Arteriosclerosis, Thrombosis, and Vascular Biology. 1996;16:546-552
© 1996 American Heart Association, Inc.
Articles |
Smoking Impairs the Activity of Endothelial Nitric Oxide Synthase in Saphenous Vein
From the Departments of Surgery (D.J.H., R.C.J.H., R.M.G., J.T.P.) and Biochemistry (A.M.J.S., J.T.P.), Charing Cross & Westminster Medical School, and the Department of Histochemistry, Royal Postgraduate Medical School (L.B., D.R.S.), London, UK.
Correspondence to Prof J.T. Powell, Department of Surgery, Charing Cross & Westminster Medical School, Fulham Palace Rd, London, W6 8RF, UK.
Abstract Smoking impairs the endothelium-dependent relaxation of arteries and veins, with the maximum relaxation in response to the calcium ionophore A23187 of saphenous vein rings being reduced from 53±4% in nonsmokers to 27±5% in smokers. We have investigated whether this endothelial dysfunction was attributable to altered activity or concentration of nitric oxide synthase (NOS). The concentration of NOS in saphenous vein endothelium, determined by Western blotting and immunohistochemistry, was not different in nonsmokers and smokers. Nitrite production from vein strips stimulated with A23187 was higher in nonsmokers (median 23.6 nmol·cm-2·h-1) than smokers (median 3.3 nmol·cm-2·h-1), P=.001, this difference being abolished when vein strips were preincubated in the presence of NG-monomethyl-L-arginine. Organ chamber studies to monitor the endothelium-dependent relaxation of vein rings in response to A23187 showed that preincubation of rings from smokers with either L-arginine (3 mmol/L) or superoxide dismutase (250 U/mL) did not improve the maximum relaxation. In contrast, preincubation of vein rings from smokers with 20 µmol/L tetrahydrobiopterin increased the maximum relaxation from 27±5% to 51±6%, P=.01. Preincubation of vein from smokers with tetrahydrobiopterin also significantly increased nitrite and cGMP production in response to stimulation with A23187. The impaired endothelium-dependent relaxation of saphenous vein rings from smokers appears to be caused by a reduction in the activity of endothelial NOS that is attributable to an inadequate supply of the coenzyme tetrahydrobiopterin.
Key Words: smoking • endothelium • nitric oxide synthase • tetrahydrobiopterin
This article has been cited by other articles:
 |
|
 |
|
  S. Kumar, X. Sun, S. Sharma, S. Aggarwal, K. Ravi, J. R. Fineman, and S. M. Black GTP cyclohydrolase I expression is regulated by nitric oxide: role of cyclic AMP Am J Physiol Lung Cell Mol Physiol, August 1, 2009; 297(2): L309 - L317. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Gamboa, C. Shibao, A. Diedrich, S. Y. Paranjape, G. Farley, B. Christman, S. R. Raj, D. Robertson, and I. Biaggioni Excessive Nitric Oxide Function and Blood Pressure Regulation in Patients With Autonomic Failure Hypertension, June 1, 2008; 51(6): 1531 - 1536. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. J. Crabtree, C. L. Smith, G. Lam, M. S. Goligorsky, and S. S. Gross Ratio of 5,6,7,8-tetrahydrobiopterin to 7,8-dihydrobiopterin in endothelial cells determines glucose-elicited changes in NO vs. superoxide production by eNOS Am J Physiol Heart Circ Physiol, April 1, 2008; 294(4): H1530 - H1540. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. T. Gao, L. J. Roman, P. Martasek, S. P. Panda, Y. Ishimura, and B. S. S. Masters Oxygen Metabolism by Endothelial Nitric-oxide Synthase J. Biol. Chem., September 28, 2007; 282(39): 28557 - 28565. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. C. Reddy, Y. Hao, S.-H. Lee, S. R. Gangireddy, C. Owyang, and M. J. DiMagno Pioglitazone reverses insulin resistance and impaired CCK-stimulated pancreatic secretion in eNOS(-/-) mice: therapy for exocrine pancreatic disorders? Am J Physiol Gastrointest Liver Physiol, July 1, 2007; 293(1): G112 - G120. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Gamboa, C. Shibao, A. Diedrich, L. Choi, B. Pohar, J. Jordan, S. Paranjape, G. Farley, and I. Biaggioni Contribution of Endothelial Nitric Oxide to Blood Pressure in Humans Hypertension, January 1, 2007; 49(1): 170 - 177. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. L. Moens and D. A. Kass Tetrahydrobiopterin and Cardiovascular Disease Arterioscler Thromb Vasc Biol, November 1, 2006; 26(11): 2439 - 2444. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X. Guo, M. J. Oldham, M. T. Kleinman, R. F. Phalen, and G. S. Kassab Effect of cigarette smoking on nitric oxide, structural, and mechanical properties of mouse arteries Am J Physiol Heart Circ Physiol, November 1, 2006; 291(5): H2354 - H2361. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Malinovschi, C. Janson, T. Holmkvist, D. Norback, P. Merilainen, and M. Hogman Effect of smoking on exhaled nitric oxide and flow-independent nitric oxide exchange parameters Eur. Respir. J., August 1, 2006; 28(2): 339 - 345. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. R. Lowe, A. C. Everett, A. J. Lee, M. Lau, A. Y. Dunbar, V. Berka, A.-l. Tsai, and Y. Osawa TIME-DEPENDENT INHIBITION AND TETRAHYDROBIOPTERIN DEPLETION OF ENDOTHELIAL NITRIC-OXIDE SYNTHASE CAUSED BY CIGARETTES Drug Metab. Dispos., January 1, 2005; 33(1): 131 - 138. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. A. Blackwell, J. P. Sorenson, D. M. Richardson, L. A. Smith, O. Suda, K. Nath, and Z. S. Katusic Mechanisms of aging-induced impairment of endothelium-dependent relaxation: role of tetrahydrobiopterin Am J Physiol Heart Circ Physiol, December 1, 2004; 287(6): H2448 - H2453. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. McGregor, L. Kempster, R. Wait, M. Gosling, M. J. Dunn, and J. T. Powell F-actin Capping (CapZ) and Other Contractile Saphenous Vein Smooth Muscle Proteins Are Altered by Hemodynamic Stress: A PROTEOMIC APPROACH Mol. Cell. Proteomics, February 1, 2004; 3(2): 115 - 124. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. R. Demady, E. R. Lowe, A. C. Everett, S. S. Billecke, Y. Kamada, A. Y. Dunbar, and Y. Osawa METABOLISM-BASED INACTIVATION OF NEURONAL NITRIC-OXIDE SYNTHASE BY COMPONENTS OF CIGARETTE AND CIGARETTE SMOKE Drug Metab. Dispos., July 1, 2003; 31(7): 932 - 937. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. S. Barua, J. A. Ambrose, S. Srivastava, M. C. DeVoe, and L.-J. Eales-Reynolds Reactive Oxygen Species Are Involved in Smoking-Induced Dysfunction of Nitric Oxide Biosynthesis and Upregulation of Endothelial Nitric Oxide Synthase: An In Vitro Demonstration in Human Coronary Artery Endothelial Cells Circulation, May 13, 2003; 107(18): 2342 - 2347. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Q. Fang, H. Sun, and W. G. Mayhan Impairment of nitric oxide synthase-dependent dilatation of cerebral arterioles during infusion of nicotine Am J Physiol Heart Circ Physiol, February 1, 2003; 284(2): H528 - H534. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. McGregor, M. Gosling, D. K Beattie, D. M.P Ribbons, A. H Davies, and J. T Powell Circumferential stretching of saphenous vein smooth muscle enhances vasoconstrictor responses by Rho kinase-dependent pathways Cardiovasc Res, January 1, 2002; 53(1): 219 - 226. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. J. Hutchison, R. E. Sievers, B.-Q. Zhu, Y.-P. Sun, D. J. Stewart, W. W. Parmley, and K. Chatterjee Secondhand Tobacco Smoke Impairs Rabbit Pulmonary Artery Endothelium-Dependent Relaxation Chest, December 1, 2001; 120(6): 2004 - 2012. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Sun, K. P. Patel, and W. G. Mayhan Tetrahydrobiopterin, a cofactor for NOS, improves endothelial dysfunction during chronic alcohol consumption Am J Physiol Heart Circ Physiol, November 1, 2001; 281(5): H1863 - H1869. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Z. S. Katusic Vascular endothelial dysfunction: does tetrahydrobiopterin play a role? Am J Physiol Heart Circ Physiol, September 1, 2001; 281(3): H981 - H986. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. A Brown and F. B Hu Dietary modulation of endothelial function: implications for cardiovascular disease Am. J. Clinical Nutrition, April 1, 2001; 73(4): 673 - 686. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Cosentino, J. E. Barker, M. P. Brand, S. J. Heales, E. R. Werner, J. R. Tippins, N. West, K. M. Channon, M. Volpe, and T. F. Luscher Reactive Oxygen Species Mediate Endothelium-Dependent Relaxations in Tetrahydrobiopterin-Deficient Mice Arterioscler Thromb Vasc Biol, April 1, 2001; 21(4): 496 - 502. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Verma, F. Lovren, A. S. Dumont, K. J. Mather, A. Maitland, T. M. Kieser, C. R. Triggle, and T. J. Anderson Tetrahydrobiopterin improves endothelial function in human saphenous veins J. Thorac. Cardiovasc. Surg., October 1, 2000; 120(4): 668 - 671. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. Szekacs, W. Dachman, and Z. Vajo Alterations of Venous Drug Reactivity in Humans: Acquired and Genetic Factors Angiology, May 1, 2000; 51(5): 361 - 366. [Abstract] [PDF]
|
|
|
|
|
|
F. H. de Man, A. W. E. Weverling-Rijnsburger, A. van der Laarse, A. H. M. Smelt, J. W. Jukema, and G. J. Blauw Not Acute but Chronic Hypertriglyceridemia Is Associated With Impaired Endothelium-Dependent Vasodilation : Reversal After Lipid-Lowering Therapy by Atorvastatin Arterioscler Thromb Vasc Biol, March 1, 2000; 20(3): 744 - 750. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Heitzer, C. Brockhoff, B. Mayer, A. Warnholtz, H. Mollnau, S. Henne, T. Meinertz, and T. Munzel Tetrahydrobiopterin Improves Endothelium-Dependent Vasodilation in Chronic Smokers : Evidence for a Dysfunctional Nitric Oxide Synthase Circ. Res., February 4, 2000; 86 (2): e36 - e41. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Ueda, H. Matsuoka, H. Miyazaki, M. Usui, S. Okuda, and T. Imaizumi Tetrahydrobiopterin restores endothelial function in long-term smokers J. Am. Coll. Cardiol., January 1, 2000; 35(1): 71 - 75. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. C. Hooper, C. Lally, H. Austin, J. Benson, A. Dilley, N. K. Wenger, C. Whitsett, P. Rawlins, and B. L. Evatt The Relationship Between Polymorphisms in the Endothelial Cell Nitric Oxide Synthase Gene and the Platelet GPIIIa Gene With Myocardial Infarction and Venous Thromboembolism in African Americans Chest, October 1, 1999; 116(4): 880 - 886. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W. G. Mayhan and G. M. Sharpe Chronic exposure to nicotine alters endothelium-dependent arteriolar dilatation: effect of superoxide dismutase J Appl Physiol, April 1, 1999; 86(4): 1126 - 1134. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Gosling, J. Golledge, R. J. Turner, and J. T. Powell Arterial Flow Conditions Downregulate Thrombomodulin on Saphenous Vein Endothelium Circulation, March 2, 1999; 99(8): 1047 - 1053. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. G. Mayhan and G. M. Sharpe Superoxide dismutase restores endothelium-dependent arteriolar dilatation during acute infusion of nicotine J Appl Physiol, October 1, 1998; 85(4): 1292 - 1298. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Moreno Jr., S. Chalon, A. Urae, O. Tangphao, A. K. Abiose, B. B. Hoffman, and T. F. Blaschke Endothelial dysfunction in human hand veins is rapidly reversible after smoking cessation Am J Physiol Heart Circ Physiol, September 1, 1998; 275(3): H1040 - H1045. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. T Powell Vascular damage from smoking: disease mechanisms at the arterial wall Vascular Medicine, February 1, 1998; 3(1): 21 - 28. [Abstract] [PDF]
|
|
|
|
|
|
R. M. F. Wever, T. F. Luscher, F. Cosentino, and T. J. Rabelink Atherosclerosis and the Two Faces of Endothelial Nitric Oxide Synthase Circulation, January 13, 1998; 97(1): 108 - 112. [Full Text] [PDF]
|
|
|
|
 |
|
 W. I. Rosenblum and Z. S. Katusic Tetrahydrobiopterin, a Cofactor for Nitric Oxide Synthase, Produces Endothelium-Dependent Dilation of Mouse Pial Arterioles Stroke, January 1, 1997; 28(1): 186 - 189. [Abstract] [Full Text]
|
|