Decreasing mitochondrial fission ameliorates HIF-1α-dependent pathological retinal angiogenesis

Acta Pharmacol Sin. 2024 Jul;45(7):1438-1450. doi: 10.1038/s41401-024-01262-3. Epub 2024 Apr 2.

Abstract

Angiogenesis plays a critical role in many pathological processes, including irreversible blindness in eye diseases such as retinopathy of prematurity. Endothelial mitochondria are dynamic organelles that undergo constant fusion and fission and are critical signalling hubs that modulate angiogenesis by coordinating reactive oxygen species (ROS) production and calcium signalling and metabolism. In this study, we investigated the role of mitochondrial dynamics in pathological retinal angiogenesis. We showed that treatment with vascular endothelial growth factor (VEGF; 20 ng/ml) induced mitochondrial fission in HUVECs by promoting the phosphorylation of dynamin-related protein 1 (DRP1). DRP1 knockdown or pretreatment with the DRP1 inhibitor Mdivi-1 (5 μM) blocked VEGF-induced cell migration, proliferation, and tube formation in HUVECs. We demonstrated that VEGF treatment increased mitochondrial ROS production in HUVECs, which was necessary for HIF-1α-dependent glycolysis, as well as proliferation, migration, and tube formation, and the inhibition of mitochondrial fission prevented VEGF-induced mitochondrial ROS production. In an oxygen-induced retinopathy (OIR) mouse model, we found that active DRP1 was highly expressed in endothelial cells in neovascular tufts. The administration of Mdivi-1 (10 mg·kg-1·d-1, i.p.) for three days from postnatal day (P) 13 until P15 significantly alleviated pathological angiogenesis in the retina. Our results suggest that targeting mitochondrial fission may be a therapeutic strategy for proliferative retinopathies and other diseases that are dependent on pathological angiogenesis.

Keywords: Dynamin-related protein 1; Mdivi-1; ROS.; glycolysis; mitochondrial fission; pathological angiogenesis.

MeSH terms

  • Angiogenesis
  • Animals
  • Cell Movement* / drug effects
  • Cell Proliferation / drug effects
  • Dynamins* / antagonists & inhibitors
  • Dynamins* / metabolism
  • Human Umbilical Vein Endothelial Cells*
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit* / metabolism
  • Mice
  • Mice, Inbred C57BL*
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Mitochondrial Dynamics* / drug effects
  • Quinazolinones* / pharmacology
  • Reactive Oxygen Species* / metabolism
  • Retinal Neovascularization* / drug therapy
  • Retinal Neovascularization* / metabolism
  • Retinal Neovascularization* / pathology
  • Vascular Endothelial Growth Factor A* / metabolism

Substances

  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Reactive Oxygen Species
  • Dynamins
  • Vascular Endothelial Growth Factor A
  • Quinazolinones
  • 3-(2,4-dichloro-5-methoxyphenyl)-2-sulfanyl-4(3H)-quinazolinone
  • Dnm1l protein, mouse
  • HIF1A protein, human
  • DNM1L protein, human