Patient-specific iPSCs carrying an SFTPC mutation reveal the intrinsic alveolar epithelial dysfunction at the inception of interstitial lung disease

Cell Rep. 2021 Aug 31;36(9):109636. doi: 10.1016/j.celrep.2021.109636.

Abstract

Alveolar epithelial type 2 cell (AEC2) dysfunction is implicated in the pathogenesis of adult and pediatric interstitial lung disease (ILD), including idiopathic pulmonary fibrosis (IPF); however, identification of disease-initiating mechanisms has been impeded by inability to access primary AEC2s early on. Here, we present a human in vitro model permitting investigation of epithelial-intrinsic events culminating in AEC2 dysfunction, using patient-specific induced pluripotent stem cells (iPSCs) carrying an AEC2-exclusive disease-associated variant (SFTPCI73T). Comparing syngeneic mutant versus gene-corrected iPSCs after differentiation into AEC2s (iAEC2s), we find that mutant iAEC2s accumulate large amounts of misprocessed and mistrafficked pro-SFTPC protein, similar to in vivo changes, resulting in diminished AEC2 progenitor capacity, perturbed proteostasis, altered bioenergetic programs, time-dependent metabolic reprogramming, and nuclear factor κB (NF-κB) pathway activation. Treatment of SFTPCI73T-expressing iAEC2s with hydroxychloroquine, a medication used in pediatric ILD, aggravates the observed perturbations. Thus, iAEC2s provide a patient-specific preclinical platform for modeling the epithelial-intrinsic dysfunction at ILD inception.

Keywords: NF-κB; autophagy; bioenergetics; iPSC-derived alveolar epithelial type 2 cells; idiopathic pulmonary fibrosis; induced pluripotent stem cells; interstitial lung disease; metabolic reprogramming; proteostasis; surfactant protein C.

Publication types

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

MeSH terms

  • Alveolar Epithelial Cells / metabolism*
  • Alveolar Epithelial Cells / pathology
  • Animals
  • Cell Line
  • Cell Proliferation
  • Energy Metabolism
  • Genetic Predisposition to Disease
  • Humans
  • Induced Pluripotent Stem Cells / metabolism*
  • Induced Pluripotent Stem Cells / pathology
  • Inflammation Mediators / metabolism
  • Lung Diseases, Interstitial / genetics*
  • Lung Diseases, Interstitial / metabolism
  • Lung Diseases, Interstitial / pathology
  • Mice
  • Mice, Knockout
  • Mutation
  • NF-kappa B / metabolism
  • Phenotype
  • Proteostasis
  • Pulmonary Surfactant-Associated Protein C / genetics*
  • Pulmonary Surfactant-Associated Protein C / metabolism
  • Signal Transduction

Substances

  • Inflammation Mediators
  • NF-kappa B
  • Pulmonary Surfactant-Associated Protein C
  • SFTPC protein, human
  • Sftpc protein, mouse