Vascular incorporation of α-tocopherol prevents endothelial dysfunction due to oxidized LDL by inhibiting protein kinase C stimulation

Journal of Clinical Investigation

Volumn 98, Issue 2, 1996, Pages 386-394

  Keaney Jr , John F ^a,b   Guo, Yue ^a   Cunningham, David ^a   Shwaery, Glenn T ^a   Xu, Aiming ^a   Vita, Joseph A ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

antioxidants; endothelium; lipoproteins; nitric oxide; vitamin E

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; LACTATE DEHYDROGENASE; NITRIC OXIDE; OXIDIZED LOW DENSITY LIPOPROTEIN; PROTEIN KINASE C; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; CORONARY ARTERY DISEASE; CYTOTOXICITY; DIET THERAPY; ENZYME ASSAY; ENZYME INHIBITION; HUMAN; HUMAN CELL; HYPERCHOLESTEROLEMIA; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RABBIT; SCANNING ELECTRON MICROSCOPY; THORACIC AORTA; VASCULAR ENDOTHELIUM; VASODILATATION;

EID: 0030036853     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI118804     Document Type: Article

References (51)

1. Furchgott, R.F., and J.V. Zawadzki. 1980. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature. (Lond.). 288:373-376.
2. Kelm, M., and J. Schrader. 1990. Control of coronary vascular tone by nitric oxide. Circ. Res. 66:1561-1575.
3. Azuma, H., M. Ishikawa, and S. Sekizaki. 1986. Endothelium-dependent inhibition of platelet aggregation. Br. J. Pharmacol. 88:411-415.
4. Ludmer, P.L., A.P. Selwyn, T.L. Shook, R.R. Wayne, G.H. Mudge, R.W. Alexander, and P. Ganz. 1986. Paradoxical vasoconstriction induced by acetylcholine in atherosclerotic coronary arteries. N. Engl. J. Med. 315:1046-1051.
5. Vita, J.A., C.B. Treasure, E.G., Nabel, J.M. McLenachan, R.D. Fish, A.C. Yeung, V.I. Vekshtein, A.P. Selwyn, and P. Ganz. 1990. Coronary vasomotor response to acetylcholine relates to risk factors for coronary artery disease. Circulation. 81:491-497.
6. Kugiyama, K., S.A. Kerns, J.D. Morrisett, R. Roberts, and P.D. Henry. 1990. Impairment of endothelium-dependent arterial relaxation by lysolecithin in modified low-density lipoproteins. Nature (Lond.). 344:160-162.
7. Chin, J.H., S. Azhar, and B.B. Hoffman. 1992. Inactivation of endothelium-derived relaxing factor by oxidized lipoproteins. J. Clin. Invest. 89:10-18.
8. Ylä-Herttuala, S., W. Palinski, M.E. Rosenfeld, S. Parthasarathy, T.E. Carew, S. Butler, J.L. Witztum, and D. Steinberg. 1989. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J. Clin. Invest. 84:1086-1095.
9. Morel, D.W., G.M. Hessler, and G.M. Chisolm. 1983. Low density lipoprotein cytotoxicity induced by free radical peroxidation of lipid. J. Lipid Res. 24:1070-1076.
10. Quinn, M.T., S. Parthasarathy, L.G. Fong, and D. Steinberg. 1987. Oxidatively modified low density lipoproteins: a potential role in recruitment and retention of monocyte/macrophages during atherogenesis. Proc. Natl. Acad. Sci. USA. 84:2995-2998.
11. Gryglewski, R.J., R.M. Palmer, and S. Moncada. 1986. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature (Lond.). 320:454-456.
12. Burton, G.W., A. Joyce, and K.U. Ingold. 1983. Is vitamin E the only lipid-soluble, chain-breaking antioxidant in human plasma and erythrocyte membranes? Arch. Biochem. Biophys. 221:281-290.
13. Reaven, P.D., A. Khouw, W.F. Beltz, S. Parthasarathy, and J.L. Witztum. 1993. Effect of dietary antioxidant combinations in humans. Protection of LDL by vitamin E but not beta carotene. Arteriosclerosis Thromb. 13:590-600.
14. Dieber-Rotheneder, M., H. Puhl, H. Waeg, G. Striegl, and H. Esterbauer. 1991. Effect of oral supplementation with D-alpha-tocopherol on the vitamin E content of human low density lipoproteins and resistance to oxidation. J. Lipid Res. 32:1325-1332.
15. Riemersma, R.A., D.A. Wood, C.C.H. Macintyre, R.A. Elton, K.F. Gey, and M.F. Oliver. 1991. Risk of angina pectoris and plasma concentrations of vitamins A, C, E, and carotene. Lancet. 337:1-5.
