Mitochondrial Oxidative Stress is Modulated by Oleic Acid Via an Epidermal Growth Factor Receptor-dependent Activation of Glutathione Peroxidase

Overview

Journal Biochem J

Specialty Biochemistry

Date 2002 Aug 3

PMID 12153397

Citations 14

Authors

Carine Duval

Nathalie Auge

Marie-Francoise Frisach

Louis Casteilla

Robert Salvayre

Anne Negre-Salvayre

Affiliations

Soon will be listed here.

Abstract

Mitochondria generate reactive oxygen species (ROS) under various pathophysiological conditions. In isolated mitochondria, fatty acids (FA) exhibit an uncoupling effect of the respiratory activity and modulate ROS generation. The effect of FA on intact cultured cells remains to be elucidated. The present study reports that FA (buffered by BSA) decrease the level of cellular ROS generated by the mitochondrial respiratory chain in cultured cells incubated with antimycin A. Both saturated and unsaturated FA are effective. This fatty acid-induced antioxidant effect does not result from a decrease in ROS production, but is subsequent to cellular glutathione peroxidase (GPx) activation and enhanced ROS degradation. This fatty acid-induced GPx activation is mediated through epidermal growth factor receptor (EGFR) signalling, since this response is (i) abrogated by the EGFR inhibitor AG1478 or by a defect in EGFR (in EGFR-deficient B82L fibroblasts), (ii) restored in B82LK+ cells expressing EGFR and (iii) mimicked by epidermal growth factor. These findings indicate that FA contribute to enhance cellular antioxidant defences against mitochondrial oxidative stress through EGFR-dependent GPx activation.

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References

Chandrasekar B, Colston J, Freeman G . Induction of proinflammatory cytokine and antioxidant enzyme gene expression following brief myocardial ischaemia. Clin Exp Immunol. 1997; 108(2):346-51. PMC: 1904669. DOI: 10.1046/j.1365-2249.1997.d01-1017.x. View

Albers D, Beal M . Mitochondrial dysfunction and oxidative stress in aging and neurodegenerative disease. J Neural Transm Suppl. 2000; 59:133-54. DOI: 10.1007/978-3-7091-6781-6_16. View

Goss J, Taffe K, Kochanek P, DeKosky S . The antioxidant enzymes glutathione peroxidase and catalase increase following traumatic brain injury in the rat. Exp Neurol. 1997; 146(1):291-4. DOI: 10.1006/exnr.1997.6515. View

Negre-Salvayre A, Hirtz C, Carrera G, Cazenave R, Troly M, Salvayre R . A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J. 1997; 11(10):809-15. View

Csonka C, Pataki T, Kovacs P, Muller S, Schroeter M, Tosaki A . Effects of oxidative stress on the expression of antioxidative defense enzymes in spontaneously hypertensive rat hearts. Free Radic Biol Med. 2000; 29(7):612-9. DOI: 10.1016/s0891-5849(00)00365-8. View

Inoguchi T, Li P, Umeda F, Yu H, Kakimoto M, Imamura M . High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C--dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes. 2000; 49(11):1939-45. DOI: 10.2337/diabetes.49.11.1939. View

Thannickal V, Fanburg B . Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol. 2000; 279(6):L1005-28. DOI: 10.1152/ajplung.2000.279.6.L1005. View

Hardy S, Langelier Y, Prentki M . Oleate activates phosphatidylinositol 3-kinase and promotes proliferation and reduces apoptosis of MDA-MB-231 breast cancer cells, whereas palmitate has opposite effects. Cancer Res. 2000; 60(22):6353-8. View

Arthur J . The glutathione peroxidases. Cell Mol Life Sci. 2001; 57(13-14):1825-35. PMC: 11147127. DOI: 10.1007/pl00000664. View

10.

Asayama K, Nakane T, Dobashi K, Kodera K, Hayashibe H, Uchida N . Effect of obesity and troglitazone on expression of two glutathione peroxidases: cellular and extracellular types in serum, kidney and adipose tissue. Free Radic Res. 2001; 34(4):337-47. DOI: 10.1080/10715760100300291. View

11.

Kondoh M, Inoue Y, Atagi S, Futakawa N, Higashimoto M, Sato M . Specific induction of metallothionein synthesis by mitochondrial oxidative stress. Life Sci. 2001; 69(18):2137-46. DOI: 10.1016/s0024-3205(01)01294-2. View

12.

Zhou L, Johnson A, Rando T . NF kappa B and AP-1 mediate transcriptional responses to oxidative stress in skeletal muscle cells. Free Radic Biol Med. 2001; 31(11):1405-16. DOI: 10.1016/s0891-5849(01)00719-5. View

13.

Boveris A, Oshino N, Chance B . The cellular production of hydrogen peroxide. Biochem J. 1972; 128(3):617-30. PMC: 1173814. DOI: 10.1042/bj1280617. View

14.

Boveris A, Chance B . The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J. 1973; 134(3):707-16. PMC: 1177867. DOI: 10.1042/bj1340707. View

15.

Loschen G, Azzi A, Richter C, Flohe L . Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Lett. 1974; 42(1):68-72. DOI: 10.1016/0014-5793(74)80281-4. View

16.

Boveris A, Cadenas E, Stoppani A . Role of ubiquinone in the mitochondrial generation of hydrogen peroxide. Biochem J. 1976; 156(2):435-44. PMC: 1163765. DOI: 10.1042/bj1560435. View

17.

Chance B, Sies H, Boveris A . Hydroperoxide metabolism in mammalian organs. Physiol Rev. 1979; 59(3):527-605. DOI: 10.1152/physrev.1979.59.3.527. View

18.

Cadenas E, Boveris A . Enhancement of hydrogen peroxide formation by protophores and ionophores in antimycin-supplemented mitochondria. Biochem J. 1980; 188(1):31-7. PMC: 1162533. DOI: 10.1042/bj1880031. View

19.

Smith P, Krohn R, Hermanson G, Mallia A, Gartner F, Provenzano M . Measurement of protein using bicinchoninic acid. Anal Biochem. 1985; 150(1):76-85. DOI: 10.1016/0003-2697(85)90442-7. View

20.

Steinbrecher U . Role of superoxide in endothelial-cell modification of low-density lipoproteins. Biochim Biophys Acta. 1988; 959(1):20-30. DOI: 10.1016/0005-2760(88)90145-2. View