Thioredoxin-interacting protein mediates dysfunction of tubular autophagy in diabetic kidneys through inhibiting autophagic flux

Lab Invest. 2014 Mar;94(3):309-20. doi: 10.1038/labinvest.2014.2. Epub 2014 Feb 3.

Abstract

Thioredoxin-interacting protein (TXNIP) expression is ubiquitous and is induced by a variety of cellular stresses, including high intracellular glucose. TXNIP is associated with activation of oxidative stress and tubulointerstitial fibrosis in diabetic nephropathy. Autophagy is a major pathway that delivers damaged proteins and organelles to lysosomes to maintain cellular homeostasis. This study aimed to investigate the dysregulation of autophagy and the regulation of TXNIP on autophagy in renal proximal tubular cells (PTCs) under diabetic conditions. The formation of autophagosomes was measured using transmission electron microscopy, and LC3-II, and the effectiveness of autophagic clearance was determined by p62 expression in diabetic kidney and in human PTCs exposed to high glucose (HG). The results collectively demonstrated increased expression of TXNIP, LC3/LC3-II and p62 in renal tubular cells of mice with diabetic nephropathy and in cultured human PTCs exposed to HG (30 mM/l) for 48 h compared with control. The formation of autophagic vacuoles was increased in HG-induced cells. Furthermore, silencing of TXNIP by siRNA transfection reduced autophagic vacuoles and the expression of LC3-II and p62 in human PTCs exposed to HG compared with control and partially reversed the accumulation of LC3-II and p62 induced by bafilomycin A1 (50 nM/l), a pharmacological inhibitor of autophagy which blocks the fusion of autophagosomes with lysosomes and impairs the degradation of LC3-II and p62. Collectively, these results suggest that hyperglycemia leads to dysfunction of autophagy in renal tubular cells and decreases autophagic clearance. HG-induced overexpression of TXNIP may contribute to the dysfunction of tubular autophagy in diabetes.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Autophagy / physiology*
  • Carrier Proteins / antagonists & inhibitors
  • Carrier Proteins / genetics
  • Carrier Proteins / physiology*
  • Cell Line
  • Diabetes Mellitus, Experimental / genetics
  • Diabetes Mellitus, Experimental / pathology
  • Diabetes Mellitus, Experimental / physiopathology
  • Diabetic Nephropathies / genetics
  • Diabetic Nephropathies / pathology*
  • Diabetic Nephropathies / physiopathology*
  • Gene Knockdown Techniques
  • Humans
  • Kidney Tubules, Proximal / pathology
  • Kidney Tubules, Proximal / physiopathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microscopy, Electron, Transmission
  • Microtubule-Associated Proteins / metabolism
  • Oxidative Stress
  • Phagosomes / metabolism
  • Phagosomes / pathology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Sequestosome-1 Protein
  • Thioredoxins / genetics
  • Thioredoxins / physiology*
  • Transcription Factor TFIIH
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Carrier Proteins
  • Gtf2h1 protein, mouse
  • MAP1LC3A protein, human
  • Map1lc3b protein, mouse
  • Microtubule-Associated Proteins
  • RNA, Messenger
  • SQSTM1 protein, human
  • Sequestosome-1 Protein
  • TXNIP protein, human
  • Transcription Factors
  • Txnip protein, mouse
  • Transcription Factor TFIIH
  • Thioredoxins