Activation of Hepatic Nrf2 in Vivo by Acetaminophen in CD-1 Mice

Hepatology

Volumn 39, Issue 5, 2004, Pages 1267-1276

  Goldring, Christopher E P ^a   Kitteringham, Neil R ^a   Elsby, Robert ^a   Randle, Laura E ^a   Clement, Yuri N ^a,b   Williams, Dominic P ^a   McMahon, Michael ^c   Hayes, John D ^c   Itoh, Ken ^d   Yamamoto, Masayuki ^d   Park, B Kevin ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF THE WEST INDIES   (Trinidad and Tobago)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BUTHIONINE SULFOXIMINE; CD1 ANTIGEN; EPOXIDE HYDROLASE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; HEME OXYGENASE 1; MALEIC ACID DIETHYL ESTER; PARACETAMOL; PROTEIN; TRANSCRIPTION FACTOR NF E2; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHEMICAL MODIFICATION; CONTROLLED STUDY; DETOXIFICATION; DRUG ACTIVATION; ENZYME ACTIVATION; ENZYME INDUCTION; GENE DELETION; GENE EXPRESSION; IN VIVO STUDY; LIVER INJURY; LIVER PARENCHYMA; MALE; MOLECULAR INTERACTION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL;

ACETAMINOPHEN; ANALGESICS, NON-NARCOTIC; ANIMALS; BLOTTING, NORTHERN; CELL NUCLEUS; DNA-BINDING PROTEINS; GENE EXPRESSION; GLUTATHIONE; LIVER; MALE; MALEATES; MICE; MICE, INBRED STRAINS; NF-E2-RELATED FACTOR 2; TRANS-ACTIVATORS;

EID: 2342613543     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1002/hep.20183     Document Type: Article

References (50)

