Blood flow and arterial endothelial dysfunction: Mechanisms and implications

Comptes Rendus Physique

Volumn 14, Issue 6, 2013, Pages 479-496

  Barakat, Abdul I ^a  

^a ECOLE POLYTECHNIQUE   (France)

Author keywords

Atherosclerosis; Blood flow; Cytoskeleton; Endothelial cells; Mechanosensors; Mechanotransduction

Indexed keywords

EID: 84880609204     PISSN: 16310705     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.crhy.2013.05.003     Document Type: Short Survey

References (155)

1. Liliensiek S.J., Wood J.A., Yong J., Auerbach R., Nealey P.F., Murphy C.J. Modulation of human vascular endothelial cell behaviors by nanotopographic cues. Biomaterials 2010, 31:5418-5426.
2. Discher D.E., Janmey P., Wang Y.-L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
3. Davies P.F. Flow-mediated endothelial mechanotransduction. Physiol. Rev. 1995, 75:519-560.
4. Fisher A.B., Chien S., Barakat A.I., Nerem R.M. Endothelial cellular response to altered shear stress. Am. J. Physiol. 2001, 281:L529-L533.
5. Chien S. Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell (review). Am. J. Physiol. 2007, 292:H1209-H1224.
6. Hahn C., Schwartz M.A. Mechanotransduction in vascular physiology and atherogenesis. Nat. Rev. Mol. Cell Biol. 2009, 10:53-62.
7. Na S., Collin O., Chowdhury F., Tay B., Ouyang M., Wang Y., Wang N. Rapid signal transduction in living cells is a unique feature of mechanotransduction. Proc. Natl. Acad. Sci. USA 2008, 105:6626-6631.
8. Wang N., Butler J.P., Ingber D.E. Mechanotransduction across the cell surface and through the cytoskeleton. Science 1993, 260:1124-1127.
9. Maniotis A.J., Chen C.S., Ingber D.E. Demonstrations of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc. Natl. Acad. Sci. USA 1997, 94:849-854.
10. Silberberg Y.R., Pelling A.E., Yakubov G.E., Crum W.R., Hawkes D.J., Horton M.A. Mitochondrial displacements in response to nanomechanical forces. J. Mol. Recognit. 2008, 21:30-36.
11. Wang N., Tytell J.D., Ingber D.E. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 2009, 10:75-82.
12. Helmlinger G., Geiger R.V., Schreck S., Nerem R.M. Effects of pulsatile flow on cultured vascular endothelial cell morphology. J. Biomech. Eng. 1991, 113:123-131.
13. Helmlinger G., Berk B.C., Nerem R.M. Calcium responses of endothelial cell monolayers subjected to pulsatile and steady laminar flow differ. Am. J. Physiol. 1995, 269:C367-C375.
14. Chappell D.C., Varner S.E., Nerem R.M., Medford R.M., Alexander R.W. Oscillatory shear stress stimulates adhesion molecule expression in cultured human endothelium. Circ. Res. 1998, 82:532-539.
15. Lum R.M., Wiley L.M., Barakat A.I. Influence of different forms of shear stress on vascular endothelial TGF-1 mRNA expression. Int. J. Mol. Med. 2000, 5:635-641.
16. Lieu D.K., Pappone P.A., Barakat A.I. Differential membrane potential and ion current responses to different types of shear stress in vascular endothelial cells. Am. J. Physiol. 2004, 286:C1367-C1375.
17. Gautam M., Shen Y., Thirkill T.L., Douglas G.C., Barakat A.I. Flow-activated chloride channels in vascular endothelium: shear stress sensitivity, desensitization dynamics, and physiological implications. J. Biol. Chem. 2006, 281:36492-36500.
18. Barakat A.I., Leaver E.V., Pappone P.A., Davies P.F. A flow-activated chloride-selective membrane current in vascular endothelial cells. Circ. Res. 1999, 85:820-828.
