HuR mediates the synergistic effects of angiotensin II and IL-1β on vascular COX-2 expression and cell migration

Br J Pharmacol. 2015 Jun;172(12):3028-42. doi: 10.1111/bph.13103. Epub 2015 Mar 27.

Abstract

Background and purpose: Angiotensin II (AngII) and IL-1β are involved in cardiovascular diseases through the induction of inflammatory pathways. HuR is an adenylate- and uridylate-rich element (ARE)-binding protein involved in the mRNA stabilization of many genes. This study investigated the contribution of HuR to the increased expression of COX-2 induced by AngII and IL-1β and its consequences on VSMC migration and remodelling.

Experimental approach: Rat and human VSMCs were stimulated with AngII (0.1 μM) and/or IL-1β (10 ng · mL(-1)). Mice were infused with AngII or subjected to carotid artery ligation. mRNA and protein levels were assayed by quantitative PCR, Western blot, immunohistochemistry and immunofluorescence. Cell migration was measured by wound healing and transwell assays.

Key results: In VSMCs, AngII potentiated COX-2 and tenascin-C expressions and cell migration induced by IL-1β. This effect of AngII on IL-1β-induced COX-2 expression was accompanied by increased COX-2 3' untranslated region reporter activity and mRNA stability, mediated through cytoplasmic HuR translocation and COX-2 mRNA binding. These effects were blocked by ERK1/2 and HuR inhibitors. VSMC migration was reduced by blockade of ERK1/2, HuR, COX-2, TXAS, TP and EP receptors. HuR, COX-2, mPGES-1 and TXAS expressions were increased in AngII-infused mouse aortas and in carotid-ligated arteries. AngII-induced tenascin-C expression and vascular remodelling were abolished by celecoxib and by mPGES-1 deletion.

Conclusions and implications: The synergistic induction of COX-2 by AngII and IL-1β in VSMCs involves HuR through an ERK1/2-dependent mechanism. The HuR/COX-2 axis participates in cell migration and vascular damage. HuR might be a novel target to modulate vascular remodelling.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / administration & dosage
  • Angiotensin II / metabolism*
  • Animals
  • Aorta / metabolism
  • Celecoxib / pharmacology
  • Cell Movement / physiology
  • Cyclooxygenase 2 / genetics*
  • Drug Synergism
  • ELAV-Like Protein 1 / metabolism*
  • Gene Expression Regulation / drug effects
  • Humans
  • Interleukin-1beta / administration & dosage
  • Interleukin-1beta / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Muscle, Smooth, Vascular / cytology
  • RNA Stability
  • RNA, Messenger / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Tenascin / genetics
  • Vascular Remodeling / drug effects

Substances

  • ELAV-Like Protein 1
  • Interleukin-1beta
  • RNA, Messenger
  • Tenascin
  • Angiotensin II
  • Cyclooxygenase 2
  • Celecoxib