Abstract
Adaptation of saphenous vein to the hemodynamic stresses of the arterial circulation is critical to the maturation of vein bypass grafts. We have investigated early adaptive responses of venous endothelium by placing excised human saphenous vein in a bypass circuit with either venous or arterial flow conditions, using external stenting to resolve the effects of longitudinal (shear) from circumferential stress. Endothelial protein concentrations were assessed by immunostaining area (ratio of protein/CD31) and Western blotting of endothelial cell lysates (staining ratio protein/vWf). In both unstented and stented veins nitric oxide synthase increased after 90 min of arterial flow: twofold increase of immunostaining area (P = 0.001), four- to fivefold increase by Western blotting (P = 0.02), and increased A23187mediated maximum endothelium-dependent relaxation of vein rings (P = 0.01). In unstented veins, ICAM-1 concentration was increased after 45 min of arterial flow: twofold increase by immunostaining (P = 0.001) and Western blotting (P = 0.038), with maximum fibrinogen-mediated endothelium-dependent relaxation increasing from 55.9+/-4.9 to 97+/-2.1% (P = 0.01). In contrast, in unstented veins there was a threefold decrease of VCAM-1 and no change in P-selectin after arterial flow for 45 and 90 min, respectively. However, no changes in ICAM-1 and VCAM-1 were observed in stented veins. The flow-induced alterations in nitric oxide synthase, ICAM-1, and VCAM-1 were abolished when 3 mM tetraethylammonium ion (K+ channel blocker) was included in the vein perfusate. The very rapid changes in ICAM-1 and VCAM-1 expression are a response to circumferential stress, whereas the slower upregulation of nitric oxide synthase is a response to longitudinal (shear) stress. Similar changes could influence the adhesiveness of endothelium in newly implanted saphenous vein bypass grafts.
Full Text
The Full Text of this article is available as a PDF (329.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Awolesi M. A., Sessa W. C., Sumpio B. E. Cyclic strain upregulates nitric oxide synthase in cultured bovine aortic endothelial cells. J Clin Invest. 1995 Sep;96(3):1449–1454. doi: 10.1172/JCI118181. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dobrin P. B., Littooy F. N., Endean E. D. Mechanical factors predisposing to intimal hyperplasia and medial thickening in autogenous vein grafts. Surgery. 1989 Mar;105(3):393–400. [PubMed] [Google Scholar]
- Hicks R. C., Golledge J., Mir-Hasseine R., Powell J. T. Vasoactive effects of fibrinogen on saphenous vein. Nature. 1996 Feb 29;379(6568):818–820. doi: 10.1038/379818a0. [DOI] [PubMed] [Google Scholar]
- Higman D. J., Strachan A. M., Buttery L., Hicks R. C., Springall D. R., Greenhalgh R. M., Powell J. T. Smoking impairs the activity of endothelial nitric oxide synthase in saphenous vein. Arterioscler Thromb Vasc Biol. 1996 Apr;16(4):546–552. doi: 10.1161/01.atv.16.4.546. [DOI] [PubMed] [Google Scholar]
- Izzat M. B., Mehta D., Bryan A. J., Reeves B., Newby A. C., Angelini G. D. Influence of external stent size on early medial and neointimal thickening in a pig model of saphenous vein bypass grafting. Circulation. 1996 Oct 1;94(7):1741–1745. doi: 10.1161/01.cir.94.7.1741. [DOI] [PubMed] [Google Scholar]
- Labadie R. F., Antaki J. F., Williams J. L., Katyal S., Ligush J., Watkins S. C., Pham S. M., Borovetz H. S. Pulsatile perfusion system for ex vivo investigation of biochemical pathways in intact vascular tissue. Am J Physiol. 1996 Feb;270(2 Pt 2):H760–H768. doi: 10.1152/ajpheart.1996.270.2.H760. [DOI] [PubMed] [Google Scholar]
