Perforin deficiency attenuates inflammation and tumor growth in colitis-associated cancer

Inflamm Bowel Dis. 2010 Apr;16(4):559-67. doi: 10.1002/ibd.21107.

Abstract

Background: Patients with inflammatory bowel disease (IBD) have a markedly increased risk to develop colon cancer, but there are only limited data about the host antitumor response in such colitis-associated cancer. In the present study we aimed at assessing the role of perforin-dependent effector mechanisms in the immune response in a murine model of colitis-associated colon cancer.

Methods: Wildtype and perforin-deficient mice were analyzed in a mouse model of colitis-associated colon cancer using azoxymethane (AOM) and dextran sodium sulfate (DSS).

Results: Tumors of wildtype mice showed infiltration of CD4+, CD8+ T cells, natural killer (NK) cells, high numbers of apoptotic cells, and expression of the transcription factor eomesodermin and cytotoxic effector proteins, suggesting a potential role of the antitumor immune response in AOM/DSS tumorigenesis. Furthermore, perforin deficiency resulted in reduced apoptosis of epithelial cells as compared to wildtype mice, whereas tumor infiltration by NK cells, CD8+, and CD4+ T cells was unchanged. However, perforin-deficient mice surprisingly developed significantly fewer tumors than wildtype mice. Subsequent studies identified an important role of perforin in regulating colitis activity, as perforin deficiency caused a significant reduction of DSS colitis activity and proinflammatory cytokine production as compared to wildtype controls.

Conclusions: Perforin is involved in both the antitumor immune response and the regulation of activity of mucosal inflammation in colitis-associated cancer. Our data emphasize the possible consequences for therapeutic strategies targeting colitis-associated colon cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • Chronic Disease
  • Colitis / chemically induced
  • Colitis / metabolism*
  • Colitis / pathology
  • Colonic Neoplasms / etiology
  • Colonic Neoplasms / metabolism*
  • Colonic Neoplasms / pathology*
  • Cytotoxicity, Immunologic
  • Dextran Sulfate / toxicity
  • Disease Models, Animal*
  • Intestinal Mucosa / immunology
  • Killer Cells, Natural / immunology
  • Mice
  • Mice, Inbred C57BL
  • Pore Forming Cytotoxic Proteins / deficiency*
  • Pore Forming Cytotoxic Proteins / physiology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Specific Pathogen-Free Organisms
  • T-Lymphocytes / immunology

Substances

  • Pore Forming Cytotoxic Proteins
  • perforin, mouse
  • Dextran Sulfate