Glutathione-deficient mice are susceptible to TCDD-induced hepatocellular toxicity but resistant to steatosis

Chemical Research in Toxicology

Volumn 25, Issue 1, 2012, Pages 94-100

  Chen, Ying ^a   Krishan, Mansi ^b   Nebert, Daniel W ^b   Shertzer, Howard G ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ADENOSINE TRIPHOSPHATE; ASPARTATE AMINOTRANSFERASE; GAMMA GLUTAMYLTRANSFERASE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; HOLOENZYME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CATALYSIS; CONTROLLED STUDY; FATTY LIVER; FEMALE; GAMMA GLUTAMYL TRANSFERASE BLOOD LEVEL; HISTOPATHOLOGY; HOMEOSTASIS; LIPID STORAGE; LIVER TOXICITY; MOUSE; NONHUMAN;

ANIMALS; ASPARTATE AMINOTRANSFERASES; ENVIRONMENTAL POLLUTANTS; FATTY LIVER; FEMALE; GAMMA-GLUTAMYLTRANSFERASE; GENE EXPRESSION REGULATION; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; LIPID METABOLISM; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TETRACHLORODIBENZODIOXIN;

MUS; MUS MUSCULUS;

EID: 84862910264     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx200242a     Document Type: Article

References (47)

1. Kretzschmar, M. (1996) Regulation of hepatic glutathione metabolism and its role in hepatotoxicity Exp. Toxicol. Pathol. 48, 439-446 (Pubitemid 26295360)
2. Meister, A. (1991) Glutathione deficiency produced by inhibition of its synthesis, and its reversal; applications in research and therapy Pharmacol. Ther. 51, 155-194
3. Dalton, T. P., Chen, Y., Schneider, S. N., Nebert, D. W., and Shertzer, H. G. (2004) Genetically altered mice to evaluate glutathione homeostasis in health and disease Free Radical Biol. Med. 37, 1511-1526 (Pubitemid 39349798)
4. Chen, Y., Shertzer, H. G., Schneider, S. N., Nebert, D. W., and Dalton, T. P. (2005) Glutamate cysteine ligase catalysis: Dependence on ATP and modifier subunit for regulation of tissue glutathione levels J. Biol. Chem. 280, 33766-33774 (Pubitemid 41443095)
5. Chen, Y., Yang, Y., Miller, M. L., Shen, D., Shertzer, H. G., Stringer, K. F., Wang, B., Schneider, S. N., Nebert, D. W., and Dalton, T. P. (2007) Hepatocyte-specific Gclc deletion leads to rapid onset of steatosis with mitochondrial injury and liver failure Hepatology 45, 1118-1128 (Pubitemid 46775773)
6. Yang, Y., Dieter, M. Z., Chen, Y., Shertzer, H. G., Nebert, D. W., and Dalton, T. P. (2002) Initial characterization of the glutamate-cysteine ligase modifier subunit Gclm(-/-) knockout mouse. Novel model system for a severely compromised oxidative stress response J. Biol. Chem. 277, 49446-49452 (Pubitemid 36014379)
7. Kann, S., Estes, C., Reichard, J. F., Huang, M. Y., Sartor, M. A., Schwemberger, S., Chen, Y., Dalton, T. P., Shertzer, H. G., Xia, Y., and Puga, A. (2005) Butylhydroquinone protects cells genetically deficient in glutathione biosynthesis from arsenite-induced apoptosis without significantly changing their prooxidant status Toxicol. Sci. 87, 365-384 (Pubitemid 41300684)
8. Giordano, G., Kavanagh, T. J., and Costa, L. G. (2008) Neurotoxicity of a polybrominated diphenyl ether mixture (DE-71) in mouse neurons and astrocytes is modulated by intracellular glutathione levels Toxicol. Appl. Pharmacol. 232, 161-168
