Exogenous and endogenous force regulation of endothelial cell behavior

Journal of Biomechanics

Volumn 43, Issue 1, 2010, Pages 79-86

  Califano, Joseph P ^a   Reinhart King, Cynthia A ^a  

^a Cornell University   (United States)

Author keywords

Angiogenesis; Cell mechanics; Cyclic strain; Shear stress; Substrate stiffness

Indexed keywords

ANGIOGENESIS; CELL MECHANICS; CELLULAR TRACTION; CYCLIC STRAIN; CYTOSKELETAL; DYNAMIC ENVIRONMENTS; ENDOTHELIAL CELL RESPONSE; EXTRACELLULAR MATRICES; FORCE GENERATION; FORCE REGULATION; HEMODYNAMIC FORCES; MECHANO-BIOLOGY; PRESSURE FORCE; VASCULAR SYSTEM;

BIOMECHANICS; BLOOD VESSEL PROSTHESES; BLOOD VESSELS; ELASTICITY; HYDRODYNAMICS; MECHANICAL PROPERTIES; SELF ASSEMBLY; SHEAR STRESS; STIFFNESS; STIFFNESS MATRIX; STRENGTH OF MATERIALS; SUBSTRATES;

ENDOTHELIAL CELLS;

ARTICLE; BLOOD VESSEL; CAPILLARY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR SYSTEM; CELL FUNCTION; CYTOSKELETON; ENDOTHELIUM CELL; FORCE; HEMODYNAMICS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MECHANOTRANSDUCTION; MICROVASCULATURE; NONHUMAN; PRESSURE; PRIORITY JOURNAL; REGULATORY MECHANISM; SHEAR STRESS; VISCOELASTICITY;

ANIMALS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; MECHANOTRANSDUCTION, CELLULAR; SHEAR STRENGTH; STRESS, MECHANICAL;

EID: 72149087688     PISSN: 00219290     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2009.09.012     Document Type: Article

References (124)

