Tumor-derived MUC1 mucins interact with differentiating monocytes and induce IL-10highIL-12low regulatory dendritic cell

J Immunol. 2004 Jun 15;172(12):7341-9. doi: 10.4049/jimmunol.172.12.7341.

Abstract

Dendritic cells (DC) initiate immunity by the activation of naive T cells and control immunity through their ability to induce unresponsiveness of lymphocytes by mechanisms that include deletion and induction of regulatory cells. An inadequate presentation to T cells by tumor-induced "regulatory" DC, among several mechanisms, can explain tolerance to tumor-associated Ags. In this study, we show that tumor-derived mucin profoundly affects the cytokine repertoire of monocyte-derived DC and switch them into IL-10(high)IL-12(low) regulatory APCs with a limited capacity to trigger protective Th1 responses. In fact, DC cocultured with pancreatic tumor cell lines in a Transwell system did not reach full maturation, had low immunostimulatory functions, did not produce IL-12, and released high levels of IL-10. The involvement of known tumor-derived immune-suppressive factors (e.g., vascular endothelial growth factor, TGF-beta, IL-6, and IL-10) was considered and excluded. We provide evidence that tumor-derived MUC1 mucins are responsible for the impaired DC maturation and function. DC obtained in the presence of tumor microenvironment preferentially polarized IL-4(+) response. Moreover, T cells primed by these regulatory DC became anergic and behaved as suppressor/regulatory cells. These findings identify mucin secretion as a novel mechanism of tumor escape from immune surveillance and provide the basis for the generation of potentially tolerogenic DC.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigen-Presenting Cells / immunology
  • Cell Differentiation
  • Cell Line, Tumor
  • Clonal Anergy
  • Coculture Techniques
  • Dendritic Cells / cytology
  • Dendritic Cells / immunology*
  • Humans
  • Immunity, Cellular
  • Interleukin-10 / biosynthesis*
  • Interleukin-12 / biosynthesis*
  • Interleukin-4 / biosynthesis
  • Membrane Proteins / metabolism
  • Membrane Proteins / physiology*
  • Monocytes / cytology
  • Pancreatic Neoplasms / metabolism*
  • Pancreatic Neoplasms / pathology
  • T-Lymphocytes / pathology

Substances

  • Membrane Proteins
  • Interleukin-10
  • Interleukin-12
  • Interleukin-4

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