- Morigi M., Zoja C., Figliuzzi M., Foppolo M., Micheletti G., Bontempelli M., Saronni M., Remuzzi G., Remuzzi A. Fluid shear stress modulates surface expression of adhesion molecules by endothelial cells. Blood. 1995 Apr 1;85(7):1696–1703. [PubMed] [Google Scholar]
- Nagel T., Resnick N., Atkinson W. J., Dewey C. F., Jr, Gimbrone M. A., Jr Shear stress selectively upregulates intercellular adhesion molecule-1 expression in cultured human vascular endothelial cells. J Clin Invest. 1994 Aug;94(2):885–891. doi: 10.1172/JCI117410. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohno M., Cooke J. P., Dzau V. J., Gibbons G. H. Fluid shear stress induces endothelial transforming growth factor beta-1 transcription and production. Modulation by potassium channel blockade. J Clin Invest. 1995 Mar;95(3):1363–1369. doi: 10.1172/JCI117787. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohno M., Gibbons G. H., Dzau V. J., Cooke J. P. Shear stress elevates endothelial cGMP. Role of a potassium channel and G protein coupling. Circulation. 1993 Jul;88(1):193–197. doi: 10.1161/01.cir.88.1.193. [DOI] [PubMed] [Google Scholar]
- Ranjan V., Diamond S. L. Fluid shear stress induces synthesis and nuclear localization of c-fos in cultured human endothelial cells. Biochem Biophys Res Commun. 1993 Oct 15;196(1):79–84. doi: 10.1006/bbrc.1993.2218. [DOI] [PubMed] [Google Scholar]
- Ranjan V., Xiao Z., Diamond S. L. Constitutive NOS expression in cultured endothelial cells is elevated by fluid shear stress. Am J Physiol. 1995 Aug;269(2 Pt 2):H550–H555. doi: 10.1152/ajpheart.1995.269.2.H550. [DOI] [PubMed] [Google Scholar]
- Resnick N., Gimbrone M. A., Jr Hemodynamic forces are complex regulators of endothelial gene expression. FASEB J. 1995 Jul;9(10):874–882. doi: 10.1096/fasebj.9.10.7615157. [DOI] [PubMed] [Google Scholar]
- Schwartz L. B., Purut C. M., Massey M. F., Pence J. C., Smith P. K., McCann R. L. Effects of pulsatile perfusion on human saphenous vein vasoreactivity: a preliminary report. Cardiovasc Surg. 1996 Apr;4(2):143–149. doi: 10.1016/0967-2109(96)82305-2. [DOI] [PubMed] [Google Scholar]
- Shyy Y. J., Hsieh H. J., Usami S., Chien S. Fluid shear stress induces a biphasic response of human monocyte chemotactic protein 1 gene expression in vascular endothelium. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4678–4682. doi: 10.1073/pnas.91.11.4678. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Springall D. R., Riveros-Moreno V., Buttery L., Suburo A., Bishop A. E., Merrett M., Moncada S., Polak J. M. Immunological detection of nitric oxide synthase(s) in human tissues using heterologous antibodies suggesting different isoforms. Histochemistry. 1992 Nov;98(4):259–266. doi: 10.1007/BF00271040. [DOI] [PubMed] [Google Scholar]
- Tsao P. S., Lewis N. P., Alpert S., Cooke J. P. Exposure to shear stress alters endothelial adhesiveness. Role of nitric oxide. Circulation. 1995 Dec 15;92(12):3513–3519. doi: 10.1161/01.cir.92.12.3513. [DOI] [PubMed] [Google Scholar]
- Wang D. L., Wung B. S., Shyy Y. J., Lin C. F., Chao Y. J., Usami S., Chien S. Mechanical strain induces monocyte chemotactic protein-1 gene expression in endothelial cells. Effects of mechanical strain on monocyte adhesion to endothelial cells. Circ Res. 1995 Aug;77(2):294–302. doi: 10.1161/01.res.77.2.294. [DOI] [PubMed] [Google Scholar]
- Zhao S., Suciu A., Ziegler T., Moore J. E., Jr, Bürki E., Meister J. J., Brunner H. R. Synergistic effects of fluid shear stress and cyclic circumferential stretch on vascular endothelial cell morphology and cytoskeleton. Arterioscler Thromb Vasc Biol. 1995 Oct;15(10):1781–1786. doi: 10.1161/01.atv.15.10.1781. [DOI] [PubMed] [Google Scholar]