Vascular endothelial responses to altered shear stress: Pathologic implications for atherosclerosis

References

• Caro CG, Fitz-Gerald JM, Schroter RC. Atheroma and arterial wall shear: observation, correlation and proposal of a shear dependent mass transfer mechanism for atherogenesis. Proc R Soc Lond B Biol Sci. 1971; 177: 109–59
   PubMed Web of Science ®Google Scholar
• Zarins CK, Giddens DP, Bharadvaj BK, Sottiurai VS, Mabon RF, Glagov S. Carotid bifurcation atherosclerosis. Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ Res. 1983; 53: 502–14
   PubMed Web of Science ®Google Scholar
• Ku DN, Giddens DP, Zarins CK, Glagov S. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis. 1985; 5: 293–302
   PubMedGoogle Scholar
• Asakura T, Karino T. Flow patterns and spatial distribution of atherosclerotic lesions in human coronary arteries. Circ Res. 1990; 66: 1045–66
   PubMed Web of Science ®Google Scholar
• Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA. 1999; 282: 2035–42
   PubMed Web of Science ®Google Scholar
• Nerem RM. Vascular fluid mechanics, the arterial wall, and atherosclerosis. J Biomech Eng. 1992; 114: 274–82
   PubMed Web of Science ®Google Scholar
• Wootton DM, Ku DN. Fluid mechanics of vascular systems, diseases, and thrombosis. Annu Rev Biomed Eng. 1999; 1: 299–329
   PubMed Web of Science ®Google Scholar
• Chien S, Li S, Shyy YJ. Effects of mechanical forces on signal transduction and gene expression in endothelial cells. Hypertension. 1998; 31: 162–9
   PubMed Web of Science ®Google Scholar
• Fisher AB, Chien S, Barakat AI, Nerem RM. Endothelial cellular response to altered shear stress. Am J Physiol Lung Cell Mol Physiol. 2001; 281: L529–33
   PubMed Web of Science ®Google Scholar
• Li YS, Haga JH, Chien S. Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech. 2005; 38: 1949–71
   PubMed Web of Science ®Google Scholar
• Chien S. Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am J Physiol Heart Circ Physiol. 2007; 292: H1209–24
   PubMed Web of Science ®Google Scholar
• Topper JN, Gimbrone MA, Jr. Blood flow and vascular gene expression: fluid shear stress as a modulator of endothelial phenotype. Mol Med Today. 1999; 5: 40–6
   PubMedGoogle Scholar
• Garin G, Berk BC. Flow-mediated signaling modulates endothelial cell phenotype. Endothelium. 2006; 13: 375–84
   PubMed Web of Science ®Google Scholar
• Gimbrone MA, Jr, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann N Y Acad Sci. 2000;902:230–39; discussion 239–40.
   PubMed Web of Science ®Google Scholar
• Davies PF. Flow-mediated endothelial mechanotransduction. Physiol Rev. 1995; 75: 519–60
   PubMed Web of Science ®Google Scholar
• Fung YC. Biomechanics: Circulation. New York, NY: Springer; 1997.
   Google Scholar
• Nerem RM, Alexander RW, Chappell DC, Medford RM, Varner SE, Taylor WR. The study of the influence of flow on vascular endothelial biology. Am J Med Sci. 1998; 316: 169–75
   PubMed Web of Science ®Google Scholar
• Kamiya A, Togawa T. Adaptive regulation of wall shear stress to flow change in the canine carotid artery. Am J Physiol. 1980; 239: H14–21
   PubMed Web of Science ®Google Scholar
• Langille BL, O'Donnell F. Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science. 1986; 231: 405–7
   PubMed Web of Science ®Google Scholar
• Girerd X, London G, Boutouyrie P, Mourad JJ, Safar M, Laurent S. Remodeling of the radial artery in response to a chronic increase in shear stress. Hypertension. 1996; 27: 799–803
   Google Scholar
• Melkumyants AM, Balashov SA, Khayutin VM. Endothelium dependent control of arterial diameter by blood viscosity. Cardiovasc Res. 1989; 23: 741–7
   PubMed Web of Science ®Google Scholar
