CD148 Deficiency in Fibroblasts Promotes the Development of Pulmonary Fibrosis

Am J Respir Crit Care Med. 2021 Aug 1;204(3):312-325. doi: 10.1164/rccm.202008-3100OC.

Abstract

Rationale: CD148/PTRJ (receptor-like protein tyrosine phosphatase η) exerts antifibrotic effects in experimental pulmonary fibrosis via interactions with its ligand syndecan-2; however, the role of CD148 in human pulmonary fibrosis remains incompletely characterized.Objectives: We investigated the role of CD148 in the profibrotic phenotype of fibroblasts in idiopathic pulmonary fibrosis (IPF).Methods: Conditional CD148 fibroblast-specific knockout mice were generated and exposed to bleomycin and then assessed for pulmonary fibrosis. Lung fibroblasts (mouse lung and human IPF lung), and precision-cut lung slices from human patients with IPF were isolated and subjected to experimental treatments. A CD148-activating 18-aa mimetic peptide (SDC2-pep) derived from syndecan-2 was evaluated for its therapeutic potential.Measurements and Main Results: CD148 expression was downregulated in IPF lungs and fibroblasts. In human IPF lung fibroblasts, silencing of CD148 increased extracellular matrix production and resistance to apoptosis, whereas overexpression of CD148 reversed the profibrotic phenotype. CD148 fibroblast-specific knockout mice displayed increased pulmonary fibrosis after bleomycin challenge compared with control mice. CD148-deficient fibroblasts exhibited hyperactivated PI3K/Akt/mTOR signaling, reduced autophagy, and increased p62 accumulation, which induced NF-κB activation and profibrotic gene expression. SDC2-pep reduced pulmonary fibrosis in vivo and inhibited IPF-derived fibroblast activation. In precision-cut lung slices from patients with IPF and control patients, SDC2-pep attenuated profibrotic gene expression in IPF and normal lungs stimulated with profibrotic stimuli.Conclusions: Lung fibroblast CD148 activation reduces p62 accumulation, which exerts antifibrotic effects by inhibiting NF-κB-mediated profibrotic gene expression. Targeting the CD148 phosphatase with activating ligands such as SDC2-pep may represent a potential therapeutic strategy in IPF.

Keywords: CD148; fibroblast; idiopathic pulmonary fibrosis; nuclear factor-kappa-B; syndecan-2.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antibiotics, Antineoplastic / toxicity
  • Autophagy / drug effects
  • Autophagy / genetics
  • Bleomycin / toxicity
  • Disease Models, Animal
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism*
  • Fibroblasts / pathology
  • Humans
  • Idiopathic Pulmonary Fibrosis / genetics*
  • Idiopathic Pulmonary Fibrosis / metabolism
  • Idiopathic Pulmonary Fibrosis / pathology
  • In Vitro Techniques
  • Lung / drug effects
  • Lung / metabolism*
  • Lung / pathology
  • Mice
  • Mice, Knockout
  • NF-kappa B / drug effects
  • NF-kappa B / metabolism
  • Peptide Fragments / pharmacology
  • Phenotype
  • Phosphatidylinositol 3-Kinases / drug effects
  • Phosphatidylinositol 3-Kinases / metabolism
  • Primary Cell Culture
  • Proto-Oncogene Proteins c-akt / drug effects
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptor-Like Protein Tyrosine Phosphatases, Class 3 / genetics
  • Receptor-Like Protein Tyrosine Phosphatases, Class 3 / metabolism
  • Signal Transduction
  • Syndecan-2 / pharmacology
  • TOR Serine-Threonine Kinases / drug effects
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • Antibiotics, Antineoplastic
  • NF-kappa B
  • Peptide Fragments
  • Bleomycin
  • Syndecan-2
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases
  • PTPRJ protein, human
  • Ptprj protein, mouse
  • Receptor-Like Protein Tyrosine Phosphatases, Class 3