1932

Abstract

This review places modern research developments in vascular mechanobiology in the context of hemodynamic phenomena in the cardiovascular system and the discrete localization of vascular disease. The modern origins of this field are traced, beginning in the 1960s when associations between flow characteristics, particularly blood flow–induced wall shear stress, and the localization of atherosclerotic plaques were uncovered, and continuing to fluid shear stress effects on the vascular lining endothelial cells (ECs), including their effects on EC morphology, biochemical production, and gene expression. The earliest single-gene studies and genome-wide analyses are considered. The final section moves from the ECs lining the vessel wall to the smooth muscle cells and fibroblasts within the wall that are fluid mechanically activated by interstitial flow that imposes shear stresses on their surfaces comparable with those of flowing blood on EC surfaces. Interstitial flow stimulates biochemical production and gene expression, much like blood flow on ECs.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-fluid-010313-141309
2014-01-03
2024-12-03
Loading full text...

Full text loading...

/deliver/fulltext/fluid/46/1/annurev-fluid-010313-141309.html?itemId=/content/journals/10.1146/annurev-fluid-010313-141309&mimeType=html&fmt=ahah

Literature Cited

  1. Abumiya T, Sasaguri T, Taba Y, Miwa Y, Miyagi M. 2002. Shear stress induces expression of vascular endothelial growth factor receptor Flk-1/KDR through the CT-rich Sp1 binding site. Arterioscler. Thromb. Vasc. Biol. 22:907–13 [Google Scholar]
  2. Ainslie KM, Garanich JS, Dull RO, Tarbell JM. 2005. Vascular smooth muscle cell glycocalyx influences shear stress–mediated contractile response. J. Appl. Physiol. 98:242–49 [Google Scholar]
  3. Akimoto S, Mitsumata M, Sasaguri T, Yoshida Y. 2000. Laminar shear stress inhibits vascular endothelial cell proliferation by inducing cyclin-dependent kinase inhibitor p21Sdi1/Cip1/Waf1. Circ. Res. 86:185–90 [Google Scholar]
  4. Alshihabi SN, Chang YS, Frangos JA, Tarbell JM. 1996. Shear stress-induced release of PGE2 and PGI2 by vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 224:808–14 [Google Scholar]
  5. Apenberg S, Freyberg MA, Friedl P. 2003. Shear stress induces apoptosis in vascular smooth muscle cells via an autocrine Fas/FasL pathway. Biochem. Biophys. Res. Commun. 310:355–59 [Google Scholar]
  6. Asada H, Paszkowiak J, Teso D, Alvi K, Thorisson A. et al. 2005. Sustained orbital shear stress stimulates smooth muscle cell proliferation via the extracellular signal-regulated protein kinase 1/2 pathway. J. Vasc. Surg. 42:772–80 [Google Scholar]
  7. Bijari PB, Antiga L, Gallo D, Wasserman BA, Steinman DA. 2012. Improved prediction of disturbed flow via hemodynamically-inspired geometric variables. J. Biomech. 45:1632–37 [Google Scholar]
  8. Bond AR, Iftikhar S, Bharath AA, Weinberg PD. 2011. Morphological evidence for a change in the pattern of aortic wall shear stress with age. Arterioscler. Thromb. Vasc. Biol. 31:543–50 [Google Scholar]
  9. Bussolari SR, Dewey CF Jr, Gimbrone MA Jr. 1982. Apparatus for subjecting living cells to fluid shear stress. Rev. Sci. Instrum. 53:1851–44 [Google Scholar]
  10. Cancel LM, Tarbell JM. 2010. The role of apoptosis in LDL transport through cultured endothelial cell monolayers. Atherosclerosis 208:335–41 [Google Scholar]
  11. Cancel LM, Tarbell JM. 2011. The role of mitosis in LDL transport through cultured endothelial cell monolayers. Am. J. Physiol. Heart Circ. Physiol. 300:H769–76 [Google Scholar]
  12. Caro CG. 2009. Discovery of the role of wall shear in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 29:158–61 [Google Scholar]
  13. Caro CG. 2012. The Mechanics of the Circulation Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  14. Caro CG, Fitz-Gerald JM, Schroter RC. 1969. Arterial wall shear and distribution of early atheroma in man. Nature 223:1159–60 [Google Scholar]
