Advertisement

Cell Biochemistry and Biophysics

, Volume 38, Issue 3, pp 323–343 | Cite as

Differential responsiveness of vascular endothelial cells to different types of fluid mechanical shear stress

  • Abdul I. Barakat
  • Deborah K. Lieu
Review Article

Abstract

Early atherosclerotic lesions localize preferentially, in arterial regions exposed to low flow, oscillatory flow, or both; however, the cellular basis of this observation remains to be determined. Atherogenesis involves dysfunction of the vascular endothelium, the cellular monolayer lining the inner surfaces of blood vessels. How low flow, oscillatory flow, or both may lead to endothelial dysfunction remains unknown. Over the past two decades, fluid mechanical shear (or frictional) stress has been shown to intricately regulate the structure and function of vascular endothelial cells (ECs). Furthermore, recent data indicate that beyond being merely responsive to shear stress, ECs are able to distinguish among and respond differently to different types of shear stress. This review focuses on EC differential responses to different types of steady and unsteady shear stress and discusses the implications of these responses for the localization of early atherosclerotic lesions. The mechanisms by which endothelial differential responsiveness to different types of flow may occur are also discussed.

Index Entries

Shear stress endothelium mechanotransduction atherosclerosis hemodynamics 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Caro, C. G., Fitzgerald, J. M., and Schroter, R. C. (1969) Arterial wall shear and distribution of early atheroma in man. Nature 223, 1159–1161.PubMedGoogle Scholar
  2. 2.
    Nerem, R. M. (1992) Vascular fluid mechanics, the arterial wall, and atherosclerosis. J. Biomech. Eng. 114, 274–282.PubMedGoogle Scholar
  3. 3.
    Svindland, A. and Walloe, L. (1985) Distribution pattern for sudanophilic plaques in the descending thoracic and proximal abdominal aorta. Atherosclerosis 57, 219–224.PubMedGoogle Scholar
  4. 4.
    Ross, R., and Glomnset, J. A. (1977) The pathogenesis of atherosclerosis. N. Engl. J. Med. 295, 369–381.CrossRefGoogle Scholar
  5. 5.
    Ross, R. (1993) The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362, 801–809.PubMedGoogle Scholar
  6. 6.
    Langille, B. L., and O'Donnell, F. (1991) Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science 231, 405–407.Google Scholar
  7. 7.
    Pohl, U., Holtz, J., Busse, R.., and Bassenge, E. (1986) Crucial role of endothelium in the vasodilator response to increased flow in vivo. Hypertension 8, 37–47.PubMedGoogle Scholar
  8. 8.
    Barakat, A. I. and Davies, P. F. (1998) Mechanisms of shear stress transmission and transduction in endothelial cells. Chest 114, 58S-63S.PubMedGoogle Scholar
  9. 9.
    Barakat, A. I. (1999) Responsiveness of vascular endothelium to shear stress: potential role of ion channels and cellular cytoskeleton. Int. J. Mol. Med. 4, 323–332.PubMedGoogle Scholar
  10. 10.
    Davies, P. F. and Tripathi, S. C. (1993) Mechanical stress mechanisms and the cell- an endothelial paradigm. Circ. Res. 72, 239–245.PubMedGoogle Scholar
  11. 11.
    Davies, P. F. (1995) Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75, 519–560.PubMedGoogle Scholar
  12. 12.
    Malek, A. M. and Izumo, S. (1994) Molecular aspects of signal transduction of shear stress in endothelial cell J. Hypertension 12, 989–999.Google Scholar
  13. 13.
