Atherosclerosis and the Role of Wall Shear Stress

  • Robert M. Nerem
Part of the Clinical Physiology Series book series (CLINPHY)

Abstract

Atherosclerosis is the chief cause of death in the United States and in much of the western world. It is a disease of the large- and medium-size arteries. It also is a disease which involves complex interactions between a wide variety of factors (41, 88–90, 101, 114–115). Included in this are: (1) the endogenous cells of the arterial wall, that is, endothelial and smooth muscle cells; (2) formed elements of blood, notably monocytes and platelets; (3) plasma proteins, including low density lipoproteins (LDL); (4) connective tissue elements of the arterial intima; (5) environmental and genetic factors; and (6) hemodynamic-related factors. In this chapter we will be exploring the last of these—the role of blood flow and in particular wall shear stress, the frictional force imposed by flowing blood.

Keywords

Cholesterol Permeability Hydrolysis Migration Ischemia 

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References

  1. 1.
    Ando, J., H. Nomura, and A. Kamiya. The effects of fluid shear stress on the migration and proliferation of cultured endothelial cells. Microvasc. Res. 33: 62–70, 1987.PubMedGoogle Scholar
  2. 2.
    Ando, J., T. Komatsuda, and A. Kamiya. Cytoplasmic calcium responses to fluid shear stress in cultured vascular endothelial cells. In Vitro Cell Dev. Biol. 24: 871–877, 1988.PubMedGoogle Scholar
  3. 3.
    Asakura, T., and T. Karino. Flow patterns and spatial distribution of atherosclerotic lesions in human coronary arteries. Circ. Res. 11: 63–73, 1972.Google Scholar
  4. 4.
    Bell, F. P., I. Adamson, and C. J. Schwartz. Aortic endothelial permeability to albumin: Focal and regional patterns of uptake and transmural distribution of 125I-albumin in the young pig. Exp. Mol. Pathol. 20: 57, 1974.PubMedGoogle Scholar
  5. 5.
    Bell, F. P., Day, A. J., Gent, M., and C. J. Schwartz. Differing patterns of cholesterol accumulation and 3H-cholesterol influx in areas of the cholesterol-fed pig aorta identified by Evans Blue dye. Exp. Mol. Pathol. 22: 366, 1975.Google Scholar
  6. 6.
    Berk, B. C., P. R. Girard, M. Mitsumato, R. W. Alexander, and R. M. Nerem. Shear stress alters the genetic growth program of cultured endothelial cells. Proc. World Congress Biomechs. 11: 315 (Abstract), 1990.Google Scholar
  7. 7.
    Brown, A. M. A cellular logic for G protein coupled ion channel pathways. Faseb J. 5: 2175–2179, 1991.PubMedGoogle Scholar
  8. 8.
    Buck, R. C. Behavior of vascular smooth muscle cells during repeated stretching of the substratum in vitro. Atherosclerosis 46: 217–223, 1983.Google Scholar
  9. 9.
    Campbell, G. R., and J. H. Campbell. Smooth muscle cell phenotypic changes in arterial wall homeostasis: Implications for the pathogenesis of atherosclerosis. Exp. Mol. Pathol. 42: 139–162, 1985.PubMedGoogle Scholar
  10. 10.
    Campbell, G. R., J. H. Campbell, J. A. Manderson, S. Horrigan, and R. E. Rennick. Arterial smooth muscle: a multifunctional mesenchymal cell. Arch. Path. Lab. Med. 112: 977–986, 1988.PubMedGoogle Scholar
  11. 11.
    Caplan, B. A., and C. J. Schwartz. Increased endothelial cell turnover in areas of in vivo Evans Blue uptake in the pig aorta. Atherosclerosis 17: 401, 1973.PubMedGoogle Scholar
  12. 12.
    Caplan, B. A., R. G. Gerrity, and C. J. Schwartz. Endothelial cell morphology in focal areas of in vivo Evans Blue uptake in the young pig aorta. I. Quantitative Light Microscopic Findings. Exp. Mol. Pathol. 21: 102, 1974.PubMedGoogle Scholar
  13. 13.
    Caro, C. G., J. M. Fitz-Gerald, and R. C. Schroter. Atheroma and Arterial wall shear. Observation, correlation and proposal of a shear-dependent mass transfer mechanism for atherogenesis. Proc. Roy. Soc., London, B 177: 109–159, 1971.Google Scholar
  14. 14.
    Caro, C. G., C. L. Dumoulin, J. M. R. Graham, K. H. Parker and S. P. SouzA. Secondary flow in the human common carotid artery imaged by MR angiography. ASME J. Biomech. Engr. 114: 147–149, 1992.Google Scholar
  15. 15.