19. Barbee K.A., Davies P.F., Lal R. Shear stress-induced reorganization of the surface topography of living endothelial cells imaged by atomic force microscopy. Circ. Res. 1994, 74:163-171.
20. Lebleu V.S., MacDonald B., Kalluri R. Structure and function of basement membranes. Exp. Biol. Med. 2007, 232:1121-1129.
21. Liliensiek S.J., Nealey P., Murphy C.J. Characterization of endothelial basement membrane nanotopography in rhesus macaque as a guide for vessel tissue engineering. Tissue Eng. Part A 2009, 15:2643-2651.
22. Vicente-Manzanares M., Ma X., Adelstein R.S., Horwitz A.R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 2009, 10:778-790.
23. Sato M., Levesque M.J., Nerem R.M. Micropipette aspiration of cultured bovine aortic endothelial cells exposed to shear stress. Arterioscler. Thromb. Vasc. Biol. 1987, 7:276-286.
24. Sato M., Ohshima N., Nerem R.M. Viscoelastic properties of cultured porcine aortic endothelial cells exposed to shear stress. J. Biomech. 1996, 29:461-467.
25. Guilak F., Tedrow J.R., Burgkart R. Viscoelastic properties of the cell nucleus. Biochem. Biophys. Res. Commun. 2000, 269:781-786.
26. Rodriguez O.C., Schaefer A.W., Mandato C.A., Forscher P., Bement W.M., Waterman-Storer C.M. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 2003, 5:599-609.
27. Cytoskeletal Mechanics: Models and Measurements 2006, 13. Cambridge University Press. R.D. Kamm, M.R.K. Mofrad (Eds.).
28. Kumar S., Maxwell I.Z., Heisterkamp A., Polte T.R., Lele T., Salanga M., Mazur E., Ingber D.E. Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization and extracellular matrix mechanics. Biophys. J. 2006, 90:3762-3773.
29. Deguchi S., Ohashi T., Sato M. Tensile properties of single stress fibers isolated from cultured vascular smooth muscle cells. J. Biomech. 2006, 39:2603-2610.
30. Lu L., Oswald S.J., Ngu H., Yin F.C.P. Mechanical properties of actin stress fibers in living cells. Biophys. J. 2008, 95:6060-6071.
31. Katoh K., Kano Y., Masuda M., Onishi H., Fujiwara K. Isolation and contraction of the stress fiber. Mol. Biol. Cell 1998, 9:1919-1938.
32. Shi Z.-D., Tarbell J.M. Fluid flow mechanotransduction in vascular smooth muscle cells and fibroblasts. Ann. Biomed. Eng. 2011, 39:1608-1619.
33. Wang D.M., Tarbell J.M. Modeling interstitial flow in an artery wall allows estimation of wall shear stress on smooth muscle cells. J. Biomech. Eng. 1995, 117:358-363.
34. Wu K.K., Thiagarajan P. Role of endothelium in thrombosis and hemostasis. Annu. Rev. Med. 1996, 47:315-331.
35. Mason R.G., Sharp D., Chuang H.Y., Mohammad S.F. The endothelium: roles in thrombosis and hemostasis. Arch. Pathol. Lab. Med. 1977, 101:61-64.
36. Bazzoni G., Dejana E. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 2004, 84:869-901.
37. Pohl U., Holtz J., Busse R., Bassenge E. Crucial role of endothelium in the vasodilator response to increased flow in vivo. Hypertension 1986, 8:37-44.
38. Langille B.L., O'Donnell F. Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science 1986, 231:405-407.
39. Clair R.W.St. Pathogenesis of the atherosclerotic lesion: current concepts of cellular and biochemical events. Recent Advances in Arterial Diseases: Atherosclerosis, Hypertension, and Vasopasm 1986, 1-29. Alan R. Liss, Inc., New York. T. Tulenko, R. Cox (Eds.).
