Fluid Shear Stress Control of Vascular Smooth Muscle

  • John M. Tarbell
  • Mete Civelek
  • Jeff S. Garanich

Abstract

In addition to neural and humoral signals, vascular smooth muscle cells (SMC) sense the mechanical environment that is imposed upon them by hemodynamic forces generated in the vascular system. The traditional view of mechanical forces and the vascular system has been that endothelial cells (EC), which line all blood vessels, sense primarily the shear stress of flowing blood on their lumenal surface (e.g. 28), whereas SMC, which lie within the wall and are normally shielded from the direct shearing forces of blood flow, sense the solid mechanical stress (hoop stress) or strain (stretch) driven by blood pressure (e.g. 102). But, it is clear that EC also experience solid mechanical stress and strain associated with vessel distension in response to the pressure pulse and are influenced by these forces (29). Perhaps less obvious is the fact that SMC, in their normal physiological environment, experience significant levels of fluid shear stress associated with transmural interstitial flow driven by the transvascular pressure differential. In addition, in cases of vascular injury, SMC may be directly exposed to the fluid shearing forces of blood flow. The nature and magnitude of these fluid mechanical forces on SMC and their pathophysiological consequences provide the focus for this review. In order to maintain a sense of balance, however, we also describe, albeit briefly, the solid mechanical environment of SMC and the influence of tissue stress and strain on SMC function.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Reference List

  1. 1.
    Alshihabi SN, Chang YS, Frangos JA, Tarbell IM (1996) Shear Stress Induced Release of PGE2 and PGI2 by Vascular Smooth Muscle. Biochem. Biophys. Res. 224 (3): 808–24.CrossRefGoogle Scholar
  2. 2.
    Ambalavanan N, Mariani G, Bulger A, Philips JB (1999) III Role of Nitric Oxide in Regulating Neonatal Porcine Pulmonary Artery Smooth Muscle Cell Proliferation. Biol. Neonate. 76: 291–300.Google Scholar
  3. 3.
    Baldwin AL, Wilson LM, Simon BR (1992) Effect of Pressure on Hydraulic Conductance. Arterioscler. Thromb. 12: 163–71.Google Scholar
  4. 4.
    Banes AJ, Gilbert J, Taylor D, Monbureau 0 (1985) A New Vacuum-operated Stress-providing Instrument that Applies Static or Variable Duration Cyclic Tension or Compression to Cells in vitro. J. Cell. Sci. 75: 35–40.Google Scholar
  5. 5.
    Barbee KA, Macarak EJ, Thibault LE (1994) Strain Measurements in Cultured Vascular Smooth Muscle Cells Subjected to Mechanical Deformation. Ann. Biomed. Eng. 22: 14–22.Google Scholar
  6. 6.
    Barbee KA, Mundel T, Lai R, Davies PF (1995) Subcellular Distribution of Shear Stress at the Surface of Flow-aligned and Nonaligned Endothelial Monolayers. Am. J. Physiol. 268, H1765–72.PubMedGoogle Scholar
  7. 7.
    Bassiouny HS, Song RH, Hong XF, Singh A, Kocharyan H, Glagov S (1998) Flow Regulation of 72kD Collagenase IV (MMP-2) after Experimental Arterial Injury. Circulation. 98: 157–63.PubMedCrossRefGoogle Scholar
  8. 8.
    Baykal D, Schmedtje Jr JF, Runge MS (1995) Role of Thrombin Receptor in Restonosis and Atherosclerosis. Am. J. Cardiol. 75: 82B - 87B.PubMedCrossRefGoogle Scholar
  9. 9.
    Bayliss WM (1902) On the Local Reactions of the Arterial Wall to Changes of Internal Pressure. J. Physiol. Lond. 28: 220–31.PubMedGoogle Scholar
  10. 10.
    Bevan JA, Henrion (1994) Pharmacological Implications of the Flow-dependence of Vascular Smooth Muscle Tone. Ann. Rev. Pharmacol. Toxicol. 34: 173–90.Google Scholar
  11. 11.
    Bevan JA, Joyce EH, Wellman GC (1988) Flow Dependent Dilation in a Resistance Artery still Occurs after Endothelium Removal. Circ. Res. 63: 980–5.Google Scholar
  12. 12.
    Bevan JA, Joyce EH (1988) Flow-dependent Contraction Observed in a Myograph-mounted Resistance Artery. Blood Vessels. 25: 261–4.PubMedGoogle Scholar
  13. 13.
    Bevan JA, Joyce EH (1990) Flow-induced Resistance Artery Tone: Balance between Constrictor and Dilator Mechanisms. Am. J. Physiol. 258: H663–8.PubMedGoogle Scholar
  14. 14.
    Bodin P, Richard S, Travo C, Berta P, Stoclet JC, Papin S, Travo P (1991) Responses of Subcultured Rat Aortic Smooth Muscle Myocytes to Vasoactive Agents and KCI-induced Depolarization. Am. J. Physiol. 260 (Cell Physiol. 29): C151–8.PubMedGoogle Scholar
  15. 15.
    Boswell CA, Majno G, Joris I, Ostrom KA (1992) Acute Endothelial Cell Contraction in vitro. Microvasc. Res. 43: 178–91.Google Scholar
  16. 16.
    Brinkman HC (1947) A Calculation of the Viscous Force Exerted by a Flowing Fluid on a Dense Swarm of Particles. Appl. Sci. Res. Al: 27–34.Google Scholar
  17. 17.
