γ-Glutamyl transpeptidase is induced by 4-hydroxynonenal via EpRE/Nrf2 signaling in rat epithelial type II cells

Free Radical Biology and Medicine

Volumn 40, Issue 8, 2006, Pages 1281-1292

  Zhang, Hongqiao ^a   Liu, Honglei ^b   Dickinson, Dale A ^a   Liu, Rui Ming ^a   Postlethwait, Edward M ^a   Laperche, Yannick ^c   Forman, Henry Jay ^b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HENRI MONDOR HOSPITAL   (France)

Author keywords

Glutamyl transpeptidase; 4 Hydroxy 2 nonenal; EpRE; Free radicals; Glutathione; Nrf2; Tissue distribution

Indexed keywords

4 HYDROXYNONENAL; FREE RADICAL; GAMMA GLUTAMYLTRANSFERASE; GLUTATHIONE; MESSENGER RNA; TRANSCRIPTION FACTOR NRF2; 4-HYDROXY-2-NONENAL; ALDEHYDE; NFE2L2 PROTEIN, RAT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASSAY; BINDING AFFINITY; CHROMATIN; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ELECTROPHILE RESPONSE ELEMENT; EPITHELIUM CELL; GENE DELETION; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT; REPORTER GENE; SIGNAL TRANSDUCTION; STATISTICAL SIGNIFICANCE; TISSUE DISTRIBUTION; ACTIVE TRANSPORT; ANIMAL; CELL LINE; DRUG EFFECT; GENE EXPRESSION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE;

ACTIVE TRANSPORT, CELL NUCLEUS; ALDEHYDES; ANIMALS; BASE SEQUENCE; CELL LINE; EPITHELIAL CELLS; GAMMA-GLUTAMYLTRANSFERASE; GENE EXPRESSION; MOLECULAR SEQUENCE DATA; MUTATION; NF-E2-RELATED FACTOR 2; PROMOTER REGIONS (GENETICS); RATS; RESPONSE ELEMENTS; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 33744970045     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2005.11.005     Document Type: Article

References (88)

1. Hanigan M.H., and Ricketts W.A. Extracellular glutathione is a source of cysteine for cells that express γ-glutamyl transpeptidase. Biochemistry 32 (1993) 6302-6306
2. Griffith O.W., and Meister A. Excretion of cysteine and γ-glutamylcysteine moieties in human and experimental animal γ-glutamyl transpeptidase deficiency. Proc. Natl. Acad. Sci. USA 77 (1980) 3384-3387
3. Lieberman M.W., Wiseman A.L., Shi Z.Z., Carter B.Z., Barrios R., Ou C.N., Chevez-Barrios P., Wang Y., Habib G.M., Goodman J.C., Huang S.L., Lebovitz R.M., and Matzuk M.M. Growth retardation and cysteine deficiency in γ-glutamyl transpeptidase-deficient mice. Proc. Natl. Acad. Sci. USA 93 (1996) 7923-7926
4. Rojas E., Valverde M., Kala S.V., Kala G., and Lieberman M.W. Accumulation of DNA damage in the organs of mice deficient in γ-glutamyltranspeptidase. Mutat. Res. 447 (2000) 305-316
5. Barrios R., Shi Z.Z., Kala S.V., Wiseman A.L., Welty S.E., Kala G., Bahler A.A., Ou C.N., and Lieberman M.W. Oxygen-induced pulmonary injury in γ-glutamyl transpeptidase-deficient mice. Lung 179 (2001) 319-330
6. Meister A. The γ-glutamyl cycle. Diseases associated with specific enzyme deficiencies. Ann. Intern. Med. 81 (1974) 247-253
7. Stark A.A., Porat N., Volohonsky G., Komlosh A., Bluvshtein E., Tubi C., and Steinberg P. The role of γ-glutamyl transpeptidase in the biosynthesis of glutathione. Biofactors 17 (2003) 139-149
8. Paolicchi A., Sotiropuolou M., Perego P., Daubeuf S., Visvikis A., Lorenzini E., Franzini M., Romiti N., Chieli E., Leone R., Apostoli P., Colangelo D., Zunino F., and Pompella A. γ-Glutamyl transpeptidase catalyses the extracellular detoxification of cisplatin in a human cell line derived from the proximal convoluted tubule of the kidney. Eur. J. Cancer 39 (2003) 996-1003
