Matrix metalloproteinase 9-dependent Notch signaling contributes to kidney fibrosis through peritubular endothelial-mesenchymal transition

Nephrol Dial Transplant. 2017 May 1;32(5):781-791. doi: 10.1093/ndt/gfw308.

Abstract

Background: Endothelial cells are known to contribute to kidney fibrosis via endothelial-mesenchymal transition (EndoMT). Matrix metalloproteinase 9 (MMP-9) is known to be profibrotic. However, whether MMP-9 contributes to kidney fibrosis via EndoMT is unknown.

Methods: Primary mouse renal peritubular endothelial cells (MRPECs) were isolated and treated by recombinant human transforming growth factor beta 1 (rhTGF-β1) with or without MMP-9 inhibitor or by recombinant human MMP-9 (rhMMP-9) alone. Kidney fibrosis was induced by unilateral ureteral obstruction (UUO) in MMP-9 knockout (KO) and wide-type (WT) control mice. The effects of MMP-9 on EndoMT of MRPECs and kidney fibrosis were examined.

Results: We showed that MRPECs underwent EndoMT after rhTGF-β1 treatment or in UUO kidney as evidenced by decreased expression of endothelial markers, vascular endothelial cadherin (VE-cadherin) and CD31, and increased levels of mesenchymal markers, α-smooth muscle actin (α-SMA) and vimentin. The expression of fibrosis markers was also up-regulated significantly after rhTGF-β1 treatment in MRPECs. The EndoMT and fibrosis markers were significantly less in rhTGF-β1-treated MMP-9 KO MRPECs, whereas MMP-9 alone was sufficient to induce EndoMT in MRPECs. UUO kidney of MMP-9 KO mice showed significantly less interstitial fibrosis and EndoMT in MRPECs. Notch signaling shown by Notch intracellular domain (NICD) was increased, while Notch-1 was decreased in rhTGF-β1-treated MRPECs of MMP-9 WT but not MMP-9 KO mice. Inhibition of MMP-9 or Notch signaling prevented rhTGF-β1- or rhMMP-9-induced α-SMA and NICD upregulation in MRPECs. UUO kidney of MMP-9 KO mice had less staining of Notch signaling transcription factor Hey-1 in VE-cadherin-positive MRPECs than WT controls.

Conclusions: Our results demonstrate that MMP-9-dependent Notch signaling plays an important role in kidney fibrosis through EndoMT of MRPECs.

Keywords: Matrix metalloproteinase 9; Notch; endothelial–mesenchymal transition; kidney fibrosis; peritubular endothelial cells.

MeSH terms

  • Animals
  • Endothelium / metabolism
  • Endothelium / pathology*
  • Fibrosis / metabolism
  • Fibrosis / pathology*
  • Humans
  • Kidney Diseases / metabolism
  • Kidney Diseases / pathology*
  • Male
  • Matrix Metalloproteinase 9 / metabolism*
  • Mesoderm / metabolism
  • Mesoderm / pathology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Receptors, Notch / metabolism*
  • Signal Transduction
  • Transforming Growth Factor beta1 / metabolism
  • Ureteral Obstruction / metabolism
  • Ureteral Obstruction / pathology

Substances

  • Receptors, Notch
  • Transforming Growth Factor beta1
  • Matrix Metalloproteinase 9