    Buck RC (1983) Behavior of Vascular Smooth Muscle Cells during Repeated Stretching of the Substratum in vitro. Atherosclerosis. 46: 217–23.PubMedCrossRefGoogle Scholar
  18. 18.
    Caro CG, Pedley TJ, Schroter RC, Seed WA (1978) The Mechanics of the Circulation, Oxford University Press, Oxford.Google Scholar
  19. 19.
    Chang YS, diTomaso E, McDonald DM, Jones R, Jain RK, Munn LL (2000a) Mosaic Blood Vessels in Tumors: Frequency of Cancer Cells in Contact with Flowing Blood. Proc. Natl. Acad. Sci. U.S.A. 97: 14608–13.Google Scholar
  20. 20.
    Chang Y, Munn L, Hillsley M, Dull R, Yuan J, Lakshiminarayanan S, Gardner T, Jain R, Tarbell JM (2000b) Effect of Vascular Endothelial Growth Factor on Cultured Endothelial Cell Monolayer Transport Properties. Microvasc. Res. 59: 265–77.Google Scholar
  21. 21.
    Chatterjee M, Tegada (1986) Phorbol Ester-induced Contraction in a Chemically Skinned Smooth Muscle. Am. J. Physiol. 251 (Cell Physiol. 20): C356–61.Google Scholar
  22. 22.
    Chen C, Hanson SR, Keefer LK, Saavedra JE, Davies KM, Hutsell TC, Hughes JD, Ku DN, Lumsden AB (1997) Boundary Layer Infusion of Nitric Oxide Reduces Early Smooth Muscle Cell Proliferation in the Endarterectomized Canine Artery. J. Surg. Res. 67: 26–32.Google Scholar
  23. 23.
    Cheng GC, Briggs WH, Gerson DS, Libby P, Grodzinsky AJ, Gray ML, Lee RT (1997) Mechanical Strain Tightly Controls Fibroblast Growth Factor-2 Release from Cultured Human Vascular Smooth Muscle Cells. Circ. Res. 80: 1–8.Google Scholar
  24. 24.
    Civelek M (2001) Smooth Muscle Cell Contraction in Response to Fluid Shear Stress. M.S. thesis, The Pennsylvania State University.Google Scholar
  25. 25.
    Clark JM, Glagov S (1985) Transmural Organization of the Arterial Media. Arteriosclerosis 5: 19–26.PubMedCrossRefGoogle Scholar
  26. 26.
    Clowes AW, Kirkman TR, Clowes MM (1986) Mechanisms of Arterial Graft Failure 4: Chronic Endothelial and Smooth Muscle Cell Proliferation in Healing Polytetrafluoroethylene Prostheses. J. Vasc. Surg. 3 (6): 877–84.PubMedGoogle Scholar
  27. 27.
    Corjay MH, Thompson MM, Lynch KR, Owens GK (1989) Differential Effect of Platelet-derived Growth Factor versus Serum-induced Growth on Smooth Muscle Alpha-actin and Nonmuscle Beta-actin mRNA Expression in Cultured Rat Aortic Smooth Muscle Cells. J. Biol. Chem. 264: 10501–6.Google Scholar
  28. 28.
    Davies PF (1995) Flow-mediated Endothelial Mechanotransduction. Physiol. Rev. 75: 519–60.PubMedGoogle Scholar
  29. 29.
    Davies PF, Tripathi SC (1993) Mechanical Stress Mechanisms and the Cell. Circ. Res. 72: 239–45.Google Scholar
  30. 30.
    Davis MJ, Meininger GA, Zawieja DC (1992) Stretch-induced Increases in Intracellular Calcium of Isolated Vascular Smooth Muscle Cells. Am. J. Physiol. 236: H1292–9.Google Scholar
  31. 31.
    Davis MJ, Wu X, Nurkiewicz TR, Kawasaki J, Davis GE, Hill MA, Meininger GA (2001) Integrins and Mechanotransduction of the Vascular Myogenic Response. Am. J. Physiol. 280: H1427–33.Google Scholar
  32. 32.
    DeMeyer GRY, Van Put DJM, Kockx MM, Van Schil P, Bosmans R, Bult H, Buyssens N, Vanmaele R, Herman AG (1997) Possible Mechanisms of Collar-induced Intimal Thickening. Arterioscler. Thromb. Vasc. Biol. 17: 1924–30.Google Scholar
  33. 33.
    Dessy C, Kim I, Sougnez CL, Laporte R, Morgan KG (1998). A Role for MAP Kinase in Differentiated Smooth Muscle Contraction Evoked by Alpha-adrenoceptor Stimulation. Am. J. Physiol. 275: C1081–6.PubMedGoogle Scholar
  34. 34.
    Dethlefsen SM, Shepro D, D’Amore PA (1996) Comparison of the Effects of Mechanical Stimulation on Venous and Arterial Smooth Muscle Cells in vitro. J. Vasc. Res. 33: 405–13.Google Scholar
  35. 35.
    Falcone JC, Davis MJ, Meininger GA (1991) Endothelial Independence of Myogenic Response in Isolated Skeletal Muscle Arterioles. Am. J. Physiol. 260: H 130–5.Google Scholar
  36. 36.
    Flaherty P, Grushkin-Lerner L (1998) Phenotypic Modulation of Aortic Smooth Muscle Cells Using Optimized Cell Culture Environments. Becton Dickinson Company Manual.Google Scholar
  37. 37.