    Papadaki, M., and Eskin, S. G. (1997) Effects of fluid shear stress on gene regulation of vascular cells. Biotechnol. Prog. 13, 209–221.PubMedGoogle Scholar
  14. 14.
    Resnick, N. and Gimbrone, M. A., Jr. (1995) Hemodynamic forces are complex regulators of endothelial gene expression. FASEB J. 9, 874–882.PubMedGoogle Scholar
  15. 15.
    Traub, O. and Berk, B. C. (1998) Laminar shear stress-mechanisms by which endothelial cells transduce an atheroprotective forces. Arterioscl. Thromb. Vasc. Biol. 18, 677–685.PubMedGoogle Scholar
  16. 16.
    Asakura, T. and Karino, T. (1990) Flow patterns and spatial distribution of atherosclerotic lesions in human coronary arteries. Circ. Res. 66, 1045–1066.PubMedGoogle Scholar
  17. 17.
    Barakat, A. I., Karino, T., and Colton, C. K. (1997a) Microcinematographic studies of the flow field in the excised rabbit aorta and its major branches. Biorheology 34, 195–221.PubMedGoogle Scholar
  18. 18.
    Ku, D. N., Giddens., D. P., Zarins, C. K., and Glagov, S. (1985) Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low and oscillating shear stress. Arteriosclerosis 5, 293–301.PubMedGoogle Scholar
  19. 19.
    Moore, J. E., Jr., Xu, C., Glagov, S., Zarins, C. K., and Ku, D. N. (1994) Fluid wall shear stress measurements in a model of the human abdominal aorta: oscillatory behavior and relationship to atherosclerosis. Atherosclerosis 110, 225–240.PubMedGoogle Scholar
  20. 20.
    Perktold, K., Florian, H., Hilbert, D., and Peter, R. (1988) Wall shear stress distribution in the human carotid siphon during pulsatile flow. J. Biomech. 21, 663–671.PubMedGoogle Scholar
  21. 21.
    Perktold, K., and Rappitsch, G. (1995) Computer simulation of local blood flow and vessel mechanics in a compliant carotid artery bifurcation model. J. Biomech. 28, 845–856.PubMedGoogle Scholar
  22. 22.
    Chien, S., Usami, S., Taylor, M., Lundberg, J. L., and Gergersem, M. I. (1966) Effects of hematocrit and plasma proteins on human blood rheology at low shear rates. J. Appl. Physiol. 21, 81–87.PubMedGoogle Scholar
  23. 23.
    Acevedo, A. D., Bowser, S. S., Gerritsen M. E., and Bizios, R. (1993) Morphological and proliferative responses of endothelial cells to hydrostatic pressure: role of fibroblast growth factor. J. Cell. Physiol. 157, 603–614.PubMedGoogle Scholar
  24. 24.
    Letsou, G. V., Rosales, O., Maitz, S., Vogt, A., and Sumpio, B. E. (1990) Stimulation of adenylate cyclase activity in cultured endothelial cells subjected to cyclic stretch. J. Cardiovasc. Surg., 31, 634–639.Google Scholar
  25. 25.
    Sumpio, B. E., Banes, A. J., Buckley, M., and Johnson, G. (1987) Alterations in endothelial cell morphology and cytoskeletal protein synthesis during cyclic tensional deformation. J. Vasc. Surg. 7, 130–138.Google Scholar
  26. 26.
    Sumpio, B. E., Banes, A. J., Link, G. W., and Iba, T. (1990) Modulation of endothelial phenotype by cyclic stretch: inhibition of collagen production J. Surg. Res. 48, 415–420.PubMedCrossRefGoogle Scholar
  27. 27.
    Hutchison, K. J., Karpinski, E., Campbell, J. D., and Potemkowski, A. P. (1988) Aortic velocity contours at abdominal branches in anesthetized dogs. J. Biomech. 21, 277–286.PubMedGoogle Scholar
  28. 28.
    Duncan D. D., Bargeron, C. D., Borchardt, S. E., Deters, O. J., Gearhart, S. A., Mark, F. F., and Friedman, M. H. (1990) The effect of compliance on wall shear in casts of a human aortic bifurcation. J. Biomech. Eng. 112, 183–188.PubMedGoogle Scholar
  29. 29.