9. Griffiths S.A., Good V.M., Gordon L.A., Hudson E.A., Barrett M.C., Munks R.J., and Manson M.M. Characterization of a promoter for γ-glutamyl transpeptidase activated in rat liver in response to aflatoxin B1 and ethoxyquin. Mol. Carcinog. 14 (1995) 251-262
10. Takahashi Y., Oakes S.M., Williams M.C., Takahashi S., Miura T., and Joyce-Brady M. Nitrogen dioxide exposure activates γ-glutamyl transferase gene expression in rat lung. Toxicol. Appl. Pharmacol. 143 (1997) 388-396
11. Kugelman A., Choy H.A., Liu R., Shi M.M., Gozal E., and Forman H.J. γ-Glutamyl transpeptidase is increased by oxidative stress in rat alveolar L2 epithelial cells. Am. J. Respir. Cell Mol. Biol. 11 (1994) 586-592
12. Liu R.M., Shi M.M., Giulivi C., and Forman H.J. Quinones increase γ-glutamyl transpeptidase expression by multiple mechanisms in rat lung epithelial cells. Am. J. Physiol. 274 (1998) L330-L336
13. Liu R.M., Hu H., Robison T.W., and Forman H.J. Differential enhancement of γ-glutamyl transpeptidase and γ-glutamylcysteine synthetase by tert-butylhydroquinone in rat lung epithelial L2 cells. Am. J. Respir. Cell Mol. Biol. 14 (1996) 186-191
14. Liu R.M., Hu H., Robison T.W., and Forman H.J. Increased γ-glutamylcysteine synthetase and γ-glutamyl transpeptidase activities enhance resistance of rat lung epithelial L2 cells to quinone toxicity. Am. J. Respir. Cell Mol. Biol. 14 (1996) 192-197
15. Knickelbein R.G., Ingbar D.H., Seres T., Snow K., Johnston Jr. R.B., Fayemi O., Gumkowski F., Jamieson J.D., and Warshaw J.B. Hyperoxia enhances expression of γ-glutamyl transpeptidase and increases protein S-glutathiolation in rat lung. Am. J. Physiol. 270 (1996) L115-L122
16. Pross M., Schulz H.U., Flechsig A., Manger T., Halangk W., Augustin W., Lippert H., and Reinheckel T. Oxidative stress in lung tissue induced by CO(2) pneumoperitoneum in the rat. Surg. Endosc. 14 (2000) 1180-1184
17. Ogihara T., Hirano K., Morinobu T., Kim H.S., Hiroi M., Ogihara H., and Tamai H. Raised concentrations of aldehyde lipid peroxidation products in premature infants with chronic lung disease. Arch. Dis. Child Fetal Neonatal Ed. 80 (1999) F21-F25
18. Hamilton Jr. R.F., Li L., Eschenbacher W.L., Szweda L., and Holian A. Potential involvement of 4-hydroxynonenal in the response of human lung cells to ozone. Am. J. Physiol. 274 (1998) L8-L16
19. Rahman I., van Schadewijk A.A., Crowther A.J., Hiemstra P.S., Stolk J., MacNee W., and DeBoer W.I. 4-Hydroxy-2-nonenal, a specific lipid peroxidation product, is elevated in lungs of patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 166 (2002) 490-495
20. Kirichenko A., Li L., Morandi M.T., and Holian A. 4-Hydroxy-2-nonenal-protein adducts and apoptosis in murine lung cells after acute ozone exposure. Toxicol. Appl. Pharmacol. 141 (1996) 416-424
21. Bouhafs R.K., Samuelson A., and Jarstrand C. Lipid peroxidation of lung surfactant due to reactive oxygen species released from phagocytes stimulated by bacteria from children with cystic fibrosis. Free Radic. Res. 37 (2003) 909-917
22. Aoshiba K., Koinuma M., Yokohori N., and Nagai A. Immunohistochemical evaluation of oxidative stress in murine lungs after cigarette smoke exposure. Inhal. Toxicol. 15 (2003) 1029-1038