40. Ross R., Glomset J.A. The pathogenesis of atherosclerosis. N. Engl. J. Med. 1976, 295:369-377.
41. Ross R., Glomset J.A. The pathogenesis of atherosclerosis. N. Engl. J. Med. 1976, 295:420-425.
42. Libby P. Inflammation in atherosclerosis. Nature 2002, 420:868-874.
43. Tedgui A., Mallat Z. Anti-inflammatory mechanisms in the vascular wall. Circ. Res. 2001, 88:877-887.
44. Schwartz C.J., Mitchell J.R.A. Observations on localization of arterial plaques. Circ. Res. 1962, 11:63-73.
45. Azuma T., Fukushima T. Flow patterns in stenotic blood vessel models. Biorheology 1976, 13:337-355.
46. Ehrlich L.W., Friedman M.H. Particle paths and stasis in unsteady flow through a bifurcation. J. Biomech. 1977, 10:561-568.
47. Karino T., Kwong H., Goldsmith H.L. Particle flow behavior in models of branching vessels. I. Vortices in 90° T-junctions. Biorheology 1979, 16:231-248.
48. Walburn F.J., Stein P.D. Flow in a symmetrically branched tube simulating the aortic bifurcation: the effects of unevenly distributed flow. Ann. Biomed. Eng. 1980, 8:159-173.
49. Bharadvaj B.K., Mabon R.F., Giddens D.P. Steady flow in a model of the human carotid bifurcation: Part I - Flow visualization. J. Biomech. 1982, 15:349-362.
50. Bharadvaj B.K., Mabon R.F., Giddens D.P. Steady flow in a model of the human carotid bifurcation: Part II - Laser-Doppler measurements. J. Biomech. 1982, 15:363-378.
51. Friedman M.H., Bargeron C.B., Hutchins G.M., Mark F.F., Deters O.J. Hemodynamic measurements in human arterial casts, and their correlation with histology and luminal area. J. Biomech. Eng. 1980, 102:247-251.
52. Asakura T., Karino T. Flow patterns and spatial distribution of atherosclerotic lesions in human coronary arteries. Circ. Res. 1990, 66:1045-1066.
53. Moore J.E., Ku D.N., Zarins C.K., Glagov S. Pulsatile flow visualization in the abdominal aorta under differing physiological conditions: implications for increased susceptibility to atherosclerosis. J. Biomech. Eng. 1992, 114:391-397.
54. Pedersen E.M., Yoganathan A.P., Lefebvre X.P. Pulsatile flow visualization in a model of the human abdominal aorta and aortic bifurcation. J. Biomech. 1992, 25:935-944.
55. Endo S., Sohara Y., Karino T. Flow patterns in dog aortic arch under a steady flow condition simulating mid-systole. Heart Ves. 1996, 11:180-191.
56. Barakat A.I., Karino T., Colton C.K. Microcinematographic studies of the flow field in the excised rabbit aorta. Biorheology 1997, 34:195-221.
57. Farthing S., Peronneau P. Flow in the thoracic aorta. Cardiovasc. Res. 1979, 13:607-620.
58. Hutchison K.J., Karpinski E., Campbell J.D., Potemkowski A.P. Aortic velocity contours at abdominal branches in anesthetized dogs. J. Biomech. 1988, 21:277-286.
59. Bell D.R., Sabbah H.N., Stein P.D. Profiles of velocity in coronary arteries of dogs indicate lower shear rate along inner arterial curvature. Arteriosclerosis 1989, 9:167-175.
60. Reneman R.S., Hoeks A.P.G. Wall shear stress as measured in vivo: consequences for the design of the arterial system. Med. Biol. Eng. Comput. 2008, 46:499-507.
61. Perktold K., Nerem R.M., Peter R.O. A numerical calculation of flow in a curved tube model of the left main coronary artery. J. Biomech. 1991, 24:175-189.
62. Perktold K., Florian H., Hilbert D., Peter R. Wall shear stress distribution in the human carotid siphon during pulsatile flow. J. Biomech. 1988, 21:663-671.
