Integrin-substrate interactions underlying shear-induced inhibition of the inflammatory response of endothelial cells

Thromb Haemost. 2013 Feb;109(2):298-308. doi: 10.1160/TH12-06-0400. Epub 2012 Dec 13.

Abstract

Conditioning of endothelial cells by shear stress suppresses their response to inflammatory cytokines. We questioned whether signalling through different integrin-matrix interactions, previously associated with the pathogenic effects of disturbed flow, supported the anti-inflammatory action of steady shear. Primary human endothelial cells were cultured on different substrates and exposed to shear stress (2.0Pa) for varying periods before stimulation with tumour necrosis factor-α (TNF). Shear-conditioning inhibited cytokine-induced recruitment of flowing neutrophils. However, the effect was similar for culture on collagen, laminin or fibronectin, even when seeding was reduced to 2 hours, and shear to 3 hours before TNF treatment (to minimise deposition of endothelial matrix). Nevertheless, in short- or longer-term cultures, reduction in expression of β(1)-integrin (but not β(3)-integrin) using siRNA essentially ablated the effect of shear-conditioning on neutrophil recruitment. Studies of focal adhesion kinase (FAK) phosphorylation, siRNA against FAK and a FAK-inhibitor (PF573228) indicated that FAK activity was an essential component downstream of β(1)-integrin. In addition, MAP-kinase p38 was phosphorylated downstream of FAK and also required for functional modification. Mechanotransduction through β(1)-integrins, FAK and p38 is required for anti-inflammatory effects of steady shear stress. Separation of the pathways which underlie pathological versus protective responses of different patterns of flow is required to enable therapeutic modification or mimicry, respectively.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cells, Cultured
  • Coculture Techniques
  • Collagen / metabolism
  • Extracellular Matrix Proteins / metabolism*
  • Fibronectins / metabolism
  • Focal Adhesion Kinase 1 / antagonists & inhibitors
  • Focal Adhesion Kinase 1 / genetics
  • Focal Adhesion Kinase 1 / metabolism
  • Human Umbilical Vein Endothelial Cells / drug effects
  • Human Umbilical Vein Endothelial Cells / immunology
  • Human Umbilical Vein Endothelial Cells / metabolism*
  • Humans
  • Inflammation / genetics
  • Inflammation / immunology
  • Inflammation / metabolism*
  • Inflammation Mediators / metabolism
  • Integrin beta1 / genetics
  • Integrin beta1 / metabolism*
  • Integrin beta3 / genetics
  • Integrin beta3 / metabolism
  • Laminin / metabolism
  • Leukocyte Rolling
  • Mechanotransduction, Cellular* / drug effects
  • Neutrophils / metabolism
  • Phosphorylation
  • Protein Kinase Inhibitors / pharmacology
  • RNA Interference
  • Stress, Mechanical
  • Time Factors
  • Transfection
  • Tumor Necrosis Factor-alpha / metabolism
  • p38 Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Extracellular Matrix Proteins
  • Fibronectins
  • ITGB3 protein, human
  • Inflammation Mediators
  • Integrin beta1
  • Integrin beta3
  • Laminin
  • Protein Kinase Inhibitors
  • Tumor Necrosis Factor-alpha
  • Collagen
  • Focal Adhesion Kinase 1
  • PTK2 protein, human
  • p38 Mitogen-Activated Protein Kinases