Time-dependent LXR/RXR pathway modulation characterizes capillary remodeling in inflammatory corneal neovascularization

Angiogenesis. 2018 May;21(2):395-413. doi: 10.1007/s10456-018-9604-y. Epub 2018 Feb 14.

Abstract

Inflammation in the normally immune-privileged cornea can initiate a pathologic angiogenic response causing vision-threatening corneal neovascularization. Inflammatory pathways, however, are numerous, complex and are activated in a time-dependent manner. Effective resolution of inflammation and associated angiogenesis in the cornea requires knowledge of these pathways and their time dependence, which has, to date, remained largely unexplored. Here, using a model of endogenous resolution of inflammation-induced corneal angiogenesis, we investigate the time dependence of inflammatory genes in effecting capillary regression and the return of corneal transparency. Endogenous capillary regression was characterized by a progressive thinning and remodeling of angiogenic capillaries and inflammatory cell retreat in vivo in the rat cornea. By whole-genome longitudinal microarray analysis, early suppression of VEGF ligand-receptor signaling and inflammatory pathways preceded an unexpected later-phase preferential activation of LXR/RXR, PPARα/RXRα and STAT3 canonical pathways, with a concurrent attenuation of LPS/IL-1 inhibition of RXR function and Wnt/β-catenin signaling pathways. Potent downstream inflammatory cytokines such as Cxcl5, IL-1β, IL-6 and Ccl2 were concomitantly downregulated during the remodeling phase. Upstream regulators of the inflammatory pathways included Socs3, Sparc and ApoE. A complex and coordinated time-dependent interplay between pro- and anti-inflammatory signaling pathways highlights a potential anti-inflammatory role of LXR/RXR, PPARα/RXRα and STAT3 signaling pathways in resolving inflammatory corneal angiogenesis.

Keywords: Angiogenesis; Cornea neovascularization; Inflammation; Remodeling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Capillaries / metabolism*
  • Capillaries / pathology
  • Corneal Neovascularization / metabolism*
  • Corneal Neovascularization / pathology
  • Inflammation / metabolism
  • Inflammation / pathology
  • Liver X Receptors / metabolism*
  • PPAR alpha / metabolism
  • Rats
  • Rats, Wistar
  • Retinoid X Receptor alpha / metabolism*
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction*
  • Vascular Remodeling*

Substances

  • Liver X Receptors
  • PPAR alpha
  • Retinoid X Receptor alpha
  • STAT3 Transcription Factor
  • Stat3 protein, rat