Leukemia inhibitory factor (LIF) receptor amplifies pathogenic activation of fibroblasts in lung fibrosis

Proc Natl Acad Sci U S A. 2024 Dec 10;121(50):e2401899121. doi: 10.1073/pnas.2401899121. Epub 2024 Dec 5.

Abstract

Fibrosis drives end-organ damage in many diseases. However, clinical trials targeting individual upstream activators of fibroblasts, such as TGFβ, have largely failed. Here, we target the leukemia inhibitory factor receptor (LIFR) as an "autocrine master amplifier" of multiple upstream activators of lung fibroblasts. In idiopathic pulmonary fibrosis (IPF), the most common fibrotic lung disease, we found that lung myofibroblasts had high LIF expression, and the fibroblasts in fibroblastic foci coexpressed LIF and LIFR. In IPF, fibroblastic foci are the "leading edge" of fibrosis and a key site of disease pathogenesis. TGFβ1, one of the principal drivers of fibrosis, up-regulated LIF expression in IPF fibroblasts. We found that TGFβ1, IL-4, and IL-13 stimulations of fibroblasts require the LIF-LIFR axis to evoke a strong fibrogenic effector response in fibroblasts. In vitro antibody blockade of LIFR on IPF lung fibroblasts reduced the induction of profibrotic genes after TGFβ1 stimulation. Silencing LIF and LIFR reduced profibrotic fibroblast activation following TGFβ1, IL-4, and IL-13 stimulations. We also demonstrated that LIFR amplified profibrotic stimuli in precision-cut lung slices from IPF patients. These LIFR signals were transduced via JAK2, and STAT1 in IPF lung fibroblasts. Together, we find that LIFR drives an autocrine circuit that amplifies and sustains pathogenic activation of IPF fibroblasts. Targeting a single, downstream master amplifier on fibroblasts, like LIFR, is an alternative therapeutic strategy that simultaneously attenuates the profibrotic effects of multiple upstream stimuli.

Keywords: autocrine communication; fibroblasts; leukemia inhibitory factor; pulmonary fibrosis; receptors OSM-LIF.

MeSH terms

  • Fibroblasts* / metabolism
  • Fibroblasts* / pathology
  • Humans
  • Idiopathic Pulmonary Fibrosis* / metabolism
  • Idiopathic Pulmonary Fibrosis* / pathology
  • Interleukin-13* / metabolism
  • Interleukin-4 / metabolism
  • Janus Kinase 2 / metabolism
  • Leukemia Inhibitory Factor Receptor alpha Subunit / genetics
  • Leukemia Inhibitory Factor Receptor alpha Subunit / metabolism
  • Leukemia Inhibitory Factor* / metabolism
  • Lung* / metabolism
  • Lung* / pathology
  • Myofibroblasts / metabolism
  • Myofibroblasts / pathology
  • Signal Transduction
  • Transforming Growth Factor beta1* / metabolism

Substances

  • Leukemia Inhibitory Factor
  • Transforming Growth Factor beta1
  • LIF protein, human
  • Interleukin-13
  • Interleukin-4
  • LIFR protein, human
  • Leukemia Inhibitory Factor Receptor alpha Subunit
  • Janus Kinase 2
  • TGFB1 protein, human
  • IL4 protein, human
  • IL13 protein, human
  • JAK2 protein, human