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Circulation. 1998;97:1129-1135

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(Circulation. 1998;97:1129-1135.)
© 1998 American Heart Association, Inc.


Clinical Investigation and Reports

Upregulation of Endothelial Nitric Oxide Synthase by HMG CoA Reductase Inhibitors

Ulrich Laufs, MD; Vito La Fata, BA; Jorge Plutzky, MD; ; James K. Liao, MD

From the Vascular Medicine and Atherosclerosis Unit, Cardiovascular Division, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Mass.

Correspondence to James K. Liao, MD, Vascular Medicine and Atherosclerosis Unit, Brigham and Women's Hospital, 221 Longwood Ave, LMRC-316, Boston, MA 02115. E-mail jkliao{at}bics.bwh.harvard.edu

Background—Oxidized low-density lipoprotein (ox-LDL) causes endothelial dysfunction in part by decreasing the availability of endothelial nitric oxide (NO). Although HMG CoA reductase inhibitors restore endothelial function by reducing serum cholesterol levels, it is not known whether they can also directly upregulate endothelial NO synthase (ecNOS) activity.

Methods and Results—Human saphenous vein endothelial cells were treated with ox-LDL (50 µg/mL thiobarbituric acid reactive substances 12 to 16 nmol/mg) in the presence of HMG CoA reductase inhibitors simvastatin and lovastatin. In a time-dependent manner, ox-LDL decreased ecNOS mRNA and protein levels (91±4% and 67±8% reduction after 72 hours, respectively). Both simvastatin (1 µmol/L) and lovastatin (10 µmol/L) upregulated ecNOS expression by 3.8-fold and 3.6-fold, respectively, and completely prevented its downregulation by ox-LDL. These effects of simvastatin on ecNOS expression correlated with changes in ecNOS activity. Although L-mevalonate alone did not affect ecNOS expression, cotreatment with L-mevalonate completely reversed ecNOS upregulation by simvastatin. Actinomycin D studies revealed that simvastatin stabilized ecNOS mRNA ({tau}1/2, 43 versus 35 hours). Nuclear run-on assays and transient transfection studies with a -1.6 kb ecNOS promoter construct showed that simvastatin did not affect ecNOS gene transcription.

Conclusions—Inhibition of endothelial HMG CoA reductase upregulates ecNOS expression predominantly by posttranscriptional mechanisms. These findings suggest that HMG CoA reductase inhibitors may have beneficial effects in atherosclerosis beyond that attributed to the lowering of serum cholesterol by increasing ecNOS activity.


Key Words: atherosclerosis • endothelium-derived factors • lipoproteins • genes




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D. A. Pascual, J. M. Arribas, P. L. Tornel, F. Marin, C. Oliver, M. Ahumada, J. Gomez-Plana, P. Martinez, R. Arcas, and M. Valdes
Preoperative Statin Therapy and Troponin T Predict Early Complications of Coronary Artery Surgery
Ann. Thorac. Surg., January 1, 2006; 81(1): 78 - 83.
[Abstract] [Full Text] [PDF]


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ANGIOLOGYHome page
M. E. Alnaeb, F. Youssef, D. P. Mikhailidis, and G. Hamilton
Short-term Lipid-Lowering Treatment with Atorvastatin Improves Renal Function But Not Renal Blood Flow Indices in Patients with Peripheral Arterial Disease
Angiology, January 1, 2006; 57(1): 65 - 71.
[Abstract] [PDF]


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Circ. Res.Home page
Y. Rikitake and J. K. Liao
Rho GTPases, Statins, and Nitric Oxide
Circ. Res., December 9, 2005; 97(12): 1232 - 1235.
[Abstract] [Full Text] [PDF]


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Eur. J. Cardiothorac. Surg.Home page
M. Chello, C. Goffredo, G. Patti, D. Candura, R. Melfi, S. Mastrobuoni, G. Di Sciascio, and E. Covino
Effects of atorvastatin on arterial endothelial function in coronary bypass surgery
Eur. J. Cardiothorac. Surg., December 1, 2005; 28(6): 805 - 810.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
J. G. Robinson, B. Smith, N. Maheshwari, and H. Schrott
Pleiotropic Effects of Statins: Benefit Beyond Cholesterol Reduction?: A Meta-Regression Analysis
J. Am. Coll. Cardiol., November 15, 2005; 46(10): 1855 - 1862.
[Abstract] [Full Text] [PDF]