63. Thiriet M., Pares C., Saltel E., Hecht F. Numerical simulation of steady flow in a model of the aortic bifurcation. J. Biomech. Eng. 1992, 114:40-49.
64. Cheer A.Y., Dwyer H.A., Barakat A.I., Sy E., Bice M. Computational study of the effect of geometric and flow parameters on the steady flow field at the rabbit aorto-celiac bifurcation. Biorheology 1998, 35:415-435.
65. Shahcheraghi N., Dwyer H.A., Cheer A.Y., Barakat A.I., Rutaganira T. Unsteady and three-dimensional simulation of blood flow in the human aortic arch. J. Biomech. Eng. 2002, 124:378-387.
66. Kazakidi A., Plata A.M., Sherwin S.J., Weinberg P.D. Effect of reverse flow on the pattern of wall shear stress near arterial branches. J. R. Soc. Interface 2011, 8:1594-1603.
67. Vincent P.E., Plata A.M., Hunt A.A., Weinberg P.D., Sherwin S.J. Blood flow in the rabbit aortic arch and descending thoracic aorta. J. R. Soc. Interface 2011, 8:1708-1719.
68. Van Doormaal M.A., Kazakidi A., Wylezinska M., Hunt A., Tremoleda J.L., Protti A., Bohraus Y., Gsell W., Weinberg P.D., Ethier C.R. Haemodynamics in the mouse aortic arch computed from MRI-derived velocities at the aortic root. J. R. Soc. Interface 2012, 9:2834-2844.
69. Lantz J., Renner J., Karlsson M. Wall shear stress in a subject specific human aorta - influence of fluid-structure interaction. Int. J. Appl. Mech. 2011, 4:759-778.
70. Rayz V.L., Berger S.A. Computational modeling of vascular hemodynamics. Computational Modeling in Biomechanics 2010, Springer. S. De, F. Guilak, M.R.K. Mofrad (Eds.).
71. Huo Y., Kassab G.S. Effect of compliance and hematocrit on wall shear stress in a model of the entire coronary arterial tree. J. Appl. Physiol. 2009, 107:500-505.
72. Younis H.F., Kaazempur-Mofrad M.R., Chan R.C., Isasi A.G., Hinton D.P., Chau A.H., Kim L.A., Kamm R.D. Hemodynamics and wall mechanics in human carotid bifurcation and its consequences for atherogenesis: investigation of inter-individual variation. Biomech. Model. Mechanobiol. 2004, 3:17-32.
73. Caro C.G., Pedley T.J., Schroter R.C., Seed W.A. The Mechanics of the Circulation 1978, Oxford University Press.
74. Pedley T.J. The Fluid Mechanics of Large Blood Vessels 1980, Cambridge University Press.
75. Hamakiotes C.C., Berger S.A. Fully developed pulsatile flow in a curved pipe. J. Fluid Mech. 1988, 195:23-55.
76. Hamakiotes C.C., Berger S.A. Periodic flows through curved tubes: the effect of the frequency parameter. J. Fluid Mech. 1990, 210:353-370.
77. Chandran K.B. Flow dynamics in the human aorta. J. Biomech. Eng. 1993, 115:611-616.
78. Ku D.N., Giddens D.P., Zarins C.K., 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.
79. Ku D.N. Blood flow in arteries. Annu. Rev. Fluid Mech. 1997, 29:399-434.
80. Choi H.W., Barakat A.I. Numerical study of the impact of non-Newtonian blood behavior on flow over a two-dimensional backward facing step. Biorheology 2005, 42:493-509.
81. Chien S. Shear dependence of effective cell volume as a determinant of blood viscosity. Science 1970, 168:977-978.
82. Dempere-Marco L., Oubel E., Castro M., Putman C., Frangi A., Cebral J. CFD analysis incorporating the influence of wall motion: application to intracranial aneurysms. Lect. Notes Comput. Sci. 2006, vol. 4191:438-445. Springer-Verlag, Berlin/Heidelberg. R. Larsen, M. Nielsen, J. Sporring (Eds.).