    Cathcart, M. K., D. W. Morel, and G. M. Chisholm. Monocytes and neutrophils oxidize low density lipoprotein making it cytotoxic. J. Leukocyte Biol. 38: 341–350, 1985.PubMedGoogle Scholar
  16. 16.
    Chuang, P., H. Cheng, S. Lin, K. Jan, and S. Chien. Macromolecular transport across arterial and venous endothelium in rats: Studies with Evans Blue-albumin and horseradish peroxidase. Arteriosclerosis 10: 188–197, 1990.PubMedGoogle Scholar
  17. 17.
    Cornhill, J. F. (Private Communication).Google Scholar
  18. 18.
    Cornhill, J. F., and M. R. Roach. A quantitative study of the localization of atherosclerotic lesions in the rabbit aorta. Atherosclerosis 23: 489–501, 1976.PubMedGoogle Scholar
  19. 19.
    Cushing, S. D., J. A. Berlinger, A. J. Valente, M. C. Territo, N. Mahamad, F. Parhami, R. Gerrity, C. J. Schwartz, and A. M. Fogelman. Minially modified low density lipoprotein induces monocyte chemotactic protein in human endothelial cells and smooth muscle cells. Proc. Natl. Acad. Sci. U.S.A. 87: 5134, 1990.PubMedGoogle Scholar
  20. 20.
    D’Amore, P. A., A. Orlidge, and I. M. Herman. Growth control in the retinal microvasculature. In Progress in Retinal Research, N. Osborne and G. Chaden, eds. New York: Pergamon Press, Vol. 7, pp. 233–258, 1987.Google Scholar
  21. 21.
    Dartsch, P. C., and E. Betz. Response of cultured endothelial cells to mechanical stimulation. Basic Res. Cardiol. 84: 268–281, 1989.PubMedGoogle Scholar
  22. 22.
    Dartsch, P. C., and H. Hammerle. Orientation response of arterial smooth muscle cells to mechanical stimulation. Eur. J. Cell Biol. 4: 339–346, 1986.Google Scholar
  23. 23.
    Dartsch, P. C., H. Hammerle, and E. Betz. Orientation of arterial smooth muscle cells growing on cyclically stretched substrates. Acta Annat. 125: 108–113, 1986.Google Scholar
  24. 24.
    Davies, P. F., C. F. Dewey, JR., S. R. Bussolari, E. F. Gordon, and M. A. Gimbrone, JR. Influence of hemodynamic forces on vascular endothelial function: in vitro studies of shear stress and pinocytosis in bovine aortic endothelial cells. J. Clin. Invest. 73: 1121–1129, 1984.PubMedGoogle Scholar
  25. 25.
    Dewey, C. F., S. R. Bussolari, M. A. Gimbrone, JR., and P. F. Davies. The dynamic response of vascular endothelial cells to fluid shear stress. ASME J. Biomech. Engr. 103: 177–181, 1981.Google Scholar
  26. 26.
    Diamond, S. L., S. G. Eskin, and L. V. Mcintire. Fluid flow stimulates tissue plasminogen activator secretion by cultured human endothelial cells. Science 243: 1483–1485, 1989.PubMedGoogle Scholar
  27. 27.
    Diamond, S. L., J. B. Sharefkin, C. Dieffenbach, K. Frazier-Scott, L. V. Mcintire, and S. G. Eskin. Tissue plasminogen activator messenger Rna levels increase in cultured human endothelial cells exposed to laminar shear stress. J. Cell. Physiol. 143: 364–371, 1990.PubMedGoogle Scholar
  28. 28.
    Dull, R. O., and P. F. Davies. Flow modulation of agonist (Atp)-response (Cam) coupling in vascular endothelial cells. Am. J. Physiol. 261 (Heart Circ. Physiol. 30 ): H149–H154, 1991.Google Scholar
  29. 29.
    Duncan, D. D., C. B. Bargeron, S. E. Borchardt, O. J. Deters, S. A. Gearhart, F. F. Mark, and M. H. Friedman. The effect of compliance on wall shear in casts of a human aortic bifurication. ASME J. Biomech. Engr. 112: 183–188, 1990.Google Scholar
  30. 30.
    Dutta, A., D. M. Wang, and J. M. Tarbell. Numerical analysis of flow in an elastic artery model. ASME J. Biomech. Engr. 114: 26–33, 1992.Google Scholar
  31. 31.
