Increased susceptibility of Nrf2-Null Mice to 1-bromopropane-induced hepatotoxicity

Toxicological Sciences

Volumn 115, Issue 2, 2010, Pages 596-606

  Liu, Fang ^a   Ichihara, Sahoko ^b   Valentine, William M ^c   Itoh, Ken ^d   Yamamoto, Masayuki ^e   Mohideen, Sahabudeen Sheik ^a   Kitohk, Junzoh ^f   Ichihara, Gaku ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b MIE UNIVERSITY   (Japan)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d HIROSAKI UNIVERSITY   (Japan)

^e TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f NAGOYA UNIVERSITY   (Japan)

Author keywords

1 bromopropane; Hepatotoxicity.; Nuclear factor erythroid 2 related factor 2; Oxidative stress

Indexed keywords

1 BROMOPROPANE; ALANINE AMINOTRANSFERASE; GLUTAMATE CYSTEINE LIGASE; GLUTAMATE SYNTHASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; HEME OXYGENASE 1; MALONALDEHYDE; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SOLVENT; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENZYME ACTIVITY; ENZYME ASSAY; GENOTYPE; HISTOPATHOLOGY; LIVER NECROSIS; LIVER TOXICITY; LIVER WEIGHT; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION;

ADMINISTRATION, INHALATION; ANIMALS; DRUG-INDUCED LIVER INJURY; ENZYMES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENETIC PREDISPOSITION TO DISEASE; HYDROCARBONS, BROMINATED; INHALATION EXPOSURE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; SOLVENTS;

MUS; RODENTIA;

EID: 77954067512     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq075     Document Type: Article

References (52)

