HTLV-1 bZIP Factor Impairs Anti-viral Immunity by Inducing Co-inhibitory Molecule, T Cell Immunoglobulin and ITIM Domain (TIGIT)

PLoS Pathog. 2016 Jan 6;12(1):e1005372. doi: 10.1371/journal.ppat.1005372. eCollection 2016 Jan.

Abstract

Human T-cell leukemia virus type 1 (HTLV-1) infects CD4+ T cells and induces proliferation of infected cells in vivo, which leads to the onset of adult T-cell leukemia (ATL) in some infected individuals. The HTLV-1 bZIP factor (HBZ) gene, which is encoded in the minus strand of HTLV-1, plays critical roles in pathogenesis. In this study, RNA-seq and ChIP-seq analyses using HBZ transduced T cells revealed that HBZ upregulates the expression and promoter acetylation levels of a co-inhibitory molecule, T cell immunoglobulin and ITIM domain (TIGIT), in addition to those of regulatory T cells related genes, Foxp3 and Ccr4. TIGIT was expressed on CD4+ T cells from HBZ-transgenic (HBZ-Tg) mice, and on ATL cells and HTLV-1 infected CD4+ T cells of HTLV-1-associated myelopathy/tropical spastic paraparesis (HAM/TSP) in vivo. Expression of Blimp1 and IL-10 was upregulated in TIGIT+CD4+ cells of HBZ-Tg mice compared with TIGIT-CD4+ T cells, suggesting the correlation between TIGIT expression and IL-10 production. When CD4+ T cells from HBZ-Tg mice were stimulated with TIGIT's ligand, CD155, their production of the inhibitory cytokine IL-10 was enhanced. Furthermore, dendritic cells from HBZ-Tg mice produced high levels of IL-10 after stimulation. These data suggest that HBZ alters immune system to suppressive state via TIGIT and IL-10. Importantly, TIGIT suppressed T-cell responses to another HTLV-1 virus protein, Tax, in vitro. Blocking of TIGIT and PD-1 slightly increased anti-Tax T-cell activity in some HAM/TSP patients. These results suggest that HBZ-induced TIGIT on HTLV-1 infected cells impairs T-cell responses to viral antigens. This study shows that HBZ-induced TIGIT plays a pivotal role in attenuating host immune responses and shaping a microenvironment favorable to HTLV-1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic-Leucine Zipper Transcription Factors / immunology*
  • CD4-Positive T-Lymphocytes / immunology
  • Chromatin Immunoprecipitation
  • Enzyme-Linked Immunosorbent Assay
  • Flow Cytometry
  • Gene Expression Regulation, Viral / immunology
  • Human T-lymphotropic virus 1 / immunology*
  • Humans
  • Immune Evasion / immunology*
  • Leukemia-Lymphoma, Adult T-Cell / virology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Oligonucleotide Array Sequence Analysis
  • Receptors, Immunologic / immunology*

Substances

  • Basic-Leucine Zipper Transcription Factors
  • Receptors, Immunologic
  • T cell Ig and ITIM domain protein, mouse
  • TIGIT protein, human

Grants and funding

This study was supported by grants from the Ministry of Education, Science, Sports, and Culture of Japan to MM (22114003) and JiY (26460554), and by JSPS KAKENHI to KY (14J03189), and MEXT KAKENHI (221S0002) for high-throughput sequencing. This study was performed as a research program of the Project for Development of Innovative Research on Cancer Therapeutics (P-DIRECT), Ministry of Education, Culture, Sports, Science and Technology of Japan (to JiY). This study was also supported in part by the JSPS Core-to-Core Program A, Advanced Research Networks. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.