochondrial reactive oxygen production is dependent on the aromatic hydrocarbon receptor. Free Radic. Biol. Med. 33 (2002) 1268-1278
75. Shangari N., and O'Brien P.J. The cytotoxic mechanism of glyoxal involves oxidative stress. Biochem. Pharmacol. 68 (2004) 1433-1442
76. Sharpley M.S., Shannon R.J., Draghi F., and Hirst J. Interactions between phospholipids and NADH:ubiquinone oxidoreductase (complex I) from bovine mitochondria. Biochemistry 45 (2006) 241-248
77. Shih C.M., Ko W.C., Wu J.S., Wei Y.H., Wang L.F., Chang E.E., Lo T.Y., Cheng H.H., and Chen C.T. Mediating of caspaseindependent apoptosis by cadmium through the mitochondria-ROS pathway in MRC-5 fibroblasts. J. Cell Biochem. 91 (2004) 384-397
78. Silberhorn E.M., Glauert H.P., and Robertson L.W. Carcinogenicity of polyhalogenated biphenyls: PCBs and PBBs. Crit. Rev. Toxicol. 20 (1990) 440-496
79. Simon T., Britt J.K., and James R.C. Development of a neurotoxic equivalence scheme of relative potency for assessing the risk of PCB mixtures. Regul. Toxicol. Pharm. 48 (2007) 148-170
80. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., and Klenk D.C. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150 (1985) 76-85
81. Song Y., Buettner G.R., Parkin S., Wagner B.A., Robertson L.W., and Lehmler H.J. Chlorination increases the persistence of semiquinone free radicals derived from polychlorinated biphenyl hydroquinones and quinones. J. Org. Chem. 73 (2008) 8296-8304
82. Song Y., Wagner B.A., Lehmler H.J., and Buettner G.R. Semiquinone radicals from oxygenated polychlorinated biphenyls: electron paramagnetic resonance studies. Chem. Res. Toxicol. 21 (2008) 1359-1367
83. Spaniol M., Bracher R., Ha H.R., Follath F., and Krähenbühl S. Toxicity of amiodarone and amiodarone analogues on isolated rat liver mitochondria. J. Hepatol. 35 (2001) 628-636
84. Sridhar M., Venkataraman P., Siva D., Arunkumar A., Aruldhas M.M., Srinivasan N., and Arunakaran J. Impact of polychlorinated biphenyl (Aroclor 1254) and vitamin C on antioxidant system of rat ventral prostate. Asian J. Androl. 6 (2004) 19-22
85. Talbot D.A., Lambert A.J., and Brand M.D. Production of endogenous matrix superoxide from mitochondrial complex I leads to activation of uncoupling protein 3. FEBS Lett. 556 (2004) 111-115
86. Tharappel J.C., Lee E.Y., Robertson L.W., Spear B.T., and Glauert H.P. Regulation of cell proliferation, apoptosis, and transcription factor activities during the promotion of liver carcinogenesis by polychlorinated biphenyls. Toxicol. Appl. Pharmacol. 179 (2002) 172-184
87. Tharappel J.C., Lehmler H.J., Srinivasan C., Robertson L.W., Spear B.T., and Glauert H.P. Effect of antioxidant phytochemicals on the hepatic tumor promoting activity of 3,3′,4,4′-tetrachlorobiphenyl (PCB-77). Food Chem. Toxicol. 46 (2008) 3467-3474
88. Thome J.P., Roelandt L., Goffinet G., Stouvenakers N., and Kremers P. Cytotoxic effects of Aroclor 1254 on ultrastructure and biochemical parameters in cultured foetal rat hepatocytes. Toxicology 98 (1995) 83-94
89. Tisdale H.D. Preparation and properties of succinic-cytochrome c reductase (complex II and III). Methods Enzymol. 10 (1967) 213-215
90. Twaroski T.P., O'Brien M.L., Larmonier N., Glauert H.P., and Robertson L.W. Polychlorinated biphenyl-induced effects on metabolic enzymes AP-1 binding, vitamin E, and oxidative stress in rat liver. Toxicol. Appl. Pharmacol. 171 (2001) 85-93
91. Twaroski T.P., O'Brien M.L., and Robertson L.W. In: Robertson L.W., and Hansen L.G. (Eds). Recent Advances in the Environmental Toxicology and Health Effects. Effects of PCB 77 (3,3′,4,4′-Tetrachlorobiphenyl) on Glutathione Peroxidase Activity and Regulatory Mechanisms (2001), The University Press of Kentucky 317-319
92. Twaroski T.P., O'Brien M.L., and Robertson L.W. Effects of selected polychlorinated biphenyl (PCB) congener on hepatic glutathione, glutathione-related enzymes, and selenium status: implications for oxidative stress. Biochem. Pharmacol. 62 (2001) 273-281
93. Uhlig S., and Wendel A. The physiological consequences of glutathione variations. Life Sci. 51 (1992) 1083-1094
94. Van den Berg M., Birnbaum L., Bosveld A.T., Brunstrom B., Cook P., Feeley M., Giesy J.P., Hanberg A., Hasegawa R., Kennedy S.W., et al. Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ. Health Perspect. 106 (1998) 775-792
95. Van den Berg M., Birnbaum L.S., Denison M., De Vito M., Farland W., Feeley M., Fiedler H., Hakansson H., Hanberg A., Haws L., Rose M., Safe S., Schrenk D., Tohyama C., Tritscher A., Tuomisto J., Tysklind M., Walker N., and Peterso R.E. The 2005 world health organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol. Sci. 93 (2006) 223-241
96. Vanden Hoek T.L., Li C., Shao Z., Schumacker P.T., and Becker L.B. Significant levels of oxidants are generated by isolated cardiomyocytes during ischemia prior to reperfusion. J. Mol. Cell. Cardiol. 29 (1997) 2571-2583
97. Venkataraman P., Krishnamoorthy G., Vengatesh G., Srinivasan N., Aruldhas M.M., and Arunakaran J. Protective role of melatonin on PCB (Aroclor 1254) induced oxidative stress and changes in acetylcholine esterases and membrane bound ATPases in cerebellum, cerebral cortex and hippocampus of adult rat brain. Int. J. Dev. Neurosci. 26 (2008) 585-591
98. Williams C.S., Jones B.C., Nchege O., and Chung R.A. Hepatocyte ultrastructure following exposure to aroclors and pure polychlorinated biphenyls. J. Environ. Pathol. Toxicol. Oncol. 12 (1993) 17-33
99. Wilson K.S., and Prochaska L.J. Phospholipid vesicles containing bovine heart mitochondrial cytochrome c oxidase and subunit III-deficient enzyme: analysis of respiratory control and proton translocating activities. Arch. Biochem. Biophys. 282 (1990) 413-420
100. Ye S.F., Hou Z.Q., and Zhang Q.Q. Protective effects of Phellinus linteus extract against iron overload-mediated oxidative stress in cultured rat hepatocytes. Phytother. Res. 21 (2007) 948-953
101. Zhao, H.X., Adamcakova-Dodd, A., Hu, D., Hornbuckle, K.C., Just, C.L., Robertson, L.W., Thorne, P.S., Lehmler, H.J., 2009. Development of a synthetic PCB mixture resembling the average polychlorinated biphenyl profile in Chicago air. Environ. Int., Apr 16.
102. Zhou C., and Zhang C. Protective effects of antioxidant vitamins on Aroclor 1254-induced toxicity in cultured chicken embryo hepatocytes. Toxicol. In Vitro 19 (2005) 665-673