Pro-atherogenic effect of interleukin-4 in endothelial cells: modulation of oxidative stress, nitric oxide and monocyte chemoattractant protein-1 expression

Atherosclerosis. 2006 Aug;187(2):285-91. doi: 10.1016/j.atherosclerosis.2005.09.016. Epub 2005 Oct 24.

Abstract

Background: Although considered as an anti-inflammatory cytokine, interleukin-4 (IL-4) has been shown to be pro-atherogenic in mice models of atherosclerosis.

Objectives: In order to elucidate this paradox, we have investigated the effects of IL-4 on characteristic atherogenic parameters in human umbilical vein endothelial cells (HUVECs): production of reactive oxygen species, expression of monocyte chemoattractant protein-1 (MCP-1) and nitric oxide (NO) bioavailability.

Results: Incubation of HUVECs with IL-4 resulted in an increased production of reactive oxygen species and extracellular O(2)(-)(*) measured using fluorogenic probes and Cytochrome c that was inhibited by superoxide dismutase or gp91ds-tat, a selective NADPH oxidase inhibitor. The latter also inhibited IL-4 induced over-expression of MCP-1 mRNA measured by classical and real time RT-PCR. Incubation of HUVECs with IL-4 reduced thrombin-induced NO release, detected by electrochemistry, an effect which was reversed by incubation with superoxide dismutase. Both production of reactive oxygen species and MCP-1 mRNA over-expression induced by IL-4 were fully inhibited by selective inhibitors of phosphatidyl inositol 3-kinase.

Conclusion: The data demonstrate that IL-4 up-regulates the expression of MCP-1 and decreases NO bioavailability through activation of NADPH oxidase in endothelial cells. These results are in favor of a pro-inflammatory and pro-atherogenic effect of IL-4 in vascular tissues.

MeSH terms

  • Arachidonic Acids / pharmacology
  • Atherosclerosis / immunology
  • Atherosclerosis / metabolism*
  • Chemokine CCL2 / genetics*
  • Chemokine CCL2 / metabolism
  • Chromones / pharmacology
  • Endothelium, Vascular / cytology
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / metabolism*
  • Enzyme Inhibitors / pharmacology
  • Humans
  • Interleukin-4 / metabolism*
  • Interleukin-4 / pharmacology
  • Morpholines / pharmacology
  • NADPH Oxidases / metabolism
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase Type II / metabolism
  • Oxidative Stress / drug effects
  • Oxidative Stress / immunology*
  • RNA, Messenger / metabolism
  • Reactive Oxygen Species / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Tumor Necrosis Factor-alpha / metabolism
  • Tumor Necrosis Factor-alpha / pharmacology
  • Umbilical Veins / cytology

Substances

  • Arachidonic Acids
  • CCL2 protein, human
  • Chemokine CCL2
  • Chromones
  • Enzyme Inhibitors
  • IL4 protein, human
  • Morpholines
  • RNA, Messenger
  • Reactive Oxygen Species
  • Tumor Necrosis Factor-alpha
  • arachidonyltrifluoromethane
  • Interleukin-4
  • Nitric Oxide
  • 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one
  • Nitric Oxide Synthase Type II
  • NADPH Oxidases