1. Acevedo A.D., Bowser S.S., Gerritsen M.E., and Bizios R. Morphological and proliferative responses of endothelial cells to hydrostatic pressure: role of fibroblast growth factor. Journal of Cellular Physiology 157 (1993) 603-614
2. Antonelli-Orlidge A., Saunders K.B., Smith S.R., and D'Amore P.A. An activated form of transforming growth factor beta is produced by cocultures of endothelial cells and pericytes. Proceedings of the National Academy of the Sciences of the United States of America 86 (1989) 4544-4548
3. Bader H. Dependence of wall stress in the human thoracic aorta on age and pressure. Circulation Research 20 (1967) 354-361
4. Baker A.B., Ettenson D.S., Jonas M., Nugent M.A., Iozzo R.V., and Edelman E.R. Endothelial cells provide feedback control for vascular remodeling through a mechanosensitive autocrine TGF-beta signaling pathway. Circulation Research 103 (2008) 289-297
5. Bergel D.H. The static elastic properties of the arterial wall. Journal of Physiology 156 (1961) 445-457
6. Bergel D.H. The dynamic elastic properties of the arterial wall. Journal of Physiology 156 (1961) 458-469
7. Berk B.C. Atheroprotective signaling mechanisms activated by steady laminar flow in endothelial cells. Circulation 117 (2008) 1082-1089
8. Bhadriraju K., Yang M., Alom Ruiz S., Pirone D., Tan J., and Chen C.S. Activation of ROCK by RhoA is regulated by cell adhesion, shape, and cytoskeletal tension. Experimental Cell Research 313 (2007) 3616-3623
9. Bonaccurso E., Cappella B., and Graf K. Local mechanical properties of plasma treated polystyrene surfaces. Journal of Physical Chemistry B 110 (2006) 17918-17924
10. Boutouyrie P., Tropeano A.I., Asmar R., Gautier I., Benetos A., Lacolley P., and Laurent S. Aortic stiffness is an independent predictor of primary coronary events in hypertensive patients: a longitudinal study. Hypertension 39 (2002) 10-15
11. Burton A.C. Relation of structure to function of the tissues of the wall of blood vessels. Physiological Reviews 34 (1954) 619-642
12. Califano J.P., and Reinhart-King C.A. A balance of substrate mechanics and matrix chemistry regulates endothelial cell network assembly. Cellular and Molecular Bioengineering 1 (2008) 122-132
13. Cameron J.D., and Dart A.M. Exercise training increases total systemic arterial compliance in humans. American Journal of Physiology 266 (1994) H693-H701
14. Chicurel M.E., Chen C.S., and Ingber D.E. Cellular control lies in the balance of forces. Current Opinion in Cell Biology 10 (1998) 232-239
15. Chen C.S. Mechanotransduction-a field pulling together?. Journal of Cell Science 121 (2008) 3285-3292
16. Chien S. Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. American Journal of Physiology-Heart and Circulatory Physiology 292 (2007) H1209-H1224
17. Costa K.D., Sim A.J., and Yin F.C. Non-Hertzian approach to analyzing mechanical properties of endothelial cells probed by atomic force microscopy. Journal of Biomechanical Engineering 128 (2006) 176-184
18. Cummins P.M., von Offenberg Sweeney N., Killeen M.T., Birney Y.A., Redmond E.M., and Cahill P.A. Cyclic strain-mediated matrix metalloproteinase regulation within the vascular endothelium: a force to be reckoned with. American Journal of Physiology-Heart and Circulatory Physiology 292 (2007) H28-H42
19. Dai G., Kaazempur-Mofrad M.R., Natarajan S., Zhang Y., Vaughn S., Blackman B.R., Kamm R.D., Garcia-Cardena G., and Gimbrone Jr. M.A. Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and-resistant regions of human vasculature. Proceedings of the National Academy of the Sciences of the United States of America 101 (2004) 14871-14876
20. Dashwood M.R., Savage K., Dooley A., Shi-Wen X., Abraham D.J., and Souza D.S. Effect of vein graft harvesting on endothelial nitric oxide synthase and nitric oxide production. Annals of Thoracic Surgery 80 (2005) 939-944
21. Davies P.F. Flow-mediated endothelial mechanotransduction. Physiological Reviews 75 (1995) 519-560
22. Davies P.F. Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nature clinical practice. Cardiovascular Medicine 6 (2009) 16-26