  15. Caro CG, Fitz-Gerald JM, Schroter RC. 1971. Atheroma and arterial wall shear: observation, correlation and proposal of a shear dependent mass transfer mechanism for atherogenesis. Proc. R. Soc. Lond. B 177:109–59Introduces the low-WSS hypothesis for the localization of atherosclerosis. [Google Scholar]
  16. Caro CG, Nerem RM. 1973. Transport of 14C-4-cholesterol between serum and wall in the perfused dog common carotid artery. Circ. Res. 32:187–205 [Google Scholar]
  17. Chappell DC, Varner SE, Nerem RM, Medford RM, Alexander RW. 1998. Oscillatory shear stress stimulates adhesion molecule expression in cultured human endothelium. Circ. Res. 82:532–39 [Google Scholar]
  18. Chatzizisis YS, Coskun AU, Jonas M, Edelman ER, Feldman CL, Stone PH. 2007. Role of endothelial shear stress in the natural history of coronary atherosclerosis and vascular remodeling: molecular, cellular, and vascular behavior. J. Am. Coll. Cardiol. 49:2379–93 [Google Scholar]
  19. Chen BP, Li YS, Zhao Y, Chen KD, Li S. et al. 2001. DNA microarray analysis of gene expression in endothelial cells in response to 24-h shear stress. Physiol. Genomics 7:55–63 [Google Scholar]
  20. Chien S. 2007. Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am. J. Physiol. Heart Circ. Physiol. 292:H1209–24 [Google Scholar]
  21. Chien S, Li S, Shyy YJ. 1998. Effects of mechanical forces on signal transduction and gene expression in endothelial cells. Hypertension 31:162–69 [Google Scholar]
  22. Cho A, Mitchell L, Koopmans D, Langille BL. 1997. Effects of changes in blood flow rate on cell death and cell proliferation in carotid arteries of immature rabbits. Circ. Res. 81:328–37 [Google Scholar]
  23. Cukierman E, Pankov R, Stevens DR, Yamada KM. 2001. Taking cell-matrix adhesions to the third dimension. Science 294:1708–12 [Google Scholar]
  24. Dai G, Kaazempur-Mofrad MR, Natarajan S, Zhang Y, Vaughn S. et al. 2004. Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature. Proc. Natl. Acad. Sci. USA 101:14871–76 [Google Scholar]
  25. Dancu MB, Berardi DE, Vanden Heuvel JP, Tarbell JM. 2004. Asynchronous shear stress and circumferential strain reduces endothelial NO synthase and cyclooxygenase-2 but induces endothelin-1 gene expression in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 24:2088–94 [Google Scholar]
  26. Dancu MB, Tarbell JM. 2007. Coronary endothelium expresses a pathologic gene pattern compared to aortic endothelium: correlation of asynchronous hemodynamics and pathology in vivo. Atherosclerosis 192:9–14 [Google Scholar]
  27. Davies PF. 1995. Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75:519–60 [Google Scholar]
  28. Davies PF. 2009. Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat. Clin. Pract. Cardiovasc. Med. 6:16–26 [Google Scholar]
  29. Davies PF, Tripathi SC. 1993. Mechanical stress mechanisms and the cell: an endothelial paradigm. Circ. Res. 72:239–45 [Google Scholar]
  30. Davis ME, Grumbach IM, Fukai T, Cutchins A, Harrison DG. 2004. Shear stress regulates endothelial nitric-oxide synthase promoter activity through nuclear factor κB binding. J. Biol. Chem. 279:163–68 [Google Scholar]
  31. Dewey CF Jr, Bussolari SR, Gimbrone MA Jr, Davies PF. 1981. The dynamic response of vascular endothelial cells to fluid shear stress. J. Biomech. Eng. 103:177–85 [Google Scholar]
  32. Domanski M, Lloyd-Jones D, Fuster V, Grundy S. 2011. Can we dramatically reduce the incidence of coronary heart disease?. Nat. Rev. Cardiol. 8:721–25 [Google Scholar]
  33. Dzau VJ, Braun-Dullaeus RC, Sedding DG. 2002. Vascular proliferation and atherosclerosis: new perspectives and therapeutic strategies. Nat. Med. 8:1249–56 [Google Scholar]
  34. Ekstrand J, Razuvaev A, Folkersen L, Roy J, Hedin U. 2010. Tissue factor pathway inhibitor-2 is induced by fluid shear stress in vascular smooth muscle cells and affects cell proliferation and survival. J. Vasc. Surg. 52:167–75 [Google Scholar]
  35. Fang Y, Shi C, Manduchi E, Civelek M, Davies PF. 2010. MicroRNA-10a regulation of proinflammatory phenotype in athero-susceptible endothelium in vivo and in vitro. Proc. Natl. Acad. Sci. USA 107:13450–55 [Google Scholar]