1. Prestera T, Zhang Y, Spencer SR, Wilczak CA, Talalay P. The electrophile counterattack response: protection against neoplasia and toxicity. Adv Enzyme Regul 1993;33:281-296.
2. Hayes JD, McMahon M. Molecular basis for the contribution of the antioxidant responsive element to cancer chemoprevention. Cancer Lett 2001;174:103-113.
3. Friling RS, Bergelson S, Daniel V. Two adjacent AP-1 like binding sites form the electrophile-responsive element of the murine glutathione S-transferase Ya subunit gene. Proc Natl Acad Sci USA 1992;89:668-672.
4. Jaiswal AK. Antioxidant response element. Biochem Pharmacol 1994;48:439-444.
5. Rushmore TH, Pickett CB. Transcriptional regulation of the rat glurathione S-transferase Ya subunit gene. Characterization of a xenobiotic-responsive element controlling inducible expression by phenolic antioxidants. J Biol Chem 1990;265:14648-14648.
6. Rushmore TH, Morton MR, Pickett CB. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem 1991;266:11632-11639.
7. Andrews NC, Erdjument-Bromage H, Davidson MB, Tempst P, Orkin SH. Erythroid transcription factor NF-E2 is a haematopoietic-specific sic-leucine zipper protein. Nature 1993;362:722-728.
8. Venugopal R, Jaiswal AK. Nrfl and Nrf2 positively and c-Fos and Fral negatively regulate the human antioxidant response element-mediated expression of NAD(P)H: quinone oxidoreductasel gene. Proc Nad Acad Sci USA 1996;93:14960-14965.
9. Wild AC, Moinova HR, Mulcahy RT. Regulation ofgamma-glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2. J Biol Chem 1999;274:33627-33636.
10. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, Cook JL. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 1999;274:26071-26078.
11. Jeyapaul J, Jaiswal AK. Nrf2 and c-Jun regulation of antioxidant response element (ARE)-mediated expression and induction of gamma-glutamylcysteine synthetase heavy subunit gene. Biochem Pharmacol 2000;59:1433-1439.
12. Chanas SA, Jiang O, McMahon M, McWalter GK, McLellan LI, Elcombe CR, et al. Loss of the Nrf2 transcription factor causes a marked reduction in constitutive and inducible expression of the glutathione S-transferase Gstal, Gsta2, Gstml, Gstm2, Gstm3 and Gstm4 genes in the livers of male and female mice. Biochem J 2002;365:405-416.
13. Chan K, Kan YW. Nrf2 is essential for protection against acute pulmonary injury in mice. Proc Nad Acad Sci USA 1999;96:12731-12736.
14. Enomoto A, Itoh K, Nagayoshi E, Haruta J, Kimura T, O'Connor T, et al. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol Sci 2001;59:169-177.
15. McMahon M, Itoh K, Yamamoto M, Chanas SA, Henderson CJ, McLellan LI, et al. The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Res 2001;61:3299-3307.
16. Kong AN, Owuor E, Yu R, Hebbar V, Chen C, Hu R, et al. Induction of xenobiotic enzymes by the map kinase pathway and the antioxidant or electrophile response element (ARE/EpRE). Drug Metab Rev 2001;33:255-271.
17. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, et al. Keapl represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 1999;13:76-86.
18. Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, Takahashi S, et al. Keap 1 -null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet 2003;35:238-245.
19. Itoh K, Wakabayashi N, Katoh Y, Ishii T, O'Connor T, Yamamoto M. Keapl regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 2003;8:379-391.
20. Nguyen T, Sherratt PJ, Huang HC, Yang CS, Pickett CB. Increased protein stability as a mechanism that enhances Nrf2 -mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. J Biol Chem 2003;278:4536-4541.
21. McMahon M, Itoh K, Yamamoto M, Hayes JD. Keapl-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J Biol Chem 2003;278:21592-21600.
22. Dinkova-Kostova AT, Massiah MA, Bozak RE, Hicks RJ, Talalay P. Potency of Michael reaction acceptors as inducers of enzymes that protect against carcinogenesis depends on their reactivity with sulfhydryl groups. Proc Natl Acad Sci USA 2001;98:3404-3409.
23. Osrapowicz G, Fontana RJ, Schiodr FV, Larson A, Davern TJ, Han SH, et al. Results of a prospective study of acute liver failure at 17 tertiary care centers in the United States. Ann Intern Med 2002;137:947-954.
24. Fagan E, Wannan G. Reducing paracetamol overdoses. Br Med J 1996;313:1417-1418.
25. Pierce RH, Franklin CC, Campbell JS, Tonge RP, Chen W, Fausto N, et al. Cell culture model for acetaminophen-induced hepatocyte death in vivo. Biochem Pharmacol 2002;64:413-424.
26. Lee SS, Buters JT, Pineau T, Femandez-Salguero P, Gonzalez FJ. Role of CYP2E1 in the hepatotoxicity of acetaminophen. J Biol Chem 1996;271:12063-12067.
27. Zaher H, Buters JT, Ward JM, Bruno MK, Lucas AM, Stern ST, et al. Protection against acetaminophen toxicity in CYP1A2 and CYP2E1 double-null mice. Toxicol Appl Pharmacol 1998;152:193-199.
