Proinflammatory CD4+ CD45RB(hi) lymphocytes promote mammary and intestinal carcinogenesis in Apc(Min/+) mice

Cancer Res. 2006 Jan 1;66(1):57-61. doi: 10.1158/0008-5472.CAN-05-3445.

Abstract

Cancers of breast and bowel are increasingly frequent in humans. Chronic inflammation is known to be a risk factor for these malignancies, yet cellular and molecular mechanisms linking inflammation and carcinogenesis remain poorly understood. Here, we apply a widely used T-cell transfer paradigm, involving adoptive transfer of proinflammatory CD4+ CD45RB(hi) (T(E)) cells to induce inflammatory bowel disease (IBD) in mice, to investigate roles of inflammation on carcinogenesis in the Apc(Min/+) mouse model of intestinal polyposis. We find that transfer of T(E) cells significantly increases adenoma multiplicity and features of malignancy in recipient Apc(Min/+) mice. Surprisingly, we find that female Apc(Min/+) recipients of T(E) cells also rapidly develop mammary tumors. Both intestinal polyposis and mammary adenocarcinoma are abolished by cotransfer of anti-inflammatory CD4+ CD45RB(lo) regulatory lymphocytes or by neutralization of key proinflammatory cytokine tumor necrosis factor-alpha. Lastly, down-regulation of cyclooxygenase-2 and c-Myc expression is observed coincident with tumor regression. These findings define a novel mouse model of inflammation-driven mammary carcinoma and suggest that epithelial carcinogenesis can be mitigated by anti-inflammatory cells and cytokines known to regulate IBD in humans and mice.

Publication types

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

MeSH terms

  • Adenocarcinoma / genetics
  • Adenocarcinoma / immunology
  • Adenoma / genetics
  • Adenoma / immunology
  • Adoptive Transfer
  • Animals
  • CD4-Positive T-Lymphocytes / immunology*
  • Disease Models, Animal
  • Down-Regulation
  • Epithelial Cells / immunology
  • Epithelial Cells / pathology
  • Female
  • Genes, APC
  • Genes, myc / genetics
  • Inflammatory Bowel Diseases / immunology
  • Intestinal Neoplasms / genetics
  • Intestinal Neoplasms / immunology*
  • Intestinal Polyps / genetics
  • Intestinal Polyps / immunology
  • Leukocyte Common Antigens / immunology*
  • Male
  • Mammary Neoplasms, Experimental / genetics
  • Mammary Neoplasms, Experimental / immunology*
  • Mice
  • Mice, Inbred C57BL
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors
  • Tumor Necrosis Factor-alpha / immunology

Substances

  • Tumor Necrosis Factor-alpha
  • Leukocyte Common Antigens