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Am J Physiol Cell Physiol 269: C1371-C1378, 1995;
0363-6143/95 $5.00
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AJP - Cell Physiology, Vol 269, Issue 6 C1371-C1378, Copyright © 1995 by American Physiological Society

ARTICLES

Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress

M. Uematsu, Y. Ohara, J. P. Navas, K. Nishida, T. J. Murphy, R. W. Alexander, R. M. Nerem and D. G. Harrison
Biomechanics Laboratory, School of Mechanical Engineering, Georgia Institute of Technology, Atlanta 30332-0405, USA.

Shear stress enhances expression of Ca(2+)-calmodulin-sensitive endothelial cell nitric oxide synthase (ecNOS) mRNA and protein in bovine aortic endothelial cells (BAEC). The present studies were performed to investigate mechanisms responsible for regulation of ecNOS mRNA expression by shear stress and to determine if this induction of ecNOS mRNA is accompanied by an enhanced nitric oxide (NO) production. Shear stresses of 15 dyn/cm2 for 3-24 h resulted in a two- to threefold increase of ecNOS mRNA content quantified by Northern analysis in BAEC. Shear stresses (1.2-15 dyn/cm2) for 3 h resulted in an induction of ecNOS mRNA in a dose-dependent manner. In human aortic endothelial cells, shear stresses of 15 dyn/cm2 for 3 h also resulted in ecNOS mRNA induction. In BAEC, this induction in ecNOS mRNA was prevented by coincubation with actinomycin D (10 micrograms/ml). The K+ channel antagonist tetraethylammonium chloride (3 mM) prevented increase in ecNOS mRNA in response to shear stress. The ecNOS promotor contains putative binding domains for AP-1 complexes, potentially responsive to activation of protein kinase C (PKC). However, selective PKC inhibitor calphostin C (100 nM) did not inhibit ecNOS induction by shear stress. Finally, production of nitrogen oxides under both basal conditions and in response to the calcium ionophore A-23187 (1 microM) by BAEC exposed to shear stress was increased approximately twofold compared with cells not exposed to shear stress. These data suggest that ecNOS mRNA expression is regulated by K+ channel opening, but not by activation of PKC, and that shear not only enhances ecNOS mRNA expression but increases capacity of endothelial cells to release NO.


