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Thromb Haemost 2002; 88(02): 335-344
DOI: 10.1055/s-0037-1613207
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Schattauer GmbH

Quenching of Intracellular ROS Generation as a Mechanism for Oleate-Induced Reduction of Endothelial Activation and Early Atherogenesis

Marika Massaro
1   Laboratory for Thrombosis and Vascular Research, C.N.R. Institute of Clinical Physiology, Pisa
3   Department of Experimental Pathology, the University of Pisa
,
Giuseppina Basta
1   Laboratory for Thrombosis and Vascular Research, C.N.R. Institute of Clinical Physiology, Pisa
,
Guido Lazzerini
1   Laboratory for Thrombosis and Vascular Research, C.N.R. Institute of Clinical Physiology, Pisa
,
Maria Annunziata Carluccio
2   Lecce, University of Pisa
,
Francesca Bosetti
4   Biochemistry Section, Scuola Superiore S. Anna, Pisa
,
Giancarlo Solaini
4   Biochemistry Section, Scuola Superiore S. Anna, Pisa
,
Francesco Visioli
5   Institute of Pharmacological Sciences, University of Milan
,
Aldo Paolicchi
3   Department of Experimental Pathology, the University of Pisa
,
Raffaele De Caterina
1   Laboratory for Thrombosis and Vascular Research, C.N.R. Institute of Clinical Physiology, Pisa
6   Chair of Cardiology, “G. d’Annunzio” University, Chieti, Italy
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Publikationsverlauf

Received 30. November 2001

Accepted after revision 30. April 2002

Publikationsdatum:
07. Dezember 2017 (online)

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Summary

We previously showed that the exposure of vascular endothelium to oleate results in reduced endothelial activation. We now investigate possible mechanisms for this effect in relation to generation of reactive oxygen species (ROS). We stimulated several types of endothelial cells with cytokines or lipopolysaccharide, with or without preincubation with 10-100 µmol/L oleate. Oleate preincubation reduced VCAM-1 expression in all cell types, as well as macrophage-colony stimulating factor release. We simultaneously measured the concentration of intracellular glutathione (GSH), the activity of GSH-related antioxidant enzymes and the production of intracellular ROS. Stimulation of endothelial cells caused a decrease of GSH and an increase in intracellular ROS. The addition of oleate before stimulation, prevented the depletion of GSH and partially prevented stimuli-induced increase of intracellular ROS. This occurred without any change in the activity of GSH-related antioxidant enzymes, superoxide dismutase and catalase. Furthermore, in a cell-free superoxide anion-generating system, oleate quenched the generation of ROS. These results indicate that oleate may exert direct vascular atheroprotective effects by inhibiting endothelial activation through a quenching of stimuli-induced increase in ROS.

Keywords

Oleate - adhesion molecules - reactive oxygen species - redox status - glutathione
 