• Levesque MJ, Nerem RM. The elongation and orientation of cultured endothelial cells in response to shear stress. J Biomech Eng. 1985; 107: 341–7
   PubMed Web of Science ®Google Scholar
• Levesque MJ, Liepsch D, Moravec S, Nerem RM. Correlation of endothelial cell shape and wall shear stress in a stenosed dog aorta. Arteriosclerosis. 1986; 6: 220–9
   PubMedGoogle Scholar
• Lin K, Hsu PP, Chen BP, Yuan S, Usami S, Shyy JY, et al. Molecular mechanism of endothelial growth arrest by laminar shear stress. Proc Natl Acad Sci USA. 2000; 97: 9385–9
   PubMed Web of Science ®Google Scholar
• Chiu JJ, Wang DL, Chien S, Skalak R, Usami S. Effects of disturbed flow on endothelial cells. J Biomech Eng. 1998; 120: 2–8
   PubMed Web of Science ®Google Scholar
• Davies PF. Spatial hemodynamics, the endothelium, and focal atherogenesis: a cell cycle link?. Circ Res. 2000; 86: 114–6
   PubMed Web of Science ®Google Scholar
• Akimoto S, Mitsumata M, Sasaguri T, Yoshida Y. Laminar shear stress inhibits vascular endothelial cell proliferation by inducing cyclin-dependent kinase inhibitor p21(Sdi1/Cip1/Waf1). Circ Res. 2000; 86: 185–90
   PubMed Web of Science ®Google Scholar
• Chien S. Molecular and mechanical bases of focal lipid accumulation in arterial wall. Prog Biophys Mol Biol. 2003; 83: 131–51
   PubMedGoogle Scholar
• Chen KD, Li YS, Kim M, Li S, Chien S, Shyy YJ. Mechanotransduction in response to shear stress. Roles of receptor tyrosine kinases, integrins, and Shc. J Biol Chem. 1999; 274: 18393–400
   PubMed Web of Science ®Google Scholar
• Jalali S, del Pozo MA, Chen KD, Miao H, Li YS, Schwartz MA, et al. Integrin-mediated mechanotransduction mechanotransduction requires its dynamic interaction with specific ECM ligands. Proc Natl Acad Sci USA. 2001; 98: 1042–6
   PubMed Web of Science ®Google Scholar
• Shyy JY, Chien S. Role of integrins in endothelial mechanosensing of shear stress. Circ Res. 2002; 91: 769–75
   PubMed Web of Science ®Google Scholar
• Florian JA, Kosky JR, Ainslie K, Pang Z, Dull RO, Tarbell JM. Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ Res. 2003; 93: E136–42
   PubMed Web of Science ®Google Scholar
• Butler PJ, Tsou TC, Li JY, Usami S, Chien S. 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. 2002; 16: 216–8
   Google Scholar
• Butler PJ, Norwich G, Weinbaum S, Chien S. Shear stress induces a time- and position-dependent increase in endothelial cell membrane fluidity. Am J Physiol Cell Physiol. 2001; 280: C962–9
   PubMed Web of Science ®Google Scholar
• Mccue S, Noria S, Langille BL. Shear-induced reorganization of endothelial cell cytoskeleton and adhesion complexes. Trends Cardiovasc Med. 2004; 14: 143–51
   PubMed Web of Science ®Google Scholar
• Davies PF, Robotewskyj A, Greim ML. Quantitative studies of endothelial cell adhesion. Directional remodeling of focal adhesion sites in response to flow forces. J Clin Invest. 1994; 93: 2031–8
   PubMed Web of Science ®Google Scholar
• Wang Y, Botvinick EL, Zhao Y, Berns MW, Usami S, Tsien RY, et al. Visualizing the mechanical activation of Src. Nature. 2005; 434: 1040–5
   PubMed Web of Science ®Google Scholar
• Li S, Butler P, Wang Y, Hu Y, Han DC, Usami S, et al. The role of the dynamics of focal adhesion kinase in the mechanotaxis of endothelial cells. Proc Natl Acad Sci USA. 2002; 99: 3546–51
   PubMedGoogle Scholar
• Chien S, Li S, Shiu YT, Li YS. Molecular basis of mechanical modulation of endothelial cell migration. Front Biosci. 2005; 10: 1985–2000
   Google Scholar
• Shyy YJ, Hsieh HJ, Usami S, Chien S. Fluid shear stress induces a biphasic response of human monocyte chemotactic protein 1 gene expression in vascular endothelium. Proc Natl Acad Sci USA. 1994; 91: 4678–82