23. Esterbauer H., Schaur R.J., and Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11 (1991) 81-128
24. Esterbauer H. Cytotoxicity and genotoxicity of lipid-oxidation products. Am. J. Clin. Nutr. 57 (1993) 779S-785S discussion 785S-786S
25. Zarkovic N. 4-Hydroxynonenal as a bioactive marker of pathophysiological processes. Mol. Aspects Med. 24 (2003) 281-291
26. Dianzani M.U. 4-Hydroxynonenal from pathology to physiology. Mol. Aspects Med. 24 (2003) 263-272
27. Chikhi N., Holic N., Guellaen G., and Laperche Y. γ-Glutamyl transpeptidase gene organization and expression: a comparative analysis in rat, mouse, pig and human species. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 122 (1999) 367-380
28. Markey C.M., Rudolph D.B., Labus J.C., and Hinton B.T. Oxidative stress differentially regulates the expression of γ-glutamyl transpeptidase mRNAs in the initial segment of the rat epididymis. J. Androl. 19 (1998) 92-99
29. Joyce-Brady M., Oakes S.M., Wuthrich D., and Laperche Y. Three alternative promoters of the rat γ-glutamyl transferase gene are active in developing lung and are differentially regulated by oxygen after birth. J. Clin. Invest. 97 (1996) 1774-1779
30. Nomura S., Lahuna O., Suzuki T., Brouillet A., Chobert M.N., and Laperche Y. A specific distal promoter controls γ-glutamyl transpeptidase gene expression in undifferentiated rat transformed liver cells. Biochem. J. 326 (1997) 311-320
31. Zhang H., Dickinson D.A., Liu R.M., and Forman H.J. 4-Hydroxynonenal increases γ-glutamyl transpeptidase gene expression through mitogen-activated protein kinase pathways. Free Radic. Biol. Med. 38 (2005) 463-471
32. Rushmore T.H., King R.G., Paulson K.E., and Pickett C.B. Regulation of glutathione S-transferase Ya subunit gene expression: identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds. Proc. Natl. Acad. Sci. USA 87 (1990) 3826-3830
33. Rushmore T.H., and Pickett C.B. Transcriptional regulation of the rat glutathione S-transferase Ya subunit gene. Characterization of a xenobiotic-responsive element controlling inducible expression by phenolic antioxidants. J. Biol. Chem. 265 (1990) 14648-14653
34. Favreau L.V., and Pickett C.B. The rat quinone reductase antioxidant response element. Identification of the nucleotide sequence required for basal and inducible activity and detection of antioxidant response element-binding proteins in hepatoma and non-hepatoma cell lines. J. Biol. Chem. 270 (1995) 24468-24474
35. Dickinson D.A., Iles K.E., Zhang H., Blank V., and Forman H.J. Curcumin alters EpRE and AP-1 binding complexes and elevates glutamate-cysteine ligase gene expression. FASEB J. 17 (2003) 473-475
36. Hayes J.D., and McMahon M. Molecular basis for the contribution of the antioxidant responsive element to cancer chemoprevention. Cancer Lett. 174 (2001) 103-113
37. Jaiswal A.K. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic. Biol. Med. 36 (2004) 1199-1207
38. Dickinson D.A., Iles K.E., Watanabe N., Iwamoto T., Zhang H., Krzywanski D.M., and Forman H.J. 4-Hydroxynonenal induces glutamate cysteine ligase through JNK in HBE1 cells. Free Radic. Biol. Med. 33 (2002) 974
39. Strohmaier H., Hinghofer-Szalkay H., and Schaur R.J. Detection of 4-hydroxynonenal (HNE) as a physiological component in human plasma. J. Lipid Mediat. Cell Signal. 11 (1995) 51-61
