LDLs impair vasomotor function of the coronary microcirculation: Role of superoxide anions

Circulation Research

Volumn 83, Issue 4, 1998, Pages 404-414

  Hein, Travis W ^a   Kuo, Lih ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

Arteriole; Atherosclerosis; Endothelium; L arginine; Nitric oxide; Superoxide anion

Indexed keywords

ADENOSINE TRIPHOSPHATE; ARGININE; IONOMYCIN; LOW DENSITY LIPOPROTEIN; N(G) METHYLARGININE; NITRIC OXIDE; OXIDIZED LOW DENSITY LIPOPROTEIN; SEROTONIN; SUPEROXIDE;

ADOLESCENT; ANIMAL TISSUE; ARTERIOLE; ARTICLE; ATHEROSCLEROSIS; BLOOD VESSEL TONE; CORONARY ARTERY BLOOD FLOW; FEMALE; MALE; MICROCIRCULATION; NONHUMAN; PRIORITY JOURNAL; SWINE; VASCULAR ENDOTHELIUM; VASODILATATION; VASOMOTOR REFLEX;

EID: 0032563652     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.83.4.404     Document Type: Article

References (66)

1. Kannel WB. Contribution of the Framingham Study to preventive cardiology. J Am Coll Cardiol. 1990;15:206-211.
2. Ylä-Herttuala S, Palinski W, Rosenfeld ME, Parthasarathy S, Carew TE, Butler S, Witztum JL, Steinberg D. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J Clin Invest. 1989;84:1086-1095.
3. Quinn MT, Parthasarathy S, Fong LG, Steinberg D. Oxidatively modified low density lipoproteins: a potential role in recruitment and retention of monocyte/macrophages during atherogenesis. Proc Natl Acad Sci U S A. 1987;84:2995-2998.
4. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL. Beyond cholesterol: modifications of low-density lipoprotein that increase its atherogenicity. N Engl J Med. 1989;320:915-924.
5. Jacobs M, Plane F, Bruckdorfer KR. Native and oxidized low-density lipoproteins have different inhibitory effects on endothelium-derived relaxing factor in the rabbit aorta. Br J Pharmacol. 1990;100:21-26.
6. Tanner FC, Noll G, Boulanger CM, Lüscher TF. Oxidized low density lipoproteins inhibit relaxations of porcine coronary arteries: role of scavenger receptor and endothelium-derived nitric oxide. Circulation. 1991;83:2012-2020.
7. Palmer RMJ, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987;327:524-526.
8. Myers PR, Minor RL, Guerra R Jr, Bates JN, Harrison DG. Vasorelaxant properties of the endothelium-derived relaxing factor more closely resemble S-nitrosocysteine than nitric oxide. Nature. 1990;345:161-163.
9. Palmer RMJ, Rees DD, Ashton DS, Moncada S. L-Arginine is the physiological precursor for the formation of nitric oxide in endothelium-dependent relaxation. Biochem Biophys Res Commun. 1988;153: 1251-1256.
10. Radomski MW, Palmer RMJ, Moncada S. An L-arginine/nitric oxide pathway present in human platelets regulates aggregation. Proc Natl Acad Sci U S A. 1990;87:5193-5197.
11. Garg UC, Hassid A. Nitric oxide-generating vasodilators and 8-bromocyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest. 1989;83: 1774-1777.
12. Kubes P, Suzuki M, Granger DN. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci U S A. 1991;88:4651-4655.
13. Galle J, Bauersachs J, Busse R, Bassenge E. Inhibition of cyclic AMP- and cyclic GMP-mediated dilations in isolated arteries by oxidized low density lipoproteins. Arterioscler Thromb. 1992;12:180-186.
14. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801-809.