  36. Faxon DP, Creager MA, Smith SC Jr, Pasternak RC, Olin JW. et al. 2004. Atherosclerotic Vascular Disease Conference: executive summary; Atherosclerotic Vascular Disease Conference proceeding for healthcare professionals from a special writing group of the American Heart Association. Circulation 1092595–604 [Google Scholar]
  37. Feintuch A, Ruengsakulrach P, Lin A, Zhang J, Zhou YQ. et al. 2007. Hemodynamics in the mouse aortic arch as assessed by MRI, ultrasound, and numerical modeling. Am. J. Physiol. Heart Circ. Physiol. 292:H884–92 [Google Scholar]
  38. Finn AV, Nakano M, Narula J, Kolodgie FD, Virmani R. 2010. Concept of vulnerable/unstable plaque. Arterioscler. Thromb. Vasc. Biol. 30:1282–92 [Google Scholar]
  39. Fitzgerald TN, Shepherd BR, Asada H, Teso D, Muto A. et al. 2008. Laminar shear stress stimulates vascular smooth muscle cell apoptosis via the Akt pathway. J. Cell Physiol. 216:389–95 [Google Scholar]
  40. Fleury ME, Boardman KC, Swartz MA. 2006. Autologous morphogen gradients by subtle interstitial flow and matrix interactions. Biophys. J. 91:113–21 [Google Scholar]
  41. Florian JA, Kosky JR, Ainslie K, Pang Z, Dull RO, Tarbell JM. 2003. Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ. Res. 93:e136–42Presents the first clear demonstration of the role of the glycocalyx as a mechanotransducer on ECs. [Google Scholar]
  42. Fox JA, Hugh AE. 1966. Localization of atheroma: a theory based on boundary layer separation. Br. Heart J. 28:388–99 [Google Scholar]
  43. Frangos JA, Eskin SG, McIntire LV, Ives CL. 1985. Flow effects on prostacyclin production by cultured human endothelial cells. Science 227:1477–79This is the first study to show a direct effect of WSS on EC biochemical production. [Google Scholar]
  44. Friedman MH, Ehrlich LW. 1984. Numerical simulation of aortic bifurcation flows: the effect of flow divider curvature. J. Biomech. 17:881–88 [Google Scholar]
  45. Friedman MH, Hutchins GM, Bargeron CB, Deters OJ, Mark FF. 1981. Correlation between intimal thickness and fluid shear in human arteries. Atherosclerosis 39:425–36 [Google Scholar]
  46. Fry DL. 1969. Certain histological and chemical responses of the vascular interface to acutely induced mechanical stress in the aorta of the dog. Circ. Res. 24:93–108 [Google Scholar]
  47. Garanich JS, Mathura RA, Shi ZD, Tarbell JM. 2007. Effects of fluid shear stress on adventitial fibroblast migration: implications for flow-mediated mechanisms of arterialization and intimal hyperplasia. Am. J. Physiol. Heart Circ. Physiol. 292:H3128–35 [Google Scholar]
  48. Garanich JS, Pahakis M, Tarbell JM. 2005. Shear stress inhibits smooth muscle cell migration via nitric oxide–mediated downregulation of matrix metalloproteinase-2 activity. Am. J. Physiol. Heart Circ. Physiol. 288:H2244–52 [Google Scholar]
  49. García-Cardeña G, Comander JI, Anderson KR, Blackman BR, Gimbrone MA Jr. 2001a. Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc. Natl. Acad. Sci. USA 98:4478–85Provides one of the earliest high-throughput gene expression studies of ECs exposed to shear stress in vitro. [Google Scholar]
  50. García-Cardeña G, Comander JI, Blackman BR, Anderson KR, Gimbrone MA Jr. 2001b. Mechanosensitive endothelial gene expression profiles: scripts for the role of hemodynamics in atherogenesis?. Ann. N. Y. Acad. Sci. 947:1–6 [Google Scholar]
  51. Ge L, Dasi LP, Sotiropoulos F, Yoganathan AP. 2008. Characterization of hemodynamic forces induced by mechanical heart valves: Reynolds versus viscous stresses. Ann. Biomed. Eng. 36:276–97 [Google Scholar]
  52. Gimbrone MA Jr, Topper JN, Nagel T, Anderson KR, García-Cardeña G. 2000. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann. N. Y. Acad. Sci. 902:230–39 Discussion. 902:239–40 [Google Scholar]
  53. Gomez D, Owens GK. 2012. Smooth muscle cell phenotypic switching in atherosclerosis. Cardiovasc. Res. 95:156–64 [Google Scholar]
  54. Gosgnach W, Challah M, Coulet F, Michel JB, Battle T. 2000a. Shear stress induces angiotensin converting enzyme expression in cultured smooth muscle cells: possible involvement of bFGF. Cardiovasc. Res. 45:486–92 [Google Scholar]
