Cellular mechanisms of redox cell signalling: Role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products

Biochemical Journal

Volumn 378, Issue 2, 2004, Pages 373-382

  Levonen, Anna Liisa ^a   Landar, Aimee ^a   Ramachandran, Anup ^a   Ceaser, Erin K ^a   Dickinson, Dale A ^b   Zanoni, Giuseppe ^c   Morrow, Jason D ^d   Darley Usmar, Victor M ^a  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF PAVIA   (Italy)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antioxidant defence; Electrophilic lipid oxidation; Glutamate cysteine ligase; Proteomics; Redox cell signalling; Thiol modification

Indexed keywords

AMINO ACIDS; ANTIOXIDANTS; DISEASES; GENES; LIPIDS; OXIDATION;

CELL SIGNALLING; PROSTAGLANDINS;

CELLS;

15 DEOXY DELTA12,14 PROSTAGLANDIN J2; 4 HYDROXYNONENAL; CYCLOPENTENONE; CYSTEINE; GLUTATHIONE; LIPID; PROSTAGLANDIN; THIOL; TRANSCRIPTION FACTOR NF E2;

ARTICLE; ATHEROSCLEROSIS; CELL ACTIVITY; EMBRYO; ENDOTHELIUM CELL; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; INFLAMMATORY DISEASE; KIDNEY CELL; LIPID OXIDATION; MOLECULAR DYNAMICS; OXIDATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN MODIFICATION; SIGNAL TRANSDUCTION;

ALDEHYDES; ANTIOXIDANTS; BASE SEQUENCE; CARRIER PROTEINS; CELL LINE; CYSTEINE; DNA-BINDING PROTEINS; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROSTAGLANDIN D2; PROSTAGLANDINS A; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS;

EID: 1642282736     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031049     Document Type: Article

References (57)

