NOS inhibition accelerates atherogenesis: Reversal by exercise

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 285, Issue 2 54-2, 2003, Pages

  Niebauer, Josef ^a,b   Maxwell, Andrew J ^a   Lin, Patrick S ^a   Wang, David ^a   Tsao, Philip S ^a   Cooke, John P ^a,c  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apolipoprotein E deficiency; Atherosclerotic lesions; NG nitro L arginine; Nitric oxide; Treadmill

Indexed keywords

CHOLESTEROL; CITRATE SYNTHASE; N(G) NITROARGININE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; EXERCISE; FEMALE; HISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TREADMILL EXERCISE; WESTERN BLOTTING;

EID: 0038299405     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.00360.2001     Document Type: Article

References (53)

1. Allain CC, Poon LS, Chan CS, Richmond W, and Fu PC. Enzymatic determination of total serum cholesterol. Clin Chem 20: 470-475, 1974.
2. Bath PMW, Hassall DG, Gladwin AM, Palmer RMJ, and Martin JF. Nitric oxide and prostacyclin. Divergence of inhibitory effects on monocyte chemotaxis and adhesion to endothelium in vitro. Arterioscler Thromb 11: 254-260, 1991.
3. Bauersachs J, Popp R, Hecker M, Sauer E, Fleming I, and Busse R. Nitric oxide attenuates the release of endothelium-derived hyperpolarizing factor. Circulation 94: 3341-3347, 1996.
4. Berdeaux A, Ghaleh B, Dubois-Rande JL, Vigue B, Drieu La Rochelle C, Hittinger L, and Giudicelli JF. Role of vascular endothelium in exercise-induced dilation of large epicardial coronary arteries in conscious dogs. Circulation 89: 2799-2808, 1994.
5. Böger RH, Bode-Böger SM, Brandes RP, Phivthong-ngam L, Böhme M, Nafe R, Mügge A, and Frölich JC. Dietary L-arginine reduces the progression of atherosclerosis in cholesterol-fed rabbits: comparison with lovastatin. Circulation 96: 1282-1290, 1997.
6. Böger RH, Bode-Böger SM, Mugge A, Kienke S, Brandes R, Dwenger A, and Fröhlich JC. Supplementation of hypercholesterolaemic rabbits with L-arginine reduces the vascular release of superoxide anions and restores NO production. Atherosclerosis 117: 273-284, 1995.
7. Böger RH, Bode-Böger SM, Szuba A, Tsao PS, Chan JR, Tangphao O, Blaschke TF, and Cooke JP. Asymmetric dimethylarginine (ADMA): a novel risk factor for endothelial dysfunction. Its role in hypercholesterolemia. Circulation 98: 1842-1847, 1998.
8. Candipan RC, Wang B-y, Buitrago R, Tsao PS, and Cooke JP. Regression or progression: dependency on vascular nitric oxide. Arterioscler Thromb Vasc Biol 16: 44-50, 1996.
9. Cayatte AJ, Palacino JJ, Horten K, and Cohen RA. Chronic inhibition of nitric oxide production accelerates neoimtima formation and impairs endothelial function in hypercholesterolemic rabbits. Arterioscler Thromb 4: 753-759, 1994.
10. Chan JR, Böger RH, Bode-Böger SM, Tangphao O, Tsao PS, Blaschke TF, and Cooke JP. Asymmetric dimethylarginine increases mononuclear cell adhesiveness in hypercholesterolemic humans. Arterioscler Thromb Vasc Biol 20: 1040-1046, 2000.
11. Clancy RM, Leszczynska P, Piziak J, and Abramson SB. Nitric oxide, an endothelial cell relaxation factor, inhibits neutrophil superoxide anion production via a direct action on NADPH oxidase. J Clin Invest 90: 1116-1121, 1992.
12. Frangos JA, Eskin SG, McIntire LV, and Ives CL. Flow effects on prostacyclin production by cultured human endothelial cells. Science 227: 1477-1479, 1985.
13. Garg UC and 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 83: 1774-1777, 1989.
14. Gimbrone MA Jr, Resnick N, Nagel T, Khachigian LM, Collins T, and Topper JN. Hemodynamics, endothelial gene expression, and atherogenesis. Ann NY Acad Sci 811: 1-10, 1997.
15. Grabowski EF, Jaffe EA, and Weksler BB. Prostacyclin production by cultured endothelial cell monolayers exposed to step increases in shear stress. J Lab Clin Med 105: 36-43, 1985.
