Abstract
Mechanotransduction, the transformation of an applied mechanical force into a cellular biomolecular response, is briefly reviewed focusing on fluid shear stress and endothelial cells. Particular emphasis is placed on recent studies of the surface proteoglycan layer (glycocalyx) as a primary sensor of fluid shear stress that can transmit force to apical structures such as the plasma membrane or the actin cortical web where transduction can take place or to more remote regions of the cell such as intercellular junctions and basal adhesion plaques where transduction can also occur. All of these possibilities are reviewed from an integrated perspective.
Similar content being viewed by others
References
Adamson, R. H., and G. Clough. Plasma proteins modify the endothelial cell glycocalyx of frog mesenteric microvessels. J. Physiol. 445:473–486, 1992.
Bao, G. Mechanics of biomolecules. J. Mech. Phys. Solids 50:2237–2274, 2002.
Butler, P. J., T. C. Tsou, J. Y. Li, S. Usami, and S. Chien. Rate sensitivity of shear-induced changes in the lateral diffusion of endothelial cell membrane lipids: A role for membrane perturbation in shear-induced MAPK activation. FASEB J. 16:216–218, 2002.
Caro, C. G., and R. M. Nerem. Transport of 14C-4-cholesterol between serum and wall in the perfused dog common carotid artery. Circ. Res. 32:187–205, 1973.
Chen, C. S., J. Tan, and J. Tien. Mechanotransduction at cell–matrix and cell–cell contacts. Annu. Rev. Biomed. Eng. 6:275–302, 2004.
Chen, K. D., Y. S. Li, M. Kim, S. Li, S. Yuan, S. Chien, and J. Y. Shyy. Mechanotransduction in response to shear stress. Roles of receptor tyrosine kinases, integrins, and Shc. J. Biol. Chem. 274:18393–18400, 1999.
Constantinescu, A. A., H. Vink, and J. A. Spaan. Elevated capillary tube hematocrit reflects degradation of endothelial cell glycocalyx by oxidized LDL. Am. J. Physiol. 280:H1051–H1057, 2001.
Damiano, E. R. The effect of the endothelial glycocalyx on the motion of red blood cells through capillaries. Microvasc. Res. 55:77–91, 1998.
Davies, P. F. Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75:519–560, 1995.
Davies, P. F. Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75:519–560, 1995.
Dewey, C. F., S. R. Bussolari, M. A. Gimbrone, P. F. Davies. The dynamic response of vascular endothelial cells to fluid shear stress. J. Biomech. Eng. 103:177–185, 1981.
Drenckhahn, D., and W. Ness. The endothelial contractile cytoskeleton. In: Vascular Endothelium: Physiology, Pathology, and Therapeutic Opportunities. New Horizon Series 3:1–25 (Schattauer, Stuttgart) 1997.
Feng, J. Weinbaum S. Lubrication theory in highly compressible porous media: The mechanics of skiing, from red cells to humans. J. Fluid. Mech. 422:281–317, 2000.
Florian, J. A., J. R. Kosky, K. Ainslie, Z. Pang, R. O. Dull, and J. M. Tarbell. Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ. Res. 93:e136–e142, 2003.
Fry, D. L. Hemodynamic forces in atherogenesis. In: Cerebrovascular Diseases, edited by P Scheinberg. Raven Press, 1976, pp. 77–95.
Geiger, B., and A. Bershadsky. Exploring the neighborhood: Adhesion-coupled cell mechanosensors. Cell 110:139–142, 2002.
Haidekker, M. A., N. L'Heureux, and J. A. Frangos. Fluid shear stress increases membrane fluidity in endothelial cells: A study with DCVJ fluorescence. Am. J. Physiol. Heart Circ. Physiol. 278:H1401–H1406, 2000.
Hamill, O. P., and B. Martinac. Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81:685–740, 2001.
Hecker, M., A. Mulsch, E. Bassenge, and R. Busse. Vasoconstriction and increased flow: Two principal mechanisms of shear stress-dependent endothelial autocoid release. Am. J. Physiol. 265:H828–H833, 1993.
Henry, C. B., and B. R. Duling. Permeation of the luminal capillary glycocalyx is determined by hyaluronan. Am. J. Physiol. 277:H508–H514, 1999.
Hu, S., J. Chen, B. Fabry, Y. Numaguchi, A. Gouldstone, D. E. Ingber, J. J. Fredberg, J. P. Butler, and N. Wang. Intracellular stress tomography reveals stress focusing and structural anisotropy in cytoskeleton of living cells. Am. J. Physiol. Cell Physiol. 285:C1082–C1090, 2003.
Ingber, D. E. Cellular basis of mechanotransduction. Biol. Bull. 194:323–325; Discussion 325–327, 1998.
Kamm, R. D., and M. R. Kaazempur-Mofrad. On the molecular basis for mechanotransduction, Mech. Chem. Biosyst. 1(4) MCB online (http://www.techscience.com/mcb), 2004.
