FoxO3 an important player in fibrogenesis and therapeutic target for idiopathic pulmonary fibrosis

EMBO Mol Med. 2018 Feb;10(2):276-293. doi: 10.15252/emmm.201606261.

Abstract

Idiopathic pulmonary fibrosis (IPF) is a progressive and fatal parenchymal lung disease with limited therapeutic options, with fibroblast-to-myofibroblast transdifferentiation and hyperproliferation playing a major role. Investigating ex vivo-cultured (myo)fibroblasts from human IPF lungs as well as fibroblasts isolated from bleomycin-challenged mice, Forkhead box O3 (FoxO3) transcription factor was found to be less expressed, hyperphosphorylated, and nuclear-excluded relative to non-diseased controls. Downregulation and/or hyperphosphorylation of FoxO3 was reproduced by exposure of normal human lung fibroblasts to various pro-fibrotic growth factors and cytokines (FCS, PDGF, IGF1, TGF-β1). Moreover, selective knockdown of FoxO3 in the normal human lung fibroblasts reproduced the transdifferentiation and hyperproliferation phenotype. Importantly, mice with global- (Foxo3-/-) or fibroblast-specific (Foxo3f.b-/-) FoxO3 knockout displayed enhanced susceptibility to bleomycin challenge, with augmented fibrosis, loss of lung function, and increased mortality. Activation of FoxO3 with UCN-01, a staurosporine derivative currently investigated in clinical cancer trials, reverted the IPF myofibroblast phenotype in vitro and blocked the bleomycin-induced lung fibrosis in vivo These studies implicate FoxO3 as a critical integrator of pro-fibrotic signaling in lung fibrosis and pharmacological reconstitution of FoxO3 as a novel treatment strategy.

Keywords: fibroblast; forkhead box O transcription factors; idiopathic pulmonary fibrosis; myofibroblast; transdifferentiation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Proliferation
  • Cell Transdifferentiation
  • Cells, Cultured
  • Cytokines / pharmacology
  • Down-Regulation
  • Fibroblasts* / metabolism
  • Fibroblasts* / pathology
  • Forkhead Box Protein O3 / genetics*
  • Forkhead Box Protein O3 / metabolism
  • Gene Knockout Techniques
  • Humans
  • Idiopathic Pulmonary Fibrosis / metabolism*
  • Idiopathic Pulmonary Fibrosis / pathology
  • Idiopathic Pulmonary Fibrosis / therapy
  • Models, Animal
  • Myofibroblasts* / metabolism
  • Myofibroblasts* / pathology
  • Phosphorylation
  • Staurosporine / chemistry
  • Staurosporine / pharmacology

Substances

  • Cytokines
  • Forkhead Box Protein O3
  • FoxO3 protein, mouse
  • Staurosporine