Docosahexaenoic acid enhances the antioxidant response of human fibroblasts by upregulating γ-glutamyl-cysteinyl ligase and glutathione reductase

British Journal of Nutrition

Volumn 95, Issue 1, 2006, Pages 18-26

  Arab, Khelifa ^a,b   Rossary, Adrien ^a,b   Flourié, Françoise ^a   Tourneur, Yves ^b   Steghens, Jean Paul ^a,b  

^a EDOUARD HERRIOT HOSPITAL   (France)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

Chemoprevention; Docosahexaenoic acid; Fibroblasts; Glutathione; Oxidative stress; Thiol redox status

Indexed keywords

ANTIOXIDANT; CELL ENZYME; DICHLOROFLUORESCEIN; DOCOSAHEXAENOIC ACID; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; HEME OXYGENASE; MESSENGER RNA; OMEGA 3 FATTY ACID; POLYUNSATURATED FATTY ACID; REACTIVE OXYGEN METABOLITE; THIOL; UNSATURATED FATTY ACID;

ARTICLE; CATALYSIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; FIBROBLAST; FIBROBLAST CULTURE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; UPREGULATION;

ANTIOXIDANTS; CELLS, CULTURED; DOCOSAHEXAENOIC ACIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; FATTY ACIDS; FIBROBLASTS; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; HEME OXYGENASE (DECYCLIZING); HUMANS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SULFHYDRYL COMPOUNDS; TIME FACTORS; UP-REGULATION;

EID: 32844456005     PISSN: 00071145     EISSN: None     Source Type: Journal    
DOI: 10.1079/BJN20051626     Document Type: Article

References (38)