40. Schwarzer E., Muller O., Arese P., Siems W.G., and Grune T. Increased levels of 4-hydroxynonenal in human monocytes fed with malarial pigment hemozoin. A possible clue for hemozoin toxicity. FEBS Lett. 388 (1996) 119-122
41. Uchida K. 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog. Lipid Res. 42 (2003) 318-343
42. Zhang D.D., and Hannink M. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol. Cell. Biol. 23 (2003) 8137-8151
43. Zhang D.D., Lo S.C., Cross J.V., Templeton D.J., and Hannink M. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol. Cell. Biol. 24 (2004) 10941-10953
44. Kaestner K.H. The hepatocyte nuclear factor 3 (HNF3 or FOXA) family in metabolism. Trends Endocrinol. Metab. 11 (2000) 281-285
45. Gregori C., Kahn A., and Pichard A.L. Activity of the rat liver-specific aldolase B promoter is restrained by HNF3. Nucleic Acids Res. 22 (1994) 1242-1246
46. Cha J.Y., Kim H., Kim K.S., Hur M.W., and Ahn Y. Identification of transacting factors responsible for the tissue-specific expression of human glucose transporter type 2 isoform gene. Cooperative role of hepatocyte nuclear factors 1alpha and 3beta. J. Biol. Chem. 275 (2000) 18358-18365
47. Sawaya P.L., Stripp B.R., Whitsett J.A., and Luse D.S. The lung-specific CC10 gene is regulated by transcription factors from the AP-1, octamer, and hepatocyte nuclear factor 3 families. Mol. Cell. Biol. 13 (1993) 3860-3871
48. Zaret K. Developmental competence of the gut endoderm: genetic potentiation by GATA and HNF3/fork head proteins. Dev. Biol. 209 (1999) 1-10
49. Mulcahy R.T., and Gipp J.J. Identification of a putative antioxidant response element in the 5′-flanking region of the human γ-glutamylcysteine synthetase heavy subunit gene. Biochem. Biophys. Res. Commun. 209 (1995) 227-233
50. Mulcahy R.T., Wartman M.A., Bailey H.H., and Gipp J.J. Constitutive and beta-naphthoflavone-induced expression of the human γ-glutamylcysteine synthetase heavy subunit gene is regulated by a distal antioxidant response element/TRE sequence. J. Biol. Chem. 272 (1997) 7445-7454
51. Moinova H.R., and Mulcahy R.T. An electrophile responsive element (EpRE) regulates beta-naphthoflavone induction of the human γ-glutamylcysteine synthetase regulatory subunit gene. Constitutive expression is mediated by an adjacent AP-1 site. J. Biol. Chem. 273 (1998) 14683-14689
52. Nguyen T., Rushmore T.H., and Pickett C.B. Transcriptional regulation of a rat liver glutathione S-transferase Ya subunit gene. Analysis of the antioxidant response element and its activation by the phorbol ester 12-O-tetradecanoylphorbol-13-acetate. J. Biol. Chem. 269 (1994) 13656-13662
53. Nguyen T., Sherratt P.J., and Pickett C.B. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol. 43 (2003) 233-260
54. Wild A.C., Gipp J.J., and Mulcahy T. Overlapping antioxidant response element and PMA response element sequences mediate basal and beta-naphthoflavone-induced expression of the human γ-glutamylcysteine synthetase catalytic subunit gene. Biochem. J. 332 Pt. 2 (1998) 373-381
55. Wasserman W.W., and Fahl W.E. Functional antioxidant responsive elements. Proc. Natl. Acad. Sci. USA 94 (1997) 5361-5366