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Vasc MedHome page
N. Nair, R. K Oka, L. D Waring, E. M Umoh, C B. Taylor, and J. P Cooke
Vascular compliance versus flow-mediated vasodilation: correlation with cardiovascular risk factors
Vascular Medicine, November 1, 2005; 10(4): 275 - 283.
[Abstract] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
T. Murata, K. Kinoshita, M. Hori, M. Kuwahara, H. Tsubone, H. Karaki, and H. Ozaki
Statin Protects Endothelial Nitric Oxide Synthase Activity in Hypoxia-Induced Pulmonary Hypertension
Arterioscler Thromb Vasc Biol, November 1, 2005; 25(11): 2335 - 2342.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
K. K. Ray, C. P. Cannon, R. Cairns, D. A. Morrow, N. Rifai, A. J. Kirtane, C. H. McCabe, A. M. Skene, C. M. Gibson, P. M. Ridker, et al.
Relationship Between Uncontrolled Risk Factors and C-Reactive Protein Levels in Patients Receiving Standard or Intensive Statin Therapy for Acute Coronary Syndromes in the PROVE IT-TIMI 22 Trial
J. Am. Coll. Cardiol., October 18, 2005; 46(8): 1417 - 1424.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
K. K. Ray and C. P. Cannon
The Potential Relevance of the Multiple Lipid-Independent (Pleiotropic) Effects of Statins in the Management of Acute Coronary Syndromes
J. Am. Coll. Cardiol., October 18, 2005; 46(8): 1425 - 1433.
[Abstract] [Full Text] [PDF]


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Eur Heart JHome page
M. D.M. Engelmann and J. H. Svendsen
Inflammation in the genesis and perpetuation of atrial fibrillation
Eur. Heart J., October 2, 2005; 26(20): 2083 - 2092.
[Abstract] [Full Text] [PDF]


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Eur Heart JHome page
A. G. Herman and S. Moncada
Therapeutic potential of nitric oxide donors in the prevention and treatment of atherosclerosis
Eur. Heart J., October 1, 2005; 26(19): 1945 - 1955.
[Abstract] [Full Text] [PDF]


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StrokeHome page
Y. Rikitake, H.-H. Kim, Z. Huang, M. Seto, K. Yano, T. Asano, M. A. Moskowitz, and J. K. Liao
Inhibition of Rho Kinase (ROCK) Leads to Increased Cerebral Blood Flow and Stroke Protection
Stroke, October 1, 2005; 36(10): 2251 - 2257.
[Abstract] [Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
J. Hetzel, B. Balletshofer, K. Rittig, D. Walcher, W. Kratzer, V. Hombach, H.-U. Haring, W. Koenig, and N. Marx
Rapid Effects of Rosiglitazone Treatment on Endothelial Function and Inflammatory Biomarkers
Arterioscler Thromb Vasc Biol, September 1, 2005; 25(9): 1804 - 1809.
[Abstract] [Full Text] [PDF]


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CirculationHome page
S. Sen-Banerjee, S. Mir, Z. Lin, A. Hamik, G. B. Atkins, H. Das, P. Banerjee, A. Kumar, and M. K. Jain
Kruppel-Like Factor 2 as a Novel Mediator of Statin Effects in Endothelial Cells
Circulation, August 2, 2005; 112(5): 720 - 726.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
K. M. Parmar, V. Nambudiri, G. Dai, H. B. Larman, M. A. Gimbrone Jr., and G. Garcia-Cardena
Statins Exert Endothelial Atheroprotective Effects via the KLF2 Transcription Factor
J. Biol. Chem., July 22, 2005; 280(29): 26714 - 26719.
[Abstract] [Full Text] [PDF]


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Diabetes CareHome page
E. D. Beishuizen, J. T. Tamsma, J. W. Jukema, M. A. van de Ree, J. C. M. van der Vijver, A. E. Meinders, and M. V. Huisman
The Effect of Statin Therapy on Endothelial Function in Type 2 Diabetes Without Manifest Cardiovascular Disease
Diabetes Care, July 1, 2005; 28(7): 1668 - 1674.
[Abstract] [Full Text] [PDF]