1. Akihisa T, Tokuda H, Ogata M, Ukiya M, Iizuka M, Suzuki T, Metori K, Shimizu N & Nishino H (2004) Cancer chemopreventive effects of polyunsaturated fatty acids. Cancer Lett 205, 9-13.
2. Alam J & Cook JL (2003) Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des 9, 2499-2511.
3. Anderson ME (1997) Glutathione and glutathione delivery compounds. Avd Pharmacol 38, 65-78.
4. Arab K & Steghens JP (2004) Plasma lipid hydroperoxides measurement by an automated xylenol orange method. Anal Biochem 325, 158-163.
5. Barker JE, Heales SJR, Cassidy A, Bolanos JP, Land JM & Clark JB (1996) Depletion of brain glutathione results in a decrease of glutathione reductase activity; an enzyme susceptible to oxidative damage. Brain Res 716, 118-122.
6. Brown ER & Subbaiah PV (1994) Differential effects of eicosapentanoic acid and docosahexaenoic acid on human skin fibroblasts. Lipids 29, 825-829.
7. Carter WO, Narayanan PK & Robinson JP (1994) Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells. J Leukoc Biol 55, 253-258.
8. Chik K, Flourie F, Arab K & Steghens JP (2005) A simple and fast kinetic LC/MS measurement of γ glutamyl-cysteinyl ligase activity. J Chromatogr B, May 16. Available online. DOI: 10.1016/j.jchromb.2004.04.040.
9. Davidson LA, Nguyen DV, Hokanson RM et al. (2004) Chemopreventive n-3 polyunsaturated fatty acids reprogram genetic signatures during colon cancer initiation and progression in the rat. Cancer Res 64, 6797-6804.
10. Dickinson DA, Iles N, Watanabe KE, Iwamoto T, Zhang H, Krzywanski DM & Forman HJ (2002) 4-Hydroxynonenal induces glutamate cysteine ligase through JNK in HBE1 cells. Free Radic Biol Med 33, 974-987.
11. Germain E, Chajes V, Cognault S, Lhuillery C & Bougnoux P (1998) Enhancement of doxorubicin cytotoxicity by polyunsaturated fatty acids in the human breast tumor cell line MDA-MB-231: relationship to lipid peroxidation. Int J Cancer 75, 578-583.
12. Habig WH, Pabst MJ & Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249, 7130-7139.
13. Kim H, Akbar M, Lau A & Esdall L (2000) Inhibition of neuronal apoptosis by docosahexaenoic acid (22:6n-3). J Biol Chem 275, 35215-35223.
14. Komatsu W, Ishihara K, Murata M, Saito H & Shinohara K (2003) Docosahexaenoic acid suppresses nitric oxide production and inducible nitric oxide synthase expression in interferon-gamma plus lipopolysaccharide-stimulated murine macrophages by inhibiting the oxidative stress. Free Radic Biol Med 34, 1006-1016.
15. Kris-Etherton PM, Harris WS & Appel LJ (2002) Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106, 2747-2757.
16. Larsson SC, Kumlin M, Ingelman-Sundberg M & Wolk A (2004) Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms. Am J Clin Nutr 79, 935-945.
17. Lee JM, Calkins MJ, Chan K, Kan YW & Johnson JA (2003a) Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J Biol Chem 278, 12029-12038.
18. Lee HT, Xu H, Ota-Setlik A & Emala CW (2003b) Oxidant preconditioning protects human proximal tubular cells against lethal oxidant injury via p38 MAPK and heme oxygenase-1. Am J Nephrol 23, 324-333.
19. Levonen AL, Landar A, Ramachandran A, Ceaser EK, Dickinson DA, Zanoni G, Morrow JD & Darley-Usmar VM (2004) Cellular mechanisms of redox cell signalling: role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. Biochem J 378, 373-382.
20. Liu W, Kato M, Akhand AA, Hayakawa A, Suzuki H, Miyata T, Kurokawa K, Hotta Y, Ishikawa N & Nakashima I (2000) 4-hydroxynonenal induces a cellular redox status-related activation of the caspase cascade for apoptotic cell death. J Cell Sci 113, 635-641.
21. LocusLink (2005) http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?CMD=search&DB=gene.
22. Lopez-Garcia E, Schulze MZ, Manson JE, Meigs JB, Albert CM, Rifai N, Willet WC & Hu FB (2004) Consumption of (n-3) fatty acids is related to plasma biomarkers of inflammation and endothelial activation in women. J Nutr 134, 1806-1811.
23. Marcheselli LV, Hong S, Lukiw JW, et al. (2003) Novel docosanoids inhibit brain ischemia-reperfusion mediated leukocyte infiltration and pro-inflammatory gene expression. J Biol Chem 278, 43807-43817.
24. Martinez M, Vazquez E, Garcia-Silva MT, Manzanares J, Bertran JM, Castello F & Mougan I (2000) Therapeutic effects of docosahexaenoic acid ethyl ester in patients with generalized peroxisomal disorders. J Clin Nutr 71, Suppl., 376S-385S.
25. Merendino N, Molinari R, Loppi B, Pessina G, D'Aquino M, Tomassi G & Velloti F (2003) Induction of apoptosis in human pancreatic cancer cell by docosahexaenoic acid. Ann N Y Acad Sci 1010, 361-364.
26. Primer3 software (2005) http://cbr-rbc.nrc-cnrc.gc.ca/cgi-bin/primer3_www.cgi.
27. Rhodes LE, Shanbakhti H, Azurdia RM, et al. (2003) Effect of eicosapentanoic acid, an omega-3 polyunsaturated fatty acid, on UVR-related cancer risk in humans. An assessment of early genotoxic markers. Carcinogenesis 24, 919-925.
28. Romero-Ramos M, Venero JL, Garcia-Rodriguez S, Ayala A, Machado A & Cano J (2003) Semichronic inhibition of glutathione reductase promotes oxidative damage to proteins and induces both transcription and translation of tyrosine hydroxylase in the nigrostriatal system. Free Radic Res 37, 1003-1012.
29. Rossi R, Milzani A, Dalle-Donne I, Giustarini D, Lusini L, Colombo R & Di Simplicio P (2002) Blood glutathione disulfide: in vivo factor or in vitro artifact?" Clin Chem 48, 742-753.
30. Rushmore TH, Morton MR & Pickett CB (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.
31. Shi MM, Kugelman A, Iwalmoto T, Tian L & Forman HJ (1994) Quinone-induced oxidative stress elevated glutathione and induces γ-glutamylcysteine synthetase activity in rat lung epithelial L2 cells. J Biol Chem 269, 26512-26517.
32. Steghens JP, Flourie F, Arab K & Collombel C (2003) Fast liquid chromatography-mass spectrometry glutathione measurement in whole blood: micromolar GSSG is a sample preparation artifact. J Chromatogr B 25, 343-349.
33. Wasserman WW & Fahl WE (1997) Functional antioxidant responsive elements. Proc Natl Acad Sci 94, 5361-5366.
34. Wen B, Deutsch E, Opolon P, Auperin A, Frascogna V, Connault E & Bourhis (2003) n-3 polyunsaturated fatty acids decrease mucosal/epidermal reactions and enhance antitumour effect of ionising radiation with inhibition of tumour angiogenesis. Br J Cancer 89, 1102-1107.
35. Wild AC, Moinova HR & Mulcahy T (1999) Regulation of γ-glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2. J Biol Chem 274, 33627-33636.
36. Worthington DJ & Rosemeyer MA (1974) Human glutathione reductase: purification of the crystalline from erythrocytes. Eur J Biochem 48, 166-177.
37. Wu G, Fang YZ, Yang S, Lupton JR & Turner ND (2004) Glutathione metabolism and its implications for health. J Nutr 134, 489-492.
38. Ziboh AV, Miller CC & Cho Y (2000) Metabolism of polyunsaturated fatty acids by skin epidermal enzymes: generation of antiinflammatory and antiproliferative metabolites. Am J Clin Nutr 71, Suppl., 361S-366S.