Department of General Thoracic Surgery, Kawasaki Medical School, Kurashiki, Japan.
Division of Thoracic Surgery, National Hospital Organization Yamaguchi Ube Medical Center, Ube, Japan.
Thorac Cancer. 2021 Mar;12(6):775-782. doi: 10.1111/1759-7714.13847. Epub 2021 Jan 24.
Immune checkpoint inhibitors targeting the programmed cell death-1 (PD-1)/PD-1 ligand 1 (PD-L1) axis have shown promising results in patients with nonsmall cell lung cancer (NSCLC). One major PD-L1 inducer is IFNγ, which is secreted by T cells and NK cells. Importantly, IFNγ-induced PD-L1 is one of the major mechanisms by which cancer cells escape host immunity.
Here, we found that the NSCLC cell line, LC-2/ad, has a unique character; the PD-L1 expression in these cells is up-regulated by both IFNγ and epidermal growth factor (EGF).
Comparative analysis of the cell signaling pathway showed that IFNγ activates STAT1 signaling, while EGF activates AKT, MAPK, and ribosomal protein S6 kinase in LC-2/ad cells. IFNγ-induced PD-L1, but not EGF-induced PD-L1, was clearly blocked by the JAK-STAT inhibitor tofacitinib. Interestingly, IFNγ decreased the expression of NK cell-activating ligands while increasing the expression of MHC class I molecules, resulting in a phenotype that can easily escape from NK cells, theoretically. Finally, we showed that IFNγ stimuli attenuated NK cell-mediated cytotoxicity in LC-2/ad cells, which was, however, blocked by tofacitinib.
Taken together, our study shows that tofacitinib blocks the IFNγ-induced transformation from an NK cell-sensitive phenotype to an NK cell-resistant one in IFNγ-reacted LC-2/ad cells, thereby implicating that tofacitinib may be a promising agent to overcome IFNγ-induced tumor immune escape, although it may be adapted to the limited number of NSCLC patients.
针对程序性细胞死亡蛋白-1(PD-1)/PD-1 配体 1(PD-L1)轴的免疫检查点抑制剂在非小细胞肺癌(NSCLC)患者中显示出了有前景的结果。IFNγ是 PD-L1 的主要诱导剂之一,由 T 细胞和 NK 细胞分泌。重要的是,IFNγ诱导的 PD-L1 是癌细胞逃避宿主免疫的主要机制之一。
在这里,我们发现 NSCLC 细胞系 LC-2/ad 具有独特的特征;这些细胞中的 PD-L1 表达受 IFNγ和表皮生长因子(EGF)的上调。
细胞信号通路的比较分析表明,IFNγ激活 STAT1 信号通路,而 EGF 在 LC-2/ad 细胞中激活 AKT、MAPK 和核糖体蛋白 S6 激酶。IFNγ诱导的 PD-L1,但不是 EGF 诱导的 PD-L1,被 JAK-STAT 抑制剂托法替尼明显阻断。有趣的是,IFNγ降低了 NK 细胞激活配体的表达,同时增加了 MHC Ⅰ类分子的表达,从而在理论上产生了一种易于逃避 NK 细胞的表型。最后,我们表明 IFNγ 刺激减弱了 LC-2/ad 细胞中 NK 细胞介导的细胞毒性,而托法替尼则阻断了这种作用。
总之,我们的研究表明,托法替尼阻断了 IFNγ 反应性 LC-2/ad 细胞中 IFNγ 诱导的从 NK 细胞敏感表型向 NK 细胞抗性表型的转化,从而暗示托法替尼可能是克服 IFNγ 诱导的肿瘤免疫逃逸的一种有前途的药物,尽管它可能适用于少数 NSCLC 患者。