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Hypertension, June 1, 1999; 33(6): 1359 - 1363.
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R. D. Rosenberg and W. C. Aird
Vascular-Bed-Specific Hemostasis and Hypercoagulable States
N. Engl. J. Med., May 20, 1999; 340(20): 1555 - 1564.
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K. Mortensen, S. Holck, I. J. Christensen, J. Skouv, D. M. Hougaard, J. Blom, and L.-I. Larsson
Endothelial Cell Nitric Oxide Synthase in Peritumoral Microvessels Is a Favorable Prognostic Indicator in Premenopausal Breast Cancer Patients
Clin. Cancer Res., May 1, 1999; 5(5): 1093 - 1097.
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E. H. BURGER and J. KLEIN-NULEND
Mechanotransduction in bone—role of the lacuno-canalicular network
FASEB J, May 1, 1999; 13(9001): 101 - 112.
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 Am. J. Physiol. Heart Circ. Physiol.Home page
H. Ando, T. Kubin, W. Schaper, and J. Schaper
Cardiac microvascular endothelial cells express alpha -smooth muscle actin and show low NOS III activity
Am J Physiol Heart Circ Physiol, May 1, 1999; 276(5): H1755 - H1768.
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 Arterioscler. Thromb. Vasc. Bio.Home page
S. Dimmeler, C. Hermann, J. Galle, and A. M. Zeiher
Upregulation of Superoxide Dismutase and Nitric Oxide Synthase Mediates the Apoptosis-Suppressive Effects of Shear Stress on Endothelial Cells
Arterioscler Thromb Vasc Biol, March 1, 1999; 19(3): 656 - 664.
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R. L. Rairigh, L. Storme, T. A. Parker, T. D. le Cras, J. P. Kinsella, M. Jakkula, and S. H. Abman
Inducible NO synthase inhibition attenuates shear stress-induced pulmonary vasodilation in the ovine fetus
Am J Physiol Lung Cell Mol Physiol, March 1, 1999; 276(3): L513 - L521.
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C. R. Woodman, J. M. Muller, J. W. E. Rush, M. H. Laughlin, and E. M. Price
Flow regulation of ecNOS and Cu/Zn SOD mRNA expression in porcine coronary arterioles
Am J Physiol Heart Circ Physiol, March 1, 1999; 276(3): H1058 - H1063.
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R. C. Tyler, M. Muramatsu, S. H. Abman, T. J. Stelzner, D. M. Rodman, K. D. Bloch, and I. F. McMurtry
Variable expression of endothelial NO synthase in three forms of rat pulmonary hypertension
Am J Physiol Lung Cell Mol Physiol, February 1, 1999; 276(2): L297 - L303.
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F. Karantzoulis-Fegaras, H. Antoniou, S.-L. M. Lai, G. Kulkarni, C. D'Abreo, G. K. T. Wong, T. L. Miller, Y. Chan, J. Atkins, Y. Wang, et al.
Characterization of the Human Endothelial Nitric-oxide Synthase Promoter
J. Biol. Chem., January 29, 1999; 274(5): 3076 - 3093.
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S. M. Black, J. R. Fineman, R. H. Steinhorn, J. Bristow, and S. J. Soifer
Increased endothelial NOS in lambs with increased pulmonary blood flow and pulmonary hypertension
Am J Physiol Heart Circ Physiol, November 1, 1998; 275(5): H1643 - H1651.
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 Am. J. Physiol. Heart Circ. Physiol.Home page
K. E. Vagnoni, C. E. Shaw, T. M. Phernetton, B. M. Meglin, I. M. Bird, and R. R. Magness
Endothelial vasodilator production by uterine and systemic arteries. III. Ovarian and estrogen effects on NO synthase
Am J Physiol Heart Circ Physiol, November 1, 1998; 275(5): H1845 - H1856.
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S. Dimmeler, B. Assmus, C. Hermann, J. Haendeler, and A. M. Zeiher
Fluid Shear Stress Stimulates Phosphorylation of Akt in Human Endothelial Cells : Involvement in Suppression of Apoptosis
Circ. Res., August 10, 1998; 83(3): 334 - 341.
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 Arterioscler. Thromb. Vasc. Bio.Home page
V. Poppa, J. K. Miyashiro, M. A. Corson, and B. C. Berk
Endothelial NO Synthase Is Increased in Regenerating Endothelium After Denuding Injury of the Rat Aorta
Arterioscler Thromb Vasc Biol, August 1, 1998; 18(8): 1312 - 1321.
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 Am. J. Physiol. Cell Physiol.Home page
J. G. Tidball, E. Lavergne, K. S. Lau, M. J. Spencer, J. T. Stull, and M. Wehling
Mechanical loading regulates NOS expression and activity in developing and adult skeletal muscle
Am J Physiol Cell Physiol, July 1, 1998; 275(1): C260 - C266.