23. Davis G.E., and Senger D.R. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circulation Research 97 (2005) 1093-1107
24. dela Paz N.G., and D'Amore P.A. Arterial versus venous endothelial cells. Cell and Tissue Research 335 (2009) 5-16
25. Dembo M., Oliver T., Ishihara A., and Jacobson K. Imaging the traction stresses exerted by locomoting cells with the elastic substratum method. Biophysical Journal 70 (1996) 2008-2022
26. Dembo M., and Wang Y.L. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophysical Journal 76 (1999) 2307-2316
27. Deroanne C.F., Lapiere C.M., and Nusgens B.V. In vitro tubulogenesis of endothelial cells by relaxation of the coupling extracellular matrix-cytoskeleton. Cardiovascular Research 49 (2001) 647-658
28. Dewey Jr. C.F., Bussolari S.R., Gimbrone Jr. M.A., and Davies P.F. The dynamic response of vascular endothelial cells to fluid shear stress. Journal of Biomechanical Engineering 103 (1981) 177-185
29. Diamond S.L., Eskin S.G., and McIntire L.V. Fluid flow stimulates tissue plasminogen activator secretion by cultured human endothelial cells. Science 243 (1989) 1483-1485
30. Driessen G.K., Scheidt-Bleichert H., Sobota A., Inhoffen W., Heidtmann H., Haest C.W., Kamp D., and Schmid-Schonbein H. Capillary resistance to flow of hardened (diamide treated) red blood cells (RBC). Pflugers Archive: European Journal of Physiology 392 (1982) 261-267
31. Engler A., Bacakova L., Newman C., Hategan A., Griffin M., and Discher D. Substrate compliance versus ligand density in cell on gel responses. Biophysical Journal 86 (2004) 617-628
32. Feaver R.E., Hastings N.E., Pryor A., and Blackman B.R. GRP78 upregulation by atheroprone shear stress via p38-, alpha2beta1-dependent mechanism in endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology 28 (2008) 1534-1541
33. Folkman J., and Haudenschild C. Angiogenesis in vitro. Nature 288 (1980) 551-556
34. Fung Y.C. Biomechanics: Mechanical Properties of Living Tissues (1993), Springer-Verlag, New York
35. Galbraith C.G., Skalak R., and Chien S. Shear stress induces spatial reorganization of the endothelial cell cytoskeleton. Cell Motility and the Cytoskeleton 40 (1998) 317-330
36. Gentile A.T., Mills J.L., Westerband A., Gooden M.A., Berman S.S., Boswell C.A., and Williams S.K. Characterization of cellular density and determination of neointimal extracellular matrix constituents in human lower extremity vein graft stenoses. Cardiovascular Surgery 7 (1999) 464-469
37. Georges P.C., and Janmey P.A. Cell type-specific response to growth on soft materials. Journal of Applied Physiology 98 (2005) 1547-1553
38. Ghosh K., Thodeti C.K., Dudley A.C., Mammoto A., Klagsbrun M., and Ingber D.E. Tumor-derived endothelial cells exhibit aberrant Rho-mediated mechanosensing and abnormal angiogenesis in vitro. Proceedings of the National Academy of the Sciences of the United States of America 105 (2008) 11305-11310
39. Gimbrone Jr. M.A., Resnick N., Nagel T., Khachigian L.M., Collins T., and Topper J.N. Hemodynamics, endothelial gene expression, and atherogenesis. Annals of the New York Academy of Sciences 811 (1997) 1-10
40. Gossl M., Rosol M., Malyar N.M., Fitzpatrick L.A., Beighley P.E., Zamir M., and Ritman E.L. Functional anatomy and hemodynamic characteristics of vasa vasorum in the walls of porcine coronary arteries. The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology 272 (2003) 526-537
41. Groothoff J.W., Gruppen M.P., Offringa M., de Groot E., Stok W., Bos W.J., Davin J.C., Lilien M.R., Van de Kar N.C., Wolff E.D., and Heymans H.S. Increased arterial stiffness in young adults with end-stage renal disease since childhood. Journal of the American Society of Nephrology 13 (2002) 2953-2961
42. Guerin A.P., Pannier B., Metivier F., Marchais S.J., and London G.M. Assessment and significance of arterial stiffness in patients with chronic kidney disease. Current Opinion in Nephrology and Hypertension 17 (2008) 635-641
43. Guo W.H., Frey M.T., Burnham N.A., and Wang Y.L. Substrate rigidity regulates the formation and maintenance of tissues. Biophysical Journal 90 (2006) 2213-2220