    Kuban, B. D. and Friedman, M. H. (1995) The effect of pulsatile frequency on wall shear in a compliant cast of a human aortic bifurcation. J. Biomech. Eng. 117, 219–223.PubMedGoogle Scholar
  30. 30.
    Chandran, K. B. (1993) Flow dynamics in the human aorta. J. Biomech. Eng. 115, 611–616.PubMedGoogle Scholar
  31. 31.
    Farthing, S. and Peronneau, P. (1979) Flow in the thoracic aorta. Cardiovasc. Res. 13, 607–620.PubMedGoogle Scholar
  32. 32.
    Hamakiotes, C. C. and Berger, S. A. (1988) Fully developed pulsatile flow in a curved pipe. J. Fluid Mech. 195, 23–55.Google Scholar
  33. 33.
    Hamakiotes, C. C. and Berger, S. A. (1990) Periodic flows through curved tubes: the effect of the frequency parameter. J. Fluid Mech. 210, 353–370.Google Scholar
  34. 34.
    Cheer, A. Y., Dwyer, H. A., Barakat A. I., Sy, E., and Bice, M. (1998) Computational study of the effect of geometric and flow parameters on the steady flow field at the rabbit aorto-celiac bifurcation. Biorheology 35, 415–435.PubMedGoogle Scholar
  35. 35.
    Sherwin, S. J., Shah, O., Doorly, D. J., Peiro, J. Papaharilaou, Y., Watkins, N., et al. (2000) The influence of out-of-plane geometry on the flow within a distal end-to-side anastomosis. J. Biomech. Eng. 122, 86–95.PubMedGoogle Scholar
  36. 36.
    Lei, M., Kleinstreuer, C., and Truskey, G. A. (1995) Numerical investigation and prediction of atherogenic sites in branching arteries. J. Biomech. Eng. 117, 350–357.PubMedGoogle Scholar
  37. 37.
    Reneman, R. S., van Merode, T., Hick, P., and Hoeks, A. P. G. (1985) Flow velocity patterns in and distensibility of the carotid artery bulb in subjects of various ages. Circulation 71, 500–509.PubMedGoogle Scholar
  38. 38.
    Liepsch, D. and Moravec, S., (1984) Pulsatile flow of non-Newtonian fluid in distensible models of human arteries. Biorheology 21, 571–586.PubMedGoogle Scholar
  39. 39.
    Kleinstreuer, C., Hyun, S., Buchanan, J. R., Jr., Longest, P. W., Archie, J. P. Jr., and Truskey, G. A. (2001) Hemodynamic parameters and early intimal thickening, in branching blood vessels. Crit. Rev. Biomed. Eng. 29, 1–64.PubMedGoogle Scholar
  40. 40.
    Barakat, A. I., Lever E. V., Pappone, P. A., and Davies, P. E. (1999) A flow-activated chloride selective membrane current in vascular endothelial cells. Circ. Res. 85, 820–828.PubMedGoogle Scholar
  41. 41.
    Jacobs, E. R., Cheliakine, C., and Davies, P. F. (1995) Shear activated channels in cell-attached patches of cultured bovine aortic endothelial cells. Pflug. Arch. 431, 129–131.Google Scholar
  42. 42.
    Nakache, M., and Gaub, H. E. (1988) Hydrodynamic hyperpolarization of endothelial cells. Proc. Natl. Acad. Sci. USA 85, 1841–1843.PubMedGoogle Scholar
  43. 43.
    Nakao, M., Ono, K., Fujisawa, F., and Iijima, T. (1999) Mechanical stress-induced Ca2+ entry and Cl current in cultured human aortic endothelial cells. Am. J. Physiol. 276, C238-C249.PubMedGoogle Scholar
  44. 44.
    Olesen, S., Clapham, D. E., and Davies, P. F. (1988) Haemodynamic shear stress activates a K+ current in vascular endothelial cells. Nature 331, 168–170.PubMedGoogle Scholar
  45. 45.
    Gudi, S. R. P., Clark, C. B., and Frangos, J. A. (1996) Fluid flow rapidly activates G proteins in human endothelial cells—involvement of G proteins in mechanochemical signal transduction. Circ. Res. 79, 834–839.PubMedGoogle Scholar
  46. 46.
    Gudi, S., Nolan, J. P., and Frangos, J. A. (1998) Modulation of GTPase activity of G proteins by fluid shear stress and phospholipid composition. Proc. Natl. Acad. Sci. USA 95, 2515–2519.PubMedGoogle Scholar