    Folkow B (1990) Structural Factor in Primary and Secondary Hypertension. Hypertension. 16: 89101.CrossRefGoogle Scholar
  38. 38.
    Friedman MH, Deters OJ, Mark FF, Bargeson CB, Hutchins GM (1983) Arterial Geometry Affects Hemodynamics: a Potential Risk Factor for Atherosclerosis. Atherosclerosis. 46: 225–31.PubMedCrossRefGoogle Scholar
  39. 39.
    Fung YC (1984) Biodynamics: Circulation. New York, Springer-Verlag.Google Scholar
  40. 40.
    Fung YC (1993) Biomechanics: Mechanical Properties of Living Tissue, New York, Springer-Verlag.Google Scholar
  41. 41.
    Geary RL, Kohler TR, Vergel S, Kirkman TR, Clowes AW (1993) Time Course of Flow-induced Smooth Muscle Cell Proliferation and Intimal Thickening in Endothelialized Baboon Vascular Grafts. Circ. Res. 74: 14–23.Google Scholar
  42. 42.
    Gilbert JA, Weinhold PS, Banes AJ, Link GW, Jones GL (1994) Strain Profiles for Circular Culture Plates Containing Flexible Surfaces Employed to Mechanically Deform Cells in vitro. J. Biomech. 27: 1169–77.PubMedCrossRefGoogle Scholar
  43. 43.
    Gong MC, Fuglsang A, Messi D, Kobayashi S, Cohen P, Somlyo AV, Somlyo AP (1992a) Arachidonic Acid Inhibits Myosin Light Chain Phosphatase and Sensitizes Smooth Muscle to Calcium. J. Biol. Chem. 267 (3): 21492–8.PubMedGoogle Scholar
  44. 44.
    Gong MC, Cohen P, Kitawaza T, Ikebe M, Masuo M, Somlyo AV, Somlyo AP (1992b) Myosin Light Chain Phosphatase Activities and the Effects of Phosphatase Inhibitors in Tonic and Phasic Smooth Muscle. J. Biol. Chem. 267 (2): 14662–8.PubMedGoogle Scholar
  45. 45.
    Gooch KJ, Dangler CA, Frangos JA (1997) Exogenous, Basal, and Flow-induced Oxide Production and Endothelial Cell Proliferation. J. Cellular Physiol. 171: 252–8.Google Scholar
  46. 46.
    Gosgnach W, Challah M, Coulet F, Michel J, 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
  47. 47.
    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. 279: C1880–8.Google Scholar
  48. 48.
    Grainger DJ, Weissberg PL, Metcalfe JC (1993) Tamoxifen Decreases the Rate of Proliferation of Rat Vascular Smooth-muscle Cells in Culture by Inducing Production of Transforming Growth Factor Beta. Biochem. J. 294: 109–12.Google Scholar
  49. 49.
    Groves PH, Banning AP, Penny WJ, Newby AC, Cheadle HA, Lewis MJ (1995) The Effects of Exogenous Nitric Oxide on Smooth Muscle Cell Proliferation Following Porcine Carotid Angioplasty. Cardiovasc. Res. 30: 87–96.Google Scholar
  50. 50.
    Haberstroh KM, Kaefer M, Retik AB, Freeman MR, Bizios R(1999) The Effects of Sustained Hydrostatic Pressure on Select Bladder Smooth Muscle Cell Functions. J. Urology. 162: 2114–8.Google Scholar
  51. 51.
    Halloran BG, Prorok GD, So BJ, Baxter BT (1995) Transforming Growth Factor-beta 1 Inhibits Human Arterial Smooth-muscle Cell Proliferation in a Growth-rate-dependent Manner. Am. J. Surg. 170: 193–7.Google Scholar
  52. 52.
    Harder DR, Gilbert R, Lombard JH (1987) Vascular Muscle Depolarization and Activation in Renal Arteries on Elevation of Transmural Pressure. Am. J. Physiol. 22: F778–81.Google Scholar
  53. 53.
    Hill MA, Zou H, Davis MJ, Potocnik SJ, Price S (2000) Transient Increases in Diameter and [Cap’]; Are not Obligatory for Myogenic Constriction. Am. J. Physiol. 278: H345–52.Google Scholar
  54. 54.
    Hirata K, Kikuchi A, Sasaki T, Kuroda S, Kaibuchi K, Matsuura Y, Seki H, Saida K, Taakai Y (1992) Involvement of rho p21 in the GTP-enhanced Calcium Ion Sensitivity of Smooth Muscle Contraction. J. Biol. Chem. 267: 8719–22.Google Scholar
  55. 55.
    Horowitz A, Menice CB, Laporte R, Morgan KG (1996a) Mechanisms of Smooth Muscle Contraction. Physiol. Rev. 76 (4): 967–1003.PubMedGoogle Scholar
  56. 56.
    Horowitz A, Chomienne O, Walsh MP, Morgan KG (1996b) Isoenzyme of Protein Kinase C Induces a Ca’-independent Contraction in Vascular Smooth Muscle. Am. J. Physiol. 217 (Cell Physiol. 40): C589–94.Google Scholar
  57. 57.
    Hosang M, Rouge M, Wipf B, Eggimann B, Kaufmann F, Hunziker W (1989) Both Homodimeric Isoforms of PDGF (AA and BB) Have Mitogenic and Chemotactic Activity and Stimulate Phosphoinositol Turnover. J. Cell Physiol. 140: 558–64.Google Scholar
  58. 58.