83. Kabinejadian F., Ghista D.N. Compliant model of a coupled sequential coronary arterial bypass graft: effects of vessel wall elasticity and non-Newtonian rheology on blood flow regime and hemodynamic parameters distribution. Med. Eng. Phys. 2012, 34:860-872.
84. Fry D.L. Acute vascular endothelial changes associated with increased blood velocity gradients. Circ. Res. 1968, 22:165-197.
85. Caro C.G., Fitz-Gerald J.M., Schroter R.C. Arterial wall shear and distribution of early atheroma in man. Nature 1969, 223:1159-1161.
86. Caro C.G., Fitz-Gerald J.M., Schroter R.C. Atheroma and arterial wall shear. Observation, correlation and proposal of a shear dependent mass transfer mechanism for atherogenesis. Proc. R. Soc. Lond. B 1971, 177:109-133.
87. Peiffer V., Rowland E.M., Cremers S.G., Weinberg P.D., Sherwin S.J. Effect of aortic taper on patterns of blood flow and wall shear stress in rabbits: association with age. Atherosclerosis 2012, 223:114-121.
88. Barnes S.E., Weinberg P.D. Contrasting patterns of spontaneous aortic disease in young and old rabbits. Arterioscler. Thromb. Vasc. Biol. 1998, 18:300-308.
89. DePaola N., Gimbrone M.A., Davies P.F., Dewey C.F. Vascular endothelium responds to fluid shear stress gradients. Arterioscler. Thromb. 1992, 12:1254-1257.
90. White C.R., Stevens H.Y., Haidekker M.A., Frangos J.A. Temporal gradients in shear, but not spatial gradients, stimulate ERK1/2 activation in human endothelial cells. Am. J. Physiol. 2005, 289:H2350-H2355.
91. Shimogonya Y., Ishikawa T., Imai Y., Matsuki N., Yamaguchi T. Can temporal fluctuation in spatial wall shear stress gradient initiate a cerebral aneurysm? A proposed novel hemodynamic index, the gradient oscillatory number (GON). J. Biomech. 2009, 42:550-554.
92. Weinberg P.D., Ethier C.R. Twenty-fold difference in hemodynamic wall shear stress between murine and human aortas. J. Biomech. 2007, 40:1594-1598.
93. Garcia-Cardena G., Comander J., Anderson K.R., Blackman B.R., Gimbrone M.A. Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc. Natl. Acad. Sci. USA 2001, 98:4478-4485.
94. Shyy J.Y., Chien S. Role of integrins in cellular responses to mechanical stress and adhesion. Curr. Opin. Cell Biol. 1997, 9:707-713.
95. + current in vascular endothelial-cells. Nature 1988, 331:168-170.
96. Hoger J.H., Ilyin V.I., Forsyth S., Hoger A. Shear stress regulates the endothelial Kir2.1 ion channel. Proc. Natl. Acad. Sci. USA 2002, 99:7780-7785.
97. Wang Y., Botvinick E.L., Zhao Y., Berns M.W., Usami S., Tsien R.Y., Chien S. Visualizing the mechanical activation of Src. Nature 2005, 434:1040-1045.
98. Gudi S.R., Clark C.B., Frangos J.A. Fluid flow rapidly activates G proteins in human endothelial cells: involvement of G proteins in mechanochemical signal transduction. Circ. Res. 1996, 79:834-839.
99. Haidekker M.A., L'Heureux N., Frangos J.A. Fluid shear stress increases membrane fluidity in endothelial cells: a study with DCVJ fluorescence. Am. J. Physiol. 2000, 278:H1401-H1406.
100. Butler P.J., Norwich G., Weinbaum S., Chien S. Shear stress induces a time- and position-dependent increase in endothelial cell membrane fluidity. Am. J. Physiol. 2001, 280:C962-C969.
101. Ziegelstein R.C., Cheng L., Capogrossi M.C. Flow-dependent cytosolic acidification of vascular endothelial cells. Science 1992, 258:656-659.