  55. Gosgnach W, Messika-Zeitoun D, Gonzalez W, Philipe M, Michel JB. 2000b. Shear stress induces iNOS expression in cultured smooth muscle cells: role of oxidative stress. Am. J. Physiol. Cell Physiol. 279:C1880–88 [Google Scholar]
  56. Grabowski EF, Jaffe EA, Weksler BB. 1985. Prostacyclin production by cultured endothelial cell monolayers exposed to step increases in shear stress. J. Lab. Clin. Med. 105:36–43 [Google Scholar]
  57. Haga JH, Li YS, Chien S. 2007. Molecular basis of the effects of mechanical stretch on vascular smooth muscle cells. J. Biomech. 40:947–60 [Google Scholar]
  58. Haga M, Yamashita A, Paszkowiak J, Sumpio BE, Dardik A. 2003. Oscillatory shear stress increases smooth muscle cell proliferation and Akt phosphorylation. J. Vasc. Surg. 37:1277–84 [Google Scholar]
  59. Hajra L, Evans AI, Chen M, Hyduk SJ, Collins T, Cybulsky MI. 2000. The NF-κB signal transduction pathway in aortic endothelial cells is primed for activation in regions predisposed to atherosclerotic lesion formation. Proc. Natl. Acad. Sci. USA 97:9052–57 [Google Scholar]
  60. He XH, Wu GF, Zhang Y, Chen XL, Zhang ZS. et al. 2008. Effect of chronic enhanced external counterpulastion on gene expression profiles of arterial endothelial cells of pigs fed with high-cholesterol diet. Nan Fang Yi Ke Da Xue Xue Bao 28:1195–97 (In Chinese) [Google Scholar]
  61. Hendrickson RJ, Okada SS, Cahill PA, Yankah E, Sitzmann JV, Redmond EM. 1999. Ethanol inhibits basal and flow-induced vascular smooth muscle cell migration in vitro. J. Surg. Res. 84:64–70 [Google Scholar]
  62. Hishikawa K, Nakaki T, Marumo T, Hayashi M, Suzuki H. et al. 1994. Pressure promotes DNA synthesis in rat cultured vascular smooth muscle cells. J. Clin. Invest. 93:1975–80 [Google Scholar]
  63. Hsiai TK, Cho SK, Wong PK, Ing M, Salazar A. et al. 2003. Monocyte recruitment to endothelial cells in response to oscillatory shear stress. FASEB J. 17:1648–57 [Google Scholar]
  64. Hsieh HJ, Li NQ, Frangos JA. 1992. Shear-induced platelet-derived growth factor gene expression in human endothelial cells is mediated by protein kinase C. J. Cell Physiol. 150:552–58 [Google Scholar]
  65. Hsu S, Chu JS, Chen FF, Wang A, Li S. 2011. Effects of fluid shear stress on a distinct population of vascular smooth muscle cells. Cell Mol. Bioeng. 4:627–36 [Google Scholar]
  66. Janiczek RL, Blackman BR, Roy RJ, Meyer CH, Acton ST, Epstein FH. 2011. Three-dimensional phase contrast angiography of the mouse aortic arch using spiral MRI. Magn. Reson. Med. 66:1382–90 [Google Scholar]
  67. Jeong SI, Kwon JH, Lim JI, Cho SW, Jung Y. et al. 2005. Mechano-active tissue engineering of vascular smooth muscle using pulsatile perfusion bioreactors and elastic PLCL scaffolds. Biomaterials 26:1405–11 [Google Scholar]
  68. Jia X, Yang J, Song W, Li P, Wang X. et al. 2013. Involvement of large conductance Ca2+-activated K+ channel in laminar shear stress–induced inhibition of vascular smooth muscle cell proliferation. Pflugers Arch. 465:221–32 [Google Scholar]
  69. Joshi AK, Leask RL, Myers JG, Ojha M, Butany J, Ethier CR. 2004. Intimal thickness is not associated with wall shear stress patterns in the human right coronary artery. Arterioscler. Thromb. Vasc. Biol. 24:2408–13 [Google Scholar]
  70. Kim HJ, Vignon-Clementel IE, Coogan JS, Figueroa CA, Jansen KE, Taylor CA. 2010. Patient-specific modeling of blood flow and pressure in human coronary arteries. Ann. Biomed. Eng. 38:3195–209 [Google Scholar]
  71. Kohler TR, Jawien A. 1992. Flow affects development of intimal hyperplasia after arterial injury in rats. Arterioscler. Thromb. 12:963–71 [Google Scholar]
  72. Korenaga R, Ando J, Tsuboi H, Yang W, Sakuma I. et al. 1994. Laminar flow stimulates ATP- and shear stress–dependent nitric oxide production in cultured bovine endothelial cells. Biochem. Biophys. Res. Commun. 198:213–19 [Google Scholar]