56. Sasaki H., Sato H., Kuriyama-Matsumura K., Sato K., Maebara K., Wang H., Tamba M., Itoh K., Yamamoto M., and Bannai S. Electrophile response element-mediated induction of the cystine/glutamate exchange transporter gene expression. J. Biol. Chem. 277 (2002) 44765-44771
57. Inamdar N.M., Ahn Y.I., and Alam J. The heme-responsive element of the mouse heme oxygenase-1 gene is an extended AP-1 binding site that resembles the recognition sequences for MAF and NF-E2 transcription factors. Biochem. Biophys. Res. Commun. 221 (1996) 570-576
58. 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. 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 (2004) 3499S-3506S
59. Leung L., Kwong M., Hou S., Lee C., and Chan J.Y. Deficiency of the Nrf1 and Nrf2 transcription factors results in early embryonic lethality and severe oxidative stress. J. Biol. Chem. 278 (2003) 48021-48029
60. Enomoto A., Itoh K., Nagayoshi E., Haruta J., Kimura T., O'Connor T., Harada T., and Yamamoto M. 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 (2001) 169-177
61. Aoki Y., Sato H., Nishimura N., Takahashi S., Itoh K., and Yamamoto M. Accelerated DNA adduct formation in the lung of the Nrf2 knockout mouse exposed to diesel exhaust. Toxicol. Appl. Pharmacol. 173 (2001) 154-160
62. Chan J.Y., and Kwong M. Impaired expression of glutathione synthetic enzyme genes in mice with targeted deletion of the Nrf2 basic-leucine zipper protein. Biochim. Biophys. Acta 1517 (2000) 19-26
63. Lee J.S., and Surh Y.J. Nrf2 as a novel molecular target for chemoprevention. Cancer Lett. 224 (2005) 171-184
64. Kobayashi M., and Yamamoto M. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox. Signal. 7 (2005) 385-394
65. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J.D., and Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13 (1999) 76-86
66. Zipper L.M., and Mulcahy R.T. Inhibition of ERK and p38 MAP kinases inhibits binding of Nrf2 and induction of GCS genes. Biochem. Biophys. Res. Commun. 278 (2000) 484-492
67. Dinkova-Kostova A.T., Holtzclaw W.D., Cole R.N., Itoh K., Wakabayashi N., Katoh Y., Yamamoto M., and Talalay P. 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. USA 99 (2002) 11908-11913
68. Huang H.C., Nguyen T., and Pickett C.B. Regulation of the antioxidant response element by protein kinase C-mediated phosphorylation of NF-E2-related factor 2. Proc. Natl. Acad. Sci. USA 97 (2000) 12475-12480
69. Bloom D.A., and Jaiswal A.K. Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response element-mediated NAD(P)H:quinone oxidoreductase-1 gene expression. J. Biol. Chem. 278 (2003) 44675-44682
70. Kang M.I., Kobayashi A., Wakabayashi N., Kim S.G., and Yamamoto M. Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. Proc. Natl. Acad. Sci. USA 101 (2004) 2046-2051
71. Wakabayashi N., Dinkova-Kostova A.T., Holtzclaw W.D., Kang M.I., Kobayashi A., Yamamoto M., Kensler T.W., and Talalay P. Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc. Natl. Acad. Sci. USA 101 (2004) 2040-2045
72. Levonen A.L., Landar A., Ramachandran A., Ceaser E.K., Dickinson D.A., Zanoni G., Morrow J.D., and Darley-Usmar V.M. Cellular mechanisms of redox cell signalling: role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. Biochem. J. 378 (2004) 373-382
73. Kakishita H., and Hattori Y. Vascular smooth muscle cell activation and growth by 4-hydroxynonenal. Life Sci. 69 (2001) 689-697
