The Early Pathogenesis of Diabetic Retinopathy and Its Attenuation by Sodium-Glucose Transporter 2 Inhibitors

Diabetes. 2024 Jul 1;73(7):1153-1166. doi: 10.2337/db22-0970.

Abstract

The early pathogenetic mechanism of diabetic retinopathy (DR) and its treatment remain unclear. Therefore, we used streptozotocin-induced diabetic mice to investigate the early pathogenic alterations in DR and the protective effect of sodium-glucose cotransporter 2 (SGLT2) inhibitors against these alterations. Retinal vascular leakage was assessed by dextran fluorescence angiography. Retinal thickness and vascular leakage were increased 2 and 4 weeks after onset of diabetes, respectively. Immunostaining showed that morphological change of microglia (amoeboid form) was observed at 2 weeks. Subsequently, increased angiopoietin-2 expression, simultaneous loss of pericytes and endothelial cells, decreased vessel density, retinal hypoxia, and increased vascular endothelial growth factor (VEGF)-A/VEGF receptor system occurred at 4 weeks. SGLT2 inhibitors (luseogliflozin and ipragliflozin) had a significant protective effect on retinal vascular leakage and retinal thickness at a low dose that did not show glucose-lowering effects. Furthermore, both inhibitors at this dose attenuated microglia morphological changes and these early pathogenic alterations in DR. In vitro study showed both inhibitors attenuated the lipopolysaccharide-induced activation of primary microglia, along with morphological changes toward an inactive form, suggesting the direct inhibitory effect of SGLT2 inhibitors on microglia. In summary, SGLT2 inhibitors may directly prevent early pathogenic mechanisms, thereby potentially playing a role in preventing DR.

MeSH terms

  • Angiopoietin-2 / antagonists & inhibitors
  • Angiopoietin-2 / metabolism
  • Animals
  • Diabetes Mellitus, Experimental* / drug therapy
  • Diabetes Mellitus, Experimental* / metabolism
  • Diabetic Retinopathy* / drug therapy
  • Diabetic Retinopathy* / metabolism
  • Diabetic Retinopathy* / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microglia* / drug effects
  • Microglia* / metabolism
  • Microglia* / pathology
  • Retina / drug effects
  • Retina / metabolism
  • Retina / pathology
  • Retinal Vessels / drug effects
  • Retinal Vessels / metabolism
  • Retinal Vessels / pathology
  • Sodium-Glucose Transporter 2 Inhibitors* / pharmacology
  • Sodium-Glucose Transporter 2 Inhibitors* / therapeutic use
  • Thiophenes / pharmacology
  • Thiophenes / therapeutic use
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Sodium-Glucose Transporter 2 Inhibitors
  • Vascular Endothelial Growth Factor A
  • Thiophenes
  • Angiopoietin-2