9. Chen, Y., Johansson, E., Fan, Y., Shertzer, H. G., Vasiliou, V., Nebert, D. W., and Dalton, T. P. (2009) Early onset senescence occurs when fibroblasts lack the glutamate-cysteine ligase modifier subunit Free Radical Biol. Med. 47, 410-418
10. Johansson, E., Wesselkamper, S. C., Shertzer, H. G., Leikauf, G. D., Dalton, T. P., and Chen, Y. (2010) Glutathione deficient C57BL/6J mice are not sensitized to ozone-induced lung injury Biochem. Biophys. Res. Commun. 396, 407-412
11. McConnachie, L. A., Mohar, I., Hudson, F. N., Ware, C. B., Ladiges, W. C., Fernandez, C., Chatterton-Kirchmeier, S., White, C. C., Pierce, R. H., and Kavanagh, T. J. (2007) Glutamate cysteine ligase modifier subunit deficiency and gender as determinants of acetaminophen-induced hepatotoxicity in mice Toxicol. Sci. 99, 628-636 (Pubitemid 351753076)
12. Haque, J. A., McMahan, R. S., Campbell, J. S., Shimizu-Albergine, M., Wilson, A. M., Botta, D., Bammler, T. K., Beyer, R. P., Montine, T. J., Yeh, M. M., Kavanagh, T. J., and Fausto, N. (2010) Attenuated progression of diet-induced steatohepatitis in glutathione-deficient mice Lab. Invest. 90, 1704-1717
13. Dalton, T. P., Puga, A., and Shertzer, H. G. (2002) Induction of cellular oxidative stress by aryl hydrocarbon receptor activation Chem.-Biol. Interact. 141, 77-95 (Pubitemid 35223206)
14. Shertzer, H. G., Clay, C. D., Genter, M. B., Chames, M. C., Schneider, S. N., Oakley, G. G., Nebert, D. W., and Dalton, T. P. (2004) Uncoupling-mediated generation of reactive oxygen by halogenated aromatic hydrocarbons in mouse liver microsomes Free Radical Biol. Med. 36, 618-631 (Pubitemid 38230178)
15. Shen, D., Dalton, T. P., Nebert, D. W., and Shertzer, H. G. (2005) Glutathione redox state regulates mitochondrial reactive oxygen production J. Biol. Chem. 280, 25305-25312 (Pubitemid 40962232)
16. Senft, A. P., Dalton, T. P., and Shertzer, H. G. (2000) Determining glutathione and glutathione disulfide using the fluorescence probe o-phthalaldehyde Anal. Biochem. 280, 80-86 (Pubitemid 30210815)
17. Shertzer, H. G., Woods, S. E., Krishan, M., Genter, M. B., and Pearson, K. J. (2011) Dietary whey protein lowers the risk for metabolic disease in mice fed a high-fat diet J. Nutr. 141, 1-6
18. Forman, H. J., Shi, M. M., Iwamoto, T., Liu, R. M., and Robison, T. W. (1995) Measurement of gamma-glutamyl transpeptidase and gamma-glutamylcysteine synthetase activities in cells Methods Enzymol. 252, 66-71
19. Schumann, G., Bonora, R., Ceriotti, F., Ferard, G., Ferrero, C. A., Franck, P. F., Gella, F. J., Hoelzel, W., Jorgensen, P. J., Kanno, T., Kessner, A., Klauke, R., Kristiansen, N., Lessinger, J. M., Linsinger, T. P., Misaki, H., Panteghini, M., Pauwels, J., Schiele, F., Schimmel, H. G., Weidemann, G., and Siekmann, L. (2002) IFCC primary reference procedures for the measurement of catalytic activity concentrations of enzymes at 37 degrees C. International Federation of Clinical Chemistry and Laboratory Medicine. Part 5. Reference procedure for the measurement of catalytic concentration of aspartate aminotransferase Clin. Chem. Lab. Med. 40, 725-733