    Hu Y, Bock G, Wick G, Xu Q (1998). Activation of PDGF Receptor a in Vascular Smooth Muscle Cells by Mechanical Stress. FASEB J. 12: 1135–42.PubMedGoogle Scholar
  59. 59.
    Huang Y, Runschitzki D, Chien S, Weinbaum S (1997) A Fiber Matrix Model for the Filtration through Fenestral Pores in a Compressible Arterial Intima. Am. J. Physiol. 272: H2023–39.PubMedGoogle Scholar
  60. 60.
    Huang Y, Runschitzki D, Chien S, Weinbaum S (1994) A Fiber Matrix Model for the Growth of Macromolecular Leakage Spots in the Arterial Initima. J. Biomech. Eng. 116: 430–45.Google Scholar
  61. 61.
    Huang Y, Jan KM, Runschitzki D, Weinbaum S (1998) Structural Changes in Rat Aortic Intima due to Transmural Pressure. Trans. ASME J. Biomech. Eng. 1220: 476–83.Google Scholar
  62. 62.
    Hull SS, Kaiser L, Jaffe MD, Sparks HV (1986) Endothelial-dependent Flow-induced Dilation of Canine Femoral and Saphenous Arteries. Blood Vessels. 23: 183–98.PubMedGoogle Scholar
  63. 63.
    Hume WR (1980) Proline and Thymidine Uptake in Rabbit Ear Artery Segments in vitro Increased by Chronic Tangential Load. Hypertension. 2: 738–43.PubMedCrossRefGoogle Scholar
  64. 64.
    Itoh H, Lederis K (1987) Contraction of Rat Thoracic Aorta Strips Induced by Phorbol 12-myristate 13-acetate. Am. J. Physiol. 252 (2 Pt 1): C244–7.PubMedGoogle Scholar
  65. 65.
    Jiang MJ, Morgan KG (1987) Intracellular Calcium Levels in Phorbol Ester-induced Contractions of Vascular Muscle. Am. J. Physiol. 253 (6 Pt 2): H1365–71.PubMedGoogle Scholar
  66. 66.
    Jiang MJ, Morgan KG (1989) Agonist-specific Myosin Phosphorylation and Intracellular Calcium During Isometric Contractions of Smooth Muscle. Pfluegers Arch. 413: 637–43.CrossRefGoogle Scholar
  67. 67.
    Kanda K, Matsuda T (1994) Mechanical Stress-induced Orientation and Ultrastructural Change of Smooth Muscle Cells in Three-dimensional Collagen Lattices. Cell Transplant. 3: 481–92.PubMedGoogle Scholar
  68. 68.
    Kohler TR, Jawien A (1992) Flow Affects Development of Intimal Hyperplasia after Arterial Injury in Rats. Arteriosclerosis and Thrombosis. 12: 963–71.PubMedCrossRefGoogle Scholar
  69. 69.
    Kohler TR, Kirkman TR, Kraiss LW, Zierler BK, Clowes AW (1991) Increased Blood Flow Inhibits Neointimal Hyperplasia in Endothelialized Vascular Grafts. Circ. Res. 69: 1557–65.Google Scholar
  70. 70.
    Koyama N, Morisaki N, Saito Y, Yoshida S (1992) Regulatory Effects of Platelet-derived Growth Factor-AA Homodimer on Migration of Vascular Smooth Muscle Cells. J. Biol. Chem. 267: 2280612.Google Scholar
  71. 71.
    Koyama N, Hart CE, Clowes AW (1994) Different Functions of the Platelet-derived Growth Factor-a and -13 receptors for the Migration and Proliferation of Cultured Baboon Smooth Muscle Cells. Circ. Res. 75: 682–91.Google Scholar
  72. 72.
    Koyama J, Owa M, Sakurai S, Shimada H, Hikita H, Higashikata T, Ikeda S (2000) Relation between Vascular Morphologic Changes During Stent Implantation and the Magnitude of In-stent Neointimal Hyperplasia. Am. J. Cardiol. 86: 753–8.Google Scholar
  73. 73.
    Kraiss LW, Kirkman TR, Kohler TR, Zierler BK, Clowes AW (1991) Shear Stress Regulates Smooth Muscle Proliferation and Neointimal Thickening in Porous Polytetrafluoroethylene Grafts. Arteriosclerosis and Thrombosis. 11: 1844–52.PubMedCrossRefGoogle Scholar
  74. 74.
    Ku DN, Giddens DP, Zarins CK, Golagov S (1985) Pulsatile Flow and Atherosclerosis in the Human Carotid Bifurcation: Positive Correlation between Plaque Location and Low and Oscillating Shear Stress. Arteriosclerosis. 5: 293–302.Google Scholar
  75. 75.
    Kuo L, Arko F, Chilian WM, Davis MJ (1993) Coronary Venular Responses to Flow and Pressure. Circ. Res. 72: 607–15.Google Scholar
  76. 76.
    Lahteenmaki T, Sievi E, Vapaatalo H (1998) Inhibitory Effects of Mesoionic 3-aryl Substituted Oxatriazole-5-imine Derivatives on Vascular Smooth Muscle Cell Mitogenesis and Proliferation in vitro. Br. J. Pharmacol. 125: 402–8.Google Scholar
  77. 77.
    Lakshminarayanan D, Gardner T, Tarbell JM (2000a) Effect of Shear Stress on the Hydraulic Conductivity of Cultured Bovine Retinal Microvascular Endothelial Cell Monolayers. Curr. Eye Res. 21: 944–51.Google Scholar
  78. 78.
