Icariin alleviates oxygen-induced retinopathy by targeting microglia hexokinase 2

Immunology. 2024 Sep;173(1):141-151. doi: 10.1111/imm.13818. Epub 2024 May 28.

Abstract

Retinopathy of prematurity (ROP) is a retinal disease-causing retinal neovascularization that can lead to blindness. Oxygen-induced retinopathy (OIR) is a widely used ROP animal model. Icariin (ICA) has anti-oxidative and anti-inflammation properties; however, whether ICA has a regulatory effect on OIR remains unclear. In this study, ICA alleviated pathological neovascularization, microglial activation and blood-retina barrier (BRB) damage in vivo. Further results indicated that endothelial cell tube formation, migration and proliferation were restored by ICA treatment in vitro. Proteomic microarrays and molecular mimicry revealed that ICA can directly bind to hexokinase 2 (HK2) and decrease HK2 protein expression in vivo and in vitro. In addition, ICA inhibited the AKT/mTOR/HIF1α pathway activation. The effects of ICA on pathological neovascularization, microglial activation and BRB damage disappeared after HK2 overexpression in vivo. Similarly, the endothelial cell function was revised after HK2 overexpression. HK2 overexpression reversed ICA-induced AKT/mTOR/HIF1α pathway inhibition in vivo and in vitro. Therefore, ICA prevented pathological angiogenesis in OIR in an HK2-dependent manner, implicating ICA as a potential therapeutic agent for ROP.

Keywords: angiogenesis; hexokinase 2; icariin; microglia; oxygen‐induced retinopathy.

MeSH terms

  • Animals
  • Cell Movement / drug effects
  • Disease Models, Animal
  • Flavonoids* / pharmacology
  • Flavonoids* / therapeutic use
  • Hexokinase* / metabolism
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Microglia* / drug effects
  • Microglia* / metabolism
  • Oxygen* / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • Retinal Neovascularization* / drug therapy
  • Retinal Neovascularization* / metabolism
  • Retinal Neovascularization* / pathology
  • Retinopathy of Prematurity* / drug therapy
  • Retinopathy of Prematurity* / metabolism
  • Retinopathy of Prematurity* / pathology
  • Signal Transduction* / drug effects
  • TOR Serine-Threonine Kinases* / metabolism

Substances

  • Flavonoids
  • Hexokinase
  • hexokinase 2, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • icariin
  • Oxygen
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases