The atypical chemokine receptor D6 suppresses the development of chemically induced skin tumors

J Clin Invest. 2007 Jul;117(7):1884-92. doi: 10.1172/JCI30068.

Abstract

A subset of CC chemokines, acting through CC chemokine receptors (CCRs) 1 to 5, is instrumental in shaping inflammatory responses. Recently, we and others have demonstrated that the atypical chemokine receptor D6 actively sequesters and destroys many of these proinflammatory CC chemokines. This is critical for effective resolution of inflammation in vivo. Inflammation can be protumorigenic, and proinflammatory CC chemokines have been linked with various aspects of cancer biology, yet there is scant evidence supporting a critical role for these molecules in de novo tumor formation. Here, we show that D6-deficient mice have increased susceptibility to cutaneous tumor development in response to chemical carcinogenesis protocols and, remarkably, that D6 deletion is sufficient to make resistant mouse strains susceptible to invasive squamous cell carcinoma. Conversely, transgenic D6 expression in keratinocytes dampens cutaneous inflammation and can confer considerable protection from tumor formation in susceptible backgrounds. Tumor susceptibility consistently correlated with the level of recruitment of T cells and mast cells, cell types known to support the development of skin tumors in mice. These data demonstrate the importance of proinflammatory CC chemokines in de novo tumorigenesis and reveal chemokine sequestration by D6 to be a novel and effective method of tumor suppression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chemokine Receptor D6
  • Disease Susceptibility
  • Disease-Free Survival
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Inflammation / chemically induced
  • Inflammation / pathology
  • Keratinocytes / metabolism
  • Mice
  • Mice, Transgenic
  • Neoplasm Invasiveness / pathology
  • Papilloma / genetics
  • Papilloma / metabolism
  • Papilloma / pathology
  • Receptors, CCR10
  • Receptors, Chemokine / deficiency
  • Receptors, Chemokine / genetics
  • Receptors, Chemokine / metabolism*
  • Skin Neoplasms / chemically induced
  • Skin Neoplasms / genetics
  • Skin Neoplasms / metabolism*
  • Skin Neoplasms / pathology*
  • Tetradecanoylphorbol Acetate / pharmacology
  • Time Factors

Substances

  • Receptors, CCR10
  • Receptors, Chemokine
  • Tetradecanoylphorbol Acetate