    Lakshminarayanan S, Antonetti D, Gardner T, Tarbell JM (2000b) Effect of VEGF on Hydraulic Conductivity of Retinal Microvascular Endothelial Monolayers - the Role of NO. Invest. Ophth. Vis. Sci. 41: 4256–61.Google Scholar
  79. 79.
    Larson RE, Higdon JJL (1987) Microscopic Flow Near the Surface of Two-dimensional Porous Media. Part 2: Transverse Flow. J. Fluid Mech. 178: 119–25.Google Scholar
  80. 80.
    Lee CS, Tarbell JM (1998) Influence of Vasoactive Drugs on Wall Shear Stress Distribution in the Abdominal Aortic Bifurcation: an in vitro Study. Ann. Biomed. Eng. 26: 200–12.Google Scholar
  81. 81.
    Lee S, Schmid-Schönbein GW (1996) Biomechanical Model for the Myogenic Response in the Microcirculation. J. Biomech. Eng. 118: 145–57.Google Scholar
  82. 82.
    Lever MJ, Tarbell JM, Caro CG (1992) The Effect of Luminal Flow in the Carotid Artery on Transmural Fluid Transport. Experimental Physiology. 77: 553–63.PubMedGoogle Scholar
  83. 83.
    Leung DYM, Glagov S, Mathews MB (1976) Cyclic Stretching Stimulates Synthesis of Matrix Components by Arterial Smooth Muscle Cells in vitro. Science. 191: 475–7.PubMedCrossRefGoogle Scholar
  84. 84.
    Lipowsky H (1995) Shear Stress in the Circulation. In: Flow Dependent Regulation of Vascular Function. Eds. Koller C, Kaley G, New York, Oxford University Press, 28–45.Google Scholar
  85. 85.
    Liu SQ (1998) Influence of Tensile Strain on Smooth Muscle Cell Orientation in Rat Blood Vessels. J. Biomech. Eng. 120: 313–20.PubMedCrossRefGoogle Scholar
  86. 86.
    Ma YH, Ling S, Ives HE (1999) Mechanical Strain Increases PDGF-band and PDGF-ß Receptor Expression in Vascular Smooth Muscle Cells. Biochem. Biophys. Res. Commun. 265: 606–10.Google Scholar
  87. 87.
    MacLeod DC, Strauss BH, DeJong M, Escaned J, Umans VA, v. Suylen R, Verkerk A, de Feyter PJ, Serruys PW (1994) Proliferation and Extracellular Matrix Synthesis of Smooth Muscle Cells Cultured from Human Coronary Atherosclerotic and Restenotic Lesions. J. Am. Coll. Cardiol. 23: 59–65.PubMedCrossRefGoogle Scholar
  88. 88.
    Marano G, Palazzesi S, Vergari A, Ferrari AU (1999) Protection by Shear Stress from Collar-induced Intimal Thickening: Role of Nitric Oxide. Arterioscler. Thromb. Vasc. Biol. 19: 2609–14.Google Scholar
  89. 89.
    Matsumoto T, Hayashi K (1994) Mechanical and Dimensional Adaptation of Rat Aorta to Hypertension. J. Biomech. Eng. 116: 278–83.Google Scholar
  90. 90.
    Mattsson EJR, Kohler TR, Vergel SM, Clowes AW (1997) Increased Blood Flow Induces Regression of Intimal Hyperplasia. Arterioscler. Thromb. Vasc. Biol. 17: 2245–9.Google Scholar
  91. 91.
    McNamara CA, Sarembock IJ, Bachuber BG (1996) Thrombin and Vascular Smooth Muscle Cell Proliferation: Implications for Atherosclerosis and Restonosis. Semin. Thromb. Haemost. 22: 13944.Google Scholar
  92. 92.
    Meguro T, Nakashima H, Kawada S, Tokunaga K, Ohmoto T (2000) Effect of External Stenting and Systemic Hypertension or Intimal Hyperplasia in Rat Vein Grafts. Neurosurgery. 46: 963–9.PubMedGoogle Scholar
  93. 93.
    Meininger GA, Davis MJ (1992) Cellular Mechanisms Involved in the Vascular Myogenic Response. Am. J. Physiol. 263: H647–59.PubMedGoogle Scholar
  94. 94.
    Michel CC, Curry FE (1999) Microvascular Permeability. Physiol. Revs. 79: 703–61.Google Scholar
  95. 95.
    Milnor WR (1989) Hemodynamics, Baltimore, Williams and Wilkins.Google Scholar
  96. 96.
    Mooradian DL, Hutsell TC, Keefer LK (1995) Nitric Oxide (NO) Donor Molecules: Effect of NO Release Rate of Vascular Smooth Muscle Cell Proliferation in vitro. J. Cardiovasc. Pharmacol. 25: 674–8.Google Scholar
  97. 97.
    Moore JA, Ethier CR (1997) Oxygen Mass Transfer Calculations in Large Arteries. J. Biomech. Eng. 119: 469–75.Google Scholar
  98. 98.
    Mulvany MJ (1992) Vascular Growth in Hypertension. J. Cardiovasc. Pharmacol. 20 (Supp1.1): S7-SI i.Google Scholar
  99. 99.
    Mulvany MJ, Baumbach GL, Aalkjaer C, Heagerty AM, Korsgaardm N, Schiffrin EL, Heistad DD (1996) Vascular Remodelling. Hypertension. 28: 505–6.PubMedGoogle Scholar
  100. 100.
