Hypercholesterolemia promotes inflammation and microvascular dysfunction: Role of nitric oxide and superoxide

Free Radical Biology and Medicine

Volumn 33, Issue 8, 2002, Pages 1026-1036

  Stokes, Karen Y ^a   Cooper, Dianne ^a   Tailor, Anitaben ^a   Granger, D Neil ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Adhesion molecules; Free radicals; Leukocyte endothelial cell adhesion; Low density lipoproteins; Nitric oxide; Platelets; Reactive oxygen species

Indexed keywords

CHOLESTEROL; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

ARTERIOLE; BIOAVAILABILITY; BIOSYNTHESIS; CAPILLARY PERMEABILITY; CELL LINE; ENDOTHELIUM; HYPERCHOLESTEROLEMIA; INFLAMMATION; ISCHEMIA; LEUKOCYTE; MICROCIRCULATION; MICROVASCULATURE; MORTALITY; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; REVIEW; TREATMENT INDICATION; VASCULAR DISEASE; VASODILATATION; VENULE;

EID: 0037108203     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(02)01015-8     Document Type: Article

References (51)

1. Ross R. Atherosclerosis an inflammatory disease . N. Engl. J. Med. 340:1999;115-126.
2. Scalia R., Appel J.Z. III, Lefer A.M. Leukocyte-endothelium interaction during the early stages of hypercholesterolemia in the rabbit role of P-selectin, ICAM-1, and VCAM-1 . Arterioscler. Thromb. Vasc. Biol. 18:1998;1093-1100.
3. Stokes K.Y., Clanton E.C., Russell J.M., Ross C.R., Granger D.N. NAD(P)H oxidase-derived superoxide mediates hypercholesterolemia-induced leukocyte-endothelial cell adhesion. Circ. Res. 88:2001;499-505.
4. Tailor A., Granger D.N. Acute hypercholesterolemia and ischemia/reperfusion-induced blood cell-endothelial cell adhesion in the murine mesenteric vascular bed. FASEB J. 15:2001;A35. (abstract).
5. Granger D.N. Ischemia/reperfusion mechanisms of microvascular dysfunction and the influence of risk factors for cardiovascular disease . Microcirculation. 6:1999;167-178.
6. Lehr H.A., Olofsson A.M., Carew T.E., Vajkoczy P., von Andrian U.H., Hubner C., Berndt M.C., Steinberg D., Messmer K., Arfors K.E. P-selectin mediates the interaction of circulating leukocytes with platelets and microvascular endothelium in response to oxidized lipoprotein in vivo. Lab. Invest. 71:1994;380-386.
7. Vink H., Constantinescu A.A., Spaan J.A. Oxidized lipoproteins degrade the endothelial surface layer implications for platelet-endothelial cell adhesion . Circulation. 101:2000;1500-1502.
8. Takahashi K., Ohyanagi M., Ikeoka K., Iwasaki T. Acetylcholine-induced response of coronary resistance arterioles in cholesterol-fed rabbits. Jpn. J. Pharmacol. 81:1999;156-162.
9. Gilligan D.M., Guetta V., Panza J.A., Garcia C.E., Quyyumi A.A., Cannon R.O. III. Selective loss of microvascular endothelial function in human hypercholesterolemia. Circulation. 90:1994;35-41.
10. Napoli C., Lerman L.O. Involvement of oxidation-sensitive mechanisms in the cardiovascular effects of hypercholesterolemia. Mayo Clin. Proc. 76:2001;619-631.
11. Lehr H.A., Krober M., Hubner C., Vajkoczy P., Menger M.D., Nolte D., Kohlschutter A., Messmer K. Stimulation of leukocyte/endothelium interaction by oxidized low-density lipoprotein in hairless mice. Involvement of CD11b/CD18 adhesion receptor complex. Lab. Invest. 68:1993;388-395.
12. Eriksson E.E., Xie X., Werr J., Thoren P., Lindbom L. Direct viewing of atherosclerosis in vivo plaque invasion by leukocytes is initiated by the endothelial selectins . FASEB J. 15:2001;1149-1157.
13. Haak E., Abletshauser C., Weber S., Goedicke C., Martin N., Hermanns N., Lackner K., Kusterer K., Usadel K.H., Haak T. Fluvastatin therapy improves microcirculation in patients with hyperlipidemia. Atherosclerosis. 155:2001;395-401.
