CXCR3+ T regulatory cells selectively accumulate in human ovarian carcinomas to limit type I immunity

Cancer Res. 2012 Sep 1;72(17):4351-60. doi: 10.1158/0008-5472.CAN-12-0579. Epub 2012 Jul 12.

Abstract

Antitumor type I T-cell responses involving IFN-γ production are critical to control cancer, but the efficacy of this response is limited by a variety of immunosuppressive mechanisms that promote tumoral immune escape. One critical mechanism involves the accumulation of FOXP3(+) T regulatory cells (Treg), a class of suppressive T cells that prevent excessive tissue destruction caused by unchecked immune responses. Recent studies have revealed that FOXP3(+) Treg include distinct subsets specifically controlling over the corresponding effector subset. In particular, CXCR3(+) Treg have been described as a subset specialized in the control of type I T-cell responses in vivo. Here, we show that CXCR3(+) Treg are highly enriched in human ovarian carcinomas, particularly in solid tumor masses, where they represent the majority of Treg. Tumor-associated CXCR3(+.) Treg coexpress T-bet but do not secrete IFN-γ ex vivo and suppress proliferation and IFN-γ secretion of T effectors. In addition, they coexpress Helios, suggesting that they originate from natural Treg. Finally, we show that the proportion of CXCR3(+) Treg at tumor sites is directly correlated with that of CXCR3(+) T effectors, consistent with expression of CXCR3 ligands. Together, our findings support the concept that natural CXCR3(+) T-bet(+) Treg selectively accumulate in ovarian tumors to control type I T-cell responses, resulting in the collateral limitation of efficient antitumor immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carcinoma / immunology*
  • Carcinoma / metabolism
  • Cell Line, Tumor
  • Female
  • Humans
  • Ikaros Transcription Factor / genetics
  • Ikaros Transcription Factor / metabolism
  • Interferon-gamma / metabolism
  • Ligands
  • Lymphocyte Activation / immunology
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Ovarian Neoplasms / immunology*
  • Ovarian Neoplasms / metabolism
  • Receptors, CXCR3 / metabolism*
  • T-Box Domain Proteins / genetics
  • T-Box Domain Proteins / metabolism
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism*
  • Th1 Cells / immunology
  • Th1 Cells / metabolism

Substances

  • IKZF2 protein, human
  • Ligands
  • Receptors, CXCR3
  • T-Box Domain Proteins
  • T-box transcription factor TBX21
  • Ikaros Transcription Factor
  • Interferon-gamma