15. Kuo L, Davis MJ, Cannon MS, Chilian WM. Pathophysiological consequences of atherosclerosis extend into the coronary microcirculation: restoration of endothelium-dependent responses by L-arginine. Circ Res. 1992;70:465-476.
16. Chilian WM, Dellsperger KC, Layne SM, Eastham CL, Armstrong MA, Marcus ML, Heistad DD. Effects of atherosclerosis on the coronary microcirculation. Am J Physiol. 1990;258:H529-H539.
17. Chilian WM, Eastham CL, Marcus ML. Microvascular distribution of coronary vascular resistance in beating left ventricle. Am J Physiol. 1986;251:H779-H788.
18. Kuo L, Davis MJ, Chilian WM. Myogenic activity in isolated subepicardial and subendocardial coronary arterioles. Am J Physiol. 1988;255: H1558-H1562.
19. Kuo L, Chilian WM, Davis MJ. Interaction of pressure- and flow-induced responses in porcine coronary resistance vessels. Am J Physiol. 1991;261: H1706-H1715.
20. Kuo L, Davis MJ, Chilian WM. Endothelium-dependent, flow-induced dilation of isolated coronary arterioles. Am J Physiol. 1990;259: H1063-H1070.
21. Esterbauer H, Striegl G, Puhl H, Rotheneder M. Continuous monitoring of in vitro oxidation of human low density lipoprotein. Free Radic Res Commun. 1989;6:67-75.
22. Chait A. Methods for assessing lipid and lipoprotein oxidation. Curr Opin Lipidol. 1992;3:389-394.
23. Markwell MAK, Haas SM, Tolbert NE, Bieber LL. Protein determination in membrane and lipoprotein samples: manual and automated procedures. Methods Enzymol. 1981;72:296-303.
24. Stork AP, Cocks TM. Pharmacological reactivity of human epicardial coronary arteries: characterization of relaxation responses to endothelium-derived relaxing factor. Br J Pharmacol. 1994;113:1099-1104.
25. Ignarro LJ. Biological actions and properties of endothelium-derived nitric oxide formed and released from artery and vein. Circ Res. 1989; 65:1-21.
26. Krishna CM, Liebmann JE, Kaufman D, DeGraff W, Hahn SM, McMurry T, Mitchell JB, Russo A. The catecholic metal sequestering agent 1,2-dihydroxybenzene-3,5-disulfonate confers protection against oxidative cell damage. Arch Biochem Biophys. 1992;294:98-106.
27. Münzel T, Sayegh H, Freeman BA, Tarpey MM, Harrison DG. Evidence for enhanced vascular superoxide anion production in nitrate tolerance: a novel mechanism underlying tolerance and cross-tolerance. J Clin Invest. 1995;95:187-194.
28. Kaminski PM, Wolin MS. Hypoxia increases superoxide anion production from bovine coronary microvessels, but not cardiac myocytes, via increased xanthine oxidase. Microcirculation. 1996;1:231-236.
29. Palinski W, Rosenfeld ME, Ylä-Herttuala S, Gurtner GC, Socher SS, Butler SW, Parthasarathy S, Carew TE, Steinberg D, Witztum JL. Low density lipoprotein undergoes oxidative modification in vivo. Proc Natl Acad Sci U S A. 1989;86:1372-1376.
30. Hodis HN, Kramsch DM, Avogaro P, Bittolo-Bon G, Cazzolato G, Hwang J, Peterson H, Sevanian A. Biochemical and cytotoxic characteristics of an in vivo circulating oxidized low density lipoprotein (LDL-). J Lipid Res. 1994;35:669-677.
31. Hammer A, Kager G, Dohr G, Rabl H, Ghassempur I, Jürgens G. Generation, characterization, and histochemical application of monoclonal antibodies selectively recognizing oxidatively modified apoB-containing serum lipoproteins. Arterioscler Thromb Vasc Biol. 1995;15: 704-713.
