Regulation of AMPK and GAPDH by Transglutaminase 2 Plays a Pivotal Role in Microvascular Leakage in Diabetic Retinas

Diabetes. 2024 Oct 1;73(10):1756-1766. doi: 10.2337/db23-0885.

Abstract

Diabetic retinopathy is the most common microvascular complication caused by chronic hyperglycemia and is a leading cause of blindness; however, the underlying molecular mechanism has not been clearly elucidated. Therefore, we investigated whether regulation of AMPK and GAPDH by transglutaminase 2 (TGase2) is important for hyperglycemia-induced microvascular leakage in the diabetic retina. In human retinal endothelial cells (HRECs) and diabetic mouse retinas, we found that TGase2, activated by sequential elevation of intracellular Ca2+ and reactive oxygen species (ROS) levels, played an essential role in hyperglycemia-induced vascular leakage. ROS generation and TGsae2 activation were involved in hyperglycemia-induced AMPK dephosphorylation, which resulted in vascular endothelial-cadherin (VE-cadherin) disassembly and increased fluorescein isothiocyanate-dextran extravasation. Furthermore, high glucose-induced TGase2 activation suppressed GAPDH activity, determined by an on-chip activity assay, through inhibition of AMPK, which induced VE-cadherin disassembly and endothelial permeability in HRECs. Overall, our findings suggest that inhibition of AMPK and GAPDH by TGase2 plays a pivotal role in hyperglycemia-induced microvascular leakage in the retinas of diabetic mice.

MeSH terms

  • AMP-Activated Protein Kinases / metabolism
  • Animals
  • Antigens, CD / genetics
  • Antigens, CD / metabolism
  • Cadherins / metabolism
  • Capillary Permeability / drug effects
  • Diabetes Mellitus, Experimental / metabolism
  • Diabetic Retinopathy* / metabolism
  • Endothelial Cells / metabolism
  • GTP-Binding Proteins* / genetics
  • GTP-Binding Proteins* / metabolism
  • Glyceraldehyde-3-Phosphate Dehydrogenase (Phosphorylating) / metabolism
  • Humans
  • Hyperglycemia / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Protein Glutamine gamma Glutamyltransferase 2* / metabolism
  • Reactive Oxygen Species / metabolism
  • Retina / metabolism
  • Transglutaminases* / metabolism

Substances

  • Transglutaminases
  • Protein Glutamine gamma Glutamyltransferase 2
  • GTP-Binding Proteins
  • Reactive Oxygen Species
  • AMP-Activated Protein Kinases
  • Cadherins
  • Glyceraldehyde-3-Phosphate Dehydrogenase (Phosphorylating)
  • cadherin 5
  • Antigens, CD