44. Guyton A.C., and Hall J.E. Textbook of Medical Physiology (2000), Saunders, Philadelphia
45. Hahn C., Orr A.W., Sanders J.M., Jhaveri K.A., and Schwartz M.A. The subendothelial extracellular matrix modulates JNK activation by flow. Circulation Research 104 (2009) 995-1003
46. Hastings N.E., Simmers M.B., McDonald O.G., Wamhoff B.R., and Blackman B.R. Atherosclerosis-prone hemodynamics differentially regulates endothelial and smooth muscle cell phenotypes and promotes pro-inflammatory priming. American Journal of Physiology-Cell Physiology 293 (2007) C1824-C1833
47. Helmke B.P. Molecular control of cytoskeletal mechanics by hemodynamic forces. Physiology (Bethesda) 20 (2005) 43-53
48. Helmke B.P., Rosen A.B., and Davies P.F. Mapping mechanical strain of an endogenous cytoskeletal network in living endothelial cells. Biophysical Journal 84 (2003) 2691-2699
49. Hofstra L., Bergmans D.C., Hoeks A.P., Kitslaar P.J., Leunissen K.M., and Tordoir J.H. Mismatch in elastic properties around anastomoses of interposition grafts for hemodialysis access. Journal of the American Society of Nephrology 5 (1994) 1243-1250
50. Hofstra L., Tordoir J.H., Kitslaar P.J., Hoeks A.P., and Daemen M.J. Enhanced cellular proliferation in intact stenotic lesions derived from human arteriovenous fistulas and peripheral bypass grafts. Does it correlate with flow parameters?. Circulation 94 (1996) 1283-1290
51. Iba T., and Sumpio B.E. Morphological response of human endothelial cells subjected to cyclic strain in vitro. Microvascular Research 42 (1991) 245-254
52. Ingber D.E., and Folkman J. Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. Journal of Cell Biology 109 (1989) 317-330
53. Joannides R., Haefeli W.E., Linder L., Richard V., Bakkali E.H., Thuillez C., and Luscher T.F. Nitric oxide is responsible for flow-dependent dilatation of human peripheral conduit arteries in vivo. Circulation 91 (1995) 1314-1319
54. Kakisis J.D., Liapis C.D., and Sumpio B.E. Effects of cyclic strain on vascular cells. Endothelium 11 (2004) 17-28
55. Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nature reviews. Cancer 3 (2003) 422-433
56. Katanosaka Y., Bao J.H., Komatsu T., Suemori T., Yamada A., Mohri S., and Naruse K. Analysis of cyclic-stretching responses using cell-adhesion-patterned cells. Journal of Biotechnology 133 (2008) 82-89
57. Kato S., Sasaguri Y., Azagami S., Nakano R., Hamada T., Arima N., Tanimoto A., and Morimatsu M. Ambient pressure stimulates immortalized human aortic endothelial cells to increase DNA synthesis and matrix metalloproteinase 1 (tissue collagenase) production. Virchows Archiv-An International Journal of Pathology 425 (1994) 385-390
58. Kaunas R., Nguyen P., Usami S., and Chien S. Cooperative effects of Rho and mechanical stretch on stress fiber organization. Proceedings of the National Academy of the Sciences of the United States of America 102 (2005) 15895-15900
59. Kenagy R.D., Fukai N., Min S.K., Jalikis F., Kohler T.R., and Clowes A.W. Proliferative capacity of vein graft smooth muscle cells and fibroblasts in vitro correlates with graft stenosis. Journal of Vascular Surgery 49 (2009) 1282-1288
60. Kniazeva E., and Putnam A.J. Endothelial cell traction and ECM density influence both capillary morphogenesis and maintenance in 3D. American Journal of Physiology-Cell Physiology 297 (2009) C179-C187
61. Kondapalli J., Flozak A.S., and Albuquerque M.L. Laminar shear stress differentially modulates gene expression of p120 catenin, Kaiso transcription factor, and vascular endothelial cadherin in human coronary artery endothelial cells. Journal of Biological Chemistry 279 (2004) 11417-11424
62. Kou B., Zhang J., and Singer D.R. Effects of cyclic strain on endothelial cell apoptosis and tubulogenesis are dependent on ROS production via NAD(P)H subunit p22phox. Microvascular Research 77 (2009) 125-133
63. Krishnan L., Underwood C.J., Maas S., Ellis B.J., Kode T.C., Hoying J.B., and Weiss J.A. Interaction of angiogenic microvessels with the extracellular matrix. American Journal of Physiology-Heart and Circulatory Physiology 293 (2007) H3650-H3658
64. Kumar S., Maxwell I.Z., Heisterkamp A., Polte T.R., Lele T.P., Salanga M., Mazur E., and Ingber D.E. Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophysical Journal 90 (2006) 3762-3773
65. Kuzuya M., Satake S., Ai S., Asai T., Kanda S., Ramos M.A., Miura H., Ueda M., and Iguchi A. Inhibition of angiogenesis on glycated collagen lattices. Diabetologia 41 (1998) 491-499
66. Kuzuya M., Satake S., Miura H., Hayashi T., and Iguchi A. Inhibition of endothelial cell differentiation on a glycosylated reconstituted basement membrane complex. Experimental Cell Research 226 (1996) 336-345
67. Langewouters G.J., Wesseling K.H., and Goedhard W.J. The static elastic properties of 45 human thoracic and 20 abdominal aortas in vitro and the parameters of a new model. Journal of Biomechanics 17 (1984) 425-435
68. Learoyd B.M., and Taylor M.G. Alterations with age in the viscoelastic properties of human arterial walls. Circulation Research 18 (1966) 278-292
69. Lee T., and Sumpio B.E. Cell signalling in vascular cells exposed to cyclic strain: the emerging role of protein phosphatases. Biotechnology and Applied Biochemistry 39 (2004) 129-139
70. Lee Y.U., Drury-Stewart D., Vito R.P., and Han H.C. Morphologic adaptation of arterial endothelial cells to longitudinal stretch in organ culture. Journal of Biomechanics 41 (2008) 3274-3277
71. Li S., Butler P., Wang Y., Hu Y., Han D.C., Usami S., Guan J.L., and Chien S. The role of the dynamics of focal adhesion kinase in the mechanotaxis of endothelial cells. Proceedings of the National Academy of the Sciences of the United States of America 99 (2002) 3546-3551
72. Liao D., Arnett D.K., Tyroler H.A., Riley W.A., Chambless L.E., Szklo M., and Heiss G. Arterial stiffness and the development of hypertension. The ARIC study. Hypertension 34 (1999) 201-206
73. Liu W.F., Nelson C.M., Tan J.L., and Chen C.S. Cadherins, RhoA, and Rac1 are differentially required for stretch-mediated proliferation in endothelial versus smooth muscle cells. Circulation Research 101 (2007) e44-e52
74. Liu X.M., Ensenat D., Wang H., Schafer A.I., and Durante W. Physiologic cyclic stretch inhibits apoptosis in vascular endothelium. Federation of European Biochemical Societies Letters 541 (2003) 52-56
75. Lu L., Feng Y., Hucker W.J., Oswald S.J., Longmore G.D., and Yin F.C. Actin stress fiber pre-extension in human aortic endothelial cells. Cell Motility and the Cytoskeleton 65 (2008) 281-294
76. Lu L., Oswald S.J., Ngu H., and Yin F.C. Mechanical properties of actin stress fibers in living cells. Biophysical Journal 95 (2008) 6060-6067
77. Mammoto A., Connor K.M., Mammoto T., Yung C.W., Huh D., Aderman C.M., Mostoslavsky G., Smith L.E., and Ingber D.E. A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457 (2009) 1103-1108
78. Mitra A.K., Gangahar D.M., and Agrawal D.K. Cellular, molecular and immunological mechanisms in the pathophysiology of vein graft intimal hyperplasia. Immunology and Cell Biology 84 (2006) 115-124
79. Nehls V., and Herrmann R. The configuration of fibrin clots determines capillary morphogenesis and endothelial cell migration. Microvascular Research 51 (1996) 347-364
80. Nelson C.M., Jean R.P., Tan J.L., Liu W.F., Sniadecki N.J., Spector A.A., and Chen C.S. Emergent patterns of growth controlled by multicellular form and mechanics. Proceedings of the National Academy of the Sciences of the United States of America 102 (2005) 11594-11599
81. Nerem R.M., Harrison D.G., Taylor W.R., and Alexander R.W. Hemodynamics and vascular endothelial biology. Journal of Cardiovascular Pharmacology 2 (1993) S6-S10
82. Ngu H., Lu L., Oswald S.J., Davis S., Nag S., and Yin F.C. Strain-induced orientation response of endothelial cells: effect of substratum adhesiveness and actin-myosin contractile level. Molecular and Cellular Biomechanics 5 (2008) 69-81
83. Noria S., Cowan D.B., Gotlieb A.I., and Langille B.L. Transient and steady-state effects of shear stress on endothelial cell adherens junctions. Circulation Research 85 (1999) 504-514
84. Parang P., and Arora R. Coronary vein graft disease: pathogenesis and prevention. Canadian Journal of Cardiology 25 (2009) e57-e62