16. Rimm, E.B., M.J. Stampfer, A. Ascherio, E. Giovannucci, G.A. Colditz, and W.C. Willett. 1993. Vitamin E consumption and the risk of coronary heart disease in men. N. Engl. J. Med. 328:1450-1456.
17. Stampfer, M.J., C.H. Hennekens, J.E. Manson, G.A. Colditz, B. Rosner, and W. Willett. 1993. Vitamin E consumption and the risk of coronary disease in women. N. Engl. J. Med. 328:1444-1449.
18. Witztum, J.L., and D. Steinberg. 1991. Role of oxidized low density lipoprotein in atherogenesis. J. Clin. Invest. 88:1785-1792.
19. Steinbrecher, U.P., S. Parthasarathy, D.S. Leake, J.L. Witztum, and D. Steinberg. 1984. Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids. Proc. Natl. Acad. Sci. USA. 81:3883-3887.
20. Verlangieri, A.J., and M.J. Bush. 1992. Effects of d-alpha-tocopherol supplementation on experimentally induced primate atherosclerosis. J. Am. Coll. Nutr. 11:131-138.
21. Godfried, S.L., G.F. Combs, J.M. Saroka, and L.A. Dillingham. 1989. Potentiation of atherosclerotic lesions in rabbits by a high dietary level of vitamin E. Br. J. Nutr. 61:607-617.
22. Keaney, J.F., Jr., J.M. Gaziano, A. Xu, B. Frei, J. Curran-Celentano, G.T. Shwaery, J. Loscalzo, and J.A. Vita. 1994. Low-dose α-tocopherol improves and high-dose α-tocopherol worsens endothelial vasodilator function in cholesterol-fed rabbits. J. Clin. Invest. 93:844-851.
23. Keaney, J.F., Jr., J.M. Gaziano, A. Xu, B. Frei, J. Curran-Celantano, G.T. Shwaery, J. Loscalzo, and J.A. Vita. 1993. Dietary antioxidants preserve endothelium-dependent vessel relaxation in cholesterol-fed rabbits. Proc. Natl. Acad. Sci. USA. 90:11880-11884.
24. Faruqi, R., C. de la Motta, and P. DiCorleto. 1994. Alpha-tocopherol inhibits agonist-induced monocytic cell adhesion to cultured human endothelial cells. J. Clin. Invest. 94:592-600.
25. Navab, M., S.S. Imes, S.Y. Hama, G.P. Hough, L.A. Ross, R.W. Bork, A.J. Valente, J.A. Berliner, D.C. Drinkwater, H. Laks, and A.M. Fogelman. 1991. Monocyte transmigration induced by modification of low density lipoprotein in cocultures of human aortic wall cells is due to induction of monocyte chemotactic protein 1 synthesis and is abolished by high density lipoprotein. J. Clin. Invest. 88:2039-2046.
26. Hennig, B., C. Enoch, and C.K. Chow. 1987. Protection by vitamin E against endothelial cell injury by linoleic acid hydroperoxides. Nutr. Res. 7: 1253-1260.
27. Boscoboinik, D., A. Szewczyk, C. Hensey, and A. Azzi. 1991. Inhibition of cell proliferation by α-tocopherol. J. Biol. Chem. 266:6188-6194.
28. Tesfamariam, B., M.L. Brown, and R.A. Cohen. 1991. Elevated glucose impairs endothelium-dependent relaxation by activating protein kinase C. J. Clin. Invest. 87:1643-1648.
29. Ohgushi, M., K. Kugiyama, K. Fukunaga, T. Murohara, S. Sugiyama, E. Miyamoto, and H. Yasue. 1993. Protein kinase C inhibitors prevent impairment of endothelium-dependent relaxation by oxidatively modified LDL. Arteriosclerosis Thromb. 13:1525-1532.
30. Chung, B.H., J.P. Segrest, M.J. Ray, J.D. Brunzell, J.E. Hokanson, R.M. Krauss, K. Beaudrie, and J.T. Cone. 1986. Single vertical spin density gradient ultracentrifugation. Methods Enzymol. 128:181-209.
31. Lowry, O.H., N.J. Rosebrough, A.L. Farr, and R.J. Randall. 1951. Protein measured with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
32. 2-isoprostanes) in plasma and low-density lipoprotein exposed to oxidative stress in vitro. J. Clin. Invest. 93: 998-1004.
33. Stocker, R., V.W. Bowry, and B. Frei. 1991. Ubiquinol-10 protects human low density lipoprotein more efficiently against lipid peroxidation than does alpha-tocopherol. Proc. Natl. Acad. Sci. USA. 88:1646-1650.
34. Williams, B., and R.W. Schrier. 1992. Characterization of glucose-induced in situ protein kinase C activity in cultured vascular smooth muscle cells. Diabetes. 41:1464-1472.
