Constitutive activation of epithelial TLR4 augments inflammatory responses to mucosal injury and drives colitis-associated tumorigenesis

Inflamm Bowel Dis. 2011 Jul;17(7):1464-73. doi: 10.1002/ibd.21527. Epub 2010 Nov 15.

Abstract

Background: Chronic intestinal inflammation culminates in cancer and a link to Toll-like receptor-4 (TLR4) has been suggested by our observation that TLR4 deficiency prevents colitis-associated neoplasia. In the current study we address the effect of the aberrant activation of epithelial TLR4 on induction of colitis and colitis-associated tumor development. We take a translational approach to address the consequences of increased TLR signaling in the intestinal mucosa.

Methods: Mice transgenic for a constitutively active TLR4 under the intestine-specific villin promoter (villin-TLR4 mice) were treated with dextran sodium sulfate (DSS) for acute colitis and azoxymethane (AOM)-DSS TLR4 expression was analyzed by immunohistochemistry in colonic tissue from patients with ulcerative colitis (UC) and UC-associated cancer. The effect of an antagonist TLR4 antibody (Ab) was tested in prevention of colitis-associated neoplasia in the AOM-DSS model.

Results: Villin-TLR4 mice were highly susceptible to both acute colitis and colitis-associated neoplasia. Villin-TLR4 mice had increased epithelial expression of COX-2 and mucosal PGE₂ production at baseline. Increased severity of colitis in villin-TLR4 mice was characterized by enhanced expression of inflammatory mediators and increased neutrophilic infiltration. In human UC samples, TLR4 expression was upregulated in almost all colitis-associated cancer and progressively increased with grade of dysplasia. As a proof of principle, a TLR4/MD-2 antagonist antibody inhibited colitis-associated neoplasia in the mouse model.

Conclusions: Our results show that regulation of TLRs can affect the outcome of both acute colitis and its consequences, cancer. Targeting TLR4 and other TLRs may ultimately play a role in prevention or treatment of colitis-associated cancer.

Publication types

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

MeSH terms

  • Animals
  • Azoxymethane / toxicity
  • Blotting, Western
  • Carcinogens / toxicity
  • Colitis, Ulcerative / chemically induced
  • Colitis, Ulcerative / complications*
  • Colonic Neoplasms / etiology*
  • Colonic Neoplasms / metabolism
  • Dextran Sulfate / toxicity
  • Enzyme-Linked Immunosorbent Assay
  • Humans
  • Immunoenzyme Techniques
  • Inflammation / complications*
  • Inflammation / immunology
  • Inflammation / pathology
  • Inflammation Mediators / metabolism
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / injuries
  • Intestinal Mucosa / pathology*
  • Mice
  • Mice, Transgenic
  • Microfilament Proteins / genetics
  • Promoter Regions, Genetic / genetics
  • RNA, Messenger / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / metabolism*
  • Toll-Like Receptor 4 / physiology*

Substances

  • Carcinogens
  • Inflammation Mediators
  • Microfilament Proteins
  • RNA, Messenger
  • TLR4 protein, human
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • villin
  • Dextran Sulfate
  • Azoxymethane