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 Arterioscler. Thromb. Vasc. Bio.Home page
O. Traub and B. C. Berk
Laminar Shear Stress : Mechanisms by Which Endothelial Cells Transduce an Atheroprotective Force
Arterioscler Thromb Vasc Biol, May 1, 1998; 18(5): 677 - 685.
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 Arterioscler. Thromb. Vasc. Bio.Home page
T. Ziegler, K. Bouzourene, V. J. Harrison, H. R. Brunner, and D. Hayoz
Influence of Oscillatory and Unidirectional Flow Environments on the Expression of Endothelin and Nitric Oxide Synthase in Cultured Endothelial Cells
Arterioscler Thromb Vasc Biol, May 1, 1998; 18(5): 686 - 692.
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 Am. J. Physiol. Heart Circ. Physiol.Home page
J. D. Hood, C. J. Meininger, M. Ziche, and H. J. Granger
VEGF upregulates ecNOS message, protein, and NO production in human endothelial cells
Am J Physiol Heart Circ Physiol, March 1, 1998; 274(3): H1054 - H1058.
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L. J. Andries, D. L. Brutsaert, and S. U. Sys
Nonuniformity of Endothelial Constitutive Nitric Oxide Synthase Distribution in Cardiac Endothelium
Circ. Res., February 9, 1998; 82(2): 195 - 203.
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S. Jalali, Y.-S. Li, M. Sotoudeh, S. Yuan, S. Li, S. Chien, and J. Y-J. Shyy
Shear Stress Activates p60src-Ras-MAPK Signaling Pathways in Vascular Endothelial Cells
Arterioscler Thromb Vasc Biol, February 1, 1998; 18(2): 227 - 234.
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 Am. J. Physiol. Heart Circ. Physiol.Home page
M. Papadaki, R. G. Tilton, S. G. Eskin, and L. V. McIntire
Nitric oxide production by cultured human aortic smooth muscle cells: stimulation by fluid flow
Am J Physiol Heart Circ Physiol, February 1, 1998; 274(2): H616 - H626.
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F. M. FARACI and D. D. HEISTAD
Regulation of the Cerebral Circulation: Role of Endothelium and Potassium Channels
Physiol Rev, January 1, 1998; 78(1): 53 - 97.
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 HypertensionHome page
A. Zuckerman, P. N. Chander, G. A. Zeballos, and C. T. Stier Jr
Regional Renal Nitric Oxide Release in Stroke-Prone Spontaneously Hypertensive Rats
Hypertension, December 1, 1997; 30(6): 1479 - 1486.
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M. Challah, S. Nadaud, M. Philippe, T. Battle, F. Soubrier, B. Corman, and J. B. Michel
Circulating and cellular markers of endothelial dysfunction with aging in rats
Am J Physiol Heart Circ Physiol, October 1, 1997; 273(4): H1941 - H1948.
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A. N. MacRitchie, S. S. Jun, Z. Chen, Z. German, I. S. Yuhanna, T. S. Sherman, and P. W. Shaul
Estrogen Upregulates Endothelial Nitric Oxide Synthase Gene Expression in Fetal Pulmonary Artery Endothelium
Circ. Res., September 19, 1997; 81(3): 355 - 362.
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S. Nadaud, M. Philippe, J.-F. Arnal, J.-B. Michel, and F. Soubrier
Sustained Increase in Aortic Endothelial Nitric Oxide Synthase Expression In Vivo in a Model of Chronic High Blood Flow
Circ. Res., October 1, 1996; 79(4): 857 - 863.
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N. Inoue, S. Ramasamy, T. Fukai, R. M. Nerem, and D. G. Harrison
Shear Stress Modulates Expression of Cu/Zn Superoxide Dismutase in Human Aortic Endothelial Cells
Circ. Res., July 1, 1996; 79(1): 32 - 37.
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 Circ. Res.Home page
J. Hoffmann, J. Haendeler, A. Aicher, L. Rossig, M. Vasa, A. M. Zeiher, and S. Dimmeler
Aging Enhances the Sensitivity of Endothelial Cells Toward Apoptotic Stimuli: Important Role of Nitric Oxide
Circ. Res., October 12, 2001; 89(8): 709 - 715.
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 Circ. Res.Home page
H. Matsushita, E. Chang, A. J. Glassford, J. P. Cooke, C.-P. Chiu, and P. S. Tsao
eNOS Activity Is Reduced in Senescent Human Endothelial Cells: Preservation by hTERT Immortalization
Circ. Res., October 26, 2001; 89(9): 793 - 798.
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 Arterioscler. Thromb. Vasc. Bio.Home page
Y. Chu, D. D. Heistad, K. L. Knudtson, K. G. Lamping, and F. M. Faraci
Quantification of mRNA for Endothelial NO Synthase in Mouse Blood Vessels by Real-Time Polymerase Chain Reaction
Arterioscler Thromb Vasc Biol, April 1, 2002; 22(4): 611 - 616.
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