   PubMed Web of Science ®Google Scholar
• Shyy JY, Lin MC, Han J, Lu Y, Petrime M, Chien S. The cis-acting phorbol ester ‘12-O-tetradecanoylphorbol 13-acetate’-responsive element is involved in shear stress-induced monocyte chemotactic protein 1 gene expression. Proc Natl Acad Sci USA. 1995; 92: 8069–73
   PubMed Web of Science ®Google Scholar
• Hsiai TK, Cho SK, Wong PK, Ing M, Salazar A, Sevanian A, et al. Monocyte recruitment to endothelial cells in response to oscillatory shear stress. FASEB J. 2003; 17: 1648–57
   PubMed Web of Science ®Google Scholar
• Sorescu GP, Sykes M, Weiss D, Platt MO, Saha A, Hwang J, et al. Bone morphogenic protein 4 produced in endothelial cells by oscillatory shear stress stimulates an inflammatory response. J Biol Chem. 2003; 278: 31128–35
   PubMed Web of Science ®Google Scholar
• Chappell DC, Varner SE, Nerem RM, Medford RM, Alexander RW. Oscillatory shear stress stimulates adhesion molecule expression in cultured human endothelium. Circ Res. 1998; 82: 532–9
   PubMed Web of Science ®Google Scholar
• Ziegler T, Bouzourene K, Harrison VJ, Brunner HR, Hayoz D. Influence of oscillatory and unidirectional flow environments on the expression of endothelin and nitric oxide synthase in cultured endothelial cells. Arterioscler Thromb Vasc Biol. 1998; 18: 686–92
   PubMed Web of Science ®Google Scholar
• Nagel T, Resnick N, Atkinson WJ, Dewey CF, Jr, Gimbrone MA, Jr. Shear stress selectively upregulates intercellular adhesion molecule-1 expression in cultured human vascular endothelial cells. J Clin Invest. 1994; 94: 885–91
   PubMed Web of Science ®Google Scholar
• Morigi M, Zoja C, Figliuzzi M, Foppolo M, Micheletti G, Bontempelli M, et al. Fluid shear stress modulates surface expression of adhesion molecules by endothelial cells. Blood. 1995; 85: 1696–703
   PubMedGoogle Scholar
• Malek AM, Greene AL, Izumo S. Regulation of endothelin 1 gene by fluid shear stress is transcriptionally mediated and independent of protein kinase C and cAMP. Proc Natl Acad Sci USA. 1993; 90: 5999–6003
   PubMed Web of Science ®Google Scholar
• Ohtsuka A, Ando J, Korenaga R, Kamiya A, Toyama-Sorimachi N, Miyasaka M. The effect of flow on the expression of vascular adhesion molecule-1 by cultured mouse endothelial cells. Biochem Biophys Res Commun. 1993; 193: 303–10
   PubMed Web of Science ®Google Scholar
• Korenaga R, Ando J, Kosaki K, Isshiki M, Takada Y, Kamiya A. Negative transcriptional regulation of the VCAM-1 gene by fluid shear stress in murine endothelial cells. Am J Physiol. 1997; 273: C1506–15
   PubMed Web of Science ®Google Scholar
• Dekker RJ, van Soest S, Fontijn RD, Salamanca S, de Groot PG, VanBavel E, et al. Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Kruppel-like factor (KLF2). Blood. 2002; 100: 1689–98
   PubMed Web of Science ®Google Scholar
• Wang N, Miao H, Li YS, Zhang P, Haga JH, Hu Y, et al. Shear stress regulation of Kruppel-like factor 2 expression is flow pattern-specific. Biochem Biophys Res Commun. 2006; 341: 1244–51
   PubMed Web of Science ®Google Scholar
• Yun S, Dardik A, Haga M, Yamashita A, Yamaguchi S, Koh Y, et al. Transcription factor Sp1 phosphorylation induced by shear stress inhibits membrane type 1-matrix metalloproteinase expression in endothelium. J Biol Chem. 2002; 277: 34808–14
   PubMed Web of Science ®Google Scholar
• Dardik A, Chen L, Frattini J, Asada H, Aziz F, Kudo FA, et al. Differential effects of orbital and laminar shear stress on endothelial cells. J Vasc Surg. 2005; 41: 869–80
   PubMed Web of Science ®Google Scholar
