Shear stress regulates angiotensin type 1 receptor expression in endothelial cells

Circ Res. 2009 Oct 23;105(9):869-75. doi: 10.1161/CIRCRESAHA.109.204040. Epub 2009 Sep 17.

Abstract

Rationale: Shear stress (SS) has an established role in atherosclerotic plaque localization, but how it exerts its protective effect is not fully understood.

Objective: To test the hypothesis that SS may downregulate angiotensin type 1 receptors (AT(1)Rs). Angiotensin II has been shown to be proinflammatory and to promote atherosclerosis.

Methods and results: Using immunohistochemistry, we found a pronounced expression of AT(1)R in the inner, atheroprone regions of the aortic arch of C57BL/6 and endothelial NO synthase-deficient (eNOS(-/-)) mice but not eNOS-overexpressing mice. In human umbilical vein endothelial cells (HUVECs), laminar SS (15 dyn/cm(2)) induced a biphasic decrease in AT(1)R protein expression characterized by a first reduction at 1 hour (31+/-4% of static control, P<0.01), partial recovery at 3 hours (65+/-9%), and a second more prolonged decline at 6, 12, and 24 hours (48+/-9%, 36+/-9%, 33+/-5%, respectively, P<0.05). One and 24 hours of SS significantly reduced fluorescent angiotensin binding compared to static HUVECs. Shear-induced downregulation of AT(1)R was abolished by treatment with protein kinase A and G inhibitors or N(G)-nitro-l-arginine methyl ester (L-NAME). Fittingly, stimulating static HUVECs with an NO donor decreased AT(1)R protein levels. RT-PCR revealed a significant (P<0.05) decrease of AT(1)R mRNA in HUVECs exposed to SS during 3 (6+/-2% of static control), 6 (4+/-1%), 12 (4+/-1%), and 24 hours (15+/-4%), suggesting a transcriptional downregulation of AT(1)R at length. Finally, angiotensin-induced vascular cell adhesion molecule was abated in HUVECs exposed to SS and in the outer aortic arch of mice.

Conclusions: Our results demonstrate that SS may convey some of its atheroprotective effects through downregulation of AT(1)R in endothelial cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / administration & dosage
  • Angiotensin II / metabolism
  • Animals
  • Atherosclerosis / metabolism*
  • Atherosclerosis / physiopathology
  • Atherosclerosis / prevention & control
  • Cells, Cultured
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Cyclic GMP-Dependent Protein Kinases / metabolism
  • Disease Models, Animal
  • Down-Regulation
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism*
  • Humans
  • Inflammation / metabolism
  • Inflammation / physiopathology
  • Inflammation / prevention & control
  • Injections, Intravenous
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Nitric Oxide / metabolism
  • Nitric Oxide Donors / pharmacology
  • Nitric Oxide Synthase Type III / deficiency
  • Nitric Oxide Synthase Type III / genetics
  • Nitric Oxide Synthase Type III / metabolism
  • Protein Kinase Inhibitors / pharmacology
  • Pulsatile Flow
  • RNA, Messenger / metabolism
  • Receptor, Angiotensin, Type 1 / genetics
  • Receptor, Angiotensin, Type 1 / metabolism*
  • Regional Blood Flow
  • Signal Transduction
  • Stress, Mechanical
  • Time Factors
  • Vascular Cell Adhesion Molecule-1 / metabolism

Substances

  • Nitric Oxide Donors
  • Protein Kinase Inhibitors
  • RNA, Messenger
  • Receptor, Angiotensin, Type 1
  • Vascular Cell Adhesion Molecule-1
  • Angiotensin II
  • Nitric Oxide
  • NOS3 protein, human
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse
  • Cyclic AMP-Dependent Protein Kinases
  • Cyclic GMP-Dependent Protein Kinases