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Vasc MedHome page
R. H Boger
Asymmetric dimethylarginine (ADMA) and cardiovascular disease: insights from prospective clinical trials
Vascular Medicine, July 1, 2005; 10(1_suppl): S19 - S25.
[Abstract] [PDF]


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CirculationHome page
Y. Rikitake and J. K. Liao
Rho-Kinase Mediates Hyperglycemia-Induced Plasminogen Activator Inhibitor-1 Expression in Vascular Endothelial Cells
Circulation, June 21, 2005; 111(24): 3261 - 3268.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
M. Weber, C. H. Hagedorn, D. G. Harrison, and C. D. Searles
Laminar Shear Stress and 3' Polyadenylation of eNOS mRNA
Circ. Res., June 10, 2005; 96(11): 1161 - 1168.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
M. Yamakuchi, J. J.M. Greer, S. J. Cameron, K. Matsushita, C. N. Morrell, K. Talbot-Fox, W. M. Baldwin III, D. J. Lefer, and C. J. Lowenstein
HMG-CoA Reductase Inhibitors Inhibit Endothelial Exocytosis and Decrease Myocardial Infarct Size
Circ. Res., June 10, 2005; 96(11): 1185 - 1192.
[Abstract] [Full Text] [PDF]


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HeartHome page
N M Rajamannan, M Subramaniam, S R Stock, N J Stone, M Springett, K I Ignatiev, J P McConnell, R J Singh, R O Bonow, and T C Spelsberg
Atorvastatin inhibits calcification and enhances nitric oxide synthase production in the hypercholesterolaemic aortic valve
Heart, June 1, 2005; 91(6): 806 - 810.
[Abstract] [Full Text] [PDF]


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Cardiovasc ResHome page
P. Di Napoli, A. A. Taccardi, A. Grilli, M. A. De Lutiis, A. Barsotti, M. Felaco, and R. De Caterina
Chronic treatment with rosuvastatin modulates nitric oxide synthase expression and reduces ischemia-reperfusion injury in rat hearts
Cardiovasc Res, June 1, 2005; 66(3): 462 - 471.
[Abstract] [Full Text] [PDF]


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CirculationHome page
U. Landmesser, F. Bahlmann, M. Mueller, S. Spiekermann, N. Kirchhoff, S. Schulz, C. Manes, D. Fischer, K. de Groot, D. Fliser, et al.
Simvastatin Versus Ezetimibe: Pleiotropic and Lipid-Lowering Effects on Endothelial Function in Humans
Circulation, May 10, 2005; 111(18): 2356 - 2363.
[Abstract] [Full Text] [PDF]


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J. Pharmacol. Exp. Ther.Home page
W. Li, T. Asagami, H. Matsushita, K.-H. Lee, and P. S. Tsao
Rosuvastatin Attenuates Monocyte-Endothelial Cell Interactions and Vascular Free Radical Production in Hypercholesterolemic Mice
J. Pharmacol. Exp. Ther., May 1, 2005; 313(2): 557 - 562.
[Abstract] [Full Text] [PDF]


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Vasc MedHome page
R. H Boger
Asymmetric dimethylarginine (ADMA) and cardiovascular disease: insights from prospective clinical trials
Vascular Medicine, May 1, 2005; 10(2_suppl): S19 - S25.
[Abstract] [PDF]


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NEJMHome page
B. Cohen, D. Singh, P. Greenland, D. M. Lloyd-Jones, A. J. Moss, B. L. Jaber, N. E. Madias, P. M Ridker, C. P. Cannon, and E. Braunwald
C-Reactive Protein Levels and Outcomes after Statin Therapy
N. Engl. J. Med., April 14, 2005; 352(15): 1603 - 1605.
[Full Text] [PDF]


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J. Am. Soc. Nephrol.Home page
V. M. Campese, M. K. Nadim, and M. Epstein
Are 3-Hydroxy-3-Methylglutaryl-CoA Reductase Inhibitors Renoprotective?
J. Am. Soc. Nephrol., March 1, 2005; 16(3_suppl_1): S11 - S17.
[Abstract] [Full Text] [PDF]


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HypertensionHome page
A. Aicher, A. M. Zeiher, and S. Dimmeler
Mobilizing Endothelial Progenitor Cells
Hypertension, March 1, 2005; 45(3): 321 - 325.
[Abstract] [Full Text] [PDF]