1. Alam, J., Stewart, D., Touchard, C., Boinapally, S., Choi, A. M. K., and Cook, J. L. (1999). Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 274, 26071-26078.
2. Aoki, Y., Sato, H., Nishimura, N., Takahashi, S., Itoh, K., and Yamamoto, M. (2001). Accelerated DNA adduct formation in the lung of the Nrf2 knockout mouse exposed to diesel exhaust. Toxicol. Appl. Pharmacol. 173, 154-160.
3. Banu, S., Ichihara, S., Huang, F., Ito, H., Inaguma, Y., Furuhashi, K., Fukunaga, Y., Wang, Q. Y., Kitoh, J., Ando, H., et al. (2007). Reversibility of the adverse effects of 1-bromopropane exposure in rats. Toxicol. Sci. 100, 504-512.
4. Barnsley, E. A., Grenby, T. H., and Young, L. (1966). Biochemical studies of toxic agents, the metabolism of 1and 2-bromopropane in rats. Biochem. J. 100, 282-288.
5. B'Hymer, C., and Cheever, K. L. (2004). Development of a gas chromatographic test for the quantification of the biomarker 3-bromopropionic acid in human urine. J. Chromatogr. B 802, 361-366.
6. Carlberg, I., and Mannervik, B. (1985). Glutathione reductase. Methods Enzymol. 113, 484-490.
7. Chan, K., and Kan, Y. W. (1999). Nrf2 is essential for protection against acute pulmonary injury in mice. Proc. Natl. Acad. Sci. USA. 96, 12731-12736.
8. Dinkova-Kostova, A. T., Holtzclaw, W. D., Cole, R. N., Itoh, K., Wakabayashi, N., Katoh, Y., Yamamoto, M., and Talalay, P. (2002). Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc. Natl. Acad. Sci. U.S.A. 99, 11908-11913.
9. Enomoto, A., Itoh, K., Nagayoshi, E., Haruta, J., Kimura, T., O'Connor, T., Harada, T., and Yamamoto, M. (2001). High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol. Sci. 59, 169-177.
10. EPA. (1999). Protection of stratospheric ozone: listing of substitutes for ozone depleting substances. Request for data and advanced notice of proposed rulemaking. 40 CFR Part 82. Fed. Regist. 64, 8043-8048.
11. EPA. (2000). Protection of stratospheric ozone: notice 14 for significant new alternatives policy program. 40 CFR Part 82. Fed. Regist. 65, 78977-78989.
12. Gao, X., and Talalay, P. (2004). Induction of phase 2 genes by sulforaphane protects retinal pigment epithelial cells against photooxidative damage. Proc. Natl. Acad. Sci. USA. 101, 10446-10451.
13. Goldring, C. E., Kitteringham, N. R., Elsby, R., Randle, L. E., Clement, Y. N., Williams, D. P., McMahon, M., Hayes, J. D., Itoh, K., Yamamoto, M., et al. (2004). Activation of hepatic Nrf2 in vivo by acetaminophen in CD-1 mice. Hepatology 39, 1267-1276.
14. Griffith, O. W. (1980). Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 106, 207-212.
15. Habig, W. H., Pabst, M. J., and Jacoby, W. B. (1974). Glutathione-S-transferase: the first step in mercapturic acid formation. J. Biol. Chem. 249, 1730-1739.
16. Hong, F., Sekhar, K. R., Freeman, M. L., and Liebler, D. C. (2005). Specific patterns of electrophile adduction trigger Keap1 ubiquitination and Nrf2 activation. J. Biol. Chem. 280, 31768-31775.
17. Ichihara, G., Asaeda, N., Kumazawa, T., Tagawa, Y., Kamijima, M., Yu, X., Kondo, H., Nakajima, T., Kitoh, J., Yu, I. J., et al. (1997). Testicular and hematopoietic toxicity of 2-bromopropane, a substitute for ozone layerdepleting chlorofluorocarbons. J. Occup. Health 39, 57-63.
18. Ichihara, G., Kitoh, J., Yu, X., Asaeda, N., Iwai, H., Kumazawa, T., Shibata, E., Yamada, T., Wang, H., Xie, Z., et al. (2000a). 1-Bromopropane, an alternative to ozone layer depleting solvents, is dose-dependently neurotoxic to rats in long-term inhalation exposure. Toxicol. Sci. 55, 116-123.
19. Ichihara, G., Miller, J. K., Ziolkokwska, A., Itohara, S., and Takeuchi, Y. (2002). Neurological disorders in three workers exposed to 1-bromopropane. J. Occup. Health 44, 1-7.
20. Ichihara, G., Yu, X., Kitoh, J., Asaeda, N., Kumazawa, T., Iwai, H., Shibata, E., Yamada, T., Wang, H., Xie, Z., et al. (2000b). Reproductive toxicity of 1-bromopropane, a newly introduced alternative to ozone layer depleting solvents, in male rats. Toxicol. Sci. 54, 416-423.
21. Ishii, T., Itoh, K., Takahashi, S., Sato, H., Yanagawa, T., Katoh, Y., Bannai, S., and Yamamoto, M. (2000). Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J. Biol. Chem. 275, 16023-16029.
22. Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., Oyake, T., Hayashi, N., Satoh, K., Hatayama, I., et al. (1997). An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236, 313-322.
23. Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., Igarashi, K., Engel, J. D., and Yamamoto, M. (1999). Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13, 76-86.
24. Janero, D. R. (1990). Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic. Biol. Med. 9, 515-540.
25. Jones, A. R., and Walsh, D. A. (1979). The oxidative metabolism of 1-bromopropane in the rat. Xenobiotica 9, 763-772.
26. Khan, S., and O'Brien, P. J. (1991). 1-Bromoalkanes as new potent nontoxic glutathione depletors in isolated rat hepatocytes. Biochem. Biophys. Res. Commun. 179, 436-441.
27. Kim, Y. C., Masutani, H., Yamaguchi, Y., Itoh, K., Yamamoto, M., and Yodoi, J. (2001). Hemin-induced activation of the thioredoxin gene by Nrf2. A differential regulation of the antioxidant responsive element by a switch of its binding factors. J. Biol. Chem. 276, 18399-18406.
28. Kobayashi, A., Kang, M. I., Okawa, H., Ohtsuji, M., Zenke, Y., Chiba, T., Igarashi, K., and Yamamoto, M. (2004). Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 24, 7130-7139.
