Enterobacteria-secreted particles induce production of exosome-like S1P-containing particles by intestinal epithelium to drive Th17-mediated tumorigenesis

Nat Commun. 2015 Apr 24:6:6956. doi: 10.1038/ncomms7956.

Abstract

Gut-associated inflammation plays a crucial role in the progression of colon cancer. Here, we identify a novel pathogen-host interaction that promotes gut inflammation and the development of colon cancer. We find that enteropathogenic bacteria-secreted particles (ET-BSPs) stimulate intestinal epithelium to produce IDENs (intestinal mucosa-derived exosome-like nanoparticles) containing elevated levels of sphingosine-1-phosphate, CCL20 and prostaglandin E2 (PGE2). CCL20 and PGE2 are required for the recruitment and proliferation, respectively, of Th17 cells, and these processes also involve the MyD88-mediated pathway. By influencing the recruitment and proliferation of Th17 cells in the intestine, IDENs promote colon cancer. We demonstrate the biological effect of sphingosine-1-phosphate contained in IDENs on tumour growth in spontaneous and transplanted colon cancer mouse models. These findings provide deeper insights into how host-microbe relationships are mediated by particles secreted from both bacterial and host cells.

Publication types

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

MeSH terms

  • Adenocarcinoma / etiology
  • Adenocarcinoma / immunology*
  • Adenocarcinoma / pathology
  • Animals
  • Azoxymethane / toxicity
  • Bacteroides fragilis / immunology*
  • Bacteroides fragilis / metabolism
  • Blotting, Western
  • Carcinogenesis / immunology*
  • Carcinogens / toxicity
  • Cell Line, Tumor
  • Cell Proliferation
  • Chemokine CCL20 / genetics
  • Chemokine CCL20 / immunology
  • Colitis / chemically induced
  • Colitis / complications
  • Colitis / immunology*
  • Colonic Neoplasms / etiology
  • Colonic Neoplasms / immunology*
  • Colonic Neoplasms / pathology
  • Dextran Sulfate / toxicity
  • Dinoprostone / genetics
  • Dinoprostone / immunology
  • Disease Models, Animal
  • Enterobacteriaceae / immunology*
  • Enterobacteriaceae / metabolism
  • Exosomes / immunology*
  • Immunohistochemistry
  • In Situ Hybridization, Fluorescence
  • Inflammation
  • Intestinal Mucosa / immunology*
  • Lysophospholipids / immunology*
  • Mice
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / immunology
  • Nanoparticles
  • Neoplasm Transplantation
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sphingosine / analogs & derivatives*
  • Sphingosine / immunology
  • Th17 Cells / immunology*

Substances

  • CCL20 protein, mouse
  • Carcinogens
  • Chemokine CCL20
  • Lysophospholipids
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • sphingosine 1-phosphate
  • Dextran Sulfate
  • Dinoprostone
  • Azoxymethane
  • Sphingosine