  73. Ku DN, Giddens DP, Zarins CK, Glagov S. 1985. Pulsatile flow and atherosclerosis in the human carotid bifurcation: positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis 5:293–302Introduces the concept of oscillatory shear (OSI) as a localizing factor in atherosclerosis. [Google Scholar]
  74. Kuchan MJ, Frangos JA. 1994. Role of calcium and calmodulin in flow-induced nitric oxide production in endothelial cells. Am. J. Physiol. 266:C628–36 [Google Scholar]
  75. Li C, Xu Q. 2007. Mechanical stress–initiated signal transduction in vascular smooth muscle cells in vitro and in vivo. Cell Signal. 19:881–91 [Google Scholar]
  76. Li S, Lao J, Chen BP, Li YS, Zhao Y. et al. 2003. Genomic analysis of smooth muscle cells in 3-dimensional collagen matrix. FASEB J. 17:97–99 [Google Scholar]
  77. Lin K, Hsu PP, Chen BP, Yuan S, Usami S. et al. 2000. Molecular mechanism of endothelial growth arrest by laminar shear stress. Proc. Natl. Acad. Sci. USA 97:9385–89 [Google Scholar]
  78. Makris GC, Nicolaides AN, Xu XY, Geroulakos G. 2010. Introduction to the biomechanics of carotid plaque pathogenesis and rupture: review of the clinical evidence. Br. J. Radiol. 83:729–35 [Google Scholar]
  79. Maldonado N, Kelly-Arnold A, Vengrenyuk Y, Laudier D, Fallon JT. et al. 2012. A mechanistic analysis of the role of microcalcifications in atherosclerotic plaque stability: potential implications for plaque rupture. Am. J. Physiol. Heart Circ. Physiol. 303:H619–28 [Google Scholar]
  80. McDonald DA. 1960. Blood Flow in Arteries Baltimore: Williams & Wilkins [Google Scholar]
  81. Michel JB, Thaunat O, Houard X, Meilhac O, Caligiuri G, Nicoletti A. 2007. Topological determinants and consequences of adventitial responses to arterial wall injury. Arterioscler. Thromb. Vasc. Biol. 27:1259–68 [Google Scholar]
  82. Milnor WR. 1989. Hemodynamics Baltimore: Williams & Wilkins [Google Scholar]
  83. Mitsumata M, Fishel RS, Nerem RM, Alexander RW, Berk BC. 1993. Fluid shear stress stimulates platelet-derived growth factor expression in endothelial cells. Am. J. Physiol. 265:H3–8 [Google Scholar]
  84. Mo M, Eskin SG, Schilling WP. 1991. Flow-induced changes in Ca2+ signaling of vascular endothelial cells: effect of shear stress and ATP. Am. J. Physiol. 260:H1698–707 [Google Scholar]
  85. Nagel T, Resnick N, Atkinson WJ, Dewey CF Jr, Gimbrone MA Jr. 1994. Shear stress selectively upregulates intercellular adhesion molecule-1 expression in cultured human vascular endothelial cells. J. Clin. Invest. 94:885–91 [Google Scholar]
  86. Nam D, Ni CW, Rezvan A, Suo J, Budzyn K. et al. 2009. Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am. J. Physiol. Heart Circ. Physiol. 297:H1535–43 [Google Scholar]
  87. Nerem RM, Levesque MJ, Cornhill JF. 1981. Vascular endothelial morphology as an indicator of the pattern of blood flow. J. Biomech. Eng. 103:172–76Demonstrates the relationship between EC morphology and flow (WSS) patterns in blood vessels. [Google Scholar]
  88. Nguyen AT, Gomez D, Bell RD, Campbell JH, Clowes AW. et al. 2013. Smooth muscle cell plasticity: fact or fiction?. Circ. Res. 112:17–22 [Google Scholar]
  89. Ni CW, Qiu H, Rezvan A, Kwon K, Nam D. et al. 2010a. Discovery of novel mechanosensitive genes in vivo using mouse carotid artery endothelium exposed to disturbed flow. Blood 116:e66–73Presents the first high-throughput gene expression study of ECs exposed to shear stress in vivo. [Google Scholar]
  90. Ni J, Waldman A, Khachigian LM. 2010b. c-Jun regulates shear- and injury-inducible Egr-1 expression, vein graft stenosis after autologous end-to-side transplantation in rabbits, and intimal hyperplasia in human saphenous veins. J. Biol. Chem. 285:4038–48 [Google Scholar]
  91. Noguchi N, Jo H. 2011. Redox going with vascular shear stress. Antioxid. Redox Signal. 15:1367–68 [Google Scholar]
  92. Oancea E, Wolfe JT, Clapham DE. 2006. Functional TRPM7 channels accumulate at the plasma membrane in response to fluid flow. Circ. Res. 98:245–53 [Google Scholar]
  93. Osanai T, Akutsu N, Fujita N, Nakano T, Takahashi K. et al. 2001. Cross talk between prostacyclin and nitric oxide under shear in smooth muscle cell: role in monocyte adhesion. Am. J. Physiol. Heart Circ. Physiol. 281:H177–82 [Google Scholar]
