Shed membrane particles from T lymphocytes impair endothelial function and regulate endothelial protein expression

Circulation. 2004 Apr 6;109(13):1653-9. doi: 10.1161/01.CIR.0000124065.31211.6E. Epub 2004 Mar 15.

Abstract

Background: Microparticles (MPs) are membrane vesicles with procoagulant and proinflammatory properties released during cell activation. The present study was designed to dissect the effects evoked by T lymphocyte-derived MPs on vascular function.

Methods and results: MPs were produced by treatment of the human lymphoid CEM T cell line with actinomycin D or phytohemagglutinin. Incubation of mouse aortic rings with 30 nmol/L MPs resulted in a time-dependent impairment of acetylcholine-induced relaxation of precontracted vessels, with a maximal reduction after 24 hours. MPs also impaired shear stress-induced dilatation of mouse small mesenteric arteries by affecting the nitric oxide (NO) and prostacyclin but not the endothelium-derived hyperpolarizing factor components of the response. However, neither alteration of calcium signaling in response to agonists nor reduction of cyclooxygenase-1 expression accounted for the impairment of the NO and prostacyclin components of the endothelial response. The effect of MPs was rather because of a decrease in expression of endothelial NO synthase and an overexpression of caveolin-1. Furthermore, lymphocyte-derived MPs from diabetic patients or in vivo circulating MPs from either diabetic or HIV-infected patients reduced endothelial NO synthase expression. Finally, the effects of MPs on endothelial cells were not driven through CD11a/CD18 adhesion molecules or the Fas/FasL pathway.

Conclusions: MPs from T cells induce endothelial dysfunction in both conductance and resistance arteries by alteration of NO and prostacyclin pathways. MPs regulate protein expression for endothelial NO synthase and caveolin-1. These data contribute to a better understanding of the deleterious effects of enhanced circulating MPs observed in disorders with cardiovascular or immune complications.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / pharmacology
  • Animals
  • Aorta / drug effects
  • Aorta / physiology
  • Biological Factors / physiology
  • Caveolin 1
  • Caveolins / biosynthesis
  • Caveolins / genetics
  • Cell Membrane / chemistry
  • Cell Membrane / ultrastructure*
  • Cells, Cultured
  • Dactinomycin / pharmacology
  • Diabetes Mellitus / immunology
  • Endothelial Cells / metabolism
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / physiology*
  • Gene Expression Regulation
  • HIV Infections / immunology
  • Humans
  • In Vitro Techniques
  • Male
  • Membrane Lipids / chemistry
  • Mesenteric Arteries / physiology
  • Mice
  • Nitric Oxide / physiology
  • Nitric Oxide Synthase / biosynthesis
  • Nitric Oxide Synthase / genetics
  • Nitric Oxide Synthase / physiology
  • Nitric Oxide Synthase Type II
  • Nitric Oxide Synthase Type III
  • Nitroarginine / pharmacology
  • Phosphatidylserines / chemistry
  • Phytohemagglutinins / pharmacology
  • Prostaglandins I / physiology
  • Stress, Mechanical
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / ultrastructure*
  • Vasodilation / physiology

Substances

  • Biological Factors
  • CAV1 protein, human
  • Cav1 protein, mouse
  • Caveolin 1
  • Caveolins
  • Membrane Lipids
  • Phosphatidylserines
  • Phytohemagglutinins
  • Prostaglandins I
  • endothelium-dependent hyperpolarization factor
  • Dactinomycin
  • Nitroarginine
  • Nitric Oxide
  • NOS3 protein, human
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type II
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse
  • Acetylcholine