Inhibition of Lysine 63 Ubiquitination Prevents the Progression of Renal Fibrosis in Diabetic DBA/2J Mice

Int J Mol Sci. 2021 May 14;22(10):5194. doi: 10.3390/ijms22105194.

Abstract

Diabetic nephropathy (DN) is the most frequent cause of end-stage renal disease. Tubulointerstitial accumulation of lysine 63 (K63)-ubiquitinated (Ub) proteins is involved in the progression of DN fibrosis and correlates with urinary miR-27b-3p downregulation. We explored the renoprotective effect of an inhibitor of K63-Ub (NSC697923), alone or in combination with the ACE-inhibitor ramipril, in vitro and in vivo. Proximal tubular epithelial cells and diabetic DBA/2J mice were treated with NSC697923 and/or ramipril. K63-Ub protein accumulation along with α-SMA, collagen I and III, FSP-1, vimentin, p16INK4A expression, SA-α Gal staining, Sirius Red, and PAS staining were measured. Finally, we measured the urinary albumin to creatinine ratio (uACR), and urinary miR-27b-3p expression in mice. NSC697923, both alone and in association with ramipril, in vitro and in vivo inhibited hyperglycemia-induced epithelial to mesenchymal transition by significantly reducing K63-Ub proteins, α-SMA, collagen I, vimentin, FSP-1 expression, and collagen III along with tubulointerstitial and glomerular fibrosis. Treated mice also showed recovery of urinary miR-27b-3p and restored expression of p16INK4A. Moreover, NSC697923 in combination with ramipril demonstrated a trend in the reduction of uACR. In conclusion, we suggest that selective inhibition of K63-Ub, when combined with the conventional treatment with ACE inhibitors, might represent a novel treatment strategy to prevent the progression of fibrosis and proteinuria in diabetic nephropathy and we propose miR-27b-3p as a biomarker of treatment efficacy.

Keywords: DBA2/J mice; diabetes; lysine 63 ubiquitination; microRNA; renal fibrosis; senescence.

MeSH terms

  • Angiotensin-Converting Enzyme Inhibitors / pharmacology
  • Animals
  • Diabetes Mellitus, Experimental / complications*
  • Diabetic Nephropathies / etiology
  • Diabetic Nephropathies / metabolism
  • Diabetic Nephropathies / pathology
  • Diabetic Nephropathies / prevention & control*
  • Drug Therapy, Combination
  • Female
  • Fibrosis / etiology
  • Fibrosis / metabolism
  • Fibrosis / pathology
  • Fibrosis / prevention & control*
  • Lysine / chemistry*
  • Mice
  • Mice, Inbred DBA
  • Nitrofurans / pharmacology*
  • Ramipril / pharmacology*
  • Sulfones / pharmacology*
  • Ubiquitination*

Substances

  • 2-((4-methylphenyl)sulfonyl)-5-nitrofuran
  • Angiotensin-Converting Enzyme Inhibitors
  • Nitrofurans
  • Sulfones
  • Lysine
  • Ramipril