  94. Owens GK, Kumar MS, Wamhoff BR. 2004. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84:767–801 [Google Scholar]
  95. Palumbo R, Gaetano C, Melillo G, Toschi E, Remuzzi A, Capogrossi MC. 2000. Shear stress downregulation of platelet-derived growth factor receptor-β and matrix metalloprotease-2 is associated with inhibition of smooth muscle cell invasion and migration. Circulation 102:225–30 [Google Scholar]
  96. Papadaki M, McIntire LV, Eskin SG. 1996. Effects of shear stress on the growth kinetics of human aortic smooth muscle cells in vitro. Biotechnol. Bioeng. 50:555–61 [Google Scholar]
  97. Papadaki M, Ruef J, Nguyen KT, Li F, Patterson C. et al. 1998a. Differential regulation of protease activated receptor-1 and tissue plasminogen activator expression by shear stress in vascular smooth muscle cells. Circ. Res. 83:1027–34 [Google Scholar]
  98. Papadaki M, Tilton RG, Eskin SG, McIntire LV. 1998b. Nitric oxide production by cultured human aortic smooth muscle cells: stimulation by fluid flow. Am. J. Physiol. 274:H616–26 [Google Scholar]
  99. Pedersen JA, Boschetti F, Swartz MA. 2007. Effects of extracellular fiber architecture on cell membrane shear stress in a 3D fibrous matrix. J. Biomech. 40:1484–92 [Google Scholar]
  100. Peiffer V, Rowland EM, Cremers SG, Weinberg PD, Sherwin SJ. 2012. Effect of aortic taper on patterns of blood flow and wall shear stress in rabbits: association with age. Atherosclerosis 223:114–21 [Google Scholar]
  101. Qiu Y, Tarbell JM. 2000. Numerical simulation of pulsatile flow in a compliant curved tube model of a coronary artery. J. Biomech. Eng. 122:77–85 [Google Scholar]
  102. Redmond EM, Cullen JP, Cahill PA, Sitzmann JV, Stefansson S. et al. 2001. Endothelial cells inhibit flow-induced smooth muscle cell migration: role of plasminogen activator inhibitor-1. Circulation 103:597–603 [Google Scholar]
  103. Rensen SS, Doevendans PA, Van Eys GJ. 2007. Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Neth. Heart J. 15:100–8 [Google Scholar]
  104. Resnick N, Collins T, Atkinson W, Bonthron DT, Dewey CF Jr, Gimbrone MA Jr. 1993. Platelet-derived growth factor B chain promoter contains a cis-acting fluid shear-stress-responsive element. Proc. Natl. Acad. Sci. USA 90:4591–95 Erratum. 90:7908Describes the discovery of the shear stress–responsive element. [Google Scholar]
  105. Rhoads DN, Eskin SG, McIntire LV. 2000. Fluid flow releases fibroblast growth factor-2 from human aortic smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 20:416–21 [Google Scholar]
  106. Rizzo V. 2009. Enhanced interstitial flow as a contributing factor in neointima formation: (shear) stressing vascular wall cell types other than the endothelium. Am. J. Physiol. Heart Circ. Physiol. 297:H1196–97 [Google Scholar]
  107. Sadeghi MR, Shirani E, Tafazzoli-Shadpour M, Samaee M. 2011. The effects of stenosis severity on the hemodynamic parameters: assessment of the correlation between stress phase angle and wall shear stress. J. Biomech. 44:2614–26 [Google Scholar]
  108. Sartore S, Chiavegato A, Faggin E, Franch R, Puato M. et al. 2001. Contribution of adventitial fibroblasts to neointima formation and vascular remodeling: from innocent bystander to active participant. Circ. Res. 89:1111–21 [Google Scholar]
  109. Schena M, Shalon D, Davis RW, Brown PO. 1995. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270:467–70 [Google Scholar]
  110. Schwartz MA. 2010. Integrins and extracellular matrix in mechanotransduction. Cold Spring Harb. Perspect. Biol. 2:a005066 [Google Scholar]
  111. Sharefkin JB, Diamond SL, Eskin SG, McIntire LV, Dieffenbach CW. 1991. Fluid flow decreases preproendothelin mRNA levels and suppresses endothelin-1 peptide release in cultured human endothelial cells. J. Vasc. Surg. 14:1–9 [Google Scholar]
  112. Sharma R, Yellowley CE, Civelek M, Ainslie K, Hodgson L. et al. 2002. Intracellular calcium changes in rat aortic smooth muscle cells in response to fluid flow. Ann. Biomed. Eng. 30:371–78 [Google Scholar]