102. Ziegelstein R.C., Blank P.S., Cheng L., Capogrossi M.C. Cytosolic alkalinization of vascular endothelial cells produced by an abrupt reduction in fluid shear stress. Circ. Res. 1998, 82:803-809.
103. Milner P., Kirkpatrick K.A., Ralevic V., Toothill V., Pearson J., Burnstock G. Endothelial cells cultured from human umbilical vein release ATP, substance P and acetylcholine in response to increased flow. Proc. Biol. Sci. 1990, 241:245-248.
104. Buga G.M., Gold M.E., Fukuto J.M., Ignarro L.J. Shear stress-induced release of nitric oxide from endothelial cells grown on beads. Hypertension 1991, 17:187-193.
105. Nerem R.M., Harrison D.G., Taylor W.R., Alexander R.W. Hemodynamics and vascular endothelial biology. J. Cardiovasc. Pharmacol. 1993, 21(Suppl. 1):S6-S10.
106. Shen J., Luscinskas F.W., Connolly A., Dewey C.F., Gimbrone M.A. Fluid shear stress modulates cytosolic free calcium in vascular endothelial cells. Am. J. Physiol. 1992, 262:C384-C390.
107. Geiger R.V., Berk B.C., Alexander R.W., Nerem R.M. Flow-induced calcium transients in single endothelial cells: spatial and temporal analysis. Am. J. Physiol. 1992, 262:C1411-C1417.
108. Tseng H., Peterson T.E., Berk B.C. Fluid shear stress stimulates mitogen-activated protein kinase in endothelial cells. Circ. Res. 1995, 77:869-878.
109. Yan C., Takahashi M., Okuda M., Lee J.D., Berk B.C. Fluid shear stress stimulates big mitogen-activated protein kinase 1 (BMK1) activity in endothelial cells. Dependence on tyrosine kinases and intracellular calcium. J. Biol. Chem. 1999, 274:143-150.
110. Lan Q., Mercurius K.O., Davies P.F. Stimulation of transcription factors NF kappa B and AP1 in endothelial cells subjected to shear stress. Biochem. Biophys. Res. Commun. 1994, 201:950-956.
111. Malek A.M., Izumo S. Molecular aspects of signal transduction of shear stress in the endothelial cell. J. Hypertens. 1994, 12:989-999.
112. Dewey C.F., Bussolari S.R., Gimbrone M.A., Davies P.F. The dynamic response of vascular endothelial cells to fluid shear stress. J. Biomech. Eng. 1981, 103:177-185.
113. Nerem R.M., Levesque M.J., Cornhill J.F. Vascular endothelial morphology as an indicator of the pattern of blood flow. J. Biomech. Eng. 1981, 103:172-176.
114. Eskin S.G., Ives C.L., McIntire L.V., Navarro L.T. Response of cultured endothelial cells to steady flow. Microvasc. Res. 1984, 28:87-94.
115. Barakat A.I., Lieu D.K. Differential responsiveness of vascular endothelial cells to different types of fluid mechanical shear stress. Cell Biochem. Biophys. 2003, 38:323-343.
116. Chien S. Molecular basis of rheological modulation of endothelial functions: Importance of stress direction. Biorheology 2006, 43:95-116.
117. Sampath R., Kukielka G.L., Smith C.W., Eskin S.G., McIntire L.V. Shear stress-mediated changes in the expression of leukocyte adhesion receptors on human umbilical vein endothelial cells in vitro. Ann. Biomed. Eng. 1995, 23:247-256.
118. Ohno M., Cooke J.P., Dzau V.J., Gibbons G.H. Fluid shear stress induces endothelial transforming growth factor beta-1 transcription and production. Modulation by potassium channel blockade. J. Clin. Invest. 1995, 95:1363-1369.
119. Jiang Z., Berceli S.A., Pfahnl C.L., Wu L., Goldman D., Tao M., Kagayama M., Matsukawa A., Ozaki C.K. Wall shear modulation of cytokines in early vein grafts. J. Vasc. Surg. 2004, 40:345-350.
120. Barakat A.I., Lieu D.K., Gojova A. Secrets of the code: do vascular endothelial cells use ion channels to decipher complex flow signals?. Biomaterials 2006, 27:671-678.
121. Tzima E., Irani-Tehrani M., Kiosses W.B., Dejana E., Schultz D.A., Engelhardt B., Cao G., DeLisser H., Schwartz M.A. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 2005, 437:426-431.
122. Gudi S., Nolan J.P., Frangos J.A. Modulation of GTPase activity of G proteins by fluid shear stress and phospholipid composition. Proc. Natl. Acad. Sci. USA 1998, 95:2515-2519.
123. Weinbaum S., Zhang X., Han Y., Vink H., Cowin S.C. Mechanotransduction and flow across the endothelial glycocalyx. Proc. Natl. Acad. Sci. USA 2003, 100:7988-7995.
124. Tarbell J.M., Pahakis M.Y. Mechanotransduction and the glycocalyx. J. Intern. Med. 2006, 259:339-350.
125. Weinbaum S., Tarbell J.M., Damiano E.R. The structure and function of the endothelial glycocalyx layer. Annu. Rev. Biomed. Eng. 2007, 9:121-167.
126. Pahakis M.Y., Kosky J.R., Dull R.O., Tarbell J.M. The role of endothelial glycocalyx components in mechanotransduction of fluid shear stress. Biochem. Biophys. Res. Commun. 2007, 355:228-233.
127. Yao Y. Three-dimensional flow-induced dynamics of the endothelial surface glycocalyx layer 2007, Ph.D. dissertation, MIT.
128. Wang N., Suo Z. Long-distance propagation of forces in a cell. Biochem. Biophys. Res. Commun. 2005, 328:1133-1138.
129. Hu S., Chen J., Fabry B., Numaguchi Y., Gouldstone A., Ingber D.E., Fredberg J.J., Butler J.P., Wang N. Intracellular stress tomography reveals stress focusing and structural anisotropy in cytoskeleton of living cells. Am. J. Physiol. 2003, 285:C1082-C1090.
130. Hwang Y., Barakat A.I. Dynamics of mechanical signal transmission through prestressed actin stress fibers. PLoS ONE 2012, 7:e35343.
131. Hwang Y., Gouget C.L.M., Barakat A.I. Mechanisms of cytoskeleton-mediated mechanical signal transmission in cells. Commun. Integr. Biol. 2012, 5:538-542.
132. Zhang Q., Skepper J.N., Yang F., Davies J.D., Hegyi L., Roberts R.G., Weissberg P.L., Ellis J.A., Shanahan C.M. Nesprins: a novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. J. Cell Sci. 2001, 114:4485-4498.
133. Starr D.A., Han M. Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 2002, 298:406-409.
134. Zhen Y.Y., Libotte T., Munck M., Noegel A.A., Korenbaum E. NUANCE a giant protein connecting the nucleus and actin cytoskeleton. J. Cell Sci. 2002, 115:3207-3222.
135. Starr D.A., Han M. ANChors away: an actin based mechanism of nuclear positioning. J. Cell Sci. 2003, 116:211-216.
136. Padmakumar V.C., Abraham S., Braune S., Noegel A.A., Tunggal B., Karakesisoglou I., Korenbaum E. Enaptin, a giant actin-binding protein, is an element of the nuclear membrane and the actin cytoskeleton. Exp. Cell Res. 2004, 295:330-339.
137. Libotte T., Zaim H., Abraham S., Padmakumar V.C., Schneider M., Lu W., Munck M., Hutchison C., Wehnert M., Fahrenkrog B., Sauder U., Aebi U., Noegel A.A., Karakesisoglou I. Lamin A/C-dependent localization of nesprin-2, a giant scaffolder at the nuclear envelope. Mol. Biol. Cell 2005, 16:3411-3424.
