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

Cell Biochemistry and Biophysics

Volumn 38, Issue 3, 2003, Pages 323-343

  Barakat, Abdul I ^a   Lieu, Deborah K ^a  

^a University of California   (United States)

Author keywords

Atherosclerosis; Endothelium; Hemodynamics; Mechanotransduction; Shear stress

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; BLOOD FLOW VELOCITY; COMPARATIVE STUDY; CYTOLOGY; HUMAN; MECHANICAL STRESS; PHYSIOLOGY; PULSATILE FLOW; REVIEW; VASCULAR ENDOTHELIUM;

ANIMALS; BLOOD FLOW VELOCITY; ENDOTHELIUM, VASCULAR; HUMANS; MODELS, BIOLOGICAL; PULSATILE FLOW; STRESS, MECHANICAL;

EID: 0242439089     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1385/CBB:38:3:323     Document Type: Review

References (107)

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.
2. Nerem, R. M. (1992) Vascular fluid mechanics, the arterial wall, and atherosclerosis. J. Biomech. Eng. 114, 274-282.
3. Svindland, A. and Walloe, L. (1985) Distribution pattern for sudanophilic plaques in the descending thoracic and proximal abdominal aorta. Atherosclerosis 57, 219-224.
4. Ross, R. and Glomnset, J. A. (1977) The pathogenesis of atherosclerosis. N. Engl J. Med. 295, 369-381.
5. Ross, R. (1993) The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362, 801-809.
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.
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.
8. Barakat, A. I. and Davies, P. F. (1998) Mechanisms of shear stress transmission and transduction in endothelial cells. Chest 114, 58S-63S.
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.
10. Davies, P. F. and Tripathi, S. C. (1993) Mechanical stress mechanisms and the cell- an endothelial paradigm. Circ. Res. 72, 239-245.
11. Davies, P. F. (1995) Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75, 519-560.
12. Malek, A. M. and Izumo, S. (1994) Molecular aspects of signal transduction of shear stress in endothelial cell. J. Hypertension 12, 989-999.
13. Papadaki, M., and Eskin, S.G. (1997) Effects of fluid shear stress on gene regulation of vascular cells. Biotechnol. Prog. 13, 209-221.
14. Resnick, N. and Gimbrone, M. A., Jr. (1995) Hemodynamic forces are complex regulators of endothelial gene expression. FASEB J. 9, 874-882.
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.
16. Asakura, T. and Karino, T. (1990) Flow patterns and spatial distribution of atherosclerotic lesions in human coronary arteries. Circ. Res. 66, 1045-1066.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
30. Chandran, K.B. (1993) Flow dynamics in the human aorta. J. Biomech. Eng. 115, 611-616.
31. Farthing, S. and Peronneau, P. (1979) Flow in the thoracic aorta. Cardiovasc. Res. 13, 607-620.
32. Hamakiotes, C. C. and Berger, S. A. (1988) Fully developed pulsatile flow in a curved pipe. J. Fluid Mech. 195, 23-55.
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.
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.
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.
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.
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.
38. Liepsch, D. and Moravec, S. (1984) Pulsatile flow of non-Newtonian fluid in distensible models of human arteries. Biorheology 21, 571-586.
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.
40. Barakat, A. I., Lever, E. V., Pappone, P. A., and Davies, P. F. (1999) A flow-activated chloride-selective membrane current in vascular endothelial cells. Circ. Res. 85, 820-828.
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.
42. Nakache, M. and Gaub, H. E. (1988) Hydrodynamic hyperpolarization of endothelial cells. Proc. Natl. Acad. Sci. USA 85, 1841-1843.
43. - current in cultured human aortic endothelial cells. Am. J. Physiol. 276, C238-C249.
44. + current in vascular endothelial cells. Nature 331, 168-170.
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.
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.
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.
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.
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.
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.
51. 2+) coupling in vascular endothelial cells. Am. J. Physiol. 161, H149-H154.
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.
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.
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.
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.
56. Ziegelstein, R. C., Cheng, L., and Capogrossi, C. (1992) Flow-dependent cytosolic acidification of vascular endothelial cells. Science 258, 656-659.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
75. Lum, R. M., Wiley, L. M., and Barakat, A. I. (2000) Influence of different forms of fluid shear stress on vascular endothelial TGF-beta1 mRNA expression. Int. J. Mol. Med. 5, 635-641.
76. Ohno, M., Cooke, J. P., Dzau, V. J., and Gibbons, G. H. (1995) Fluid shear stress induces endothelial transforming growth factor beta-1transcription and production. J. Clin. Invest. 95, 1363-1369.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
89. - channels. Am. J. Physiol. 180, C216-C227.
90. Nilius, B. and Droogmans, G. (2001) Ion channels and their functional role in vascular endothelium. Physiol. Rev. 81, 1415-1459.
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.
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, H1765-1772.
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.
94. Davies, P. F., Remuzzi, A., Gordon, E. J., Dewey, C. F., Jr., and Gimbrone, M. A., Jr. (1986) Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro. Proc. Natl. Acad. Sci. 83, 2114-2117.
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.
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.
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.
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.
99. Levesque, M. J. and Nerem, R. M. (1990) Vascular endothelial cell proliferation in cultured and the influence of flow. Biomaterials 11, 702-707.
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.
101. ++ responses to flow in vascular endothelial cells. Biochem. Biophys. Res. Commun. 190, 716-723.
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.
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.
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.
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.
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.
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.