Eliminating roles for T-bet and IL-2 but revealing superior activation and proliferation as mechanisms underpinning dominance of regulatory T cells in tumors

Oncotarget. 2015 Sep 22;6(28):24649-59. doi: 10.18632/oncotarget.5584.

Abstract

Foxp3(+) regulatory T cells (Tregs) are often highly enriched within the tumor-infiltrating T cell pool. Using a well-characterised model of carcinogen-induced fibrosarcomas we show that the enriched tumor-infiltrating Treg population comprises largely of CXCR3(+) T-bet(+) 'TH1-like' Tregs which are thymus-derived Helios(+) cells. Whilst IL-2 maintains homeostatic ratios of Tregs in lymphoid organs, we found that the perturbation in Treg frequencies in tumors is IL-2 independent. Moreover, we show that the TH1 phenotype of tumor-infiltrating Tregs is dispensable for their ability to influence tumor progression. We did however find that unlike Tconvs, the majority of intra-tumoral Tregs express the activation markers CD69, CD25, ICOS, CD103 and CTLA4 and are significantly more proliferative than Tconvs. Moreover, we have found that CD69(+) Tregs are more suppressive than their CD69- counterparts. Collectively, these data indicate superior activation of Tregs in the tumor microenvironment, promoting their suppressive ability and selective proliferation at this site.

Keywords: CD69; Immune response; Immunity; Immunology Section; T-bet; Treg; cancer; proliferation.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal / pharmacology
  • Biomarkers, Tumor / immunology
  • Biomarkers, Tumor / metabolism
  • Cell Proliferation* / drug effects
  • Cells, Cultured
  • Fibrosarcoma / chemically induced
  • Fibrosarcoma / genetics
  • Fibrosarcoma / immunology
  • Fibrosarcoma / metabolism*
  • Forkhead Transcription Factors / genetics
  • Forkhead Transcription Factors / metabolism
  • Inflammation Mediators / immunology
  • Inflammation Mediators / metabolism
  • Interleukin-2 / antagonists & inhibitors
  • Interleukin-2 / immunology
  • Interleukin-2 / metabolism*
  • Lymphocyte Activation* / drug effects
  • Lymphocytes, Tumor-Infiltrating / drug effects
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Lymphocytes, Tumor-Infiltrating / metabolism*
  • Methylcholanthrene
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Phenotype
  • Sarcoma, Experimental / chemically induced
  • Sarcoma, Experimental / genetics
  • Sarcoma, Experimental / immunology
  • Sarcoma, Experimental / metabolism*
  • Signal Transduction
  • T-Box Domain Proteins / deficiency
  • T-Box Domain Proteins / genetics
  • T-Box Domain Proteins / metabolism*
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism*
  • Th1 Cells / immunology
  • Th1 Cells / metabolism
  • Tumor Microenvironment

Substances

  • Antibodies, Monoclonal
  • Biomarkers, Tumor
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Inflammation Mediators
  • Interleukin-2
  • T-Box Domain Proteins
  • T-box transcription factor TBX21
  • Methylcholanthrene