TGF-β induces miR-30d down-regulation and podocyte injury through Smad2/3 and HDAC3-associated transcriptional repression

J Mol Med (Berl). 2016 Mar;94(3):291-300. doi: 10.1007/s00109-015-1340-9. Epub 2015 Oct 3.

Abstract

The microRNA-30 family plays important roles in maintaining kidney homeostasis. Patients with focal segmental glomerulosclerosis (FSGS) have reduced miR-30 levels in glomerulus. TGF-β represses miR-30s in kidney podocytes, which leads to cytoskeleton damage and podocyte apoptosis. In this study, we investigated the mechanism by which TGF-β represses miR-30d in vitro. The human miR-30d promoter contains multiple copies of Smad binding element-like sequences. A fragment of 150 base pairs close to the transcription start site was negatively regulated by TGF-β to a similar extent as the 1.8 kb promoter, which was blocked by histone-deacetylase inhibition. TGF-β specifically enhanced HDAC3 expression. Knockdown of HDAC3 by shRNA or a selective inhibitor RGFP966 significantly relieved the repression of miR-30d mRNA and the promoter transcription. TGF-β promoted HDAC3 association with Smad2/3 and NCoR and caused their accumulation at the putative Smad binding site on the miR-30d promoter, which was prohibited by TSA or RGFP966. Furthermore, TSA or RGFP966 treatment reversed TGF-β-induced up-regulation of miR-30d targets Notch1 and p53 and alleviated the podocyte cytoskeleton damage and apoptosis. Taken together, these findings pinpoint that TGF-β represses miR-30d through a Smad2/3-HDAC3-NCoR repression complex and provide novel insights into a potential target for the treatment of podocyte injury-associated glomerulopathies. Key message: MiR-30d promoter is negatively regulated by TGF-β. TGF-β down-regulates miR-30 through Smad signaling pathway. HDAC3 and NCoR are recruited by Smad2/3 to mediate miR-30d repression by TGF-β. HDAC3 acts as a critical player in TGF-β-induced miR-30d repression and podocyte injuries.

Keywords: HDAC3; Podocyte; Smad; TGF-β; Transcriptional repression; miR-30d.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • Down-Regulation*
  • Histone Deacetylases / metabolism*
  • Humans
  • MicroRNAs / genetics*
  • Podocytes / metabolism
  • Podocytes / pathology*
  • Promoter Regions, Genetic
  • Smad2 Protein / metabolism*
  • Smad3 Protein / metabolism*
  • Transcriptional Activation
  • Transforming Growth Factor beta / metabolism*

Substances

  • MIRN30b microRNA, human
  • MicroRNAs
  • SMAD2 protein, human
  • SMAD3 protein, human
  • Smad2 Protein
  • Smad3 Protein
  • Transforming Growth Factor beta
  • Histone Deacetylases
  • histone deacetylase 3