Soluble CEACAM8 interacts with CEACAM1 inhibiting TLR2-triggered immune responses

PLoS One. 2014 Apr 17;9(4):e94106. doi: 10.1371/journal.pone.0094106. eCollection 2014.

Abstract

Lower respiratory tract bacterial infections are characterized by neutrophilic inflammation in the airways. The carcinoembryonic antigen-related cell adhesion molecule (CEACAM) 8 is expressed in and released by human granulocytes. Our study demonstrates that human granulocytes release CEACAM8 in response to bacterial DNA in a TLR9-dependent manner. Individuals with a high percentage of bronchial lavage fluid (BALF) granulocytes were more likely to have detectable levels of released CEACAM8 in the BALF than those with a normal granulocyte count. Soluble, recombinant CEACAM8-Fc binds to CEACAM1 expressed on human airway epithelium. Application of CEACAM8-Fc to CEACAM1-positive human pulmonary epithelial cells resulted in reduced TLR2-dependent inflammatory responses. These inhibitory effects were accompanied by tyrosine phosphorylation of the immunoreceptor tyrosine-based inhibitory motif (ITIM) of CEACAM1 and by recruitment of the phosphatase SHP-1, which could negatively regulate Toll-like receptor 2-dependent activation of the phosphatidylinositol 3-OH kinase-Akt kinase pathway. Our results suggest a new mechanism by which granulocytes reduce pro-inflammatory immune responses in human airways via secretion of CEACAM8 in neutrophil-driven bacterial infections.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD / chemistry*
  • Antigens, CD / metabolism*
  • Bronchi / cytology
  • Bronchi / immunology*
  • Bronchoalveolar Lavage Fluid
  • Cell Adhesion Molecules / chemistry*
  • Cell Adhesion Molecules / metabolism*
  • Cell Count
  • Cell Line
  • Cytochalasin D / pharmacology
  • Epithelial Cells / cytology
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • GPI-Linked Proteins / chemistry
  • GPI-Linked Proteins / metabolism
  • Granulocytes / cytology
  • Granulocytes / drug effects
  • Humans
  • Protein Binding
  • Rats
  • Signal Transduction / drug effects
  • Solubility
  • Toll-Like Receptor 2 / metabolism*
  • Toll-Like Receptor 9 / metabolism

Substances

  • Antigens, CD
  • CD66 antigens
  • CEACAM8 protein, human
  • Cell Adhesion Molecules
  • GPI-Linked Proteins
  • TLR2 protein, human
  • Toll-Like Receptor 2
  • Toll-Like Receptor 9
  • Cytochalasin D

Grants and funding

Supported by the Deutsche Forschungsgemeinschaft (SL 153/1-2), by the International Graduate School (IRTG) GRK1673 and by the Federal Ministry for Education and Science (grant BMBF 03Z2JN22) all to HS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.