20. Nebert, D. W. and Gelboin, H. V. (1968) Substrate-inducible microsomal aryl hydroxylase in mammalian cell culture. I. Assay and properties of induced enzyme J. Biol. Chem. 243, 6242-6249
21. Shertzer, H. G., Nebert, D. W., Senft, A. P., Dingeldein, M., Genter, M. B., and Dalton, T. P. (2001) Spectrophotometric assay for acetanilide 4-hydroxylase, an estimate of CYP1A2 enzyme activity Toxicol. Methods 11, 81-88
22. 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. (2002) Mitochondrial reactive oxygen production is dependent on the aromatic hydrocarbon receptor Free Radical Biol. Med. 33, 1268-1278 (Pubitemid 35246595)
23. Tranter, M., Ren, X., Forde, T., Wilhide, M. E., Chen, J., Sartor, M. A., Medvedovic, M., and Jones, W. K. (2010) NF-kappaB driven cardioprotective gene programs; Hsp70.3 and cardioprotection after late ischemic preconditioning J. Mol. Cell Cardiol. 49, 664-672
24. Huang, d. W., Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 4, 44-57
25. Huang, d. W., Sherman, B. T., and Lempicki, R. A. (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists Nucleic Acids Res. 37, 1-13
26. Livak, K. J. and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25, 402-408 (Pubitemid 34164012)
27. Pohl, H. R., Llados, F., Ingerman, L., Cunningham, P., Raymer, J. H., Wall, C., Gasiewicz, T. A., and DeRosa, C. T. (2000) ATSDR Evaluation of Health Effects of Chemicals. VII: Chlorinated Dibenzo- p -dioxins Toxicol. Ind. Health 16, 85-201
28. Mandal, P. K. (2005) Dioxin: A review of its environmental effects and its aryl hydrocarbon receptor biology J. Comp. Physiol., B 175, 221-230 (Pubitemid 40764087)
29. Matsumura, F. (2009) The significance of the nongenomic pathway in mediating inflammatory signaling of the dioxin-activated Ah receptor to cause toxic effects Biochem. Pharmacol. 77, 608-626
30. Reichard, J. F., Dalton, T. P., Shertzer, H. G., and Puga, A. (2005) Induction of Oxidative Stress Responses by Dioxin and other Ligands of the Aryl Hydrocarbon Receptor Dose Response 3, 306-331
31. Shertzer, H. G. (2010) Protective effects of the antioxidant 4b,5,9b,10-tetrahydroindeno[1,2-b]indole against TCDD toxicity in C57BL/6J mice Int. J. Toxicol. 29, 40-48
32. Ishida, T., Takeda, T., Koga, T., Yahata, M., Ike, A., Kuramoto, C., Taketoh, J., Hashiguchi, I., Akamine, A., Ishii, Y., and Yamada, H. (2009) Attenuation of 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity by resveratrol: a comparative study with different routes of administration Biol. Pharm. Bull. 32, 876-881
33. Kawada, T., Goto, T., Hirai, S., Kang, M. S., Uemura, T., Yu, R., and Takahashi, N. (2008) Dietary regulation of nuclear receptors in obesity-related metabolic syndrome Asia Pac. J. Clin. Nutr. 17 (Suppl. 1) 126-130
34. Sugden, M. C., Caton, P. W., and Holness, M. J. (2010) PPAR control: It's SIRTainly as easy as PGC J. Endocrinol. 204, 93-104
35. Konig, B., Koch, A., Spielmann, J., Hilgenfeld, C., Hirche, F., Stangl, G. I., and Eder, K. (2009) Activation of PPARa and PPARg reduces triacylglycerol synthesis in rat hepatoma cells by reduction of nuclear SREBP-1 Eur. J. Pharmacol. 605, 23-30