  47. 47.
    Cooke, J. P., Rossitch, E., Jr., Andon, N. A., Loscalzo, J., and Dzau, V. J. (1991) Flow activates an endothelial potassium channel to release an endogenous nitrovasodilator J. Clin. Invest. 88, 1663–1671.PubMedGoogle Scholar
  48. 48.
    Milner, P., Kirkpatric, K. A., Ralevic, V., Toothill, M., Pearson, J., and Burnstock, G. (1990) Endothelial cells cultured from human umbilical vein release ATP, substance P and acetylcholine in response to increased flow. Proc. R. Soc. Lond. Biol. 241, 245–248.Google Scholar
  49. 49.
    Noris, M., Morigi, M., Donadelli, R., Aiello, S., Foppolo, M., Todeschini, M., et al. (1995) Nitric oxide synthesis by cultured endothelial cells is modulated by flow conditions. Circ. Res. 76, 536–543.PubMedGoogle Scholar
  50. 50.
    Ando, J., Komatsuda, T., and Kamiya, A. (1988) Cytoplasmic calcium response to fluid shear stress in cultured vascular endothelial cells. In Vitro Cell Dev. Biol. 24, 871–877.PubMedGoogle Scholar
  51. 51.
    Dull, R. O., and Davies, P. F. (1991) Flow modulation of agonist (ATP)-response (Ca2+) coupling in vascular endothelial cells. Am. J. Physiol. 161, H149-H154.Google Scholar
  52. 52.
    Geiger, R. V., Berk, B. C., Alexander, R. W., and Nerem, R. M. (1992) Flow-induced calcium transients in single endothelial cells: spatial and temporal analysis. Am. J. Physiol. 262, C1411-C1417.PubMedGoogle Scholar
  53. 53.
    Shen, J., Luscinskas, F. W., Connolly, A., Dewey, Jr., C. F., and Gimbrone, M. A., Jr. (1992) Fluid shear stress modulates cytosolic free calcium in vascular endothelial cells. Am. J. Physiol. 262, C384-C390.PubMedGoogle Scholar
  54. 54.
    Butler, P. J., Norwich, G., Weinbaum, S., and Chien, S. (2001) Shear stress induces a time-and position-dependent increase in endothelial cell membrane fluidity. Am. J. Physiol. 280, C962-C969.Google Scholar
  55. 55.
    Haidekker, M. A., L'Heureux, N., and Frangos, J. A. (2000) Fluid shear stress increases membrane fluidity in endothelial cells, a study with DCVJ fluorescence. Am. J. Physiol. 278, H1401-H1406.Google Scholar
  56. 56.
    Ziegelstein, R. C., Cheng, L., and Capogrossi, C. (1992) Flow-dependent cytosolic acidification of vascular endothelial cells. Science 258, 656–659.PubMedGoogle Scholar
  57. 57.
    Ohno, M., Gibbons, G. H., Dzau, V. J., and Cooke, J. P. (1993) Shear stress elevates endothelial cGMP-role of a potassium channel and G protein coupling. Circulation 88, 193–197.PubMedGoogle Scholar
  58. 58.
    Frangos, J. A., Eskin, S. G., McIntire, L. V., and Ives, C. L. (1985) Flow effects on prostacyclin production by cultured human endothelial cells. Science 227, 1477–1479.PubMedGoogle Scholar
  59. 59.
    Grabowski, E. F., Jaffe, E. A., and Weksler, B. B. (1985) Prostacyclin production by cultured endothelial cell monolayers exposed to step increases in shear stress. J. Lab. Clin. Med. 105, 36–43.PubMedGoogle Scholar
  60. 60.
    Helmke, B. P., Goldman, R. D., and Davies, P. F. (2000) Rapid displacement of vimentin intermediate filaments in living endothelial cells exposed to flow. Circ. Res. 86, 745–752.PubMedGoogle Scholar
  61. 61.
    Tseng, H., Peterson, T. E., and Berk, B. C. (1995) Fluid shear stress stimulates mitogen-activated protein kinase in endothelial cells. Circ. Res. 77, 869–878.PubMedGoogle Scholar
  62. 62.
    Yan, C., Takahashi, M., Okuda, M., Lee, J., and Berk, B. C. (1999) Fluid shear stress stimulates big mitogen-activated protein kinase 1 (BMK1) activity in endothelial cells. J. Biol. Chem. 274, 143–150.PubMedGoogle Scholar
