A nonaggregating surfactant protein C mutant is misdirected to early endosomes and disrupts phospholipid recycling

Traffic. 2011 Sep;12(9):1196-210. doi: 10.1111/j.1600-0854.2011.01223.x. Epub 2011 Jun 28.

Abstract

Interstitial lung disease in both children and adults has been linked to mutations in the lung-specific surfactant protein C (SFTPC) gene. Among these, the missense mutation [isoleucine to threonine at codon 73 = human surfactant protein C (hSP-C(I73T) )] accounts for ∼30% of all described SFTPC mutations. We reported previously that unlike the BRICHOS misfolding SFTPC mutants, expression of hSP-C(I73T) induces lung remodeling and alveolar lipoproteinosis without a substantial Endoplasmic Reticulum (ER) stress response or ER-mediated intrinsic apoptosis. We show here that, in contrast to its wild-type counterpart that is directly routed to lysosomal-like organelles for processing, SP-C(I73T) is misdirected to the plasma membrane and subsequently internalized to the endocytic pathway via early endosomes, leading to the accumulation of abnormally processed proSP-C isoforms. Functionally, cells expressing hSP-C(I73T) demonstrated both impaired uptake and degradation of surfactant phospholipid, thus providing a molecular mechanism for the observed lipid accumulation in patients expressing hSP-C(I73T) through the disruption of normal phospholipid recycling. Our data provide evidence for a novel cellular mechanism for conformational protein-associated diseases and suggest a paradigm for mistargeted proteins involved in the disruption of the endosomal/lysosomal sorting machinery.

Publication types

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

MeSH terms

  • Adult
  • Cell Membrane / metabolism
  • Cells, Cultured
  • Child
  • Endocytosis / physiology
  • Endoplasmic Reticulum / metabolism
  • Endosomes / chemistry
  • Endosomes / metabolism*
  • Humans
  • Lung Diseases, Interstitial / genetics*
  • Lung Diseases, Interstitial / pathology
  • Lung Diseases, Interstitial / physiopathology
  • Lysosomes / metabolism
  • Mutation*
  • Phospholipids / metabolism*
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • Protein Precursors / genetics
  • Protein Precursors / metabolism
  • Protein Transport / physiology
  • Pulmonary Surfactant-Associated Protein C / genetics*
  • Pulmonary Surfactant-Associated Protein C / metabolism*
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Transferrin / metabolism
  • Transport Vesicles / metabolism

Substances

  • Phospholipids
  • Protein Isoforms
  • Protein Precursors
  • Pulmonary Surfactant-Associated Protein C
  • Recombinant Fusion Proteins
  • Transferrin