    Murray TR, Marshall BE, Macarak EJ (1990) Contraction of Vascular Smooth Muscle in Culture. J. Cell. Physiol. 143: 26–38.Google Scholar
  101. 101.
    Myers JG, Moore JA, Ojha M, Johnston KW, Ethier CR (2001) Factors Influencing Blood Flow Patterns in the Human Right Coronary Artery. Ann. Biomed. Eng. 29: 109–20.Google Scholar
  102. 102.
    Osol G (1995) Mechanotransduction by Smooth Muscle. J. Vasc. Res. 32: 275–92.PubMedGoogle Scholar
  103. 103.
    Owen N (1985) Prostacyclin Can Inhibit DNA Synthesis in Vascular Smooth Muscle Cells. In: Prostaglandins, Kukotrienes, and Lipoxins: Biochemistry, Mechanisms of Action, and Clinical Applications, edited by J. Bailey. New York, Plenum Press.Google Scholar
  104. 104.
    Owens GK (1996) Regulation of Differentiation of Vascular Smooth Muscle Cells. Physiol. Rev. 75 (3): 487–517.Google Scholar
  105. 105.
    Palumbo R, Gaetano C, Melillo G, Toschi E, Remuzzi A, Capogrossi MC (2000) Shear Stress Downregulation of Platelet-derived Growth Factor-B and Matrix Metalloprotease-2 Is Associated with Inhibition of Smooth Muscle Cell Invasion and Migration. Circulation. 102: 225–30.PubMedCrossRefGoogle Scholar
  106. 106.
    Papadaki M, Eskin SG, Ruef J, Runge MS, McIntire LV (1999) Fluid Shear Stress as a Regulator of Gene Expression in Vascular Cells: Possible Correlations with Diabetic Abnormalities. Diab. Res. and Clin. Practice. 45: 89–99.Google Scholar
  107. 107.
    Papadaki M, Ruef J, Nguyen KT, Li F, Patterson C, Eskin SG, McIntire LV, Runge MS (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
  108. 108.
    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 (Heart Circ. Physiol, 43): H616–26.PubMedGoogle Scholar
  109. 109.
    Papadaki M, McIntire LV, Eskin SG (1996) Effects of Shear Stress on the Growth Kinetics of Human Aortic Smooth Muscle Cells in vitro. Biotech. Bioeng. 50: 555–61.Google Scholar
  110. 110.
    Pares-Herbute N, Fliche E, Monnier L (1999) Involvement of Nitric Oxide in the Inhibition of Aortic Smooth Muscle Cell Proliferation by Calcium Dobesilate. Int. J. Angiol. 8: 5–10.Google Scholar
  111. 111.
    Parker JC, Ivey CL (1997) Isoproterenol Attenuates High Vascular Pressure-induced Permeability Increases in Isolated Rat Lungs. J. Appl. Physiol. 83: 1962–7.Google Scholar
  112. 112.
    Pohl U, Herlan K, Huang A, Bassenge E (1991) EDRT-mediated Shear-induced Dilation Opposes Myogenic Vasoconstriction in Small Rabbit Arteries. Am. J. Physiol. 261: H2016–23.PubMedGoogle Scholar
  113. 113.
    Pohl U, Holtz J, Busse R, Bassenge E (1986) Crucial Role of Endothelium in the Vasodilator Response to Increased Flow in vivo. Hypertension. 8: 37–44.PubMedCrossRefGoogle Scholar
  114. 114.
    Powell JT, Gosling M (1998) Molecular and Cellular Changes in Vein Grafts: Influence of Pulsatile Stretch. Curr. Opin. Cardiol. 13: 453–8.Google Scholar
  115. 115.
    Predel H, von Segesser L, Bühler FR, Yang Z, Turina M, Löscher TF (1992) Implications of Pulsatile Stretch on Growth of Saphenous Vein and Mammary Artery Smooth Muscle. Lancet. 340: 878–9.PubMedCrossRefGoogle Scholar
  116. 116.
    Pries AR, Secomb TW (2000) Microcirculatory Network Structures and Models. Ann. Biomed. Eng. 28: 916–21.Google Scholar
  117. 117.
    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
  118. 118.
    Rappitsch G, Perktold K (1996) Computer Simulation of Convective Diffusion Processes in Large Arteries. J. Biomechanics. 29: 207.CrossRefGoogle Scholar
  119. 119.
    Rasmussen H, Foder J, Kolima I, Scriabine A (1984) TPA-induced Contraction of Isolated Rabbit Vascular Smooth Muscle. Biochem. Biophys. Res. Commun. 122: 776–84.Google Scholar
  120. 120.
    Reddy KB, Howe PH (1993) Transforming Growth Factor Beta 1-mediated Inhibition of Smooth Muscle Cell Proliferation Is Associated with a Late GI Cell Cycle Arrest. J. Cell. Physiol. 156: 48–55.Google Scholar
  121. 121.
    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
  122. 122.
    Roach MR, Song SH (1988) Arterial Elastin as Seen with Scanning Electron Microscopy. Scanning Microscopy. 2: 993–1004.Google Scholar
  123. 123.
    Rosati C, Garay R (1991) Flow-dependent Stimulation of Sodium and Cholesterol Uptake and Cell Growth in Cultured Vascular Smooth Muscle. J. Hypertension. 9: 1029–33.CrossRefGoogle Scholar
  124. 124.