85. Passerini A.G., Polacek D.C., Shi C., Francesco N.M., Manduchi E., Grant G.R., Pritchard W.F., Powell S., Chang G.Y., Stoeckert Jr. C.J., and Davies P.F. Coexisting proinflammatory and antioxidative endothelial transcription profiles in a disturbed flow region of the adult porcine aorta. Proceedings of the National Academy of the Sciences of the United States of America 101 (2004) 2482-2487
86. Paszkowiak J.J., and Dardik A. Arterial wall shear stress: observations from the bench to the bedside. Vascular and Endovascular Surgery 37 (2003) 47-57
87. Peng X., Haldar S., Deshpande S., Irani K., and Kass D.A. Wall stiffness suppresses Akt/eNOS and cytoprotection in pulse-perfused endothelium. Hypertension 41 (2003) 378-381
88. Peyton S.R., Ghajar C.M., Khatiwala C.B., and Putnam A.J. The emergence of ECM mechanics and cytoskeletal tension as important regulators of cell function. Cell Biochemistry and Biophysics 47 (2007) 300-320
89. Peyton S.R., and Putnam A.J. Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. Journal of Cell Physiology 204 (2005) 198-209
90. Pless D.D., Lee Y.C., Roseman S., and Schnaar R.L. Specific cell adhesion to immobilized glycoproteins demonstrated using new reagents for protein and glycoprotein immobilization. Journal of Biological Chemistry 258 (1983) 2340-2349
91. Posch K., Schmidt K., and Graier W.F. Selective stimulation of l-arginine uptake contributes to shear stress-induced formation of nitric oxide. Life Sciences 64 (1999) 663-670
92. Pradhan S., and Sumpio B. Molecular and biological effects of hemodynamics on vascular cells. Frontiers in Bioscience 9 (2004) 3276-3285
93. Rabodzey A., Alcaide P., Luscinskas F.W., and Ladoux B. Mechanical forces induced by the transendothelial migration of human neutrophils. Biophysical Journal 95 (2009) 1428-1438
94. Reinhart-King C.A. Endothelial cell adhesion and migration. Methods in Enzymology 443 (2008) 45-64
95. Reinhart-King C.A., Dembo M., and Hammer D.A. Cell-cell mechanical communication through compliant substrates. Biophysical Journal 95 (2008) 6044-6051
96. Reinhart-King C.A., Fujiwara K., and Berk B.C. Physiologic stress-mediated signaling in the endothelium. Methods in Enzymology 443 (2008) 25-44
97. Reinhart-King C.A., Dembo M., and Hammer D.A. The dynamics and mechanics of endothelial cell spreading. Biophysical Journal 89 (2005) 676-689
98. Reinhart-King C.A., Dembo M., and Hammer D.A. Endothelial cell traction forces on RGD-derivatized polyacrylamide substrata. Langmuir 19 (2003) 1573-1579
99. Roach M.R. Biophysical analyses of blood vessel walls and blood flow. Annual Review of Physiology 39 (1977) 51-71
100. Schram M.T., Henry R.M., van Dijk R.A., Kostense P.J., Dekker J.M., Nijpels G., Heine R.J., Bouter L.M., Westerhof N., and Stehouwer C.D. Increased central artery stiffness in impaired glucose metabolism and type 2 diabetes: the Hoorn Study. Hypertension 43 (2004) 176-181
101. Shaik S.S., Soltau T.D., Chaturvedi G., Totapally B., Hagood J.S., Andrews W.W., Athar M., Voitenok N.N., Killingsworth C.R., Patel R.P., Fallon M.B., and Maheshwari A. Low intensity shear stress increases endothelial ELR+ CXC chemokine production via a focal adhesion kinase-p38beta MAPK-NF-B pathway. Journal of Biological Chemistry 284 (2009) 5945-5955
102. Sheriff D. Point: the muscle pump raises muscle blood flow during locomotion. Journal of Applied Physiology 99 (2005) 371-372 discussion 374-5
103. Shi F., Chiu Y.J., Cho Y., Bullard T.A., Sokabe M., and Fujiwara K. Down-regulation of ERK but not MEK phosphorylation in cultured endothelial cells by repeated changes in cyclic stretch. Cardiovascular Research 73 (2007) 813-822
104. Sieminski A.L., Hebbel R.P., and Gooch K.J. The relative magnitudes of endothelial force generation and matrix stiffness modulate capillary morphogenesis in vitro. Experimental Cell Research 297 (2004) 574-584
105. Staton C.A., Stribbling S.M., Tazzyman S., Hughes R., Brown N.J., and Lewis C.E. Current methods for assaying angiogenesis in vitro and in vivo. International Journal of Experimental Pathology 85 (2004) 233-248
