MicroRNA-26a inhibits TGF-β-induced extracellular matrix protein expression in podocytes by targeting CTGF and is downregulated in diabetic nephropathy

Diabetologia. 2015 Sep;58(9):2169-80. doi: 10.1007/s00125-015-3642-4. Epub 2015 Jun 11.

Abstract

Aims/hypothesis: The accumulation of extracellular matrix (ECM) is a characteristic of diabetic nephropathy, and is partially caused by profibrotic proteins TGF-β and connective tissue growth factor (CTGF). We aimed to identify microRNAs (miRNAs) targeting CTGF on podocytes in diabetic nephropathy.

Methods: We investigated miRNAs targeting CTGF on podocytes with miRNA array analysis and identified a candidate miRNA, miR-26a. Using overexpression and silencing of miR-26a in cultured podocytes, we examined changes of ECM and its host genes. We further investigated glomerular miR-26a expression in humans and in mouse models of diabetic nephropathy.

Results: miR-26a, which was downregulated by TGF-β1, was expressed in glomerular cells including podocytes and in tubules by in situ hybridisation. Glomerular miR-26a expression was downregulated by 70% in streptozotocin-induced diabetic mice. Transfection of miR-26a mimics in cultured human podocytes decreased the CTGF protein level by 50%, and directly inhibited CTGF expression in podocytes, as demonstrated by a reporter assay with the 3'-untranslated region of the CTGF gene. This effect was abolished by a mutant plasmid. miR-26a mimics also inhibited TGF-β1-induced collagen expression, SMAD-binding activity and expression of its host genes CTDSP2 and CTDSPL. Knockdown of CTDSP2 and CTDSPL increased collagen expression in TGF-β-stimulated podocytes, suggesting that host genes also regulate TGF-β/SMAD signalling. Finally, we observed a positive correlation between microdissected glomerular miR-26a expression levels and estimated GFR in patients with diabetic nephropathy.

Conclusions/interpretation: The downregulation of miR-26a is involved in the progression of diabetic nephropathy both in humans and in mice through enhanced TGF-β/CTGF signalling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions
  • Animals
  • Base Sequence
  • Biopsy
  • Connective Tissue Growth Factor / metabolism*
  • Diabetes Mellitus, Experimental
  • Diabetic Nephropathies / metabolism*
  • Disease Progression
  • Down-Regulation
  • Extracellular Matrix / metabolism*
  • Female
  • Gene Expression Regulation
  • Gene Silencing
  • Glomerular Filtration Rate
  • Humans
  • Kidney Glomerulus / metabolism
  • Male
  • Mice
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Microdissection
  • Middle Aged
  • Molecular Sequence Data
  • Nuclear Proteins / metabolism
  • Phosphoprotein Phosphatases / metabolism
  • Podocytes / metabolism*
  • Smad Proteins / metabolism
  • Streptozocin
  • Transforming Growth Factor beta1 / antagonists & inhibitors*
  • Tumor Suppressor Proteins / metabolism

Substances

  • 3' Untranslated Regions
  • CCN2 protein, human
  • CCN2 protein, mouse
  • CTDSPL protein, human
  • MIRN26A microRNA, human
  • MicroRNAs
  • Mirn26 microRNA, mouse
  • Nuclear Proteins
  • Smad Proteins
  • TGFB1 protein, human
  • Tgfb1 protein, mouse
  • Transforming Growth Factor beta1
  • Tumor Suppressor Proteins
  • Connective Tissue Growth Factor
  • Streptozocin
  • CTDSP2 protein, human
  • Phosphoprotein Phosphatases