  • References

  • 1 Lusis A. Atherosclerosis. Nature 2000; 407: 233-41.
    CrossrefPubMedGoogle Scholar
  • 2 Ross R. Atherosclerosis – An inflammatory disease. N Engl J Med 1999; 340: 115-26.
    CrossrefPubMedGoogle Scholar
  • 3 Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T. Transcriptional regulation of endothelial cell adhesion molecules: NF-κB and cytokine-inducible enhancers. Faseb J 1995; 09: 899-909.
    CrossrefPubMedGoogle Scholar
  • 4 Brigham KL, Meyrick B, Berry LC, Repine JE. Antioxidants protect cultured bovine lung endothelial cells from injury by endotoxin. J Appl Physiol 1987; 63: 840-50.
    CrossrefPubMedGoogle Scholar
  • 5 Lo SK, Janakidevi K, Lai L, Malik AA. Hydrogen peroxide-induced increase in endothelial adhesiveness independent on ICAM-1 activation. Am J Physiol 1993; 264: 406-12.
    PubMedGoogle Scholar
  • 6 Spolarics Z, Stein DS, Garcia ZC. Endotoxin stimulates hydrogen peroxide detoxifying activity in rat hepatic endothelial cells. Hepatology 1996; 24: 691-6.
    CrossrefPubMedGoogle Scholar
  • 7 Baeuerle PA, Henkel T. Function and activation of NF-κB in the immune system. Annu Rev Immunol 1994; 12: 141-79.
    CrossrefPubMedGoogle Scholar
  • 8 Rahman A, Kefer J, Bando M, Niles WD, Malik AB. E-Selectin expression in human endothelial cells by TNF-α-induced oxidant generation and NF-κB activation. Am J Physiol 1998; 275: L533-L544.
    PubMedGoogle Scholar
  • 9 Pahl H, Baeuerle PA. Oxygen and the control of gene expression. Bioessays 1994; 16: 479-501.
    PubMedGoogle Scholar
  • 10 Toborek M, Barger SW, Mattson MP, McClain CJ, Henning B. Role of glutathione redox cycle in TNF-α-mediated endothelial cell dysfunction. Atherosclerosis 1995; 117: 178-88.
    PubMedGoogle Scholar
  • 11 Sen CK, Khanna S, Reznick AZ, Roy S, Packer L. Glutathione regulation of tumor necrosis factor-α-induced NF-κB activation in skeletal musclederived L6 cells. Biochem Biophys Res Commun 1997; 237: 645-9.
    CrossrefPubMedGoogle Scholar
  • 12 Tsan M, Danis EH, Del Vecchio PJ, Rosano CL. Enhancement of intracellular glutathione protects endothelial cells against oxydant damage. Biochem Biophys Res Commun 1985; 127: 270-6.
    CrossrefPubMedGoogle Scholar
  • 13 Chang M, Shi M, Forman HJ. Exogenous glutathione protects endothelial cells from menadion toxicity. Am J Physiol 1992; 06: L637-L643.
    PubMedGoogle Scholar
  • 14 Faruqi RM, Poptic EJ, Faruqi TR, De La Motte C, DiCorleto PE. Distinct mechanisms for N-acetylcysteine inhibition of cytokine-induced E-selectin and VCAM-1 expression. Am J Physiol 1997; 273: 817-26.
    PubMedGoogle Scholar
  • 15 Visner GA, Dougall WC, Wilson JM, Burr IA, Nick HS. Regulation of manganese superoxide dismutase by lipopolysaccharide, interleukin-1, and tumor necrosis factor, Role in acute inflammatory response. J Biol Chem 1990; 265: 2856-64.
    PubMedGoogle Scholar
  • 16 Harlan JM, Levine JD, Callahan KS, Schwartz BR. Glutathione redox cycle protects cultured endothelial cells against lysis by extracellularly generated hydrogen peroxide. J Clin Invest 1984; 73: 706-713.
    CrossrefPubMedGoogle Scholar
  • 17 Buckley BJ, Tanswell AK, Freeman BA. Liposome mediated augmentation of catalase in alveolar type II cells protects against H2O2 injury. J Appl Physiol 1987; 63: 359-67.
    CrossrefPubMedGoogle Scholar
  • 18 Schmidt KN, Amstad P, Cerutti P, Baeuerle A. The roles of hydrogen peroxide and superoxide as messengers in the activation of trascriptional factor NF-κB. Chem Biol 1995; 02: 13-22.
    CrossrefPubMedGoogle Scholar
  • 19 Brigelius-Flohe R, Friedrichs B, Maurer S, Schultz M, Streicher R. Interleukin-1-induced nuclear factor kB activation is inhibited by overexpression of phospholipid hydroperoxide glutathione peroxidase in a human endothelial cell line. Biochem J 1997; 328: 199-203.
    CrossrefPubMedGoogle Scholar
  • 20 Keys A, Menotti A, Martti JK. et al. The diet and 15-year death rate in the Seven Countries Study. Am J Epidemiol 1986; 124: 903-15.