35. Keaney, J.F., Jr., and B. Frei. 1994. Antioxidant protection of low-density lipoprotein and its role in the prevention of atherosclerotic vascular disease. In Natural Antioxidants in Human Health and Disease. B. Frei, editor. Academic Press, San Diego, 303-352.
36. Reid, V.C., and M.J. Mitchinson. 1993. Toxicity of oxidised low density lipoprotein towards mouse peritoneal macrophages in vitro. Atherosclerosis. 98: 17-24.
37. Mahoney, C.W., and A. Azzi. 1988. Vitamin E inhibits protein kinase C activity. Biochem. Biophys. Res. Commun. 154:694-697.
38. Chatelain, E., D.O. Boscoboinik, G.M. Bartoli, V.E. Kagan, F.K. Geiy, L. Packer, and A. Azzi. 1993. Inhibition of smooth muscle cell proliferation and protein kinase C activity by tocopherols and tocotrienols. Biochim. Biophys. Acta. 1176:83-89.
39. Raij, L., J. Jagy, K. Coffee, and E.G., DeMaster. 1993. Hypercholesterolemia promotes endothelial dysfunction in vitamin E- and selenium-deficient rats. Hypertension (Dallas). 22:55-61.
40. Andersson, T.L.G., J. Matz, G.A.A. Ferns, and E.E. Änggård. 1994. Vitamin E reverses cholesterol-induced endothelial dysfunction in the rabbit coronary circulation. Atherosclerosis. 111:39-45.
41. Stewart-Lee, A.L., L.A. Forster, J. Nourooz-Zadeh, G.A.A. Ferns, and E.E. Änggård. 1994. Vitamin E protects against impairment of endothelium-mediated relaxations in cholesterol-fed rabbits. Arteriosclerosis Thromb. 14: 494-499.
42. Sugiyama, S., K. Kugiyama, M. Ohgushi, K. Fujimoto, and H. Yasue. 1994. Lysophosphatidylcholine in oxidized low-density lipoprotein increases endothelial susceptibility to polymorphonuclear leukocyte-induced endothelial dysfunction in porcine coronary arteries: role of protein kinase C. Circ. Res. 74: 565-575.
43. Kunisaki, M., S.-E. Bursell, F. Umeda, H. Nawata, and G.L. King. 1994. Normalization of diacylglycerol-protein kinase C activation by vitamin E in aorta of diabetic rats and cultured rat smooth muscle cells exposed to elevated glucose levels. Diabetes. 43:1372-1377.
44. Castagna, M., M.Y. Takai, K. Kaibuchi, K. Sano, U. Kikkawa, and Y. Nishizuka. 1982. Direct activation of calcium-activated phospholipid-dependent protein kinase by tumor promoting phorbol esters. J. Biol. Chem. 257: 7847-7851.
45. Flavahan, N.A., H. Shimokawa, and P.M. Vanhoutte. 1991. Inhibition of endothelium-dependent relaxations by phorbol myristate acetate in canine coronary arteries: role of a pertussis toxin-sensitive G-protein. J. Pharmacol. Exp. Ther. 256:50-55.
46. Richardson, R.M., J. Ptasienski, and M.M. Hosey. 1992. Functional effects of protein kinase C-mediated phosphorylation of chick heart muscarinic cholinergic receptors. J. Biol. Chem. 267:10127-10132.
47. Bredt, D.S., C.G. Ferris, and S.H. Snyder. 1992. Nitric oxide synthase regulatory sites: phosphorylation by cyclic AMP-dependent protein kinase, protein kinase C, and calcium/calmodulin protein kinase; identification of flavin and calmodulin binding sites. J. Biol. Chem. 267:10976-10981.
48. Ohara, Y., H.S. Sayegh, J.J. Yamin, and D.G. Harrison. 1995. Regulation of endothelial constitutive nitric oxide synthase by protein kinase C. Hypertension (Dallas). 25:415-420.
49. Ohara, Y., T.E. Peterson, B. Zheng, J.F. Kuo, and D.G. Harrison. 1994. Lysophosphatidylcholine increases vascular superoxide anion production via protein kinase C activation. Arteriosclerosis Thromb. 14:1007-1013.
50. Boscoboinik, D., A. Szewczyk, and A. Azzi. 1991. Alpha-tocopherol (vitamin E) regulates vascular smooth muscle cell proliferation and protein kinase C activity. Arch. Biochem. Biophys. 286:264-269.
51. Rais, S., C. Combadiere, J. Hakin, and A. Perianan. 1994. Staurosporine up-regulates the expression of phorbol dibutyrate binding sites in human platelets. Biochem. Pharmacol. 47:1797-1804.