    Eskin, S. G., C. L. Ives, L. V. Mcintire, and L. T. Navarro. Response of cultured endothelial cells to steady flow. Microvasc. Res. 28: 87–94, 1984.PubMedGoogle Scholar
  32. 32.
    Feigl, E. O. Edrf—a protective factor? Nature 331: 490–491, 1988.PubMedGoogle Scholar
  33. 33.
    Flaherty, J. R., J. R. Pierce, V. J. Ferrans, D. J. Patel, W. K. Tucker, and D. L. Fry. Endothelial nuclear patterns in the canine arterial tree with particular reference to hemodynamic events. Circ. Res. 30: 23, 1972.PubMedGoogle Scholar
  34. 34.
    Frangos, J. A., L. V. Mcintire, S. G. Eskin, and C. L. Ives. Flow effects on prostacyclin production by cultured human endothelial cells. Science 227: 1477–1479, 1985.PubMedGoogle Scholar
  35. 35.
    Friedman, M. H., V. O’Brien, and L. W. Ehrlich. Calculations of pulsatile flow through a branch. Implications for the hemodynamics of atherogenesis. Circ. Res. 36: 277–285, 1975.PubMedGoogle Scholar
  36. 36.
    Friedman, M. H., O. J. Deters, F. F. Mark, C. B. Bargeron, and G. M. Hutchins. Arterial geometry affects hemodynamics: a potential risk factor for atherosclerosis. Atherosclerosis 46: 225–231, 1983.PubMedGoogle Scholar
  37. 37.
    Friedman, M. H., O. J. Peters, C. B. Bargeron, G. M. Hutchins, and F. F. Mark. Shear-dependent thickening of the human arterial intima. Atherosclerosis 60: 161–171, 1986.PubMedGoogle Scholar
  38. 38.
    Geiger, R. V., B. C. Berk, R. W. Alexander, and R. M. Nerem. Flow-induced calcium transients on single endothelial cells: spatial and temporal analysis. Am. J. Physiol. (Cell Physiol.) 262: C1411 - C1417, 1992.Google Scholar
  39. 39.
    Gerrity, R. G., J. A. Goss, and L. Soby. Control of monocyte recruitment by chemotactic factor(s) in lesion-prone areas of swine aorta. Arteriosclerosis 5: 55–66, 1985.PubMedGoogle Scholar
  40. 40.
    Girard, P. R., and R. M. Nerem. Role of protein kinase C in the transduction of shear stress to alterations in endothelial cell morphology. J. Cell Biochem. 14E: 21 (Abstract), 1990.Google Scholar
  41. 41.
    Glagov, S., C. K. Zarins, D. P. Giddens, and H. R. Davis, JR. Atherosclerosis: what is the nature of the plaque? In Vascular Diseases: Current Research and Clinical Applications, D. E. Strandness, Jr., P. Didishein, A. W. Glowes, and J. T. Watson, eds. Orlando: Grune and Stratton, pp. 15–33, 1987.Google Scholar
  42. 42.
    Goldstein, J. L., and M. S. Brown. The low-density lipoprotein pathway and its relation to atherosclerosis. Annual Rev. Biochem. 46: 897–930, 1977.Google Scholar
  43. 43.
    Gorfien, S. F., S. K. Winston, L. E. Thibault, and E. J. Macarak. Effects of biaxial deformation on pulmonary artery endothelial cells. J. Cell Physiol. 139: 492–500, 1989.PubMedGoogle Scholar
  44. 44.
    Grabowski, E. F., E. A. Jaffe, and B. B. Weksler. Prostacyclin production by culture human endothelial cells exposed to step increases in shear stress. J. Lab. Clin. Med. 105: 36–43, 1985.PubMedGoogle Scholar
  45. 45.
    Grande, J. P., S. Glagov, S. R. Bates, A. L. Horwitz, and M. B. Matthews. Effect of normolipemic and hyperlipemic serum on biosynthetic response to cyclic stretching of aortic smooth muscle cells. Arteriosclerosis 9: 446–452, 1989.PubMedGoogle Scholar
  46. 46.
    Grottum, P., A. Svindland, and L. Walloe. Localization of atherosclerotic lesions in the bifurcation of the left main coronary artery. Atherosclerosis 47: 55–62, 1983.PubMedGoogle Scholar
  47. 47.
    Hajjar, D. P., J. F. Domenick, J. B. Amberson, and J. M. Hefton. Interaction of arterial cells. 1. Endothelial cells alter cholesterol metabolism in co-cultured smooth muscle cells. J. Lipid Res. 26: 1212–1223, 1985.Google Scholar
  48. 48.
