Elevated level of interleukin-35 in colorectal cancer induces conversion of T cells into iTr35 by activating STAT1/STAT3

Oncotarget. 2016 Nov 8;7(45):73003-73015. doi: 10.18632/oncotarget.12193.

Abstract

IL-35 is a novel heterodimeric and inhibitory cytokine, composed of interleukin-12 subunit alpha (P35) and Epstein-Barr virus -induced gene 3 (EBI3). IL-35 has been reported to be produced by a range of cell types, especially regulatory T cells, and to exert immunosuppressive effects via the STATx signaling pathway. In this study, we demonstrated that IL-35 expression was elevated in both serum and tumors in patients with colorectal cancer. IL-35 mainly expressed in CD4+ T cells in human colorectal cancer tumors and adjacent tissues. Increased IL-35 expression in tumor-adjacent tissues was significantly associated with tumor metastasis. IL-35 inhibited the proliferation of CD4+CD25- T effector cells in vitro in a dose-dependent manner, and its suppression was partially reversed by applying IL-35-neutralizing antibodies. IL-35 treatment activated the phosphorylation of both STAT1 and STAT3 in human CD4+ T cells. Meanwhile, IL-35 induced a positive feedback loop to promote its own production. We observed that Tregs obtained from colorectal cancer patients were capable of inducing more IL-35 production. In addition, EBI3 promoter-driven luciferase activity was higher than that of the mock plasmid after IL-35stimulation. Thus, our study indicates that the high level of IL-35 in colorectal cancer promotes the production of IL-35 via STAT1 and STAT3, which suppresses T cell proliferation and may participate in tumor immunotolerance.

Keywords: STAT1; STAT3; colorectal cancer; interleukin-35.

MeSH terms

  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / immunology
  • Colorectal Neoplasms / metabolism*
  • Colorectal Neoplasms / pathology
  • Female
  • Flow Cytometry
  • Gene Expression
  • Humans
  • Interleukins / genetics
  • Interleukins / metabolism*
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology
  • Male
  • Minor Histocompatibility Antigens / genetics
  • Neoplasm Grading
  • Neoplasm Metastasis
  • Neoplasm Staging
  • Promoter Regions, Genetic
  • STAT1 Transcription Factor / metabolism*
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism*
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism*
  • Transcriptional Activation

Substances

  • EBI3 protein, human
  • Interleukins
  • Minor Histocompatibility Antigens
  • STAT1 Transcription Factor
  • STAT3 Transcription Factor
  • interleukin-35, human