36. De Souza, A. T., Dai, X., Spencer, A. G., Reppen, T., Menzie, A., Roesch, P. L., He, Y., Caguyong, M. J., Bloomer, S., Herweijer, H., Wolff, J. A., Hagstrom, J. E., Lewis, D. L., Linsley, P. S., and Ulrich, R. G. (2006) Transcriptional and phenotypic comparisons of Ppara knockout and siRNA knockdown mice Nucleic Acids Res. 34, 4486-4494 (Pubitemid 44567048)
37. Yasui, K., Harano, Y., Mitsuyoshi, H., Tsuji, K., Endo, M., Nakajima, T., Minami, M., Itoh, Y., Zen, Y., Nakanuma, Y., Yoshikawa, T., and Okanoue, T. (2010) Steatosis and hepatic expression of genes regulating lipid metabolism in Japanese patients infected with hepatitis C virus J. Gastroenterol. 45, 95-104
38. Bettzieche, A., Brandsch, C., Hirche, F., Eder, K., and Stangl, G. I. (2008) L-cysteine down-regulates SREBP-1c-regulated lipogenic enzymes expression via glutathione in HepG2 cells Ann. Nutr. Metab. 52, 196-203 (Pubitemid 351990889)
39. Lin, C. C. and Yin, M. C. (2008) Effects of cysteine-containing compounds on biosynthesis of triacylglycerol and cholesterol and anti-oxidative protection in liver from mice consuming a high-fat diet Br. J. Nutr. 99, 37-43
40. Diniz, Y. S., Rocha, K. K., Souza, G. A., Galhardi, C. M., Ebaid, G. M., Rodrigues, H. G., Novelli Filho, J. L., Cicogna, A. C., and Novelli, E. L. (2006) Effects of N-acetylcysteine on sucrose-rich diet-induced hyperglycaemia, dyslipidemia and oxidative stress in rats Eur. J. Pharmacol. 543, 151-157 (Pubitemid 44092691)
41. Chen, Y., Johansson, E., Yang, Y., Miller, M. L., Shen, D., Orlicky, D. J., Shertzer, H. G., Vasiliou, V., Nebert, D. W., and Dalton, T. P. (2010) Oral N-acetylcysteine rescues lethality of hepatocyte-specific Gclc-knockout mice, providing a model for hepatic cirrhosis J. Hepatol. 53, 1085-1094
42. Garcia, M. C., Amankwa-Sakyi, M., and Flynn, T. J. (2011) Cellular glutathione in fatty liver in vitro models Toxicol. in Vitro 25, 1501-1506
43. Samuhasaneeto, S., Thong-Ngam, D., Kulaputana, O., Patumraj, S., and Klaikeaw, N. (2007) Effects of N-acetylcysteine on oxidative stress in rats with non-alcoholic steatohepatitis J. Med. Assoc. Thai. 90, 788-797
44. Pan, S. Y., Dong, H., Guo, B. F., Zhang, Y., Yu, Z. L., Fong, W. F., Han, Y. F., and Ko, K. M. (2011) Effective kinetics of schisandrin B on serum/hepatic triglyceride and total cholesterol levels in mice with and without the influence of fenofibrate Naunyn-Schmiedeberg's Arch. Pharmacol. 383, 585-591
45. Leong, P. K., Chiu, P. Y., Chen, N., Leung, H., and Ko, K. M. (2011) Schisandrin B elicits a glutathione antioxidant response and protects against apoptosis via the redox-sensitive ERK/Nrf2 pathway in AML12 hepatocytes Free Radical Res. 45, 483-495
46. Lu, H., Cui, W., and Klaassen, C. D. (2011) Nrf2 protects against 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-induced oxidative injury and steatohepatitis Toxicol. Appl. Pharmacol. 256, 122-135
47. Lee, J. H., Wada, T., Febbraio, M., He, J., Matsubara, T., Lee, M. J., Gonzalez, F. J., and Xie, W. (2010) A novel role for the dioxin receptor in fatty acid metabolism and hepatic steatosis Gastroenterology 139, 653-663