  63. 63.
    Lan, Q., Mercurius, K. O., and Davies, P. F. (1994) Stimulation of transcription factors NF_B and AP1 in endothelial cells subjected to shear stress. Biochem. Biophys. Res. Commun. 201, 950–956.PubMedGoogle Scholar
  64. 64.
    Hsieh, H., Li, N., and Frangos, J. A. (1993) Pulsatile and steady flow induces c-fos expression in human endothelial cells. J. Cell Physiol. 154, 143–151.PubMedGoogle Scholar
  65. 65.
    Ranjan, V., and Diamond, S. L. (1993) Fluid shear stress induces synthesis and nuclear localization of c-fos in cultured human endothelial cells. Biochem. Biophys. Res. Commun. 196, 79–84.PubMedGoogle Scholar
  66. 66.
    Braddock, M., Schwachtgen, J., Houston, P., Dickson, M. C., Lee, M. J., and Campbell, C. J. (1998) Fluid shear stress modulation of gene expression in endothelial cells. News Physiol. Sci. 13, 241–246.PubMedGoogle Scholar
  67. 67.
    Garcia-Cardena, G., Comander, J., Anderson, K. R., Blackman, B. R., and Gimbrone, M. A., Jr. (2001) Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc. Natl. Acad. Sci. USA 98, 4478–4485.PubMedGoogle Scholar
  68. 68.
    Malek, A. M., and Izumo, S. (1992) Physiological fluid shear stress causes downregulation of endothelin-1 mRNA bovine aortic endothelium. Am. J. Physiol. 263, C389-C396.PubMedGoogle Scholar
  69. 69.
    Yoshizumi, M., Kurihara, H., Sugiyama, T., Takaku, F., Yanagisawa, M., Masaki, T., and Yazaki, Y. (1989) Hemodynamic shear stress stimulates endothelin production by cultured endothelial cells. Biochem. Biophys. Res. Commun. 161, 859–864.PubMedGoogle Scholar
  70. 70.
    Malek, A. M., Izumo, S., and Alper, S. L. (1999) Modulation by pathophysiological stimuli of the shear stress-induced up-regulation of endothelial nitric oxide synthase expression in endothelial cells. Neurosurgery 45, 334–345.PubMedGoogle Scholar
  71. 71.
    Uematsu, M., Ohara, Y., Navas, J. P., Nishida, K., Murphy, T. J., Alexander, R. W., et al. (1995) Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress. Am. J. Physiol. 269, C1371-C1378.PubMedGoogle Scholar
  72. 72.
    Bao, X., Lu, C., and Frangos, J. A. (1999) Temporal gradients in shear but not steady shear stress induces PDGF-A and MCP-1 expression in endothelial cells—role of NO, NFκB, and egr-1. Arterioscler. Thromb. Vasc. Biol. 19, 996–1003.PubMedGoogle Scholar
  73. 73.
    Hsieh, H., Li, N., and Frangos, J. A. (1991) Shear stress increases endothelial platelet-derived growth factor mRNA levels. Am. J. Physiol. 29, H642-H646.Google Scholar
  74. 74.
    Malek, A. M., Gibbons, G. H., Dzau, V. J., and Izumo, S. (1993) Fluid shear stress differentially modulates expression of genes encoding basic fibroblast growth factor and platelet-derived growth factor B chain in vascular endothelium. J. Clin. Invest. 92, 2013–2021.PubMedGoogle Scholar
  75. 75.
    Lum, R. M., Wiley, L. M., and Barakat, A. I. (2000) Influence of different forms of fluid shear stress on vascular endothelial TGF-betal1 mRNA expression. Int. J. Mol. Med. 5, 635–641.PubMedGoogle Scholar
  76. 76.
    Ohno, M., Cooke, J. P., Dzau, V. J., and Gibbons, G. H. (1995) Fluid shear stress induces endothelial transforming growth factor beta-1 transcription and production. J. Clin. Invest. 95, 1363–1369.PubMedCrossRefGoogle Scholar
  77. 77.
    Nagel, T., Resnick, N., Atkinson, W. J., Dewey, Jr., C. F., and Gimbrone, Jr., M. A. (1994) Shear stress selectively upregulates, intercellular adhesion molecule-1 expression in cultured human vascular endothelial cells. J. Clin. Invest. 94, 885–891.PubMedGoogle Scholar
