Myocardin-Related Transcription Factor Mediates Epithelial Fibrogenesis in Polycystic Kidney Disease

Cells. 2024 Jun 5;13(11):984. doi: 10.3390/cells13110984.

Abstract

Polycystic kidney disease (PKD) is characterized by extensive cyst formation and progressive fibrosis. However, the molecular mechanisms whereby the loss/loss-of-function of Polycystin 1 or 2 (PC1/2) provokes fibrosis are largely unknown. The small GTPase RhoA has been recently implicated in cystogenesis, and we identified the RhoA/cytoskeleton/myocardin-related transcription factor (MRTF) pathway as an emerging mediator of epithelium-induced fibrogenesis. Therefore, we hypothesized that MRTF is activated by PC1/2 loss and plays a critical role in the fibrogenic reprogramming of the epithelium. The loss of PC1 or PC2, induced by siRNA in vitro, activated RhoA and caused cytoskeletal remodeling and robust nuclear MRTF translocation and overexpression. These phenomena were also manifested in PKD1 (RC/RC) and PKD2 (WS25/-) mice, with MRTF translocation and overexpression occurring predominantly in dilated tubules and the cyst-lining epithelium, respectively. In epithelial cells, a large cohort of PC1/PC2 downregulation-induced genes was MRTF-dependent, including cytoskeletal, integrin-related, and matricellular/fibrogenic proteins. Epithelial MRTF was necessary for the paracrine priming of the fibroblast-myofibroblast transition. Thus, MRTF acts as a prime inducer of epithelial fibrogenesis in PKD. We propose that RhoA is a common upstream inducer of both histological hallmarks of PKD: cystogenesis and fibrosis.

Keywords: epithelium-initiated fibrosis; myocardin-related transcription factor; profibrotic epithelial phenotype; ∙ polycystic kidney disease.

MeSH terms

  • Animals
  • Cytoskeleton / metabolism
  • Epithelial Cells* / metabolism
  • Epithelial Cells* / pathology
  • Fibrosis
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Polycystic Kidney Diseases* / genetics
  • Polycystic Kidney Diseases* / metabolism
  • Polycystic Kidney Diseases* / pathology
  • TRPP Cation Channels* / genetics
  • TRPP Cation Channels* / metabolism
  • Trans-Activators / metabolism
  • rhoA GTP-Binding Protein* / metabolism

Substances

  • Mrtfa protein, mouse
  • polycystic kidney disease 1 protein
  • polycystic kidney disease 2 protein
  • rhoA GTP-Binding Protein
  • Trans-Activators
  • TRPP Cation Channels