    Holenstein, R., P. Niederer, and M. Anliker. A viscoelastic model for use in predicting arterial pulse waves. ASME J. Biomech. Engr. 102: 318–325, 1980.Google Scholar
  49. 49.
    Karino, T., and M. Motomiya. Flow visualization in isolated transparent natural blood vessels. Biorheology 20: 119–127, 1983.PubMedGoogle Scholar
  50. 50.
    Kim, D. W., A. I. Gotlieb, and B. L. Langille. In vivo modulation of endothelial F-actin microfilaments by experimental alterations in shear stress. Arteriosclerosis 9: 439–445, 1989.PubMedGoogle Scholar
  51. 51.
    Klanchar, M., J. M. Tarbell, and D. M. Wang. In vitro study of the influence of radial wall motion on wall shear stress in an elastic tube model of the aorta. Circ. Res. 66: 1624, 1990.PubMedGoogle Scholar
  52. 52.
    Kollros, P. R., S. R. Bates, M. B. Matthews, A. L. Horwitz, and S. Glagov. Cyclic Amp inhibits increased collagen production by cyclically stretched smooth muscle cells. Lab. Invest. 56: 410–417, 1987.PubMedGoogle Scholar
  53. 53.
    Ku, D. N., and D. P. Giddens. Laser dooppler anemometer measurements of pulsatile flow in a model carotid bifurcation. J. Biomechanics 20: 407–421, 1987.Google Scholar
  54. 54.
    Ku, D. N., and D. Liepsch. The effects of non-Newtonian viscosity and wall elasticity on flow at a 90° bifurcation. Biorheol. 23: 359–370, 1986.Google Scholar
  55. 55.
    Ku, D. N., D. P. Giddens, C. K. Zarins, and S. Glagov. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Arteriosclerosis 5: 293–302, 1985.PubMedGoogle Scholar
  56. 56.
    Kubes, P., M. Suzuki, and D. N. Granger. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl. Acad. Sci. U.S.A. 88: 4651–4655, 1991.PubMedGoogle Scholar
  57. 57.
    KuLik, T. J., R. A. Bialecki, W. S. ColuccI, A. Rothman, and E. T. Glennon. Underwood RH. Stretch increases inositol triphosphate and inositol tetrakiphosphate in cultured pulmonary vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 180 (2): 982–987, 1991.Google Scholar
  58. 58.
    Laher, I., C. Van Breeman, and J. A. Bevan. Stretch-dependent calcium uptake associated with myogenic tone in rabbit facial vein. Circ. Res. 63: 669–772, 1988.PubMedGoogle Scholar
  59. 59.
    Laher, I., P. Vorkapic, A. L. DowD, and J. A. Bevan. Protein Kinase C potentiates stretch-induced cerebral artery tone by increasing intracellular sensitivity to Ca“. Biochem. Biophys. Res. Common. 165: 312–318, 1989.Google Scholar
  60. 60.
    Lansman, J. B., T. J. Hallam, and T. J. Rink. Single stretch-activated ion channels in vascular endothelial cells as mechanotransducers? Nature 325: 811–813, 1987.PubMedGoogle Scholar
  61. 61.
    Leung, D., S. Glagov, and M. Mathews. Cyclic stretching stimulates synthesis of matrix components by arterial smooth muscle cells in vitro. Science 191: 475–477, 1976.Google Scholar
  62. 62.
    Leung, D. Y. M., S. Glagov, and M. B. Mathews. A new in vitro system for studying cell response to mechanical stimulation: Different effects of cyclic stretching and agitation on smooth muscle cell biosynthesis. Exp. Cell Res. 109: 285–298, 1977.PubMedGoogle Scholar
  63. 63.
    Levesque, M. J., and R. M. Nerem. The elongation and orientation of cultured endothelial cells in response to shear stress. ASME J. Biomech. Engr. 106: 341–347, 1985.Google Scholar
  64. 64.
    Levesque, M. J., and R. M. Nerem. The studyof rheological effects on vascular endothelial cells in culture. Biorheology 26: 345–357, 1989.PubMedGoogle Scholar
  65. 65.
    Levesque, M. J., D. Liepsch, S. Moravec, and R. M. Nerem. Correlation of endothelial cell shape and wall shear stress in a stenosed dog aorta. Arteriosclerosis 6: 220–229, 1986.PubMedGoogle Scholar
  66. 66.
    Levesque, M. J., E. A. Sprague, and R. M. Nerem. Vascular endothelial cell proliferation in culture and the influence of flow. Biomaterials 11: 702–707, 1990.PubMedGoogle Scholar
  67. 67.