14. Kohno M., Murakawa K., Yasunari K., Yokokawa K., Horio T., Kano H., Minami M., Yoshikawa J. Improvement of erythrocyte deformability by cholesterol-lowering therapy with pravastatin in hypercholesterolemic patients. Metabolism. 46:1997;287-291.
15. Mori N., Horie Y., Nimura Y., Wolf R., Granger D.N. Hepatic microvascular responses to ischemia/reperfusion in low-density lipoprotein receptor knockout mice. Am. J. Physiol. Gastrointest. Liver Physiol. 279:2000;G1257-G1264.
16. Gauthier T.W., Scalia R., Murohara T., Guo J.P., Lefer A.M. Nitric oxide protects against leukocyte-endothelium interactions in the early stages of hypercholesterolemia. Arterioscler. Thromb. Vasc. Biol. 15:1995;1652-1659.
17. Kurtel H., Liao L., Grisham M.B., Tso P., Aw T.Y., Anderson D.C., Miyasaka M., Granger D.N. Mechanisms of oxidized chylomicron-induced leukocyte-endothelial cell adhesion. Am. J. Physiol. 268:1995;H2175-H2182.
18. Steinberg H.O., Bayazeed B., Hook G., Johnson A., Cronin J., Baron A.D. Endothelial dysfunction is associated with cholesterol levels in the high normal range in humans. Circulation. 96:1997;3287-3293.
19. Babior B.M. NADPH oxidase an update . Blood. 93:1999;1464-1476.
20. Ohara Y., Peterson T.E., Sayegh H.S., Subramanian R.R., Wilcox J.N., Harrison D.G. Dietary correction of hypercholesterolemia in the rabbit normalizes endothelial superoxide anion production. Circulation. 92:1995;898-903.
21. Landmesser U., Hornig B., Drexler H. Endothelial dysfunction in hypercholesterolemia mechanisms, pathophysiological importance, and therapeutic interventions . Semin. Thromb. Hemost. 26:2000;529-537.
22. Vergnani L., Hatrik S., Ricci F., Passaro A., Manzoli N., Zuliani G., Brovkovych V., Fellin R., Malinski T. Effect of native and oxidized low-density lipoprotein on endothelial nitric oxide and superoxide production key role of L-arginine availability . Circulation. 101:2000;1261-1266.
23. Cosentino F., Katusic Z.S. Tetrahydrobiopterin and dysfunction of endothelial nitric oxide synthase in coronary arteries. Circulation. 91:1995;139-144.
24. Napoli C., Ignarro L.J. Nitric oxide and atherosclerosis. Nitric Oxide. 5:2001;88-97.
25. Kuhlencordt P.J., Chen J., Han F., Astern J., Huang P.L. Genetic deficiency of inducible nitric oxide synthase reduces atherosclerosis and lowers plasma lipid peroxides in apolipoprotein E knockout mice. Circulation. 103:2001;3099-3104.
26. Kurose I., Wolf R., Grisham M.B., Granger D.N. Effects of an endogenous inhibitor of nitric oxide synthesis on postcapillary venules. Am. J. Physiol. 268:1995;H2224-H2231.
27. Böger R.H., Bode-Böger S.M., Mügge A., Kienke S., Brandes R., Dwenger A., Frölich J.C. Supplementation of hypercholesterolemic rabbits with L-arginine reduces the vascular release of superoxide anions and restores NO production. Atherosclerosis. 117:1995;273-284.
28. Yu X.J., Li Y.J., Xiong Y. Increase of an endogenous inhibitor of nitric oxide synthesis in serum of high cholesterol fed rabbits. Life Sci. 54:1994;753-758.
29. Jiang J.L., Li N.S., Li Y.J., Deng H.W. Probucol preserves endothelial function by reduction of the endogenous nitric oxide synthase inhibitor level. Br. J. Pharmacol. 135:2002;1175-1782.
30. Böger R.H., Bode-Böger S.M., Tsao P.S., Lin P.S., Chan J.R., Cooke J.P. An endogenous inhibitor of nitric oxide synthase regulates endothelial adhesiveness for monocytes. J. Am. Coll. Cardiol. 36:2000;2287-2295.
31. Harrison D.G. Cellular and molecular mechanisms of endothelial cell dysfunction. J. Clin. Invest. 100:1997;2153-2157.
32. Guzik T.J., West N.E., Black E., McDonald D., Ratnatunga C., Pillai R., Channon K.M. Vascular superoxide production by NAD(P)H oxidase association with endothelial dysfunction and clinical risk factors . Circ. Res. 86:2000;E85-E90.