  78. 78.
    Tsuboi, H., Ando, J., Korenga, R., Takada, Y., and Kamiya, A. (1995) Flow stimulates ICAM-1 expression time and shear stress dependently in cultured human endothelial cells. Biochem. Biophys. Res. Commun. 206, 988–996.PubMedGoogle Scholar
  79. 79.
    Kudo, S., Morigaki, R., Saito, J., Ikeda, M., Oka, K., and Tanishita, K. (2000) Shear-stress effect on mitochondrial membrane potential and albumin uptake in cultured endothelial cells. Biochem. Biophys. Res. Commun. 270, 616–621.PubMedGoogle Scholar
  80. 80.
    Sprague, E. A., Steinbach, B. L., Nerem, R. M., and Schwartz, C. J. (1987) Influence of a luminar steady-state fluid-imposed wall shear stress on the binding, internalization, and degradation of low-density lipoprotein by cultured arterial endothelium. Circulation 76, 648–656.PubMedGoogle Scholar
  81. 81.
    Sato, M., Levesque, M. J., and Nerem, R. M. (1987) Micropipette aspiration of cultured bovine aortic endothelial cells exposed to shear stress. Arteriosclerosis 7, 276–286.PubMedGoogle Scholar
  82. 82.
    Sato, M., Ohshima, N., and Nerem, R. M. (1996) Viscoelastic properties of cultured porcine aortic endothelial cells exposed to shear stress. J. Biomech. 29, 461–467.PubMedGoogle Scholar
  83. 83.
    Nerem, R. M., Levesque, M. J., and Cornhill, J. F. (1981) Vascular endothelial morphology as an indicator of the pattern of blood flow. J. Biomech. Eng. 103, 172–177.PubMedGoogle Scholar
  84. 84.
    Ookawa, K., Sato, M., and Ohshima, N. (1992) Changes in the microstructure of cultured porcine aortic endothelial cells in the early stage after applying a fluid-imposed shear stress. J. Biomech. 25, 1321–1328.PubMedGoogle Scholar
  85. 85.
    Wechezak, A. R., Viggers, R. F., and Sauvage, L. R. (1985) Fibronectin and F-actin redistribution in cultured endothelial cells exposed to shear stress. Lab. Invest. 53, 639–647.PubMedGoogle Scholar
  86. 86.
    Wechezak, A. R., Wight, T. N., Viggers, R. F., and Sauvage, L. R. (1989) Endothelial adherence under shear stress is dependent upon microfilament reorganization. J. Cell Physiol. 139, 136–146.PubMedGoogle Scholar
  87. 87.
    Dewey, Jr., C. F., Bussolari, S. R., Gimbrone, Jr., M. A., and Davies, P. F. (1981) The dynamic response of vascular endothelial cells to fluid shear stress. J. Biomech. Eng. 103, 177–185.PubMedGoogle Scholar
  88. 88.
    Eskin, S. G., Ives, C. L., McIntire, L. V., and Navarro, L. T. (1984) Response of cultured endothelial cells to steady flow. Microvasc. Res. 28, 87–93.PubMedGoogle Scholar
  89. 89.
    Suvatne, J., Barakat, A. I., and O'Donnell, M. A. (2001) Flow-induced expression of endothelial Na−K−Cl cotransport: dependence on K+ and Cl channels Am. J. Physiol. 180, C216-C227.Google Scholar
  90. 90.
    Nilius, B., and Droogmans, G. (2001) Ion channels and their functional role in vascular endothelium. Physiol. Rev. 81, 1415–1459.PubMedGoogle Scholar
  91. 91.
    Berthiaume, F., and Frangos, J. A. (1992) Flow-induced prostacyclin production is mediated by a pertussis toxin-sensitive G protein. FEBS Lett. 308, 277–279.PubMedGoogle Scholar
  92. 92.
    Barbee, K. A., Mundel, T., Lal, R., and Davies, P. F. (1995) Subcellular distribution of shear stress at the surface of flow aligned and non-aligned endothelial monolayers. Am. J. Physiol. 268, H1765-H1772.PubMedGoogle Scholar
  93. 93.