106. Sumagin R., Brown III C.W., Sarelius I.H., and King M.R. Microvascular endothelial cells exhibit optimal aspect ratio for minimizing flow resistance. Annals of Biomedical Engineering 36 (2008) 580-585
107. Sumpio B.E., Banes A.J., Levin L.G., and Johnson Jr. G. Mechanical stress stimulates aortic endothelial cells to proliferate. Journal of Vascular Surgery 6 (1987) 252-256
108. Toikka J.O., Laine H., Ahotupa M., Haapanen A., Viikari J.S., Hartiala J.J., and Raitakari O.T. Increased arterial intima-media thickness and in vivo LDL oxidation in young men with borderline hypertension. Hypertension 36 (2000) 929-933
109. Tokunaga O., Fan J.L., and Watanabe T. Atherosclerosis and endothelium. Part II. Properties of aortic endothelial and smooth muscle cells cultured at various ambient pressures. Acta Pathologica Japonica 39 (1989) 356-362
110. Traub O., and Berk B.C. Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force. Arteriosclerosis, Thrombosis, and Vascular Biology 18 (1998) 677-685
111. Ukropec J.A., Hollinger M.K., and Woolkalis M.J. Regulation of VE-cadherin linkage to the cytoskeleton in endothelial cells exposed to fluid shear stress. Experimental Cell Research 273 (2002) 240-247
112. Vailhe B., Ronot X., Tracqui P., Usson Y., and Tranqui L. In vitro angiogenesis is modulated by the mechanical properties of fibrin gels and is related to alpha(v)beta3 integrin localization. In Vitro Cellular and Developmental Biology-Animal 33 (1997) 763-773
113. Vernon R.B., Lara S.L., Drake C.J., Iruela-Arispe M.L., Angello J.C., Little C.D., Wight T.N., and Sage E.H. Organized type I collagen influences endothelial patterns during "spontaneous angiogenesis in vitro": planar cultures as models of vascular development. In Vitro Cellular and Developmental Biology-Animal 31 (1995) 120-131
114. von Tell D., Armulik A., and Betsholtz C. Pericytes and vascular stability. Experimental Cell Research 312 (2006) 623-629
115. Vouyouka A.G., Jiang Y., Rastogi R., and Basson M.D. Ambient pressure upregulates nitric oxide synthase in a phosphorylated-extracellular regulated kinase- and protein kinase C-dependent manner. Journal of Vascular Surgery 44 (2006) 1076-1084
116. Wang Y.L., and Pelham Jr. R.J. Preparation of a flexible, porous polyacrylamide substrate for mechanical studies of cultured cells. Methods in Enzymology 298 (1998) 489-496
117. Wedding K.L., Draney M.T., Herfkens R.J., Zarins C.K., Taylor C.A., and Pelc N.J. Measurement of vessel wall strain using cine phase contrast MRI. Journal of Magnetic Resonance Imaging 15 (2002) 418-428
118. Wong J.Y., Velasco A., Rajagopalan P., and Pham Q. Directed movement of vascular smooth muscle cells on gradient compliant hydrogels. Langmuir 19 (2003) 1908-1913
119. Yamamura N., Sudo R., Ikeda M., and Tanishita K. Effects of the mechanical properties of collagen gel on the in vitro formation of microvessel networks by endothelial cells. Tissue Engineering 13 (2007) 1443-1453
120. Yano Y., Geibel J., and Sumpio B.E. Tyrosine phosphorylation of pp125FAK and paxillin in aortic endothelial cells induced by mechanical strain. American Journal of Physiology 271 (1996) C635-C649
121. Yeung T., Georges P.C., Flanagan L.A., Marg B., Ortiz M., Funaki M., Zahir N., Ming W., Weaver V., and Janmey P.A. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motility and the Cytoskeleton 60 (2005) 24-34
122. Zhang J., Burridge K.A., and Friedman M.H. In vivo differences between endothelial transcriptional profiles of coronary and iliac arteries revealed by microarray analysis. American Journal of Physiology-Heart and Circulatory Physiology 295 (2008) H1556-H1561
123. Zhou X., Rowe R.G., Hiraoka N., George J.P., Wirtz D., Mosher D.F., Virtanen I., Chernousov M.A., and Weiss S.J. Fibronectin fibrillogenesis regulates three-dimensional neovessel formation. Genes and Development 22 (2008) 1231-1243
124. Zieman S.J., Melenovsky V., and Kass D.A. Mechanisms, pathophysiology, and therapy of arterial stiffness. Arteriosclerosis, Thrombosis, and Vascular Biology 25 (2005) 932-943