Abstract
The intermediate filament vimentin might play a key role in vascular resistance to mechanical stress. We investigated the responses to pressure (tensile stress) and flow (shear stress) of mesenteric resistance arteries perfused in vitro from vimentin knockout mice. Arteries were isolated from homozygous (Vim-/-, n = 14) or heterozygous vimentin-null mice (Vim+/-, n = 5) and from wild-type littermates (Vim+/+, n = 9). Passive arterial diameter (175+/-15 micron in Vim+/+ at 100 mmHg) and myogenic tone were not affected by the absence of vimentin. Flow-induced (0-150 microl/min) dilation (e. g., 19+/-3 micron dilation at 150 mmHg in Vim+/+) was significantly attenuated in Vim-/- mice (13+/-2 micron dilation, P < 0.01). Acute blockade of nitric oxide synthesis (NG-nitro- L-arginine, 10 microM) significantly decreased flow-induced dilation in both groups, whereas acute blockade of prostaglandin synthesis (indomethacin, 10 microM) had no significant effect. Mean blood pressure, in vivo mesenteric blood flow and diameter, and mesenteric artery media thickness or media to lumen ratio were not affected by the absence of vimentin. Thus, the absence of vimentin decreased selectively the response of resistance arteries to flow, suggesting a role for vimentin in the mechanotransduction of shear stress.
Full Text
The Full Text of this article is available as a PDF (206.4 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Banes A. J., Tsuzaki M., Yamamoto J., Fischer T., Brigman B., Brown T., Miller L. Mechanoreception at the cellular level: the detection, interpretation, and diversity of responses to mechanical signals. Biochem Cell Biol. 1995 Jul-Aug;73(7-8):349–365. doi: 10.1139/o95-043. [DOI] [PubMed] [Google Scholar]
- Bevan J. A., Henrion D. Pharmacological implications of the flow-dependence of vascular smooth muscle tone. Annu Rev Pharmacol Toxicol. 1994;34:173–190. doi: 10.1146/annurev.pa.34.040194.001133. [DOI] [PubMed] [Google Scholar]
- Bevan J. A., Laher I. Pressure and flow-dependent vascular tone. FASEB J. 1991 Jun;5(9):2267–2273. doi: 10.1096/fasebj.5.9.1860618. [DOI] [PubMed] [Google Scholar]
- Colucci-Guyon E., Portier M. M., Dunia I., Paulin D., Pournin S., Babinet C. Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell. 1994 Nov 18;79(4):679–694. doi: 10.1016/0092-8674(94)90553-3. [DOI] [PubMed] [Google Scholar]
- Cucina A., Sterpetti A. V., Pupelis G., Fragale A., Lepidi S., Cavallaro A., Giustiniani Q., Santoro D'Angelo L. Shear stress induces changes in the morphology and cytoskeleton organisation of arterial endothelial cells. Eur J Vasc Endovasc Surg. 1995 Jan;9(1):86–92. doi: 10.1016/s1078-5884(05)80230-8. [DOI] [PubMed] [Google Scholar]
- D'Angelo G., Meininger G. A. Transduction mechanisms involved in the regulation of myogenic activity. Hypertension. 1994 Jun;23(6 Pt 2):1096–1105. doi: 10.1161/01.hyp.23.6.1096. [DOI] [PubMed] [Google Scholar]
- Davies P. F. Flow-mediated endothelial mechanotransduction. Physiol Rev. 1995 Jul;75(3):519–560. doi: 10.1152/physrev.1995.75.3.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Davies P. F., Tripathi S. C. Mechanical stress mechanisms and the cell. An endothelial paradigm. Circ Res. 1993 Feb;72(2):239–245. doi: 10.1161/01.res.72.2.239. [DOI] [PubMed] [Google Scholar]
- Falcone J. C., Granger H. J., Meininger G. A. Enhanced myogenic activation in skeletal muscle arterioles from spontaneously hypertensive rats. Am J Physiol. 1993 Dec;265(6 Pt 2):H1847–H1855. doi: 10.1152/ajpheart.1993.265.6.H1847. [DOI] [PubMed] [Google Scholar]
- Friebel M., Klotz K. F., Ley K., Gaehtgens P., Pries A. R. Flow-dependent regulation of arteriolar diameter in rat skeletal muscle in situ: role of endothelium-derived relaxing factor and prostanoids. J Physiol. 1995 Mar 15;483(Pt 3):715–726. doi: 10.1113/jphysiol.1995.sp020616. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Girard P. R., Nerem R. M. Shear stress modulates endothelial cell morphology and F-actin organization through the regulation of focal adhesion-associated proteins. J Cell Physiol. 1995 Apr;163(1):179–193. doi: 10.1002/jcp.1041630121. [DOI] [PubMed] [Google Scholar]
- Halpern W., Osol G., Coy G. S. Mechanical behavior of pressurized in vitro prearteriolar vessels determined with a video system. Ann Biomed Eng. 1984;12(5):463–479. doi: 10.1007/BF02363917. [DOI] [PubMed] [Google Scholar]
- Hecker M., Mülsch A., Bassenge E., Busse R. Vasoconstriction and increased flow: two principal mechanisms of shear stress-dependent endothelial autacoid release. Am J Physiol. 1993 Sep;265(3 Pt 2):H828–H833. doi: 10.1152/ajpheart.1993.265.3.H828. [DOI] [PubMed] [Google Scholar]
