Paracrine Wnt1 Drives Interstitial Fibrosis without Inflammation by Tubulointerstitial Cross-Talk

J Am Soc Nephrol. 2016 Mar;27(3):781-90. doi: 10.1681/ASN.2014121188. Epub 2015 Jul 23.

Abstract

AKI with incomplete epithelial repair is a major contributor to CKD characterized by tubulointerstitial fibrosis. Injury-induced epithelial secretion of profibrotic factors is hypothesized to underlie this link, but the identity of these factors and whether epithelial injury is required remain undefined. We previously showed that activation of the canonical Wnt signaling pathway in interstitial pericytes cell autonomously drives myofibroblast activation in vivo. Here, we show that inhibition of canonical Wnt signaling also substantially prevented TGFβ-dependent myofibroblast activation in vitro. To investigate whether Wnt ligand derived from proximal tubule is sufficient for renal fibrogenesis, we generated a novel mouse strain with inducible proximal tubule Wnt1 secretion. Adult mice were treated with vehicle or tamoxifen and euthanized at 12 or 24 weeks postinjection. Compared with vehicle-treated controls, kidneys with tamoxifen-induced Wnt1 expression from proximal tubules displayed interstitial myofibroblast activation and proliferation and increased matrix protein production. PDGF receptor β-positive myofibroblasts isolated from these kidneys exhibited increased canonical Wnt target gene expression compared with controls. Notably, fibrotic kidneys had no evidence of inflammatory cytokine expression, leukocyte infiltration, or epithelial injury, despite the close histologic correlation of each with CKD. These results provide the first example of noninflammatory renal fibrosis. The fact that epithelial-derived Wnt ligand is sufficient to drive interstitial fibrosis provides strong support for the maladaptive repair hypothesis in the AKI to CKD transition.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism
  • Animals
  • Antineoplastic Agents, Hormonal / pharmacology
  • Cell Proliferation
  • Disease Models, Animal
  • Fibronectins / metabolism
  • Fibrosis
  • Gene Expression
  • Inflammation / complications
  • Kidney Tubules, Proximal / metabolism*
  • Kidney Tubules, Proximal / pathology*
  • Ligands
  • Mice
  • Myofibroblasts / metabolism*
  • Myofibroblasts / physiology
  • Paracrine Communication*
  • Receptor, Platelet-Derived Growth Factor beta / metabolism
  • Tamoxifen / pharmacology
  • Transforming Growth Factor beta / metabolism*
  • Wnt Signaling Pathway* / genetics
  • Wnt1 Protein / genetics
  • Wnt1 Protein / metabolism*

Substances

  • Actins
  • Antineoplastic Agents, Hormonal
  • Fibronectins
  • Ligands
  • Transforming Growth Factor beta
  • Wnt1 Protein
  • alpha-smooth muscle actin, mouse
  • Tamoxifen
  • Receptor, Platelet-Derived Growth Factor beta