16. Hajjar DP. Prostaglandins and cyclic nucleotides: modulators of arterial cholesterol metabolism. Biochem Pharmacol 34: 295-300, 1985.
17. Hambrecht R, Wolf A, Gielen S, Linke A, Hofer J, Erbs S, Schoene N, and Schuler G. Effect of exercise on coronary endothelial function in patients with coronary artery disease. N Engl J Med 342: 454-460, 2000.
18. Haskell WL, Alderman EL, Fair JM, Maron DJ, Mackey SF, Superko HR, Williams PT, Johnstone IM, Champagne MA, Krauss RM, and Farquhar JW. Effects of intensive multiple risk factor reduction on coronary atherosclerosis and clinical cardiac events in men and women with coronary artery disease. The Stanford Coronary Risk Intervention Project (SCRIP). Circulation 89: 975-990, 1994.
19. Haskell WL, Sims C, Myll J, Bortz WM, St. Goar FG, and Alderman EL. Coronary artery size and dilating capacity in ultra-distance runners. Circulation 87: 1076-1082, 1993.
20. Higgs EA, Moncada S, Vane JR, Caen JP, Michel H, and Tobelem G. Effect of prostacyclin (PG12) on platelet adhesion to rabbit arterial subendothelium. Prostaglandins 16: 17-22, 1978.
21. Inoue NRS, Fukai T, Nerem RM, and Harrison DG. Shear stress modulates expression of Cu/Zn superoxide dismutase in human aortic endothelial cells. Circ Res 79: 32-37, 1996.
22. Kauser K, da Cunha V, Fitch R, Mallari C, and Rubanyi GM. Role of endogenous nitric oxide in progression of atherosclerosis in apolipoprotein E-deficient mice. Am J Physiol Heart Circ Physiol 278: H1679-H1685, 2000.
23. Koller A, Huang A, Sun D, and Kaley G. Exercise training augments flow-dependent dilation in rat skeletal muscle arterioles: role of endothelial nitric oxide and prostaglandins. Circ Res 76: 544-550, 1995.
24. Koller A and Kaley G. Prostaglandins mediate arteriolar dilation to increased blood flow velocity in skeletal muscle microcirculation. Circ Res 67: 529-534, 1990.
25. Lawn RM, Wade DP, Hammer RE, Chiesa G, Verstuyft JG, and Rubin EM. Atherogenesis in transgenic mice expressing human apolipoprotein (a). Nature 360: 670-672, 1992.
26. Maxwell AJ, Schauble E, Bernstein D, and Cooke JP. Limb blood flow during exercise is dependent on nitric oxide. Circulation 98: 369-74, 1998.
27. Nagel T, Resnick N, Atkinson WJ, Dewey CF Jr, and Gimbrone MA Jr. Shear stress selectively upregulates intercellular adhesion molecule-1 expression in cultured human vascular endothelial cells. J Clin Invest 94: 885-891, 1994.
28. Naruse K, Shimizu K, Muramatsu M, Toki Y, Miyazaki Y, Okumura K, Hashimoto H, and Ito T. Prostaglandin H2 does not contribute to impaired endothelium-dependent relaxation, and long-term inhibition of nitric oxide synthesis promotes atherosclerosis in hypercholesterolemic rabbit thoracic aorta. Arterioscler Thromb 14: 746-752, 1994.
29. Niebauer J and Cooke JP. Cardiovascular effects of exercise: role of endothelial shear stress. J Am Coll Cardiol 28: 1652-1660, 1996.
30. Niebauer J, Dulak J, Chan JR, Tsao PS, and Cooke JP. Gene transfer of nitric oxide synthase: effects on endothelial biology. J Am Coll Cardiol 34: 1201-1207, 1999.
31. Niebauer J, Hambrecht R, Velich T, Hauer K, Marburger C, Kälberer B, Weiss C, von Hodenberg E, Schlierf G, Schuler G, Zimmermann R, and Kübler W. Attenuated progression of coronary artery disease after 6 years of multifactorial risk intervention: role of physical exercise. Circulation 96: 2534-2541, 1997.
32. Niebauer J, Maxwell AJ, Lin PS, Tsao PS, Kosek J, Bernstein D, and Cooke JP. Impaired aerobic capacity in hypercholesterolemic mice: partial reversal by exercise training. Am J Physiol Heart Circ Physiol 276: H1346-H1354, 1999.