    Libby, P., and G. K. Hansson. Involvement of the immune system in human atherogenesis: current knowledge and unanswered questions. Lab. Invest. 64: 5–15, 1991.PubMedGoogle Scholar
  68. 68.
    Majesky, M. W., and S. M. Schwartz. Smooth muscle diversity in arterial wound repair. Toxic. Path. 18: 554–559, 1990.Google Scholar
  69. 69.
    Mitsumata, M., R. M. Nerem, R. W. Alexander, and B. C. Berk. Shear stress inhibits endothelial cell proliferation by growth arrest in the Go/G, phase of the cell cycle. FASEB J. 5(4): A527 (Abstract), 1991.Google Scholar
  70. 70.
    Mitsumata, M., R. M. Nerem, R. W. Alexander, and B. C. Berk. Inverse relationship in mRna expression between c-sis and Gapdh in endothelial cells subjected to shear stress. Abstract Book of Workshop on Mechanical Stress Effects on Vascular Cells. Atlanta, Ga: April 20–21, 1991.Google Scholar
  71. 71.
    Montenegro, M. R., and D. A. Eggen. Topography of atherosclerosis in the coronary arteries. Lab. Invest. 18: 586–593, 1968.PubMedGoogle Scholar
  72. 72.
    Mo, M., S. G. Eskin, and W. P. Schilling. Flow-induced changes in Ca“ signaling of vascular endothelial cells: effect of shear stress and Atp. Am. J. Physiol. 260 (Heart Circ. Physiol. 29 ): H1698 - H1707, 1991.Google Scholar
  73. 73.
    MooRE, J. E., JR., D. N. Ku, C. K. Zarins, and S. Glagov. Pulsatile flow visualization in the abdominal aorta under differing physiologic conditions: Implications for increased susceptibility to atherosclerosis. ASME J. Biomech. Engr. 114: 391–397, 1992.Google Scholar
  74. 74.
    Navab, M., S. S. Imes, S. Hama, G. P. Hough, L. A. Ross, R. W. Bork, A. J. Valente, J. A. Berliner, D. C. Drinkwater, H. Laks, and A. M. Fogelman. Monocyte transmigration induced by modification of low density lipoprotein in co-cultures of human aortic wall cells is due to induction of monocyte chemotatic protein 1 synthesis and is abolished by high density lipoprotein. J. Clin. Invest. 88: 2039–2046, 1991.PubMedGoogle Scholar
  75. 75.
    Nerem, R. M. Arterial fluid dynamics and interactions with the vessel wall. In Structure and Function of the Circulation, C. J. Schwartz, N. T. Werthessen, and S. Wolf, eds. New York: Plenum Publishing Corp., Vol. 11, 719–835, 1981.Google Scholar
  76. 76.
    Nerem, R. M., and P. R. Girard. Hemodynamic influences on vascular endothelial biology. Toxic. Path. 18: 572–582, 1990.Google Scholar
  77. 77.
    Nerem, R. M., and M. J. Levesque. The case for fluid dynamics as a localizing factor in atherogenesis. In Fluid Dynamics as a Localizing Factor for Atherosclerosis, G. Schettler, R. M. Nerem, H. Schmid-Schronbein, H. Mori, and C. Diehm, eds. Heidelberg, Frg: Springer-Verlag, pp. 26–37, 1983.Google Scholar
  78. 78.
    Nerem, R. M., and W. A. Seed. An in vivo study of aortic flow disturbances. Cardiovasc. Res. 6 (1): 1–14, 1972.PubMedGoogle Scholar
  79. 79.
    Nerem, R. M., M. J. Levesque, and J. F. Cornhill. Vascular endothelial morphology as an indicator of blood flow. ASME J. Biomech. Engr. 103: 172–176, 1981.Google Scholar
  80. 80.
    Nerem, R. M., J. A. Rumberger, D. R. Gross, R. L. Hamlin, and R. L. Geiger. Hot film anemometer velocity measurements of arterial flow in horses. Circ. Res. 34: 193–204, 1974.PubMedGoogle Scholar
  81. 81.
    Nerem, R. M., J. A. Rumberger, D. R. Gross, W. W. Muir, and G. L. Geiger. Hot-film artery velocity measurements in horses. Cardiovasc. Res. 10: 301–313, 1976.PubMedGoogle Scholar
  82. 82.
    Mimi, H. Role of stress concentration in arterial walls in atherosclerosis. Biorheology 16: 223–230, 1979.Google Scholar
  83. 83.
    Nollert, M. V., and L. V. Mcintire. Convective mass transfer effects on the intracellular calcium resonse of endothelial cells. ASME J. Biomech. Engr. 114: 321–326, 1992.Google Scholar
  84. 84.