• De Keulenaer GW, Chappell DC, Ishizaka N, Nerem RM, Alexander RW, Griendling KK. Oscillatory and steady laminar shear stress differentially affect human endothelial redox state: role of a superoxide-producing NADH oxidase. Circ Res. 1998; 82: 1094–101
   PubMed Web of Science ®Google Scholar
• Hwang J, Saha A, Boo YC, Sorescu GP, McNally JS, Holland SM, et al. Oscillatory shear stress stimulates endothelial production of O2- from p47phox-dependent NAD(P)H oxidases, leading to monocyte adhesion. J Biol Chem. 2003; 278: 47291–8
   PubMed Web of Science ®Google Scholar
• McNally JS, Davis ME, Giddens DP, Saha A, Hwang J, Dikalov S, et al. Role of xanthine oxidoreductase and NAD(P)H oxidase in endothelial superoxide production in response to oscillatory shear stress. Am J Physiol Heart Circ Physiol. 2003; 285: H2290–7
   PubMed Web of Science ®Google Scholar
• Silacci P, Desgeorges A, Mazzolai L, Chambaz C, Hayoz D. Flow pulsatility is a critical determinant of oxidative stress in endothelial cells. Hypertension. 2001; 38: 1162–6
   PubMed Web of Science ®Google Scholar
• Hwang J, Ing MH, Salazar A, Lassegue B, Griendling KK, Navab M, et al. Pulsatile versus oscillatory shear stress regulates NADPH oxidase subunit expression: implication for native LDL oxidation. Circ Res. 2003; 93: 1225–32
   PubMed Web of Science ®Google Scholar
• Bhagyalakshmi A, Frangos JA. Mechanism of shear-induced prostacyclin production in endothelial cells. Biochem Biophys Res Commun. 1989; 158: 31–7
   PubMed Web of Science ®Google Scholar
• Kuchan MJ, Jo H, Frangos JA. Role of G protein in shear stress-mediated nitric oxide production by endothelial cells. Am J Physiol. 1994; 267: C753–8
   PubMedGoogle Scholar
• Uematsu M, Ohara Y, Navas JP, Nishida K, Murphy TJ, Alexander RW, et al. Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress. Am J Physiol. 1995; 269: C1371–8
   PubMed Web of Science ®Google Scholar
• Topper JN, Cai J, Falb D, Gimbrone MA, Jr. Identification of vascular endothelial genes differentially responsive to fluid mechanical stimuli: cyclooxygenase-2, manganese superoxide dismutase, and endothelial cell nitric oxide synthase are selectively up-regulated by steady laminar shear stress. Proc Natl Acad Sci USA. 1996; 93: 10417–22
   PubMed Web of Science ®Google Scholar
• Silacci P, Formentin K, Bouzourene K, Daniel F, Brunner HR, Hayoz D. Unidirectional and oscillatory shear stress differentially modulate NOS III gene expression. Nitric Oxide. 2000; 4: 47–56
   Google Scholar
• Cooke JP. Flow, NO, and atherogenesis. Proc Natl Acad Sci USA. 2003; 100: 768–70
   PubMedGoogle Scholar
• Conklin BS, Zhong DS, Zhao W, Lin PH, Chen C. Shear stress regulates occluding and VEGF expression in porcine arterial endothelial cells. J Surg Res. 2002; 102: 13–21
   PubMedGoogle Scholar
• Nagel T, Resnick N, Dewey CF, Jr, Gimbrone MA, Jr. Vascular endothelial cells respond to spatial gradients in fluid shear stress by enhanced activation of transcription factors. Arterioscler Thromb Vasc Biol. 1999; 19: 1825–34
   PubMed Web of Science ®Google Scholar
• Chiu JJ, Chen CN, Lee PL, Yang CT, Chuang HS, Chien S, et al. Analysis of the effect of disturbed flow on monocytic adhesion to endothelial cells. J Biomech. 2003; 36: 1883–95
   PubMed Web of Science ®Google Scholar
• Liu Y, Chen BP, Lu M, Zhu Y, Stemerman MB, Chien S, et al. Shear stress activation of SREBP1 in endothelial cells is mediated by integrins. Arterioscler Thromb Vasc Biol. 2002; 22: 76–81
   PubMed Web of Science ®Google Scholar
• Bao X, Lu C, Frangos JA. Temporal gradient in shear but not steady shear stress induces PDGF-A and MCP-1 expression in endothelial cells: role of NO, NF kappa B, and egr-1. Arterioscler Thromb Vasc Biol. 1999; 19: 996–1003
   PubMedGoogle Scholar