    CrossrefPubMedGoogle Scholar
  • 21 Kafatos A, Kouromalis I, Vlachonikolis I, Theodorou C, Labadorios D. Coronary-heart-disease risk factor status of the Cretan urban population in the 1980s. Am J Clin Nutr 1991; 54: 591-8.
    CrossrefPubMedGoogle Scholar
  • 22 Hart CM, Andreoli SP, Patterson CE, Garcia JGN. Oleic acid supplementation reduces oxidant-mediated dysfunction of cultured porcine pulmonary artery endothelial cells. J Cell Physiol 1993; 156: 24-34.
    CrossrefPubMedGoogle Scholar
  • 23 Carluccio MA, Massaro M, Bonfrate C. et al. Oleic acid inhibits endothelial cell activation. Arterioscler Thromb Vasc Biol 1999; 19: 220-8.
    CrossrefPubMedGoogle Scholar
  • 24 Gimbrone MA. Culture of vascular endothelium. In: Progress in Hemostasis and Thrombosis. Spaet TH. ed. New York: Grune & Stratton; 1976: 1-28.
    Google Scholar
  • 25 De Caterina R, Tanaka H, Tetsuro N, Huptman PJ, Libby P. The direct effect of injectable cyclosporine and its vehicle, cremophor, on endothelial vascular cell adhesion molecule-1 expression. Transplantation 1995; 60: 270-5.
    CrossrefPubMedGoogle Scholar
  • 26 Ades EW, Candal FJ, Swerlick RA. et al. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 1992; 99: 683-90.
    CrossrefPubMedGoogle Scholar
  • 27 De Caterina R, Libby P, Peng HB. et al. Nitric oxide decreases cytokineinduced endothelial activation. J Clin Invest 1995; 96: 60-8.
    CrossrefPubMedGoogle Scholar
  • 28 Peterson GL. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 1977; 83: 346-56.
    CrossrefPubMedGoogle Scholar
  • 29 Peng HB, Rajavashisth P, Libby P, Liao K. Nitric oxide inhibits macrophage-colony stimulating factor gene transcription in vascular endothelial cell. J Biol Chem 1995; 270: 17050-5.
    CrossrefPubMedGoogle Scholar
  • 30 Hong YH, Peng HB, La Fata V, Liao KJ. Hydrogen peroxide-mediated transcriptional induction of macrophage colony-stimulating factor by TGF-β1. J Immunol 1997; 159: 2418-23.
    PubMedGoogle Scholar
  • 31 Royall JA, Ischiropoulos H. Evaluation of 2’,7’-dichlorofluorescin and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells. Arch Biochem Biophys 1993; 302: 348-55.
    CrossrefPubMedGoogle Scholar
  • 32 LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of the probe 2’,7’-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 1992; 05: 227-31.
    CrossrefPubMedGoogle Scholar
  • 33 Tieze F. Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione. Anal Biochem 1969; 27: 502-22.
    CrossrefPubMedGoogle Scholar
  • 34 Paglia DE, Valentine WN. Studies on the qualitative and quantitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967; 70: 158-69.
    PubMedGoogle Scholar
  • 35 Carlberg I, Mannervik B. Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 1975; 250: 5475-80.
    PubMedGoogle Scholar
  • 36 Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferase. J Biol Chem 1974; 249: 7130-9.
    PubMedGoogle Scholar
  • 37 McCord JM, Fridowich I. Superoxide dismutase. J Biol Chem 1969; 244: 6049-55.
    PubMedGoogle Scholar
  • 38 Beers RF, Sizer W. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 1952; 193: 133-40.
    PubMedGoogle Scholar
  • 39 Kossenjans W, Rymaszewski Z, Barankiewicz J, Robst-Ashraf M. Menadione-induced oxidative stress in bovine heart microvascular endothelial cells. Microcirculation 1996; 03: 39-47.
    CrossrefPubMedGoogle Scholar
  • 40 De Caterina R, Cybulsky MI, Clinton SK, Gimbrone MA, Libby P. The omega-3 fatty acid docosahexaenoate reduces cytokine-induced expression of proatherogenic and proinflammatory proteins in human endothelial cells. Arterioscler Thromb 1994; 14: 1829-36.
    CrossrefPubMedGoogle Scholar
  • 41 De Caterina R, Bernini W, Carluccio MA, Liao JK, Libby P. Structural requirements for inhibition of cytokine-induced endothelial activation by unsaturated fatty acids. J Lipid Res 1998; 30: 1062-70.