33. Niebauer J, Schwarzacher SP, Hayase M, Wang B, Kernoff RS, Cooke JP, and Yeung AC. Local L-arginine delivery after balloon angioplasty reduces monocyte binding and induces apoptosis. Circulation 100: 1830-1835, 1999.
34. Ornish D, Brown SE, Scherwitz LW, Billings JH, Armstrong WT, Ports TA, McLanahan SM, Kirkeeide RL, Brand R, and Gould KI. Can lifestyle changes reverse coronary heart disease? Lancet 336: 129-133, 1990.
35. Paigen B, Ishida BY, Verstuyft J, Winters RB, and Albee D. Arteriosclerosis susceptibility differences among progenitors of recombinant inbred strains of mice. Arteriosclerosis 10: 316-323, 1990.
36. Paigen B, Morrow A, Holmes PA, Mitchell D, and Williams RA. Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis 68: 231-240, 1987.
37. Piedrahita JA, Zhang SH, Hagaman JR, Oliver PM, and Maeda N. Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc Natl Acad Sci USA 89: 4471-4475, 1992.
38. Plump AS, Smith JD, Hayeck T, Aalto-Setälä K, Walsh A, Verstuyft JG, Rubin EM, and Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 71: 343-353, 1992.
39. Resnick N, Collins T, Atkinson W, Bonthron DT, Dewey CF Jr, and Gimbrone MA Jr. Platelet-derived growth factor B chain promoter contains a cis-acting fluid shear-stress-responsive element. Proc Natl Acad Sci USA 90: 4591-4595, 1993.
40. Resnick N and Gimbrone MA Jr. Hemodynamic forces are complex regulators of endothelial gene expression. FASEB J 9: 874-882, 1995.
41. Sessa WC, Pritchard K, Seyedi N, Wang J, and Hintze TH. Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide synthase gene expression. Circ Res 74: 349-353, 1994.
42. Srere PA. Citrate synthase. Methods Enzymol 13: 3-5, 1969.
43. Tsao PS, Buitrago R, Chan JR, and Cooke JP. Fluid flow inhibits endothelial adhesiveness. Nitric oxide and transcriptional replication of VCAM-1. Circulation 94: 1682-1689, 1996.
44. Tsao PS, McEvoy Drexler HD, Butcher EC, and Cooke JP. Enhanced endothelial adhesiveness in hypercholesterolemia is attenuated by L-arginine. Circulation 89: 2176-2182, 1994.
45. Tsao PS, Wang B, Buitrago R, Shyy JY, and Cooke JP. Nitric oxide regulates monocyte chemotactic protein-1. Circulation 96: 934-940, 1997.
46. Uematsu M, Ohara Y, Navas JP, Nishida K, Murphy TJ, Alexander RW, Nerem RM, and Harrison DG. Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress. Am J Physiol Cell Physiol 269: C1371-C1378, 1995.
47. Wang B, Singer AH, Tsao P, Drexler H, Kosek J, and Cooke JP. Dietary arginine prevents atherogenesis in the coronary artery of the hypercholesterolemic rabbit. J Am Coll Cardiol 23: 452-458, 1994.
48. Wang BY, Ho HK, Lin PS, Schwarzacher SP, Pollman MJ, Gibbons GH, Tsao PS, and Cooke JP. Regression of atherosclerosis: role of nitric oxide and apoptosis. Circulation 99: 1236-1241, 1999.
49. Wang J, Wolin MS, and Hintze TH. Chronic exercise enhances endothelium-mediated dilation of epicardial coronary artery in conscious dogs. Circ Res 73: 829-838, 1993.
50. Willis AL, Smith DL, Vigo C, and Kluge AF. Effects of prostacyclin and orally stable mimetic agent RS-93427-007 on basic mechanisms of atherogenesis. Lancet 2: 682-683, 1986.
51. Wolf A, Zalpour C, Theilmeier G, Wang BY, Ma A, Anderson B, Tsao PS, and Cooke JP. Dietary L-arginine supplementation normalized platelet aggregation in hypercholesterolemic humans. J Am Coll Cardiol 29: 479-485, 1997.
52. Yao S, Ober JC, Krishnaswami AK, Ferguson JJ, Anderson HV, Lokino P, Buha KM, and Willerson JT. Endogenous nitric oxide protects against platelet aggregation and cyclic flow variations in stenosed and endothelium-injured arteries. Circulation 86: 1302-1309, 1992.
53. Zhao G, Zhang X, Xu X, Ochoa M, and Hintze TH. Short-term exercise training enhances reflex cholinergic nitric oxide-dependent coronary vasodilation in conscious dogs. Circ Res 80: 868-876, 1997.