Interaction between Wall Shear Stress and Circumferential Strain Affects Endothelial Cell Biochemical Production

The wall shear stress (WSS) of flowing blood and the circumferential strain (CS) driven by the pressure pulse interact to impose a dynamic force pattern on endothelial cells (ECs) which can be characterized by the temporal phase angle between WSS and CS, a quantity which varies significantly throughout the circulation. To study the interaction of WSS and CS on endothelial production of vasodilators (prostacyclin and nitric oxide) and a vasoconstrictor (endothelin-1), bovine aortic ECs were cultured on the inner surface of compliant tubes and subjected to various flow conditions: steady shear (10 dyn/cm2), oscillatory shear (10 ± 10 dyn/cm2, rigid tube), and oscillatory shear (10 ± 10 dyn/cm2) with CS (8%) either in or out of phase with shear. The 4-hour production rates of vasoactive agents show that steady shear stimulates the highest production of vasodilators whereas oscillatory shear stimulates the highest vasoconstrictor production. The addition of CS in concert with oscillatory shear enhances the production of vasodilators and inhibits the production of vasoconstrictors, and this effect is modulated by the phase angle between WSS and CS. These data suggest that the interactions of WSS and CS are important in vascular regulation and remodeling.

[1]  J. Tarbell,et al.  A study of the wall shear rate distribution near the end-to-end anastomosis of a rigid graft and a compliant artery. , 1994, Journal of biomechanics.

[2]  W. Sessa,et al.  Cyclic strain upregulates nitric oxide synthase in cultured bovine aortic endothelial cells. , 1995, The Journal of clinical investigation.

[3]  J. M. Tarbell,et al.  Nonlinear analysis of flow in an elastic tube (artery): steady streaming effects , 1992, Journal of Fluid Mechanics.

[4]  D. L. Wang,et al.  Cyclic strain enhances adhesion of monocytes to endothelial cells by increasing intercellular adhesion molecule-1 expression. , 1996, Hypertension.

[5]  J. Tarbell,et al.  Endothelial albumin permeability is shear dependent, time dependent, and reversible. , 1991, The American journal of physiology.

[6]  R M Nerem,et al.  Pulsatile and steady flow-induced calcium oscillations in single cultured endothelial cells. , 1996, Journal of vascular research.

[7]  Herbert H. Lipowsky,et al.  Shear Stress in the Circulation , 1995 .

[8]  N. E. Owen.  Prostacyclin Can Inhibit DNA Synthesis in Vascular Smooth Muscle Cells , 1985 .

[9]  D. L. Fry.  Acute Vascular Endothelial Changes Associated with Increased Blood Velocity Gradients , 1968, Circulation research.

[10]  J. Tarbell,et al.  Numerical simulation of pulsatile flow in a compliant curved tube model of a coronary artery. , 2000, Journal of biomechanical engineering.

[11]  D. Ku,et al.  Pulsatile Flow and Atherosclerosis in the Human Carotid Bifurcation: Positive Correlation between Plaque Location and Low and Oscillating Shear Stress , 1985, Arteriosclerosis.

[12]  G. L’italien,et al.  A compliant tubular device to study the influences of wall strain and fluid shear stress on cells of the vascular wall. , 1994, Journal of vascular surgery.

[13]  M. Kuchan,et al.  Shear stress regulates endothelin-1 release via protein kinase C and cGMP in cultured endothelial cells. , 1993, The American journal of physiology.

[14]  K J Gooch,et al.  Exogenous, basal, and flow‐induced nitric oxide production and endothelial cell proliferation , 1997, Journal of cellular physiology.

[15]  L V McIntire,et al.  Flow effects on prostacyclin production by cultured human endothelial cells. , 1985, Science.

[16]  J A Frangos,et al.  Shear stress increases hydraulic conductivity of cultured endothelial monolayers. , 1995, The American journal of physiology.

[17]  Y. Yazaki,et al.  Hemodynamic shear stress stimulates endothelin production by cultured endothelial cells. , 1989, Biochemical and biophysical research communications.

[18]  P. Davies,et al.  Flow-mediated endothelial mechanotransduction. , 1995, Physiological reviews.

[19]  D. Hayoz,et al.  Influence of oscillatory and unidirectional flow environments on the expression of endothelin and nitric oxide synthase in cultured endothelial cells. , 1998, Arteriosclerosis, thrombosis, and vascular biology.

[20]  J. Tarbell,et al.  Computational simulation of flow in the end-to-end anastomosis of a rigid graft and a compliant artery. , 1996, ASAIO journal.

[21]  D. J. Patel,et al.  Longitudinal Tethering of Arteries in Dogs , 1966, Circulation research.

[22]  D. L. Wang,et al.  Cyclic strain-induced plasminogen activator inhibitor-1 (PAI-1) release from endothelial cells involves reactive oxygen species. , 1996, Biochemical and biophysical research communications.

[23]  J. Womersley.  Method for the calculation of velocity, rate of flow and viscous drag in arteries when the pressure gradient is known , 1955, The Journal of physiology.

[24]  John A. Frangos,et al.  Physical forces and the mammalian cell , 1993 .

[25]  E. Jaffe,et al.  Prostacyclin production by cultured endothelial cell monolayers exposed to step increases in shear stress. , 1985, The Journal of laboratory and clinical medicine.

[26]  Albert J. Banes,et al.  CHAPTER 3 – Mechanical Strain and the Mammalian Cell , 1993 .

[27]  W E Walker,et al.  Input Impedance of the Systemic Circulation in Man , 1977, Circulation research.

[28]  C. Tang,et al.  Cyclical strain increases endothelin-1 secretion and gene expression in human endothelial cells. , 1993, Biochemical and biophysical research communications.

[29]  J. Tarbell,et al.  Nonlinear analysis of oscillatory flow, with a nonzero mean, in an elastic tube (artery). , 1995, Journal of biomechanical engineering.

[30]  G. Remuzzi,et al.  Nitric oxide synthesis by cultured endothelial cells is modulated by flow conditions. , 1995, Circulation research.

[31]  J. Frangos,et al.  CHAPTER 5 – Effects of Flow on Anchorage-Dependent Mammalian Cells—Secreted Products , 1993 .

[32]  M. Kuchan,et al.  Role of calcium and calmodulin in flow-induced nitric oxide production in endothelial cells. , 1994, The American journal of physiology.

[33]  R. Schroter,et al.  Atheroma and arterial wall shear - Observation, correlation and proposal of a shear dependent mass transfer mechanism for atherogenesis , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[34]  J. Tarbell,et al.  Wall shear rate distribution in an abdominal aortic bifurcation model: effects of vessel compliance and phase angle between pressure and flow waveforms. , 1997, Journal of biomechanical engineering.

[35]  P. Dobrin,et al.  Mechanical properties of arteries , 1978, Physiological reviews.

[36]  L V McIntire,et al.  Cyclical strain effects on production of vasoactive materials in cultured endothelial cells , 1992, Journal of cellular physiology.

[37]  S. Izumo,et al.  Physiological fluid shear stress causes downregulation of endothelin-1 mRNA in bovine aortic endothelium. , 1992, The American journal of physiology.