    Sakamoto H, Nozaki S, Misumi K, Kurose M, Sohara H, Amitani S, Miyahara K (1996) Smooth Muscle Cell Proliferation in the Arterial Intima after Stretch Injury. Exp. Anim. 45: 89–93.Google Scholar
  125. 125.
    Saltis J, Agrotis A, Kanellakis P, Bobik A (1994) Developmentally Regulated Transforming Growth Factor-beta 1 Action on Vascular Smooth Muscle Cell Growth in the SHR. Clin. Exp. Pharmacol. Physiol. 21: 149–52.Google Scholar
  126. 126.
    Sarkar R, Gordon D, Stanley JC, Webb RC (1997) Dual Cell-cycle Specific Mechanisms Mediate the Antimitogenic Effects of Nitric Oxide in Vascular Smooth Muscle Cells. J. Hypertens. 15: 275–83.PubMedCrossRefGoogle Scholar
  127. 127.
    Schwartz RS (1993) Coronary Restenosis. Blackwell Scientific, Cambridge, MA.Google Scholar
  128. 128.
    Secomb TW, Hsu R, Pries AR (1998) A Model for Red Blood Cell Motion in Glycocalyx-lined Capillaries. Am. J. Physiol. 274: H1016–22.PubMedGoogle Scholar
  129. 129.
    Seki J, Nishio M, Kato Y, Motoyama Y, Yoshida K (1995) FK409, a New Nitric-oxide Donor, Suppresses Smooth Muscle Cell Proliferation in the Rat Model of Balloon Angioplasty. Atherosclerosis. 117: 97–106.Google Scholar
  130. 130.
    Sharma R, Yellowley C, Ainslie K, Civelek M, Hodgson L, Tarbell JM, Donahue HJ Intracellular Calcium Changes in Rat Aortic Smooth Muscle Cells in Response to Fluid Flow. Ann. Biomed. Eng. 30: 371–8.Google Scholar
  131. 131.
    Shigematsu K, Yasuhara H, Shigematsu H, Muto T (2000) Direct and Indirect Effects of Pulsatile Shear Stress on the Smooth Muscle Cell. Int. Angiol. 19: 39–46.Google Scholar
  132. 132.
    Sill HW, Chang YS, Artman JR, Frangos JA, Hollis TM, Tarbell JM (1995) Shear Stress Increases Hydraulic Conductivity of Cultured Endothelial Monolayers. Am. J. Physiol. 268: H535–43.PubMedGoogle Scholar
  133. 133.
    Simionescu M, Simionescu N (1984) Ultrastructure of the Microvascular Wall: Functional Correlations. In: Handbook of Physiology, edited by EM Renkin and CC Michel. Washington, D.C.: American Physiological Society, pp. 41–101.Google Scholar
  134. 134.
    Singer HA, Baker KM (1987) Calcium Dependence of Phorbol 12,13-dibutyrate-induced Force and Myosin Light Chain Phosphorylation in Arterial Smooth Muscle. J. Pharmacol. Exp. Ther. 243 (3): 814–21.PubMedGoogle Scholar
  135. 135.
    Sipkema P, Westerhoff N, Hoogerwerf N (1997) Rate of the Myogenic Response Increases with the Constriction Level in Rabbit Femoral Arteries. Ann. Biomed. Eng. 25: 278–85.Google Scholar
  136. 136.
    Somlyo AP, Somlyo AV (1994) Signal Transduction and Regulation in Smooth Muscle. Nature. 372: 231–6.PubMedCrossRefGoogle Scholar
  137. 137.
    Song RH, Kocharyan HK, Fortunato JE, Glagov S, Bassiouny HS (2000) Increased Flow and Shear Stress Enhance Transforming Growth Factor-(31 after Experimental Arterial Injury. Arterioscler. Thromb. Vasc. Biol. 20: 923–30.Google Scholar
  138. 138.
    Sterpetti AV, Cucina A, Fragale A, Leipidi S, Cavallaro A, Santaro-D’Angelo L (1994) Shear Stress Influences 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
  139. 139.
    Sterpetti AV, Cucina A, D’Angelo LS, Cardillo B, Cavallaro A (1992a) Response of Arterial Smooth Muscle Cells to Laminar Flow. J. Cardiovasc. Surg. 33: 619–24.Google Scholar
  140. 140.
    Sterpetti AV, Cucina A, Santaro L, Cardillo B, Cavallaro A (1992b) Modulation of Arterial Smooth Muscle Cell Growth by Haemodynamic Forces. Eur. J. Vasc. Surg. 6 (1): 16–20.PubMedCrossRefGoogle Scholar
  141. 141.
    Sumpio BE, Banes AJ (1988a) Response of Porcine Aortic Smooth Muscle Cells to Cyclic Tensional Deformation in Culture. J. Surg. Res. 44: 696–701.Google Scholar
  142. 142.
    Sumpio BE, Banes AJ, Link WG, Johnson G (1988b) Enhanced Collagen Production by Smooth Muscle Cells During Repetitive Mechanical Stretching. Arch. Surg. 123: 1233–6.Google Scholar
  143. 143.
    Sybertz EJ, Desiderio DM, Tetzloff G, Chiu PJ (1986) Phorbol Bibutyrate Contractions in Rabbit Aorta: Calcium Dependence and Sensitivity to Nitrovasodilators and 8-BR-cyclic GMP. J. Pharmacol. Exp. Ter. 239 (1): 78–83.Google Scholar
  144. 144.