    Nollert M. U., S. G. Eskin, and L. V. Mcintire. Shear stress increases inositol trisphosphate levels in human endothelial cells. Biochem. Biophys. Res. Commun. 170: 281–287, 1990.PubMedGoogle Scholar
  85. 85.
    Olesen, S. P., D. E. Clapham, and P. F. Davies. Hemodynamic shear stress activates a K* current in vascular endothelial cells. Nature 331: 168–170, 1987.Google Scholar
  86. 86.
    Perktold, K., R. M. Nerem, and R. O. Peter. A numerical calculation of flow in a curved tube model of the left main coronary artery. J. Biomechanics. 24: 175–189, 1991.Google Scholar
  87. 87.
    Prasad, A. R. S., R. M. Nerem, C. J. Schwartz, and E. A. Sprague. Stimulation Of phosphoinositide hydrolysis in bovine aortic endothelial cells exposed to elevated shear stress. J. Cell. Biol. 109: 331a (Abstract), 1989.Google Scholar
  88. 88.
    Ross, R. Atherosclerosis: a problem of biology of arterial wall cells and their interaction with blood components. Atherosclerosis 1: 293–311, 1981.Google Scholar
  89. 89.
    Ross, R. Mechanisms of atherosclerosis-a review. Adv. Nephrol. 19: 79, 1990.Google Scholar
  90. 90.
    Ross, R., and J. Glomset. The pathogenesis of atherosclerosis. New England J. Med. 295: 369–377, 420–425, 1976.Google Scholar
  91. 91.
    Ross, R., and S. Klebanoff. The smooth muscle cell. I. In vivo synthesis of connective tissue proteins. J. Cell Biol. 50: 159–171, 1971.PubMedGoogle Scholar
  92. 92.
    Rabinovitz, R. S., M. J. Levesque, and R. M. Nerem. Effects of branching angle in the left main coronary bifurication. Circulation 76 (Supplement): IV - 387, 1987.Google Scholar
  93. 93.
    Rozek, M. M., A. J. Valente, A. J. Cayatte, E. A. Sprague, and C. J. Schwartz. The influence of smooth muscle cell-derived monocyte chemotactic protein (Mcp-I) on monocyte adherence to cultured vascular endothelial cells. Circulation 82: 363 (Abstract), 1990.Google Scholar
  94. 94.
    Rubanyi, G. M., J. C. Romero, and P. M. Vanhoutte. Flow-induced release of endothelium-derived relaxing factor. Am. J. Physiol. 250 (Heart Circ. Physiol. 19 ): H1145 - H1149, 1986.Google Scholar
  95. 95.
    Sakata, N., K. Kawamura, and S. Takebayashi. Effects of collagen matrix on proliferation and differentiation of vascular smooth muscle cells in vitro. Exp. Mol. Path. 52: 179–191, 1990.Google Scholar
  96. 96.
    Sato, M., M. J. Levesque, and R. M. Nerem. Micropipette aspiration of cultured bovine aortic endothelial cells exposed to shear stress. Arteriosclerosis 7: 276–286, 1987.PubMedGoogle Scholar
  97. 97.
    Sato, M., D. P. Theret, L. T. Wheeler, N. Ohshima, and R. M. Nerem. Application of the micropipette technique to the measurement of cultured borcine aortic endothelial cell viscoelastic properties. ASME J. Biomech. Eng. 112: 263–268, 1990.Google Scholar
  98. 98.
    Schwartz, C. J., and J. R. A. Mitchell. Observations on localizations of arterial plaques. Circ. Res. 11: 63–73, 1972.Google Scholar
  99. 99.
    Schwartz, C. J., E. A. Sprague, S. R. Fowler, and J. L. Kelley. Cellular participation in atherogenesis: Selected facets of endothelium, smooth muscle, and peripheral blood monocyte. In Fluid Dynamics as a Localizing Factor for Atherosclerosis, G. Schettler, R. M. Nerem, H. Schmid-Schonbein, H. Mori, and D. Diehm, eds. Heidelberg Frg: Springer-Verlag, pp. 200–207, 1983.Google Scholar
  100. 100.
    Schwartz, C. J., A. J. Valente, E. A. Sprague, J. L. Kelley, C. A. Suenram, D. T. Graves, M. M. Rozek, E. H. Edwards, and R. Delgade. Monocyte-macrophage participation in atherogenesis: inflammatory components of pathogenesis. Semin. Thromb. Hemost. 12: 79–86, 1986.PubMedGoogle Scholar
  101. 101.