138. Wilhelmsen K., Litjens S.H., Kuikman I., Tshimbalanga N., Janssen H., van den Bout I., Raymond K., Sonnenberg A. Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J. Cell Biol. 2005, 171:799-810.
139. Padmakumar V.C., Libotte T., Lu W., Zaim H., Abraham S., Noegel A.A., Gotzmann J., Foisner R., Karakesisoglou I. The inner nuclear membrane protein Sun1 mediates the anchorage of nesprin-2 to the nuclear envelope. J. Cell Sci. 2005, 118:3419-3430.
140. Grady R.M., Starr D.A., Ackerman G.L., Sanes J.R., Han M. Syne proteins anchor muscle nuclei at the neuromuscular junction. Proc. Natl. Acad. Sci. USA 2005, 102:4359-4364.
141. Morgan J.T., Pfeiffer E.R., Thirkill T.L., Kumar P., Peng G., Fridolfsson H.N., Douglas G.C., Starr D.A., Barakat A.I. Nesprin-3 regulates endothelial cell morphology, perinuclear cytoskeletal architecture, and flow-induced polarization. Mol. Biol. Cell 2011, 22:4324-4334.
142. Morgan J.T. Internal and external biophysical regulation of endothelial cell morphology and function 2011, Ph.D. dissertation, University of California, Davis.
143. Chancellor T.J., Lee J., Thodeti C.K., Lele T. Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation. Biophys. J. 2010, 99:115-123.
144. Brosig M., Ferralli J., Gelman L., Chiquet M., Chiquet-Ehrismann R. Interfering with the connection between the nucleus and the cytoskeleton affects nuclear rotation, mechanotransduction and myogenesis. Int. J. Biochem. Cell Biol. 2010, 42:1717-1728.
145. Lombardi M.L., Jaalouk D.E., Shanahan C.M., Burke B., Roux K.J., Lammerding J. The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton. J. Biol. Chem. 2011, 286:26743-26753.
146. Hoffman B.D., Grashoff C., Schwartz M.A. Dynamic molecular processes mediate cellular mechanotransduction. Nature 2011, 475:316-323.
147. Lee S.E., Kamm R.D., Mofrad M.R.K. Force-induced activation of Talin and its possible role in focal adhesion mechanotransduction. J. Biomech. 2007, 40:2096-2106.
148. del Rio A., Perez-Jimenez R., Liu R., Roca-Cusachs P., Fernandez J.M., Sheetz M.P. Stretching single talin rod molecules activates vinculin binding. Science 2009, 323:638-641.
149. Osawa M., Masuda M., Kusano K., Fujiwara K. Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule?. J. Cell Biol. 2002, 158:773-785.
150. Brangwynne C.P., MacKintosh F.C., Kumar S., Geisse N.A., Talbot J., Mahadevan L., Parker K.K., Ingber D.E., Weitz D.A. Microtubules can bear enhanced compressive loads in living cells because of lateral reinforcement. J. Cell Biol. 2006, 173:733-741.
151. Morgan J.T., Wood J.A., Shah N.M., Hughbanks M.L., Russel P., Barakat A.I., Murphy C.J. Integration of basal topographic cues and apical shear stress in vascular endothelial cells. Biomaterials 2012, 33:4126-4135.
152. Zhu L., He P. Platelet activating factor increases endothelial [Ca2+]i and nitric oxide production in individually perfused intact microvessels. Am. J. Physiol. 2005, 288:H2869-H2877.
153. Zhou X., He P. Endothelial [Ca2+]i and caveolin-1 antagonistically regulate eNOS activity and microvessel permeability in rat venules. Cardiovasc. Res. 2010, 87:340-347.
154. Potter D.R., Jiang J., Damiano E.R. The recovery time course of the endothelial cell glycocalyx in vivo and its implications in vitro. Circ. Res. 2009, 104:1318-1325.
155. Lasheras J.C. The biomechanics of arterial aneurysms. Annu. Rev. Fluid Mech. 2007, 39:293-319.