32. Plane F, Bruckdorfer KR, Kerr P, Steuer A, Jacobs M. Oxidative modification of low-density lipoproteins and the inhibition of relaxations mediated by endothelium-derived nitric oxide in rabbit aorta. Br J Pharmacol. 1992;105:216-222.
33. Heitzer T, Ylä-Herttuala S, Luoma J, Kurz S, Münzel T, Just H, Olschewski M, Drexler H. Cigarette smoking potentiates endothelial dysfunction of forearm resistance vessels in patients with hypercholesterolemia: role of oxidized LDL. Circulation. 1996;93:1346-1353.
34. Rangaswamy S, Penn MS, Saidel GM, Chisolm GM. Exogenous oxidized low-density lipoprotein injures and alters the barrier function of endothelium in rats in vivo. Circ Res. 1997;80:37-44.
35. Simon BC, Cunningham LD, Cohen RA. Oxidized low density lipoproteins cause contraction and inhibit endothelium-dependent relaxation in the pig coronary artery. J Clin Invest. 1990;86:75-79.
36. Abebe W, Mustafa SJ. Effect of low density lipoprotein on adenosine receptor-mediated coronary vasorelaxation in vitro. J Pharmacol Exp Ther. 1997;282:851-857.
37. Richard V, Tanner FC, Tschudi M, Lüscher TF. Different activation of L-arginine pathway by bradykinin, serotonin, and clonidine in coronary arteries. Am J Physiol. 1990;259:H1433-H1439.
38. White TD, Angus JA. Relaxant effects of ATP and adenosine on canine large and small coronary arteries in vitro. Eur J Pharmacol. 1987;143: 119-126.
39. Hein TW, Kuo L. Oxidized LDL specifically impairs nitric oxide-mediated dilation of coronary arterioles. Circulation. 1997;96(suppl II): 1-114. Abstract.
40. Ishizaka H, Kuo L. Endothelial ATP-sensitive potassium channels mediate coronary microvascular dilation to hyperosmolarity. Am J Physiol. 1997;273:H104-H112.
41. Shimokawa H, Flavahan NA, Vanhoutte PM. Loss of endothelial pertussis toxin-sensitive G protein function in atherosclerotic porcine coronary arteries. Circulation. 1991;83:652-660.
42. Bossaller C, Habib GB, Yamamoto H, Williams C, Wells S, Henry PD. Impaired muscarinic endothelium-dependent relaxation and cyclic guanosine 5′-monophosphate formation in atherosclerotic human coronary artery and rabbit aorta. J Clin Invest. 1987;79:170-174.
43. Flavahan NA. Atherosclerosis or lipoprotein-induced endothelial dysfunction: potential mechanisms underlying reduction in EDRF/nitric oxide activity. Circulation. 1992;85:1927-1938.
44. Galle J, Mülsch A, Busse R, Bassenge E. Effects of native and oxidized low density lipoproteins on formation and inactivation of endothelium-derived relaxing factor. Arterioscler Thromb. 1991;11:198-203.
45. Mombouli J-V, Bissiriou I, Agboton V, Vanhoutte PM. Endothelium-derived hyperpolarizing factor: a key mediator of the vasodilator action of bradykinin. Immunopharmacology. 1996;33:46-50.
46. Mombouli J-V, Bissiriou I, Agboton VD, Vanhoutte PM. Bioassay of endothelium-derived hyperpolarizing factor. Biochem Biophys Res Commun. 1996;221:484-488.
47. Osborne JA, Lento PH, Siegfried MR, Stahl GL, Fusman B, Lefer AM. Cardiovascular effects of acute hypercholesterolemia in rabbits: reversal with lovastatin treatment. J Clin Invest. 1989;83:465-473.
48. Anderson TJ, Meredith IT, Yeung AC, Frei B, Selwyn AP, Ganz P. The effect of cholesterol-lowering and antioxidant therapy on endothelium-dependent coronary vasomotion. N Engl J Med. 1995;332:488-493.
