Yasuma Keiko, Yasunaga Jun-ichirou, Takemoto Keiko, Sugata Kenji, Mitobe Yuichi, Takenouchi Norihiro, Nakagawa Masanori, Suzuki Yutaka, Matsuoka Masao
Laboratory of Virus Control, Institute for Virus Research, Kyoto University, Sakyo-ku, Kyoto, Japan.
Laboratory of Biological Protection, Institute for Virus Research, Kyoto University, Sakyo-ku, Kyoto, Japan.
PLoS Pathog. 2016 Jan 6;12(1):e1005372. doi: 10.1371/journal.ppat.1005372. eCollection 2016 Jan.
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.
人类嗜T细胞病毒1型(HTLV-1)感染CD4+ T细胞,并在体内诱导受感染细胞增殖,这导致一些受感染个体发生成人T细胞白血病(ATL)。HTLV-1 bZIP因子(HBZ)基因编码于HTLV-1的负链中,在发病机制中起关键作用。在本研究中,使用HBZ转导的T细胞进行的RNA测序和染色质免疫沉淀测序分析显示,HBZ除了上调调节性T细胞相关基因Foxp3和Ccr4的表达及启动子乙酰化水平外,还上调共抑制分子T细胞免疫球蛋白和免疫酪氨酸抑制基序(TIGIT)的表达。TIGIT在HBZ转基因(HBZ-Tg)小鼠的CD4+ T细胞上表达,并在体内ATL细胞以及HTLV-1相关脊髓病/热带痉挛性截瘫(HAM/TSP)患者的HTLV-1感染CD4+ T细胞上表达。与TIGIT-CD4+ T细胞相比,HBZ-Tg小鼠的TIGIT+CD4+细胞中Blimp1和IL-10的表达上调,这表明TIGIT表达与IL-10产生之间存在相关性。当用TIGIT的配体CD155刺激HBZ-Tg小鼠的CD4+ T细胞时,它们抑制性细胞因子IL-10的产生增强。此外,HBZ-Tg小鼠的树突状细胞在刺激后产生高水平的IL-10。这些数据表明,HBZ通过TIGIT和IL-10将免疫系统改变为抑制状态。重要的是,TIGIT在体外抑制T细胞对另一种HTLV-1病毒蛋白Tax的反应。在一些HAM/TSP患者中,阻断TIGIT和程序性死亡受体1(PD-1)可略微增加抗Tax T细胞活性。这些结果表明,HTLV-1感染细胞上由HBZ诱导的TIGIT损害T细胞对病毒抗原的反应。本研究表明,HBZ诱导的TIGIT在减弱宿主免疫反应和形成有利于HTLV-1的微环境中起关键作用。