74. Soh Y., Jeong K.S., Lee I.J., Bae M.A., Kim Y.C., and Song B.J. Selective activation of the c-Jun N-terminal protein kinase pathway during 4-hydroxynonenal-induced apoptosis of PC12 cells. Mol. Pharmacol. 58 (2000) 535-554
75. Camandola S., Poli G., and Mattson M.P. The lipid peroxidation product 4-hydroxy-2,3-nonenal increases AP-1- binding activity through caspase activation in neurons. J. Neurochem. 74 (2000) 159-168
76. Tamagno E., Robino G., Obbili A., Bardini P., Aragno M., Parola M., and Danni O. H2O2 and 4-hydroxynonenal mediate amyloid beta-induced neuronal apoptosis by activating JNKs and p38MAPK. Exp. Neurol. 180 (2003) 144-155
77. Bruckner S.R., and Estus S. JNK3 contributes to c-jun induction and apoptosis in 4-hydroxynonenal-treated sympathetic neurons. J. Neurosci. Res. 70 (2002) 665-670
78. Song B.J., Soh Y., Bae M., Pie J., Wan J., and Jeong K. Apoptosis of PC12 cells by 4-hydroxy-2-nonenal is mediated through selective activation of the c-Jun N-terminal protein kinase pathway. Chem. -Biol. Interact. 130-132 (2001) 943-954
79. Kumagai T., Nakamura Y., Osawa T., and Uchida K. Role of p38 mitogen-activated protein kinase in the 4-hydroxy-2-nonenal-induced cyclooxygenase-2 expression. Arch. Biochem. Biophys. 397 (2002) 240-245
80. Li Y., and Jaiswal A.K. Human antioxidant-response-element-mediated regulation of type 1 NAD(P)H:quinone oxidoreductase gene expression. Effect of sulfhydryl modifying agents. Eur. J. Biochem. 226 (1994) 31-39
81. Gong P., Stewart D., Hu B., Li N., Cook J., Nel A., and Alam J. Activation of the mouse heme oxygenase-1 gene by 15-deoxy-Delta(12,14)-prostaglandin J(2) is mediated by the stress response elements and transcription factor Nrf2. Antioxid. Redox. Signal. 4 (2002) 249-257
82. Martin D., Rojo A.I., Salinas M., Diaz R., Gallardo G., Alam J., De Galarreta C.M., and Cuadrado A. Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol. J. Biol. Chem. 279 (2004) 8919-8929
83. Liu S., and Pickett C.B. The rat liver glutathione S-transferase Ya subunit gene: characterization of the binding properties of a nuclear protein from HepG2 cells that has high affinity for the antioxidant response element. Biochemistry 35 (1996) 11517-11521
84. Hayashi A., Suzuki H., Itoh K., Yamamoto M., and Sugiyama Y. Transcription factor Nrf2 is required for the constitutive and inducible expression of multidrug resistance-associated protein 1 in mouse embryo fibroblasts. Biochem. Biophys. Res. Commun. 310 (2003) 824-829
85. Moinova H.R., and Mulcahy R.T. Up-regulation of the human γ-glutamylcysteine synthetase regulatory subunit gene involves binding of Nrf-2 to an electrophile responsive element. Biochem. Biophys. Res. Commun. 261 (1999) 661-668
86. Wild A.C., Moinova H.R., and Mulcahy R.T. Regulation of γ-glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2. J. Biol. Chem. 274 (1999) 33627-33636
87. Zhang, H.; Liu, H.; Iles, K. E.; Liu, R. M.; Postlethwait, E. M.; Laperche, Y.; Forman, H. J. 4-Hydroxynonenal induces rat γ-glutamyl transpeptidase through MAPK mediated EpRE/Nrf2 signaling. Am. J. Respir. Cell Mol. Biol., 2005 (in press).
88. Parola M., Bellomo G., Robino G., Barrera G., and Dianzani M.U. 4-Hydroxynonenal as a biological signal: molecular basis and pathophysiological implications. Antioxid. Redox. Signal. 1 (1999) 255-284