  113. Shen J, Luscinskas FW, Connolly A, Dewey CF Jr, Gimbrone MA Jr. 1992. Fluid shear stress modulates cytosolic free calcium in vascular endothelial cells. Am. J. Physiol. 262:C384–90 [Google Scholar]
  114. Shi Y, O'Brien JE, Fard A, Mannion JD, Wang D, Zalewski A. 1996. Adventitial myofibroblasts contribute to neointimal formation in injured porcine coronary arteries. Circulation 94:1655–64 [Google Scholar]
  115. Shi ZD, Abraham G, Tarbell JM. 2010a. Shear stress modulation of smooth muscle cell marker genes in 2-D and 3-D depends on mechanotransduction by heparan sulfate proteoglycans and ERK1/2. PLoS One 5:e12196 [Google Scholar]
  116. Shi ZD, Ji XY, Berardi DE, Qazi H, Tarbell JM. 2010b. Interstitial flow induces MMP-1 expression and vascular SMC migration in collagen I gels via an ERK1/2-dependent and c-Jun-mediated mechanism. Am. J. Physiol. Heart Circ. Physiol. 298:H127–35 [Google Scholar]
  117. Shi ZD, Ji XY, Qazi H, Tarbell JM. 2009. Interstitial flow promotes vascular fibroblast, myofibroblast, and smooth muscle cell motility in 3-D collagen I via upregulation of MMP-1. Am. J. Physiol. Heart Circ. Physiol. 297:H1225–34 [Google Scholar]
  118. Shi ZD, Tarbell JM. 2011. Fluid flow mechanotransduction in vascular smooth muscle cells and fibroblasts. Ann. Biomed. Eng. 39:1608–19 [Google Scholar]
  119. Shi ZD, Wang H, Tarbell JM. 2011. Heparan sulfate proteoglycans mediate interstitial flow mechanotransduction regulating MMP-13 expression and cell motility via FAK-ERK in 3D collagen. PLoS One 6:e15956 [Google Scholar]
  120. Shou Y, Jan KM, Rumschitzki DS. 2006. Transport in rat vessel walls. I. Hydraulic conductivities of the aorta, pulmonary artery, and inferior vena cava with intact and denuded endothelia. Am. J. Physiol. Heart Circ. Physiol. 291:H2758–71 [Google Scholar]
  121. Shyy YJ, Hsieh HJ, Usami S, Chien S. 1994. Fluid shear stress induces a biphasic response of human monocyte chemotactic protein 1 gene expression in vascular endothelium. Proc. Natl. Acad. Sci. USA 91:4678–82 [Google Scholar]
  122. Stegemann JP, Hong H, Nerem RM. 2005. Mechanical, biochemical, and extracellular matrix effects on vascular smooth muscle cell phenotype. J. Appl. Physiol. 98:2321–27 [Google Scholar]
  123. Stenmark KR, Davie N, Frid M, Gerasimovskaya E, Das M. 2006. Role of the adventitia in pulmonary vascular remodeling. Physiology 21:134–45 [Google Scholar]
  124. Sterpetti AV, Cucina A, D'Angelo LS, Cardillo B, Cavallaro A. 1993. Shear stress modulates the proliferation rate, protein synthesis, and mitogenic activity of arterial smooth muscle cells. Surgery 113:691–99 [Google Scholar]
  125. Sterpetti AV, Cucina A, Fragale A, Lepidi S, Cavallaro A, Santoro-D'Angelo L. 1994. Shear stress influences the release of platelet derived growth factor and basic fibroblast growth factor by arterial smooth muscle cells. Eur J. Vasc. Surg. 8:138–42 [Google Scholar]
  126. Tada S, Dong C, Tarbell JM. 2007. Effect of the stress phase angle on the strain energy density of the endothelial plasma membrane. Biophys. J. 93:3026–33 [Google Scholar]
  127. Tada S, Tarbell JM. 2005. A computational study of flow in a compliant carotid bifurcation-stress phase angle correlation with shear stress. Ann. Biomed. Eng. 33:1202–12 [Google Scholar]
  128. Tang Z, Wang A, Yuan F, Yan Z, Liu B. et al. 2012. Differentiation of multipotent vascular stem cells contributes to vascular diseases. Nat. Commun. 3:875 [Google Scholar]
  129. Tarbell JM. 2003. Mass transport in arteries and the localization of atherosclerosis. Annu. Rev. Biomed. Eng. 5:79–118 [Google Scholar]
  130. Tarbell JM. 2010. Shear stress and the endothelial transport barrier. Cardiovasc. Res. 87:320–30 [Google Scholar]
  131. Tarbell JM, Ebong EE. 2008. The endothelial glycocalyx: a mechano-sensor and -transducer. Sci. Signal. 1:pt8 [Google Scholar]