49. Rossitch E Jr, Alexander E III, Black PM, Cooke JP. L-Arginine normalizes endothelial function in cerebral vessels from hypercholesterolemic rabbits. J Clin Invest. 1991;87:1295-1299.
50. Creager MA, Gallagher SJ, Girerd XJ, Coleman SM, Dzau VJ, Cooke JP. L-Arginine improves endothelium-dependent vasodilation in hypercholesterolemic humans. J Clin Invest. 1992;90:1248-1253.
51. Drexler H, Zeiher AM, Meinzer K, Just H. Correction of endothelial dysfunction in coronary microcirculation of hypercholesterolaemic patients by L-arginine. Lancet. 1991;338:1546-1550.
52. Nakaki T, Kata R. Beneficial circulatory effect of L-arginine. Jpn J Pharmacol. 1994;66:167-171.
53. Pollock JS, Förstermann U, Mitchell JA, Warner TD, Schmidt HHHW, Nakane M, Murad F. Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc Natl Acad Sci U S A. 1991;88: 10480-10484.
54. Amezcua JL, Palmer RMJ, de Souza BM, Moncada S. Nitric oxide synthesized from L-arginine regulates vascular tone in the coronary circulation of the rabbit. Br J Pharmacol. 1989;97:1119-1124.
55. Pou S, Pou WS, Bredt DS, Snyder SH, Rosen GM. Generation of superoxide by purified brain nitric oxide synthase. J Biol Chem. 1992; 267:24173-24176.
56. 2+/calmodulin-dependent formation of hydrogen peroxide by brain nitric oxide synthase. Biochem J. 1992;281:627-630.
57. Pritchard KA Jr, Groszek L, Smalley DM, Sessa WC, Wu M, Villalon P, Wolin MS, Stemerman MB. Native low-density lipoprotein increases endothelial cell nitric oxide synthase generation of superoxide anion. Circ Res. 1995;77:510-518.
58. Ohara Y, Peterson TE, Harrison DG. Hypercholesterolemia increases endothelial superoxide anion production. J Clin Invest. 1993;91:2546-2551.
59. Maeba R, Maruyama A, Tarutani O, Ueta N, Shimasaki H. Oxidized low-density lipoprotein induces the production of superoxide by neutrophils. FEBS Lett. 1995;377:309-312.
60. Gryglewski RJ, Palmer RMJ, Moncada S. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature. 1986;320:454-456.
61. Ohara Y, Peterson TE, Sayegh HS, Subramanian RR, Wilcox JN, Harrison DG. Dietary correction of hypercholesterolemia in the rabbit normalizes endothelial superoxide anion production. Circulation. 1995; 92:898-903.
62. White CR, Brock TA, Chang L-Y, Crapo J, Briscoe P, Ku D, Bradley WA, Gianturco SH, Gore J, Freeman BA, Tarpey MM. Superoxide and peroxynitrite in atherosclerosis. Proc Natl Acad Sci U S A. 1994;91: 1044-1048.
63. Hecker M, Sessa WC, Harris HJ, Änggård EE, Vane JR. The metabolism of L-arginine and its significance for the biosynthesis of endothelium-derived relaxing factor: cultured endothelial cells recycle L-citrulline to L-arginine. Proc Natl Acad Sci U S A. 1990;87:8612-8616.
64. Böger RH, Bode-Böger SM, Mügge A, Kienke S, Brandes R, Dwenger A, Frölich JC. Supplementation of hypercholesterolaemic rabbits with L-arginine reduces the vascular release of superoxide anions and restores NO production. Atherosclerosis. 1995;117:273-284.
65. Keaney JF Jr, Xu A, Cunningham D, Jackson T, Frei B, Vita JA. Dietary probucol preserves endothelial function in cholesterol-fed rabbits by limiting vascular oxidative stress and superoxide generation. J Clin Invest. 1995;95:2520-2529.
66. Levine GN, Frei B, Koulouris SN, Gerhard MD, Keaney JF Jr, Vita JA. Ascorbic acid reverses endothelial vasomotor dysfunction in patients with coronary artery disease. Circulation. 1996;93:1107-1113.