    Tada S, Tarbell JM (2000) Interstitial Flow Through the Internal Elastic Lamina Affects Shear Stress on Smooth Muscle Cells in the Artery Wall. Am. J. Physiol. 278: H1589–97.Google Scholar
  145. 145.
    Tada S, Tarbell JM. Fenestral Pore Size in the Internal Elastic Lamina Affects Transmural Flow Distribution in the Artery Wall. Ann. Biomed. Eng. in press.Google Scholar
  146. 146.
    Tagami M, Nara Y, Kubota A, Sunaga T, Maezawa H, Fujino H, Yamori Y (1986) Morphological and Functional Differentiation of Cultured Vascular Smooth Muscle Cells. Cell and Tiss. Res. 245: 2616.Google Scholar
  147. 147.
    Tarbell JM, Chang LJ, Hollis TM (1982) A Note on Wall Shear Stress in the Aorta. J. Biomech. Eng. 104: 343–6.Google Scholar
  148. 148.
    Tarbell JM, DeMaio L, Zaw MM (1999) Effect of Pressure on Hydraulic Conductivity of Endothelial Monolayers: The Role of Endothelial Cleft Shear Stress. J. Appl. Physiol. 87: 261–8.Google Scholar
  149. 149.
    Tedgui A, Lever MJ (1984) Filtration Through Damaged and Undamaged Rabbit Thoracic Aorta. Am. J. Physiol. 247: H784–91.PubMedGoogle Scholar
  150. 150.
    Thorin-Trescases N, Bevan JA (1998) High Levels of Myogenic Tone Antagonize the Dilator Response to Flow of Small Rabbit Arterial Cerebral Arteries. Stroke. 29: 1194–201.PubMedCrossRefGoogle Scholar
  151. 151.
    Ueba H, Kawakami M, Yaginuma T (1997) Shear Stress as an Inhibitor of Vascular Smooth Muscle Cell Proliferation: Role of Transforming Growth Factor-131 and Tissue-type Plasminogen Activator. Arterioscler. Thromb. Vasc. Biol. 17: 1512–6.Google Scholar
  152. 152.
    Wagner CT, Durante W, Christodoulides N, Hellium JD, Schafer AI (1997) Hemodynamic Forces Induce the Expression of Heme Oxygenase in Cultured Vascular Smooth Muscle Cells. J. Clin. Invest. 100 (3): 589–96.PubMedCrossRefGoogle Scholar
  153. 153.
    Walsh PM, Andrea JE, Allen BG, Clement-Chomienne O, Collins EM, Morgan KG (1994) Smooth Muscle Protein Kinase C. Can. J. Physiol. Pharmacol. 72: 1392–9.Google Scholar
  154. 154.
    Wang DM, Tarbell JM (2000). Effect of Fluid Flow on Smooth Muscle Cells in a 3-dimensional Collagen Gel Model. Arterioscler. Thromb. Vast. Biol. 20 (10): 2220–5.CrossRefGoogle Scholar
  155. 155.
    Wang DM, Tarbell JM (1995) Modeling Interstitial Flow Through Arterial Media. J. Biomech. Eng. 117: 358–63.Google Scholar
  156. 156.
    Watase M, Awolesi MA, Ricotta J, Sumpio BE (1997) Effect of Pressure on Cultured Smooth Muscle Cells. Life Sciences. 61: 987–96.PubMedCrossRefGoogle Scholar
  157. 157.
    Wilson E, Mai Q, Sudhir K, Weiss RH, Ives HE (1993) Mechanical Strain Induces Growth of Vascular Smooth Muscle Cells via Autocrine Action of PDGF. J. Cell. Biol. 123: 741–7.Google Scholar
  158. 158.
    Williams D (1999) Network Assessment of Capillary Hydraulic Conductivity after Abrupt Changes in Fluid Shear Stress. Microvascular Res. 57: 107–17.CrossRefGoogle Scholar
  159. 159.
    Yamamoto C, Kaji T, Sakamoto M, Kozuka H (1996) Effects of Cadmium on the Release of Tissue Plasminogen Activator and Plasminogen Activator Inhibitor Type 1 from Cultured Human Vascular Smooth Muscle Cells and Fibroblasts. Toxicology. 106 (1–3): 179–85.PubMedCrossRefGoogle Scholar
  160. 160.
    Yang Z, Noll G, Löscher TF (1993) Calcium Antagonists Differently Inhibit Proliferation of Human Coronary Smooth Muscle Cells in Response to Pulsatile Stretch and Platelet-derived Growth Factor. Circulation. 88: 832–6.PubMedCrossRefGoogle Scholar
  161. 161.
    Yuan F, Chien S, Weinbaum S (1991) A New View of Convective-diffusive Transport Processes in the Arterial Intima. Trans. ASME J. Biomech. Eng. 113: 314–29.CrossRefGoogle Scholar
  162. 162.
    Zhuang YJ, Singh TM, Zarins CK, Masuda H (1998) Sequential Increases and Decreases in Blood Flow Stimulates Progressive Intimai Thickening. Eur. J. Vasc. Endovasc. Surg. 16: 301–10.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag France 2003

Authors and Affiliations

  • John M. Tarbell
    • 1
  • Mete Civelek
    • 1
  • Jeff S. Garanich
    • 1
  1. 1.Departments of Chemical Engineering and BioengineeringThe Pennsylvania State UniversityUSA

Personalised recommendations