33. Laufs U., Endres M., Custodis F., Gertz K., Nickenig G., Liao J.K., Bohm M. Suppression of endothelial nitric oxide production after withdrawal of statin treatment is mediated by negative feedback regulation of rho GTPase gene transcription. Circulation. 102:2000;3104-3110.
34. Takemoto M., Liao J.K. Pleiotropic effects of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors. Arterioscler. Thromb. Vasc. Biol. 21:2001;1712-1719.
35. Lefer A.M., Scalia R., Lefer D.J. Vascular effects of HMG CoA-reductase inhibitors (statins) unrelated to cholesterol lowering new concepts for cardiovascular disease . Cardiovasc. Res. 49:2001;281-287.
36. Liao L., Granger D.N. Modulation of oxidized low-density lipoprotein-induced microvascular dysfunction by nitric oxide. Am. J. Physiol. 268:1995;H1643-H1650.
37. Collins T., Read M.A., Neish A.S., Whitley M.Z., Thanos D., Maniatis T. Transcriptional regulation of endothelial cell adhesion molecules NF-κB and cytokine-inducible enhancers . FASEB J. 9:1995;899-909.
38. De Caterina R., Libby P., Peng H.B., Thannickal V.J., Rajavashisth T.B., Gimbrone M.A. Jr, Shin W.S., Liao J.K. Nitric oxide decreases cytokine-induced endothelial activation. Nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J. Clin. Invest. 96:1995;60-68.
39. Spiecker M., Liao J.K. Assessing induction of IκB by nitric oxide. Methods Enzymol. 300:1999;374-388.
40. Niebauer J., Dulak J., Chan J.R., Tsao P.S., Cooke J.P. Gene transfer of nitric oxide synthase effects on endothelial biology . J. Am. Coll. Cardiol. 34:1999;1201-1207.
41. Weber C., Erl W., Pietsch A., Strobel M., Ziegler-Heitbrock H.W., Weber P.C. Antioxidants inhibit monocyte adhesion by suppressing nuclear factor-κB mobilization and induction of vascular cell adhesion molecule-1 in endothelial cells stimulated to generate radicals. Arterioscler. Thromb. 14:1994;1665-1673.
42. Matthews J.R., Botting C.H., Panico M., Morris H.R., Hay R.T. Inhibition of NF-κB DNA binding by nitric oxide. Nucl. Acids Res. 24:1996;2236-2242.
43. Cerwinka W.H., Granger D.N. Influence of hypercholesterolemia and hypertension on ischemia/reperfusion-induced P-selectin expression. Atherosclerosis. 154:2001;337-344.
44. Roselaar S.E., Kakkanathu P.X., Daugherty A. Lymphocyte populations in atherosclerotic lesions of apoE -/- and LDL receptor -/- mice. Decreasing density with disease progression. Arterioscler. Thromb. Vasc. Biol. 16:1996;1013-1018.
45. de Boer O.J., van der Wal A.C., Verhagen C.E., Becker A.E. Cytokine secretion profiles of cloned T cells from human aortic atherosclerotic plaques. J. Pathol. 188:1999;174-179.
46. Hansson G.K. Immune mechanisms in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 21:2001;1876-1890.
47. Fyfe A.I., Qiao J.H., Lusis A.J. Immune-deficient mice develop typical atherosclerotic fatty streaks when fed an atherogenic diet. J. Clin. Invest. 94:1994;2516-2520.
48. Song L., Leung C., Schindler C. Lymphocytes are important in early atherosclerosis. J. Clin. Invest. 108:2001;251-259.
49. Berton G., Zeni L., Cassatella M.A., Rossi F. Gamma interferon is able to enhance the oxidative metabolism of human neutrophils. Biochem. Biophys. Res. Commun. 138:1986;1276-1282.
50. Clements K.P., Stokes K.Y., Clanton E.C., Granger D.N. Interferon-γ contributes to hypercholesterolemia-induced leukocyte-endothelial cell adhesion. (abstract). FASEB J. 15:2001;A120.
51. Laurat E., Poirier B., Tupin E., Caligiuri G., Hansson G.K., Bariety J., Nicoletti A. In vivo downregulation of T helper cell 1 immune responses reduces atherogenesis in apolipoprotein E knockout mice. Circulation. 104:2001;197-202.