• Bao X, Clark CB, Frangos JA. Temporal gradient in shear-induced signaling pathway: involvement of MAP kinase, c-fos, and connexin43. Am J Physiol Heart Circ Physiol. 2000; 278: H1598–605
   Google Scholar
• White CR, Haidekker M, Bao X, Frangos JA. Temporal gradients in shear, but not spatial gradients, stimulate endothelial cell proliferation. Circulation. 2001; 103: 2508–13
   PubMed Web of Science ®Google Scholar
• Bao X, Lu C, Frangos JA. Mechanism of temporal gradients in shear-induced ERK1/2 activation and proliferation in endothelial cells. Am J Physiol Heart Circ Physiol. 2001; 281: H22–9
   Google Scholar
• Butler PJ, Weinbaum S, Chien S, Lemons DE. Endothelium-dependent, shear-induced vasodilation is rate-sensitive. Microcirculation. 2000; 7: 53–65
   PubMed Web of Science ®Google Scholar
• Garcia-Cardena G, Comander J, Anderson KR, Blackman BR, Gimbrone MA, Jr. Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc Natl Acad Sci USA. 2001; 98: 4478–85
   PubMed Web of Science ®Google Scholar
• McCormick SM, Eskin SG, McIntire LV, Teng CL, Lu CM, Russell CG, et al. DNA microarray reveals changes in gene expression of shear stressed human umbilical vein endothelial cells. Proc Natl Acad Sci USA. 2001; 98: 8955–60
   PubMed Web of Science ®Google Scholar
• Chen BP, Li YS, Zhao Y, Chen KD, Li S, Lao J, et al. DNA microarray analysis of gene expression in endothelial cells in response to 24-h shear stress. Physiol Genomics. 2001; 7: 55–63
   PubMed Web of Science ®Google Scholar
• Wasserman SM, Mehraban F, Komuves LG, Yang RB, Tomlinson JE, Zhang Y, et al. Gene expression profile of human endothelial cells exposed to sustained fluid shear stress. Physiol Genomics. 2002; 12: 13–23
   PubMed Web of Science ®Google Scholar
• Brooks AR, Lelkes PI, Rubanyi GM. Gene expression profiling of human aortic endothelial cells exposed to disturbed flow and steady laminar flow. Physiol Genomics. 2002; 9: 27–41
   PubMed Web of Science ®Google Scholar
• Dai G, Kaazempur-Mofrad MR, Natarajan S, Zhang Y, Vaughn S, Blackman BR, et al. Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature. Proc Natl Acad Sci USA. 2004; 101: 14871–6
   PubMed Web of Science ®Google Scholar
• Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993; 362: 801–9
   PubMed Web of Science ®Google Scholar
• Karino T, Goldsmith HL. Adhesion of human platelets to collagen on the walls distal to a tubular expansion. Microvasc Res. 1979; 17: 238–62
   PubMed Web of Science ®Google Scholar
• Pritchard WF, Davies PF, Derafshi Z, Polacek DC, Tsao R, Dull RO, et al. Effects of wall shear stress and fluid recirculation on the localization of circulating monocytes in a three-dimensional flow model. J Biomech. 1995; 28: 1459–69
   PubMed Web of Science ®Google Scholar
• Barber KM, Pinero A, Truskey GA. Effects of recirculating flow on U-937 cell adhesion to human umbilical vein endothelial cells. Am J Physiol. 1998; 275: H591–9
   Google Scholar
• Hinds MT, Park YJ, Jones SA, Giddens DP, Alevriadou BR. Local hemodynamics affect monocytic cell adhesion to a three-dimensional flow model coated with E-selectin. J Biomech. 2001; 34: 95–103
   PubMed Web of Science ®Google Scholar
• Skilbeck C, Westwood SM, Walker PG, David T, Nash GB. Dependence of adhesive behavior of neutrophils on local fluid dynamics in a region with recirculating flow. Biorheology. 2001; 38: 213–27
   PubMed Web of Science ®Google Scholar
• Chen CN, Chang SF, Lee PL, Chang K, Chen LJ, Usami S, et al. Neutrophils, lymphocytes, and monocytes exhibit diverse behaviors in transendothelial and subendothelial migrations under coculture with smooth muscle cells in disturbed flow. Blood. 2006; 107: 1933–42
   PubMedGoogle Scholar