- Henrion D., Dechaux E., Dowell F. J., Maclour J., Samuel J. L., Lévy B. I., Michel J. B. Alteration of flow-induced dilatation in mesenteric resistance arteries of L-NAME treated rats and its partial association with induction of cyclo-oxygenase-2. Br J Pharmacol. 1997 May;121(1):83–90. doi: 10.1038/sj.bjp.0701109. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Henrion D., Laher I., Bevan J. A. Intraluminal flow increases vascular tone and 45Ca2+ influx in the rabbit facial vein. Circ Res. 1992 Aug;71(2):339–345. doi: 10.1161/01.res.71.2.339. [DOI] [PubMed] [Google Scholar]
- Hutcheson I. R., Griffith T. M. Mechanotransduction through the endothelial cytoskeleton: mediation of flow- but not agonist-induced EDRF release. Br J Pharmacol. 1996 Jun;118(3):720–726. doi: 10.1111/j.1476-5381.1996.tb15459.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Janmey P. A., Euteneuer U., Traub P., Schliwa M. Viscoelastic properties of vimentin compared with other filamentous biopolymer networks. J Cell Biol. 1991 Apr;113(1):155–160. doi: 10.1083/jcb.113.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Juncos L. A., Garvin J., Carretero O. A., Ito S. Flow modulates myogenic responses in isolated microperfused rabbit afferent arterioles via endothelium-derived nitric oxide. J Clin Invest. 1995 Jun;95(6):2741–2748. doi: 10.1172/JCI117977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koller A., Huang A. Impaired nitric oxide-mediated flow-induced dilation in arterioles of spontaneously hypertensive rats. Circ Res. 1994 Mar;74(3):416–421. doi: 10.1161/01.res.74.3.416. [DOI] [PubMed] [Google Scholar]
- Koller A., Sun D., Kaley G. Role of shear stress and endothelial prostaglandins in flow- and viscosity-induced dilation of arterioles in vitro. Circ Res. 1993 Jun;72(6):1276–1284. doi: 10.1161/01.res.72.6.1276. [DOI] [PubMed] [Google Scholar]
- Laher I., Bevan J. A. Staurosporine, a protein kinase C inhibitor, attenuates Ca2+-dependent stretch-induced vascular tone. Biochem Biophys Res Commun. 1989 Jan 16;158(1):58–62. doi: 10.1016/s0006-291x(89)80176-7. [DOI] [PubMed] [Google Scholar]
- Langille B. L., Adamson S. L. Relationship between blood flow direction and endothelial cell orientation at arterial branch sites in rabbits and mice. Circ Res. 1981 Apr;48(4):481–488. doi: 10.1161/01.res.48.4.481. [DOI] [PubMed] [Google Scholar]
- Levy B. I., Benessiano J., Henrion D., Caputo L., Heymes C., Duriez M., Poitevin P., Samuel J. L. Chronic blockade of AT2-subtype receptors prevents the effect of angiotensin II on the rat vascular structure. J Clin Invest. 1996 Jul 15;98(2):418–425. doi: 10.1172/JCI118807. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Malek A. M., Izumo S. Molecular aspects of signal transduction of shear stress in the endothelial cell. J Hypertens. 1994 Sep;12(9):989–999. [PubMed] [Google Scholar]
- Morita T., Kurihara H., Maemura K., Yoshizumi M., Nagai R., Yazaki Y. Role of Ca2+ and protein kinase C in shear stress-induced actin depolymerization and endothelin 1 gene expression. Circ Res. 1994 Oct;75(4):630–636. doi: 10.1161/01.res.75.4.630. [DOI] [PubMed] [Google Scholar]
- Morita T., Kurihara H., Maemura K., Yoshizumi M., Yazaki Y. Disruption of cytoskeletal structures mediates shear stress-induced endothelin-1 gene expression in cultured porcine aortic endothelial cells. J Clin Invest. 1993 Oct;92(4):1706–1712. doi: 10.1172/JCI116757. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oike M., Schwarz G., Sehrer J., Jost M., Gerke V., Weber K., Droogmans G., Nilius B. Cytoskeletal modulation of the response to mechanical stimulation in human vascular endothelial cells. Pflugers Arch. 1994 Oct;428(5-6):569–576. doi: 10.1007/BF00374579. [DOI] [PubMed] [Google Scholar]
- Osol G., Laher I., Kelley M. Myogenic tone is coupled to phospholipase C and G protein activation in small cerebral arteries. Am J Physiol. 1993 Jul;265(1 Pt 2):H415–H420. doi: 10.1152/ajpheart.1993.265.1.H415. [DOI] [PubMed] [Google Scholar]
- Osol G. Mechanotransduction by vascular smooth muscle. J Vasc Res. 1995 Sep-Oct;32(5):275–292. doi: 10.1159/000159102. [DOI] [PubMed] [Google Scholar]
- Segal S. S. Cell-to-cell communication coordinates blood flow control. Hypertension. 1994 Jun;23(6 Pt 2):1113–1120. doi: 10.1161/01.hyp.23.6.1113. [DOI] [PubMed] [Google Scholar]
- Sun D., Messina E. J., Kaley G., Koller A. Characteristics and origin of myogenic response in isolated mesenteric arterioles. Am J Physiol. 1992 Nov;263(5 Pt 2):H1486–H1491. doi: 10.1152/ajpheart.1992.263.5.H1486. [DOI] [PubMed] [Google Scholar]
- Terzi F., Maunoury R., Colucci-Guyon E., Babinet C., Federici P., Briand P., Friedlander G. Normal tubular regeneration and differentiation of the post-ischemic kidney in mice lacking vimentin. Am J Pathol. 1997 Apr;150(4):1361–1371. [PMC free article] [PubMed] [Google Scholar]
- Thoumine O., Ziegler T., Girard P. R., Nerem R. M. Elongation of confluent endothelial cells in culture: the importance of fields of force in the associated alterations of their cytoskeletal structure. Exp Cell Res. 1995 Aug;219(2):427–441. doi: 10.1006/excr.1995.1249. [DOI] [PubMed] [Google Scholar]