    PubMedGoogle Scholar
  • 42 Thanos D, Maniatis T. NF-κB: a lesson in family values. Cell 1995; 80: 529-32.
    CrossrefPubMedGoogle Scholar
  • 43 Hart CM, Tolson JK, Block ER. Fatty acid supplementation protects pulmonary artery endothelial cells from oxidant injury. Am J Respir Cell Mol Biol 1990; 03: 479-89.
    CrossrefPubMedGoogle Scholar
  • 44 Hart MC, Tolson JK, Block ER. Supplemental fatty acids alter lipid peroxidation and oxidant injury in endothelial cells. Am J Physiol 1991; 260: L481-L488.
    PubMedGoogle Scholar
  • 45 Loeb GA, Skelton DC, Forman HJ. Dependence of mixed disulfide formation in alveolar macrophage upon production of oxidized glutathione: effect of selenium depletion. Biochem Pharmacol 1989; 38: 3119-21.
    CrossrefPubMedGoogle Scholar
  • 46 Porter NA, Caldwell SE, Mills KA. Mechanism of free radical oxidation of unsaturated lipids. Lipids 1995; 30: 277-90.
    CrossrefPubMedGoogle Scholar
  • 47 Weber C, Erl W, Pietsch A, Danesch U, Weber P. Docosahexaenoic acid selectively attenuates induction of vascular cell adhesion molecule-1 and subsequent monocytic cell adhesion to human endothelial cells stimulated by tumor necrosis factor-α. Arterioscler Thromb Vasc Biol 1995; 15: 622-8.
    CrossrefPubMedGoogle Scholar
  • 48 GISSI-Prevenzione Investigators (Gruppo Italiano per lo Studio della Sopravvivenza nell’Infarto Miocardico). Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. Lancet 1999; 354: 447-55.
    CrossrefPubMedGoogle Scholar
  • 49 Ober M, Hart C. Attenuation of oxidant-mediated endothelial cell injury with docosahexaenoic acid: the role of intracellular iron. Prostaglandins Leukot Essent Fatty Acids 1998; 59: 127-35.
    CrossrefPubMedGoogle Scholar
  • 50 Joulain C, Prigent A, Nemoz G, Lagarde M. Increased glutathione peroxidase activity in human blood mononuclear cells upon in vitro incubation with n-3 fatty acids. Biochem Pharmacol 1994; 47: 1315-23.
    CrossrefPubMedGoogle Scholar
  • 51 Clarke SD, Thuillier P, Baillie RA, Sha X. Peroxisome proliferatoractivated receptors: a family of lipid-activated transcription factors. Am J Clin Nutr 1999; 70: 566-71.
    CrossrefPubMedGoogle Scholar
  • 52 Marx N, Sukhova GK, Collins T, Libby P, Plutzky J. PPARalpha activators inhibit cytokine-induced vascular cell adhesion molecule-1 expression in human endothelial cells. Circulation 1999; 99: 3125-31.
    CrossrefPubMedGoogle Scholar
  • 53 Forman BM, Chen J, Evans RM. Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta. Proc Natl Acad Sci USA 1997; 94: 4312-7.
    CrossrefPubMedGoogle Scholar
  • 54 Inoue M, Itoh H, Tanaka T. et al. Oxidized LDL regulates vascular endothelial growth factor expression in human macrophages and endothelial cells through activation of peroxisome proliferator-activated receptor-gamma. Arterioscler Thromb Vasc Biol 2001; 21: 560-6.
    CrossrefPubMedGoogle Scholar
  • 55 Rao C, Zang E, Reddy B. Effect of high fat corn oil, olive oil and fish oil on phospholipids fatty acid composition in male F344 rats. Lipids 1993; 28: 441-47.
    CrossrefPubMedGoogle Scholar
  • 56 Yaqoob P, Sherrington E, Jeffrey N. et al. Comparison of the effects of a range of dietary lipids upon serum and tissue lipid composition in the rat. Int J Biochem Cell Biol 1995; 27: 297-310.
    CrossrefPubMedGoogle Scholar
  • 57 Ryan M, McInerney D, Owens D, Collins P, Johnson A, Tomkin J. Diabetes and Mediterranean diet: a beneficial effect of oleic acid on insulin sensitivity, adipocyte glucose transport and endothelium-dependent vasoreactivity. Q J Med 2000; 93: 85-91.
    CrossrefPubMedGoogle Scholar
  • 58 Tsimikas S, Philis-Tsimikas A, Alexopoulos S, Sigari F, Lee C, Reaven P. LDL isolated from Greek subjects on a typical diet or from American subjects on an oleate-supplemented diet induces less monocyte chemotaxis and adhesion when exposed to oxidative stress. Arterioscler Thromb Vasc Biol 1999; 19: 122-30.
    CrossrefPubMedGoogle Scholar