29. Lamlé, J., Marhenke, S., Borlak, J., von Wasielewski, R., Eriksson, C. J., Geffers, R., Manns, M. P., Yamamoto, M., and Vogel, A. (2008). Nuclear factor-eythroid 2-related factor 2 prevents alcohol-induced fulminant liver injury. Gastroenterology 134, 1159-1168.
30. Lee, S. K., Jeon, T. W., Kim, Y. B., Lee, E. S., Jeong, H. G., and Jeong, T. C. (2007). Role of glutathione conjugation in the hepatotoxicity and immunotoxicity induced by 1-bromopropane in female BALB/C mice. J. Appl. Toxicol. 27, 358-367.
31. Lee, S. K., Jo, S. W., Jeon, T. W., Jun, I. H., Jin, C. H., Kim, G. H., Lee, D. J., Kim, T. O., Lee, E. S., and Jeong, T. C. (2005). Hepatotoxic effect of 1-bromopropane and its conjugation with glutathione in male ICR mice. Arch. Pharm. Res. 28, 1177-1182.
32. Liu, F., Ichihara, S., Mohideen, S. S., Sai, U., Kitoh, J., and Ichihara, G. (2009). Comparative study on susceptibility to 1-bromopropane in three mice strains. Toxicol. Sci. 112, 100-110.
33. Maher, J. M., Dieter, M. Z., Aleksunes, L. M., Slitt, A. L., Guo, G., Tanaka, Y., Scheffer, G. L., Chan, J. Y., Manautou, J. E., Chen, Y., et al. (2007). Oxidative and electrophilic stress induces multidrug resistance-associated protein transporters via the nuclear factor-E2-related factor-2 transcriptional pathway. Hepatology 46, 1597-1610.
34. Majersik, J. J., Caravati, E. M., and Steffens, J. D. (2007). Severe neurotoxicity associated with exposure to the solvent 1-bromopropane (n-propyl bromide). Clin. Toxicol. 45, 270-276.
35. McWalter, G. K., Higgins, L. G., McLellan, L. I., Henderson, C. J., Song, L., Thornalley, P. J., Itoh, K., Yamamoto, M., and Hayes, J. D. (2004). Transcription factor Nrf2 is essential for induction of NAD(P)H:quinone oxidoreductase 1, glutathione S-transferases, and glutamate cysteine ligase by broccoli seeds and isothiocyanates. J. Nutr. 134, 3499S-3506S.
36. Mohideen, S. S., Ichihara, S., Banu, S., Liu, F., Kitoh, J., and Ichihara, G. (2009). Changes in neurotransmitter receptor expression levels in rat brain after 4-week exposure to 1-bromopropane. Neurotoxicology 30, 1078-1083.
37. Moi, P., Chan, K., Asunis, I., Cao, A., and Kan, Y. W. (1994). Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc. Natl. Acad. Sci. U.S.A. 91, 9926-9930.
38. National Center for Biotechnology Information (NCBI). (2009). U.S. National Library of Medicine, Bethesda MD. Available at: http://www.ncbi.nlm.nih .gov/guide/.
39. Norris, M. D., Burkhart, C. A., Marshall, G. M., Weiss, W. A., and Haber, M. (2000). Expression of N-myc and MRP genes and their relationship to N-myc gene dosage and tumor formation in a murine neuroblastoma model. Med. Pediatr. Oncol. 35, 585-589.
40. Paglia, D. E., and Valentine, W. N. (1967). Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 70, 158-169.
41. Ramos-Gomez, M., Dolan, P. M., Itoh, K., Yamamoto, M., and Kensler, T. W. (2003). Interactive effects of nrf2 genotype and oltipraz on benzo[a]pyrene-DNA adducts and tumor yield in mice. Carcinogenesis 24, 461-467.
42. Reisman, S. A., Csanaky, I. L., Yeager, R. L., and Klaassen, C. D. (2009). Nrf2 activation enhances biliary excretion of sulfobromophthalein by inducing glutathione-S-transferase activity. Toxicol. Sci. 109, 24-30.
43. Sclar, G. (1999). Encephalomyeloradiculoneuropathy following exposure to an industrial solvent. Clin. Neurol. Neurosurg. 101, 199-202.
44. Takeuchi, Y., Huang, J., Shibata, E., Hisanaga, N., and Ono, Y. (1989). A trial to automatize an organic solvent exposure system for small animals. Jpn. J. Ind. Health 31, 722.
45. Tanaka, Y., Aleksunes, L. M., Yeager, R. L., Gyamfi, M. A., Esterly, N., Guo, G. L., and Klaassen, C. D. (2008). NF-E2-related factor 2 inhibits lipid accumulation and oxidative stress in mice fed a high-fat diet. J. Pharmacol. Exp. Ther. 325, 655-664.
46. Umemura,T.,Kuroiwa,Y.,Kitamura,Y.,Ishii,Y.,Kanki,K.,Kodama,Y., Itoh,K.,Yamamoto,M.,Nishikawa,A.,andHirose,M.(2006).Acrucial role of Nrf2 in in vivo defense against oxidative damage by an environmental pollutant, pentachlorophenol. Toxicol. Sci. 90, 111-119.
47. Valentine, H., Amarnath, K., Amarnath, V., Li, W., Ding, X., Valentine, W. M., and Ichihara, G. (2007). Globin s-propyl cysteine and urinary N-acetyl-S-propylcysteine as internal biomarkers of 1-bromopropane exposure. Toxicol. Sci. 98, 427-435.
48. Venugopal, R., and Jaiswal, A. K. (1996). Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc. Natl. Acad. Sci. USA. 93, 14960-14965.
49. Walsh, A. C. (2003). Regulation of nrf2-mediated induction of glutamate cysteine ligase modulatory gene (GCLM) expression: considerations for future studies. Toxicol. Sci. 73, 1-3.
50. Wang, H., Ichihara, G., Ito, H., Kato, K., Kitoh, J., Yamada, T., Yu, X., Tsuboi, S., Moriyama, Y., Sakatani, R., et al. (2002). Biochemical changes in the central nervous system of rats exposed to 1-bromopropane for seven days. Toxicol. Sci. 67, 114-120.
51. Wang, H., Ichihara, G., Ito, H., Kato, K., Kitoh, J., Yamada, T., Yu, X., Tsuboi, S., Moriyama, Y., and Takeuchi, Y. (2003). Dose-dependent biochemical changes in rat central nervous system after 12-week exposure to bromopropane. Neurotoxicology 24, 199-206.
52. Yamada, T., Ichihara, G., Wang, H., Yu, X., Maeda, K., Tsukamura, H., Kamijima, M., Nakajima, T., and Takeuchi, Y. (2003). Exposure to 1-bromopropane causes ovarian dysfunction in rats. Toxicol. Sci. 71, 96-103.