  132. Tarbell JM, Shi ZD. 2013. Effect of the glycocalyx layer on transmission of interstitial flow shear stress to embedded cells. Biomech. Model. Mechanobiol. 12:111–21Theoretical modeling shows that interstitial flow–imposed solid shear stress transmitted through the glycocalyx layer on a cell embedded in a 3D ECM could be of the order of 20 dyn/cm2, similar to that experienced by ECs. [Google Scholar]
  133. Topper JN, Cai J, Falb D, Gimbrone MA Jr. 1996. 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 93:10417–22 [Google Scholar]
  134. Torii R, Wood NB, Hadjiloizou N, Dowsey AW, Wright AR. et al. 2009. Stress phase angle depicts differences in coronary artery hemodynamics due to changes in flow and geometry after percutaneous coronary intervention. Am. J. Physiol. Heart Circ. Physiol. 296:H765–76 [Google Scholar]
  135. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA. et al. 2005. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437:426–31Presents the discovery of a mechanosensory complex upstream of integrins that transduces shear stress on ECs. [Google Scholar]
  136. Ueba H, Kawakami M, Yaginuma T. 1997. Shear stress as an inhibitor of vascular smooth muscle cell proliferation: role of transforming growth factor-β1 and tissue-type plasminogen activator. Arterioscler. Thromb. Vasc. Biol. 17:1512–16 [Google Scholar]
  137. Uhl M, Mellert K, Striegl B, Deibler M, Lamla M. et al. 2011. Cyclic stretch increases splicing noise rate in cultured human fibroblasts. BMC Res. Notes 4:470 [Google Scholar]
  138. Vasava P, Jalali P, Dabagh M, Kolari PJ. 2012. Finite element modelling of pulsatile blood flow in idealized model of human aortic arch: study of hypotension and hypertension. Comput. Math. Methods Med. 2012:861837 [Google Scholar]
  139. Vincent PE, Plata AM, Hunt AA, Weinberg PD, Sherwin SJ. 2011. Blood flow in the rabbit aortic arch and descending thoracic aorta. J. R. Soc. Interface 8:1708–19 [Google Scholar]
  140. Wagner CT, Durante W, Christodoulides N, Hellums JD, Schafer AI. 1997. Hemodynamic forces induce the expression of heme oxygenase in cultured vascular smooth muscle cells. J. Clin. Invest. 100:589–96 [Google Scholar]
  141. Wang DM, Tarbell JM. 1995. Modeling interstitial flow in an artery wall allows estimation of wall shear stress on smooth muscle cells. J. Biomech. Eng. 117:358–63 [Google Scholar]
  142. Wang H, Yan S, Chai H, Riha GM, Li M. et al. 2006. Shear stress induces endothelial transdifferentiation from mouse smooth muscle cells. Biochem. Biophys. Res. Commun. 346:860–65 [Google Scholar]
  143. Wang S, Tarbell JM. 2000. Effect of fluid flow on smooth muscle cells in a 3-dimensional collagen gel model. Arterioscler. Thromb. Vasc. Biol. 20:2220–25This is the first study to investigate effects of interstitial flow on SMCs in a 3D in vitro model. [Google Scholar]
  144. Weinbaum S, Tarbell JM, Damiano ER. 2007. The structure and function of the endothelial glycocalyx layer. Annu. Rev. Biomed. Eng. 9:121–67 [Google Scholar]
  145. Weinbaum S, Tzeghai G, Ganatos P, Pfeffer R, Chien S. 1985. Effect of cell turnover and leaky junctions on arterial macromolecular transport. Am. J. Physiol. 248:H945–60 [Google Scholar]
  146. White GE, Gimbrone MA Jr, Fujiwara K. 1983. Factors influencing the expression of stress fibers in vascular endothelial cells in situ. J. Cell Biol. 97:416–24 [Google Scholar]
  147. Winter DC, Nerem RM. 1984. Turbulence in pulsatile flows. Ann. Biomed. Eng. 12:357–69 [Google Scholar]
  148. Wong AJ, Pollard TD, Herman IM. 1983. Actin filament stress fibers in vascular endothelial cells in vivo. Science 219:867–69 [Google Scholar]
  149. Zarins CK, Giddens DP, Bharadvaj BK, Sottiurai VS, Mabon RF, Glagov S. 1983. Carotid bifurcation atherosclerosis: quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ. Res. 53:502–14 [Google Scholar]
  150. Zeng Y, Ebong EE, Fu BM, Tarbell JM. 2012. The structural stability of the endothelial glycocalyx after enzymatic removal of glycosaminoglycans. PLoS One 7:e43168 [Google Scholar]
/content/journals/10.1146/annurev-fluid-010313-141309
Loading
/content/journals/10.1146/annurev-fluid-010313-141309
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error