Karcher, H., J. Lammerding, H. Huang, R. T. Lee, R. D. Kamm, and M. R. Kaazempur-Mofrad. A three-dimensional viscoelastic model for cell deformation with experimental verification. Biophys. J. 85:3336–3349, 2003.
Lehoux, S., and A. Tedgui. Cellular mechanics and gene expression in blood vessels. J. Biomech. 36:631–643, 2003.
Luft, J. H. Fine structure of capillary and endocapillary layer as revealed by ruthenium red. Fed. Proc. 25:1773–1783, 1966.
Mack, P. J., M. R. Kaazempur-Mofrad, H. Karcher, R. T. Lee, and R. D. Kamm. Force-induced focal adhesion translocation: Effects of force amplitude and frequency. Am. J. Physiol. Cell Physiol. 287:C954–C962, 2004.
Mochizuki, S., H. Vink, O. Hiramatsu, T. Kajita, F. Shigeto, J. Spaan, and F. Kajiya. Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. Am. J. Physiol. 285:H722–H726, 2003.
Mulivor, A. W., and H. H. Lipowsky. Role of glycocalyx in leukocyte-endothelial cell adhesion. Am. J. Physiol. 283:H1282–H1291, 2002.
Norvell, S. M., S. M. Ponik, D. K. Bowen, R. Gerard, and F. M. Pavalko. Fluid shear stress induction of COX-2 protein and prostaglandin release in cultured MC3T3-E1 osteoblasts does not require intact microfilaments or microtubules. J. Appl. Physiol. 96:957–966, 2004.
Odde, D. J., L. Ma, A. H. Briggs, A. DeMarco, and M. W. Kirschner. Microtubule bending and breaking in living fibroblasts. J. Cell Sci. 112(Pt 19):3283–3288, 1999.
Pohl, U., K. Herlan, A. Huang, and E. Bassenge. EDRF-mediated shear-induced dilation opposes myogenic vasoconstriction in small rabbit arteries. Am. J. Physiol. 261: H2106–H2113, 1991.
Pries, A. R., T. W. Secomb, and P. Gaehtgens. The endothelial surface layer. Eur. J. Physiol. 440:653–666, 2000.
Riveline, D., E. Zamir, N. Q. Balaban, U. S. Schwarz, T. Ishizaki, S. Narumiya, Z. Kam, B. Geiger, and A. D. Bershadsky. Focal contacts as mechanosensors: Externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J. Cell Biol. 153:1175–1186, 2001.
Sawada, Y., and M. P. Sheetz. Force transduction by Triton cytoskeletons. J. Cell Biol. 156:609–615, 2002.
Schnittler, H. J., S. W. Schneider, H. Raifer, F. Luo, P. Dieterich, I. Just, and K. Aktories. Role of actin filaments in endothelial cell-cell adhesion and membrane stability under fluid shear stress. Pflugers Arch. 442:675–687, 2001.
Secomb, T. W., R. Hsu, and A. R. Pries. Effect of the endothelial surface layer on transmission of fluid shear stress to endothelial cells. Biorheology 38:143–150, 2001.
Squire, J. M., M. Chew, G. Nneji, C. Neal, J. Barry, and C. Michel. Quasi-periodic substructure in the microvessel endothelial glycocalyx: A possible explanation for molecular filtering? J. Struct. Biol. 136:239–255, 2001.
Tarbell, J. M. Mass transport in arteries and the localization of atherosclerosis. Annu. Rev. Biomed. Eng. 5:79–118, 2003.
Thi, M. M., J. M. Tarbell, S. Weinbaum, and D. C. Spray. The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: A “bumper car” model. Proc. Natl. Acad. Sci. U.S.A. 101:16483–16485, 2004.
Tschumperlin, D. J. EGRF autocrine signaling in a compliant interstitial space: Mechanotransduction from the outside-in. Cell Cycle 3:996–997, 2004.
van den Berg, B. M., H. Vink, and J. A. Spaan. The endothelial glycocalyx protects against myocardial edema. Circ. Res. 92:e592–e594, 2003.
Vink, H., A. A. Constantinescu, and J. A. Spaan. Oxidized lipoproteins degrade the endothelial surface layer: Implications for platelet-endothelial cell adhesion. Circulation 101:1500–1502, 2000.
Weinbaum, S., X. Zhang, Y. Han, H. Vink, and S. C. Cowin. Mechanotransduction and flow across the endothelial glycocalyx. Proc. Natl. Acad. Sci. U.S.A. 100:7988–7995, 2003.
Zamir, E., and B. Geiger. Molecular complexity and dynamics of cell-matrix adhesions. J. Cell Sci. 114:3583–3590, 2001.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tarbell, J.M., Weinbaum, S. & Kamm, R.D. Cellular Fluid Mechanics and Mechanotransduction. Ann Biomed Eng 33, 1719–1723 (2005). https://doi.org/10.1007/s10439-005-8775-z
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10439-005-8775-z