1. 2 and related compounds: an update. Prostaglandins Leukot. Essent. Fatty Acids 47, 1-12
2. 2) in vivo. Biochim. Biophys. Acta 1436, 550-556
3. 4-neuroprostanes) in vivo from docosahexaenoic acid. J. Biol. Chem. 277, 36076-36084
4. Gilroy, D. W., Colville-Nash, P. R., Willis, D., Chivers, J., Paul-Clark, M. J. and Willoughby, D. A. (1999) Inducible cyclooxygenase may have anti-inflammatory properties. Nat. Med. (N.Y.) 5, 698-701
5. 2 inhibition of NF-κB-DNA binding through covalent modification of the p50 subunit. J. Biol. Chem. 276, 35530-35536
6. Rossi, A., Kapahi, P., Natoli, G., Takahashi, T., Chen, Y., Karin, M. and Santoro, M. G. (2000) Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IκB kinase. Nature (London) 403, 103-108
7. 2 inhibits multiple steps in the NF-κB signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 97, 4844-4849
8. Eguchi, Y., Eguchi, N., Oda, H., Seiki, K., Kijima, Y., Matsu-ura, Y., Urade, Y. and Hayaishi, O. (1997) Expression of lipocalin-type prostaglandin D synthase (β-trace) in human heart and its accumulation in the coronary circulation of angina patients. Proc. Natl. Acad. Sci. U.S.A. 94, 14689-14694
9. Schonbeck, U., Sukhova, G. K., Graber, P., Coulter, S. and Libby, P. (1999) Augmented expression of cyclooxygenase-2 in human atherosclerotic lesions. Am. J. Pathol. 155, 1281-1291
10. 2 metabolite generated during inflammatory processes. J. Biol. Chem. 277, 10459-10466
11. 2 on glutathione induction and apoptosis in human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 21, 1846-1851
12. Moellering, D. R., Levonen, A. L., Go, Y. M., Patel, R. P., Dickinson, D. A., Forman, H. J. and Darley-Usmar, V. M. (2002) Induction of glutathione synthesis by oxidized low-density lipoprotein and 1-palmitoyl-2-arachidonyl phosphatidylcholine: protection against quinone-mediated oxidative stress. Biochem. J. 362, 51-59
13. 2 is mediated by the stress response elements and transcription factor Nrf2. Antioxid. Redox Signal. 4, 249-257
14. 2 in porcine aortic endothelial cells. Prostaglandins 43, 121-131
15. Huang, C. S., Anderson, M. E. and Meister, A. (1993) Amino acid sequence and function of the light subunit of rat kidney γ-glutamylcysteine synthetase. J. Biol. Chem. 268, 20578-20583
16. Huang, C. S., Chang, L. S., Anderson, M. E. and Meister, A. (1993) Catalytic and regulatory properties of the heavy subunit of rat kidney γ-glutamylcysteine synthetase. J. Biol. Chem. 268, 19675-19680
17. Wild, A. C. and Mulcahy R. T. (2000) Regulation of γ- glutamylcysteine synthetase subunit gene expression: insights into transcriptional control of antioxidant defenses. Free Radical Res. 32, 281-301
18. Moinova, H. R. and Mulcahy, R. T. (1998) An electrophile responsive element (EpRE) regulates β-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, 14683-14689
19. Mulcahy, R. T., Wartman, M. A., Bailey, H. H. and Gipp, J. J. (1997) Constitutive and β-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, 7445-7454
20. Rahman, I., Bel, A., Mulier, B., Lawson, M. F., Harrison, D. J., MacNee, W. and Smith, C. A. (1996) Transcriptional regulation of γ- glutamylcysteine synthetase-heavy subunit by oxidants in human alveolar epithelial cells. Biochem. Biophys. Res. Commun. 229, 832-837
21. Iwanaga, M., Mori, K., Iida, T., Urata, Y., Matsuo, T., Yasunaga, A., Shibata, S. and Kondo, T. (1998) Nuclear factor κB dependent induction of γ-glutamylcysteine synthetase by ionizing radiation in T98G human glioblastoma cells. Free Radical Biol. Med. 24, 1256-1268
22. Rushmore, T. H., King, R. G., Paulson, K. E. and Pickett, C. B. (1990) 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. U.S.A. 87, 3826-3830
23. Favreau, L. V. and Pickett, C. B. (1991) Transcriptional regulation of the rat NAD(P)H:quinone reductase gene. Identification of regulatory elements controlling basal level expression and inducible expression by planar aromatic compounds and phenolic antioxidants. J. Biol. Chem. 266, 4556-4561
24. Nguyen, T., Sherratt, P. J. and Pickett, C. B. (2003) Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol. 43, 233-260
25. Rushmore, T. H., Morton, M. R. and Pickett, C. B. (1991) The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J. Biol. Chem. 266, 11632-11639
26. Wasserman, W. W. and Fahl, W. E. (1997) Functional antioxidant responsive elements. Proc. Natl. Acad. Sci. U.S.A. 94, 5361-5366
27. Erickson, A. M., Nevarea, Z., Gipp, J. J. and Mulcahy, R. T. (2002) Identification of a variant antioxidant response element in the promoter of the human glutamate-cysteine ligase modifier subunit gene. Revision of the ARE consensus sequence. J. Biol. Chem. 277, 30730-30737
28. Nioi, P., McMahon, M., Itoh, K., Yamamoto, M. and Hayes, J. D. (2003) Identification of a novel Nrf2-regulated antioxidant response element (ARE) in the mouse NAD(P)H:quinone oxidoreductase 1 gene: reassessment of the ARE consensus sequence. Biochem. J. 374, 337-348
29. Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., O'Connor, T. and Yamamoto, M. (2003) Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 8, 379-391
30. McMahon, M., Itoh, K., Yamamoto, M. and Hayes, J. D. (2003) Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J. Biol. Chem. 278, 21592-21600
31. Nguyen, T., Sherrad, P. J., Huang, H. C., Yang, C. S. and Pickett, C. B. (2003) 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. 278, 4536-4541
32. Sekhar, K. R., Yan, X. X. and Freeman, M. L. (2002) Nrf2 degradation by the ubiquitin proteasome pathway is inhibited by KIAA0132, the human homolog to INrf2. Oncogene 21, 6829-6834
33. Stewart, D., Killeen, E., Naquin, R., Alam, S. and Alam, J. (2003) Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J. Biol. Chem. 278, 2396-2402
34. 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
35. 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
36. Zipper, L. M. and Mulcahy, R. T. (2002) The Keap1 BTB/POZ dimerization function is required to sequester Nrf2 in cytoplasm. J. Biol. Chem. 277, 36544-36552
37. 2 protein interactions and inhibition of cellular proliferation. Prostaglandins 50, 359-375
38. 2 isoprostane. J. Org. Chem. 67, 4346-4351
39. Tietze, F. (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 27, 502-522
40. Kim, J. R., Yoon, H. W., Kwon, K. S., Lee, S. R. and Rhee, S. G. (2000) Identification of proteins containing cysteine residues that are sensitive to oxidation by hydrogen peroxide at neutral pH. Anal. Biochem. 283, 214-221
41. Esterbauer, H., Schaur, R. J. and Zollner, H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biol. Med. 11, 81-128
42. Sekhar, K. R., Crooks, P. A., Sonar, V. N., Friedman, D. B., Chan, J. Y., Meredith, M. J., Starnes, J. H., Kelton, K. R., Summar, S. R., Sasi, S. et al. (2003) NADPH oxidase activity is essential for Keap1/Nrf2-mediated induction of GCLC in response to 2-indol-3-yl-methylenequinuclidin-3-ols. Cancer Res. 63, 5636-5645
43. Glass, C. K. and Witztum, J. L. (2001) Atherosclerosis. The road ahead. Cell (Cambridge, Mass.) 104, 503-516
44. Watson, A. D., Subbanagounder, G., Welsbie, D. S., Faull, K. F., Navab, M., Jung, M. E., Fogelman, A. M. and Berliner, J. A. (1999) Structural identification of a novel pro-inflammatory epoxyisoprostane phospholipid in mildly oxidized low density lipoprotein. J. Biol. Chem. 274, 24787-24798
45. Bea, F., Hudson, F. N., Chait, A., Kavanagh, T. J. and Rosenfeld, M. E. (2003) Induction of glutathione synthesis in macrophages by oxidized low-density lipoproteins is mediated by consensus antioxidant response elements. Circ. Res. 92, 386-393
46. Zhang, X., Garfinkel, M. and Ruden, D. M. (2003) Phylogenetic conservation of the Nrf2-Keap1 signaling system. In Signal Transduction by Reactive Oxygen and Nitrogen Species: Pathways and Chemical Principles (Forman, H. J., Torres, M. and Fukuto, J., eds.), Kluwer Academic Publishers, Dordrecht
47. Dinkova-Kostova, A. T., Massiah, M. A., Bozak, R. E., Hicks, R. J. and Talalay, P. (2001) Potency of Michael reaction acceptors as inducers of enzymes that protect against carcinogenesis depends on their reactivity with sulfhydryl groups. Proc. Natl. Acad. Sci. U.S.A. 98, 3404-3409
48. Esterbauer, H., Eckl, P. and Ortner, A. (1990) Possible mutagens derived from lipids and lipid precursors. Mutat. Res. 238, 223-233
49. 2 and the ligation of PPARγ. J. Clin. Invest. 112, 945-955
50. 2, to glutathione. Biochim. Biophys. Acta 1584, 37-45
51. Hubatsch, I., Ridderstrom, M. and Mannervik, B. (1998) Human glutathione transferase A4-4: an Alpha class enzyme with high catalytic efficiency in the conjugation of 4-hydroxynonenal and other genotoxic products of lipid peroxidation. Biochem. J. 330, 175-179
52. 2), is efficiently conjugated with glutathione by human and rat glutathione transferase A4-4. Chem. Res. Toxicol. 15, 1114-1118
53. Lee, S. R., Kwon, K. S., Kim, S. R. and Rhee, S. G. (1998) Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J. Biol. Chem. 273, 15366-15372
54. 2 binds to and activates H-Ras. Proc. Natl. Acad. Sci. U.S.A. 100, 4772-4777
55. Zipper, L. M. and Mulcahy, R. T. (2000) Inhibition of ERKand p38 MAP kinases inhibits binding of Nrf2 and induction of GCS genes. Biochem. Biophys. Res. Commun. 278, 484-492
56. Rossi, A., Kapahi, P., Natoli, G., Takahashi, T., Chen, Y., Karin, M. and Santoro, M. G. (2000) Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IκB kinase. Nature (London) 403, 103-108
57. Shibata, T., Yamada, T., Ishii, T., Kumazawa, S., Nakamura, H., Masutani, H., Yodoi, J. and Uchida, K. (2003) Thioredoxin as a molecular target of cyclopentenone prostaglandins. J. Biol. Chem. 278, 26046-26054