    Schwartz, C. J., A. J. Valente, E. A. Sprague, J. L. Kelley, and R. M. Nerem. The pathogenesis of atherosclerosis: an overview. Clinical Cardiology 14: 1–1–16, 1991.Google Scholar
  102. 102.
    Schwartz, S. M., G. R. Campbell, and J. H. Campbell. Replication of smooth muscle cells in vascular disease. Circ. Res. 58: 427–444, 1986.PubMedGoogle Scholar
  103. 103.
    Schwenke, D. C., and T. E. Carew. Initiation of atherosclerotic lesions in cholesterol-fed rabbits: II. selective retention of Ldl vs. selective increases in Ldl permeability in susceptible sites of arteries. Arteriosclerosis 9: 908–918, 1989.PubMedGoogle Scholar
  104. 104.
    Seidel, C. L., and L. A. Schildmeyer. Vascular smooth muscle adaptation to increased load. Annual Rev. Physiol. 49: 489–499, 1987.PubMedGoogle Scholar
  105. 105.
    Shen, J., and C. F. Dewey, JR. Fluid shear stress modulates cytosolic free calcium in vascular endothelial cells. Am. J. Physiol. 262 (Cell Physiol. 31 ): C384 - C390, 1992.Google Scholar
  106. 106.
    Shirinsky, V. P., A. S. Antonov, K. G. Birukov, A. V. Sobolevsky, Y. A. Romanov, N. V. Kabaeva, G. N. Anonova, and V. N. Smirnov. Mechano-chemical control of human endothelium orientation and size. J. Cell Biol. 109: 331–339, 1989.PubMedGoogle Scholar
  107. 107.
    Silkworth, J. B., and W. E. Stehbens. The shape of endothelial cells in en face preparations of rabbit blood vessels. Angiology 26: 474–487, 1975.Google Scholar
  108. 108.
    Simon, M. I., M. P. Strathmann, and N. Gautam. Diversity of G proteins in signal transduction. Science 252: 802–808, 1991.PubMedGoogle Scholar
  109. 109.
    Sottiurai, V. S., P. Kollros, S. Glagov, C. K. Zarins, and M. B. Mathews. Morphologic alteration of cultured arterial smooth muscle cells by cyclic stretching. J. Surg. Res. 35: 490–497, 1983.PubMedGoogle Scholar
  110. 110.
    Sparks, H. V., and L. Kaiser. Endothelial cells: not just a cellophane wrapper. Arch. Intern. Med. 147: 169–573, 1987.Google Scholar
  111. 111.
    Sprague, E. A., M. J. Levesque, M. M. Rozek, C. J. Schwartz, and R. M. Nerem. Shear stress related decreases in cell proliferation and platelet and monocyte adherence to bovine aortic endothelial cells seeded on solid and porous polyester substrates. ASME Adv. in Bioeng. 17: 357–360, 1990.Google Scholar
  112. 112.
    Sprague, E. A., B. L. Steinbach, R. M. Nerem, and C. J. Schwartz. Influence of a laminar steady-stage fluid-imposed wall shear stress on the binding, internalization, and degradation of low density lipoproteins by cultured arterial endothelium. Circulation 76: 648–656, 1987.PubMedGoogle Scholar
  113. 113.
    Stary, H. C., D. H. Blankenhorn, A. B. Chandler, S. Glagov, W. Insull, JR., M. Richardson, M. E. Rosenfeld, S. A. Schaffer, C. J. Schwartz, W. D. Wagner, and R. W. Wissler. A definition of the intima of human arteries and its atherosclerosis-prone regions. Arteriosclerosis and Thrombosis 12 (1): 120–134, 1992.Google Scholar
  114. 114.
    Steinberg, D. Lipoproteins and atherosclerosis: a look back and a look ahead. Arteriosclerosis 3: 283–301, 1983.PubMedGoogle Scholar
  115. 115.
    Steinberg, D., S. Pathasarathy, T. E. Carew, J. C. KHoo, and J. L. Witzum. Beyond cholesterol: modifications of low-density lipoprotein that increase its atherogenicity. New England J. Med. 320: 915–924, 1989.Google Scholar
  116. 116.
    Sumpio, B. E., A. J. Banes, L. G. Levin, and G. Johnson, JR. Mechanical stress stimulates aortic endothelial cells to proliferate. J. Vasc. Surg. 6: 252–256, 1987.PubMedGoogle Scholar
  117. 117.
    Sumpio, B. E., and A. J. Banes. Prostacyclin synthetic activity in cultured aortic endothelial cells undergoing cyclic stretch. Surgery 104: 383–389, 1988.PubMedGoogle Scholar
  118. 118.
