Interleukin-6 inhibits endothelial nitric oxide synthase activation and increases endothelial nitric oxide synthase binding to stabilized caveolin-1 in human vascular endothelial cells

J Hypertens. 2010 May;28(5):940-51. doi: 10.1097/HJH.0b013e32833992ef.

Abstract

Objective: We hypothesized a possible mechanism for atherosclerosis in which interleukin-6 (IL-6) might affect the endothelial nitric oxide synthase (eNOS)-caveolin-1 interaction and result in decreased nitric oxide bioavailability in the setting of low-grade inflammation.

Methods: Because eNOS and caveolin-1 are crucial for vascular tone control, we studied the effects of IL-6 on the expression and activation of eNOS and caveolin-1 in human vascular endothelial cells.

Results: IL-6 inhibited the phosphorylation of eNOS at Ser1177 and the bradykinin-stimulated nitric oxide production; however, eNOS protein expression was not changed. In addition, IL-6 inhibited bradykinin-stimulated Akt phosphorylation at Ser473 and Thr 308 without affecting the Akt protein expression. IL-6 did not alter the mRNA level of caveolin-1; however, the caveolin-1 protein level was significantly increased dose-dependently. The binding of eNOS and caveolin-1 in endothelial cells, as demonstrated by coimmunoprecipitation assay, was increased by IL-6 treatment. IL-6 treatment was found to stabilize caveolin-1 protein and its half-life was estimated to prolong from 7.5 h to longer than 12 h. Furthermore, treatment with PD98059 and short interference RNA of extracellular signal-regulated kinase gene reversed the effects of IL-6 on eNOS and caveolin-1.

Conclusion: In addition to decreasing Akt phosphorylation, the results of this study demonstrate, for the first time, the molecular mechanism underlying the effect of IL-6 to decrease the nitric oxide bioavailability by increasing the half-life and, therefore, the protein levels of caveolin-1. The increased caveolin-1 proteins bind more eNOS and consequently decrease eNOS activation by reducing the Ser1177 phosphorylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Atherosclerosis / etiology
  • Atherosclerosis / metabolism
  • Base Sequence
  • Caveolin 1 / genetics
  • Caveolin 1 / metabolism*
  • Cells, Cultured
  • Endothelial Cells / drug effects*
  • Endothelial Cells / metabolism*
  • Enzyme Activation / drug effects
  • Extracellular Signal-Regulated MAP Kinases / antagonists & inhibitors
  • Extracellular Signal-Regulated MAP Kinases / genetics
  • Flavonoids / pharmacology
  • Humans
  • Interleukin-6 / metabolism
  • Interleukin-6 / pharmacology*
  • Models, Cardiovascular
  • Nitric Oxide Synthase Type III / chemistry
  • Nitric Oxide Synthase Type III / metabolism*
  • Phosphorylation / drug effects
  • Protein Binding / drug effects
  • Protein Stability / drug effects
  • Proto-Oncogene Proteins c-akt / chemistry
  • Proto-Oncogene Proteins c-akt / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / genetics
  • Recombinant Proteins / pharmacology
  • Signal Transduction

Substances

  • CAV1 protein, human
  • Caveolin 1
  • Flavonoids
  • IL6 protein, human
  • Interleukin-6
  • RNA, Messenger
  • RNA, Small Interfering
  • Recombinant Proteins
  • NOS3 protein, human
  • Nitric Oxide Synthase Type III
  • Proto-Oncogene Proteins c-akt
  • Extracellular Signal-Regulated MAP Kinases
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one