β1-Integrin Accumulates in Cystic Fibrosis Luminal Airway Epithelial Membranes and Decreases Sphingosine, Promoting Bacterial Infections

Cell Host Microbe. 2017 Jun 14;21(6):707-718.e8. doi: 10.1016/j.chom.2017.05.001. Epub 2017 May 25.

Abstract

Chronic pulmonary colonization with bacterial pathogens, particularly Pseudomonas aeruginosa, is the primary cause of morbidity and mortality in patients with cystic fibrosis (CF). We observed that β1-integrins accumulate on the luminal membrane of upper-airway epithelial cells from mice and humans with CF. β1-integrin accumulation is due to increased ceramide and the formation of ceramide platforms that trap β1-integrins on the luminal pole of bronchial epithelial cells. β1-integrins downregulate acid ceramidase expression, resulting in further accumulation of ceramide and consequent reduction of surface sphingosine, a lipid that kills bacteria. Interrupting this vicious cycle by triggering surface β1-integrin internalization via anti-β1-integrin antibodies or the RGD peptide ligand-or by genetic or pharmacological correction of ceramide levels-normalizes β1-integrin distribution and sphingosine levels in CF epithelial cells and prevents P. aeruginosa infection in CF mice. These findings suggest a therapeutic avenue to ameliorate CF-associated bacterial infections.

Keywords: Cystic fibrosis; Pseudomonas aeruginosa; acid ceramidase; ceramide; epithelial cells; integrin; membrane domains; pneumonia; receptor clustering; sphingosine.

MeSH terms

  • Acid Ceramidase / metabolism
  • Animals
  • Bacterial Infections / complications*
  • Cell Membrane / metabolism
  • Ceramides / metabolism
  • Cystic Fibrosis / complications*
  • Cystic Fibrosis / metabolism*
  • Cystic Fibrosis / microbiology
  • Epithelial Cells / microbiology
  • Female
  • Humans
  • Integrin beta1 / metabolism*
  • Lung / metabolism
  • Lung / microbiology
  • Male
  • Mice
  • Pseudomonas Infections / complications
  • Pseudomonas Infections / microbiology
  • Pseudomonas Infections / prevention & control
  • Pseudomonas aeruginosa / pathogenicity
  • Sphingosine / metabolism*
  • Sphingosine / pharmacology

Substances

  • Ceramides
  • Integrin beta1
  • ASAH1 protein, human
  • Acid Ceramidase
  • Sphingosine