    Barakat, A. I., Marini, R. P., and Colton, C. K. (1997b) Measurement of flow rates through aortic branches in the anesthetized rabbits. Lab. Anim. Sci. 47, 184–189.PubMedGoogle Scholar
  94. 94.
    Davies, P. F., Remuzzi, A., Gordon, E. J., Dewey, C. F., Jr., and Gimbrone, E. A., Jr. (1986) Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro. Proc. Natl. Acad. Sci. 83, 2114–2117.PubMedGoogle Scholar
  95. 95.
    Malek, A. M., Jackman, R., Rosenberg, R. D., and Izumo, S. (1994) Endothelial expression of thrombomodulin is reversibly regulated by fluid shear stress. Circ. Res. 74, 852–860.PubMedGoogle Scholar
  96. 96.
    Helminger, G., Berk, B. C., and Nerem, R. M. (1995) Calcium responses of endothelial cell monolayers subjected to pulsatile and steady laminar flow differ. Am. J. Physiol. 269, C367-C375.Google Scholar
  97. 97.
    Peng, X., Recchia, F. A., Byrne, B. J., Wittstein, I. S., Ziegelstein, R. C., and Kass, D. A. (2000) In vitro system to study realistic pulsatile flow and stretch signaling in cultured vascular cells. Am. J. Physiol. 279, C797-C805.Google Scholar
  98. 98.
    Lieu, D. K., Pappone, P. A., and Barakat, A. I. (2001) Role of ion channels in shear stress sensing in vascular endothelial cells. Ann. Biomed. Eng. 29, S-27.Google Scholar
  99. 99.
    Levesque, M. J., and Nerem, R. M. (1990) Vascular endothelial cell proliferation in cultured and the influence of flow. Biomaterials 11, 702–707.PubMedGoogle Scholar
  100. 100.
    Helminger, G., Geiger, R. V., Schreck, S., and Nerem, R. M. (1991) Effects of pulsatile flow on cultured vascular endothelial cell morphology. J. Biomech. Eng. 113, 123–131.Google Scholar
  101. 101.
    Ando, J., Ohtsuka, A., Korenaga, R., Kawamura, T., and Kamiya, A. (1993) Wall shear stress rather than shear rate regulates cytoplasmic Ca++ responses to flow in vascular endothelial cells. Biochem. Biophys. Res. Commun. 190, 716–723.PubMedGoogle Scholar
  102. 102.
    Nollert, M. U., and McIntire, L. V. (1992) Convective mass transfer effects on the intracellular calcium response of endothelial cells. J. Biomech. Eng. 114, 321–326.PubMedGoogle Scholar
  103. 103.
    Shen, J., Gimbrone, M. A., Jr., Luscinskas, F. W., and Dewey, C. F. Jr. (1993) Regulation of adenine nucleotide concentration at endothelium-fluid interface by viscous shear stress. Biophys. J. 64, 1323–1330.PubMedGoogle Scholar
  104. 104.
    John, K., and Barakat, A. I. (2001) Modulation of ATP/ADP concentration at the endothelial surface by shear stress: effect of flow-induced ATP release. Ann. Biomed. Eng. 29, 740–751.PubMedGoogle Scholar
  105. 105.
    Barakat, A. I. (2001) A model for shear, stress-induced deformation of a flow sensor on the surface of vascular endothelial cells. J. Theor. Biol. 210, 221–236.PubMedGoogle Scholar
  106. 106.
    Ziegler, T., Bouzourene, K., Harrison, V. J., Brunner, H. R., and Hayoz, D. (1998) Influence of oscillatory and unidirectional flow environments on the expression of endothelin and nitric oxide synthase in cultured endothelial cells. Arterioscler. Thromb. Vasc. Biol. 18, 686–692.PubMedGoogle Scholar
  107. 107.
    Manevich, Y., Al-Mehdi, A., Muzykantov, V., and Fisher, A. B. (2001) Oxidative burst and NO generation as initial response to ischemia in flow-adapted endothelial cells. Am. J. Physiol. 280, H2126-H2135.Google Scholar

Copyright information

© Humana Press Inc 2003

Authors and Affiliations

  1. 1.Department of Mechanical and Aeronautical EngineeringUniversity of CaliforniaDavis

Personalised recommendations