    Sumpio, B. E., and A. J. Banes. Response of porcine aortic smooth muscle cells to cyclic tensional deformation in culture. J. Surg. Res. 44: 696–701, 1988.PubMedGoogle Scholar
  119. 119.
    Sumpio, B. E., A. J. Banes, L. G. Levin, and G. Johnson, JR. Alternations in aortic endothelial cell morphology and cytoskeleton protein synthesis during cyclic tensional deformation. J. Vasc. Surg. 7: 130–138, 1988.PubMedGoogle Scholar
  120. 120.
    Sumpio, B. E., A. J. Banes, W. G. Link, and G. Johnson. Enhanced collagen production by smooth muscle cells during repetitive mechanical stretching. Arch. Surg. 123: 1233–1236, 1988.PubMedGoogle Scholar
  121. 121.
    Tang, T. D., D. P. Giddens, S. A. Jones, C. K. Zarins, and S. Glagov. Estimation of coronary artery wall shear stress and its implications for atherogenesis. In Digest of Papers, 10th Southern Biomedical Engineering Conference, held in Atlanta, Ga., Oct. 18–21, 1991, pp. 151–154, 1991.Google Scholar
  122. 122.
    Taylor, W. R., D. G. Harrison, R. M. Nerem, T. E. Peterson, and R. W. Alexander. Characterization of the release of endothelium-derived nitrogen oxides by shear stress. Faseb J. (Abstract) 56 (6): A1727, 1991.Google Scholar
  123. 123.
    Theret, D. P., M. J. Levesque, M. Sato, R. M. Nerem, and L. T. Wheeler. The application of a homogeneous half-space model in the analysis of endothelial cell micropipette measurements. ASME J. Biomech. Eng. 110: 190–199, 1988.Google Scholar
  124. 124.
    Thubrikar, M. J., J. W. Baker, and P. N. Stanton. Inhibition of atherosclerosis associated with reduction of arterial intramural stress in rabbits. Arteriosclerosis 8: 410–420, 1988.PubMedGoogle Scholar
  125. 125.
    Valente, A. J., S. R. Fowler, E. A. Sprague, J. L. Kelley, C. A. Suenram, and C. J. Schwartz. Initial characterization of a peripheral blood mononuclear cell chemoattractant derived from cultured arterial smooth muscle cells. Am. J. Pathol. 117: 409–417, 1984.Google Scholar
  126. 126.
    Valente, A. J., D. T. Graves, C. E. Vialle-Valentin, R. Delgado, and C. J. Schwartz. Purification of a monocyte chemotactic factor secreted by non-human primate vascular cells in culture. Biochemistry 27: 4162–4168, 1988.PubMedGoogle Scholar
  127. 127.
    Velican, D., and C. Velican. Accelerated atherosclerosis in subjects with some minor deviations from the common type distribution of human coronary arteries. Atherosclerosis 40: 309–313, 1981.PubMedGoogle Scholar
  128. 128.
    Watson, P. A. Function follows form: generation of intracellular signals by cell deformation. FASEB J. 5: 2013–2019, 1991.PubMedGoogle Scholar
  129. 129.
    Wechezak, A. R., R. F. Viggers, and L. R. Sauvage. Fibronectin and F-actin redistribution in cultured endothelial cells exposed to shear stress. Lab. Invest. 53: 639–647, 1985.PubMedGoogle Scholar
  130. 130.
    White, G. E., and K. Fujiwara. Expression of intracellular distribution of stress fibers in aortic endothelium. J. Cell Biol. 103: 63–70, 1986.PubMedGoogle Scholar
  131. 131.
    Wissler, R. W., ET AL. Relationships of atherosclerosis in young men to serum lipoprotein cholesterol concentrations and smoking. J. Amer. Med. Assoc. 264: 3018–3024, 1990.Google Scholar
  132. 132.
    Yoshida, Y., M. Okano, S. Wang, M. Kobayashi, and M. Shimisu. Endothelial functions modulated by hemorheological forces. In Atherosclerosis IX, Proceedings of the 9th International Symposium on Atherosclerosis. RandL Creative Communications, Ltd., Tel Aviv, Israel, 571–575, 1992.Google Scholar
  133. 133.
    Yuan, F., S. Chien and S. Weinbaum. A new view of convective-diffusive transport processes in the arterial intima. ASME J. Biomech. Engr. 113: 314–329, 1991.Google Scholar

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© American Physiological Society 1995

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  • Robert M. Nerem

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