Skip to main content
Log in

Cellular Fluid Mechanics and Mechanotransduction

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Adamson, R. H., and G. Clough. Plasma proteins modify the endothelial cell glycocalyx of frog mesenteric microvessels. J. Physiol. 445:473–486, 1992.

    Google Scholar 

  2. Bao, G. Mechanics of biomolecules. J. Mech. Phys. Solids 50:2237–2274, 2002.

    MathSciNet  MATH  Google Scholar 

  3. 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.

    Google Scholar 

  4. 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.

    Google Scholar 

  5. Chen, C. S., J. Tan, and J. Tien. Mechanotransduction at cell–matrix and cell–cell contacts. Annu. Rev. Biomed. Eng. 6:275–302, 2004.

    Article  Google Scholar 

  6. 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.

    Google Scholar 

  7. 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.

    Google Scholar 

  8. Damiano, E. R. The effect of the endothelial glycocalyx on the motion of red blood cells through capillaries. Microvasc. Res. 55:77–91, 1998.

    Article  Google Scholar 

  9. Davies, P. F. Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75:519–560, 1995.

    Google Scholar 

  10. Davies, P. F. Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75:519–560, 1995.

    Google Scholar 

  11. 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.

    Article  Google Scholar 

  12. 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.

    Google Scholar 

  13. 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.

    Article  MathSciNet  MATH  Google Scholar 

  14. 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.

    Article  Google Scholar 

  15. Fry, D. L. Hemodynamic forces in atherogenesis. In: Cerebrovascular Diseases, edited by P Scheinberg. Raven Press, 1976, pp. 77–95.

  16. Geiger, B., and A. Bershadsky. Exploring the neighborhood: Adhesion-coupled cell mechanosensors. Cell 110:139–142, 2002.

    Article  Google Scholar 

  17. 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.

    Google Scholar 

  18. Hamill, O. P., and B. Martinac. Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81:685–740, 2001.

    Google Scholar 

  19. 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.

    Google Scholar 

  20. Henry, C. B., and B. R. Duling. Permeation of the luminal capillary glycocalyx is determined by hyaluronan. Am. J. Physiol. 277:H508–H514, 1999.

    Google Scholar 

  21. 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.

    Google Scholar 

  22. Ingber, D. E. Cellular basis of mechanotransduction. Biol. Bull. 194:323–325; Discussion 325–327, 1998.

    Google Scholar 

  23. 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.

  24. 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.

    Article  Google Scholar 

  25. Lehoux, S., and A. Tedgui. Cellular mechanics and gene expression in blood vessels. J. Biomech. 36:631–643, 2003.

    Article  Google Scholar 

  26. Luft, J. H. Fine structure of capillary and endocapillary layer as revealed by ruthenium red. Fed. Proc. 25:1773–1783, 1966.

    Google Scholar 

  27. 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.

    Article  Google Scholar 

  28. 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.

    Google Scholar 

  29. Mulivor, A. W., and H. H. Lipowsky. Role of glycocalyx in leukocyte-endothelial cell adhesion. Am. J. Physiol. 283:H1282–H1291, 2002.

    Google Scholar 

  30. 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.

    Google Scholar 

  31. 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.

    Google Scholar 

  32. 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.

    Google Scholar 

  33. Pries, A. R., T. W. Secomb, and P. Gaehtgens. The endothelial surface layer. Eur. J. Physiol. 440:653–666, 2000.

    Article  Google Scholar 

  34. 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.

    Article  Google Scholar 

  35. Sawada, Y., and M. P. Sheetz. Force transduction by Triton cytoskeletons. J. Cell Biol. 156:609–615, 2002.

    Article  Google Scholar 

  36. 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.

    Article  Google Scholar 

  37. 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.

    Google Scholar 

  38. 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.

    Article  Google Scholar 

  39. Tarbell, J. M. Mass transport in arteries and the localization of atherosclerosis. Annu. Rev. Biomed. Eng. 5:79–118, 2003.

    Article  Google Scholar 

  40. 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.

    Article  Google Scholar 

  41. Tschumperlin, D. J. EGRF autocrine signaling in a compliant interstitial space: Mechanotransduction from the outside-in. Cell Cycle 3:996–997, 2004.

    Google Scholar 

  42. van den Berg, B. M., H. Vink, and J. A. Spaan. The endothelial glycocalyx protects against myocardial edema. Circ. Res. 92:e592–e594, 2003.

    Article  Google Scholar 

  43. 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.

    Google Scholar 

  44. 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.

    Article  Google Scholar 

  45. Zamir, E., and B. Geiger. Molecular complexity and dynamics of cell-matrix adhesions. J. Cell Sci. 114:3583–3590, 2001.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John M. Tarbell.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-005-8775-z

Keywords

Navigation