28. Potter WZ, Thorgeirsson SS, Jollow DJ, Mitchell JR. Acetaminophen-induced hepatic necrosis. V. Correlation of hepatic necrosis, covalent binding and glurathione depletion in hamsters. Pharmacology 1974;12:129-143.
29. Muldrew KL, James LP, Coop L, McCullough SS, Hendrickson HP, Hinson JA, et al. Determination of aceraminophen-protein adducts in mouse liver and serum and human serum after hepatotoxic doses of acetaminophen using high-performance liquid chromatography with electro-chemical detection. Drug Metab Dispos 2002;30:446-451.
30. Harman AW. The effectiveness of antioxidants in reducing paracetamol-induced damage subsequent to paraceramol activation. Res Commun Chem Pathol Pharmacol 1985;49:215-228.
31. Cohen SD, Hoivik DJ, Khairallah EA. In: Plaa GL, Hewitt WR, eds. Toxicology of the Liver. Vol. 1. 2nd ed. Washington D.C.: Taylor & Francis; 1998;159-186.
32. Jaeschke H, Knight TR, Bajt ML. The role of oxidant stress and reactive nitrogen species in acetaminophen hepatotoxicity. Toxicol Lett 2003;144:279-288.
33. Chan K, Han XD, Kan YW. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc Natl Acad Sci USA 2001;98:4611-4616.
34. Kitteringham NR, Powell H, Clement YN, Dodd CC, Tettey JN, Pirmohamed M, et al. Hepatocellular response to chemical stress in CD-1 mice: induction of early genes and gamma-glutamylcysteine synthetase. HEPATOLOGY 2000;32:321-333.
35. Vandeputte C, Guizon I, Genestie-Denis I, Vannier B, Lorenzon G. A microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells: performance study of a new miniaturized protocol. Cell Biol Toxicol 1994;10:415-421.
36. Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nucli. Nuclic Acids Res 1983;11:1475-1489.
37. Israel N, Gougerot-Pocidalo MA, Aillet F, Virelizier JL. Redox status of cells influences constitutive or induced NF-kappa B translocation and HIV long terminal repeat activity in human T and monocytic cell lines. J Immunol 1992;149:3386-3393.
38. Nguyen T, Sherratt PJ, Pickett CB. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol 2003;43:233-260.
39. Liu RM, Hu H, Robison TW, Forman HJ. Differential enhancement of gamma-glutamyl transpeptidase and gamma-glutamylcysteine syntherase by tert-butylhydroquinone in rat lung epithelial L2 cells. Am J Respir Cell Mol Biol 1996;14:186-191.
40. Hayes JD, Chanas SA, Henderson CJ, McMahon M, Sun C, Moffat GJ, et al. The Nrf2 transcription factor contributes both to the basal expression of glutathione S-transferases in mouse liver and to their induction by the chemopreventive synthetic antioxidants, butylated hydroxyanisole and ethoxyquin. Biochem Soc Trans 2000;28:33-41.
41. Sekhar KR, Long M, Long J, Xu ZQ, Summar ML, Freeman ML. Alteration of transcriptional and post-transcriptional transcripdonal expression of gamma-gluramylcysteine synthetase by diethyl maleate. Radiat Res 1997;147:592-597.
42. Kwak MK, Itoh K, Yamamoto M, Sutter TR, Kensler TW. Role of transcription factor Nrf2 in the induction ofhepatic phase 2 and antioxidative enzymes in vivo by the cancer chemoprotective agent, 3H-1, 2-dimethiole-3-thione. Mol Med 2001;7:135-145.
43. Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yamamoto M, Talalay P, et al. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci USA 2001;98:3410-3415.
44. Mitchell JR, Jollow DJ, Potter WZ, Gillette JR, Brodie BB. Acetaminophen-induced hepatic nectosis. IV. Protective role of glurathione. J Pharmacol Exp Ther 1973;187:211-217.
45. Qiu Y, Benet LZ, Burlingame AL. Identification of the hepatic protein targets of reactive merabolites of acetaminophen in vivo in mice using two-dimensional gel electrophoresis and mass spectrometry. J Biol Chem 1998;273:17940-17953.
46. Dinkova-Kostova AT, Holtzdaw WD, Cole RN, Itoh K, Wakabayashi N, WakabayashiN, Katoh Y, et al. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Nad Acad Sci USA 2002;99:11908-11913.
47. Sekhar KR, Crooks PA, Sonar VN, Friedman DB, Chan JY, Meredith MJ, et al. NADPH Oxidase Activity Is Essendal for Keap1/Nrf2 Induction of GCLC in Response to 2-Indol-3-yl- methylenequinuclidin 3-ols. Cancer Res 2003;63:5636-5645.
48. Shibata T, Kondo M, Osawa T, Shibara N, Kobayashi M, Uchida K. 15-deoxy-delta 12,14-prostaglandin J2. A prostaglandin D2 metabolite generated during inflammatory processes. J Biol Chem 2002;277:10459-10466.
49. Shibata T, Yamada T, Ishii T, Kumazawa S, Nakamura H, Masutani H, et al. Thioredoxin as a molecular target of cyclopentenone Prostaglandins. J Biol Chem 2003;278:26046-26054.
50. Levonen AL, Landar A, Ramachandran A, Ceaser EK, Dickinson DA, Zanoni G, et al. Cellular mechanisms of redox cell signaling: role of cysteine modification in controlling andoxidant defenses in response to electrophilic lipid oxidation products. Biochem J 2004;378:373-382.