Nrf2 Activator RS9 Suppresses Pathological Ocular Angiogenesis and Hyperpermeability

Invest Ophthalmol Vis Sci. 2019 May 1;60(6):1943-1952. doi: 10.1167/iovs.18-25745.

Abstract

Purpose: Ocular angiogenesis, including retinopathy of prematurity, diabetic retinopathy, and exudative age-related macular degeneration, are closely related to oxidative stress. Many reports have shown that the cellular protective mechanism against oxidative stress and inflammatory response has nuclear factor-erythroid 2-related factor-2 (Nrf2) activity. The aim of this study was to investigate the effectiveness and mechanism of Nrf2 activation in treating the ocular diseases with abnormal vessels.

Methods: The effects of Nrf2 activators, bardoxolone methyl (BARD) and RS9, were evaluated against vascular endothelial growth factor (VEGF)-induced cell migration in human retinal microvascular endothelial cells (HRMECs). We measured the expression of the Nrf2 target genes, Ho-1 and Nqo-1 mRNA, in mouse retinas after a single injection of BARD and RS9. The effects and mechanisms of RS9 against retinal angiogenesis were evaluated using an oxygen-induced retinopathy (OIR) model in mice. Moreover, the effect of RS9 against choroidal neovascularization (CNV) was evaluated in a laser-induced CNV monkey model.

Results: Both BARD and RS9 decreased VEGF-induced cell migration, and significantly increased Ho-1 mRNA expression; however, only RS9 significantly increased Nqo-1 mRNA. RS9 decreased retinal neovascularization through suppressing VEGF expression and increasing Nrf2, HO-1, platelet-derived growth factor receptor (PDGFR)-β, and tight junction proteins in OIR murine retinas. Furthermore, RS9 showed a tendency toward decreasing CNV lesions, and improved vascular leakage in a CNV monkey model.

Conclusions: These data indicate that a Nrf2 activator might be a candidate for treatment of ocular diseases characterized by pathophysiological angiogenesis and hyperpermeability.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Membrane Permeability / drug effects
  • Cell Movement / drug effects
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Choroidal Neovascularization / drug therapy*
  • Choroidal Neovascularization / metabolism
  • Choroidal Neovascularization / pathology
  • Disease Models, Animal
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Fluorescein Angiography
  • Fundus Oculi
  • Humans
  • Immunoblotting
  • Macaca fascicularis
  • Male
  • Mice
  • Mice, Inbred C57BL
  • NF-E2-Related Factor 2 / drug effects
  • NF-E2-Related Factor 2 / metabolism*
  • Oleanolic Acid / analogs & derivatives*
  • Oleanolic Acid / pharmacology
  • Retinal Neovascularization / drug therapy*
  • Retinal Neovascularization / metabolism
  • Retinal Neovascularization / pathology
  • Retinal Vessels / metabolism*
  • Retinal Vessels / pathology
  • Tomography, Optical Coherence
  • Triterpenes / pharmacology*

Substances

  • NF-E2-Related Factor 2
  • NFE2L2 protein, human
  • RS9 triterpenoid
  • Triterpenes
  • Oleanolic Acid
  • bardoxolone methyl