Department of Pathology, Tohoku University School of Medicine, Miyagi, Japan.
Department of Respiratory Medicine, Sendai Kousei Hospital, Miyagi, Japan.
Cancer Med. 2021 Jan;10(2):718-727. doi: 10.1002/cam4.3639. Epub 2020 Dec 11.
Immunotherapy is considered one of the most important therapeutic strategies for patients with lung adenocarcinoma after the development of epidermal growth factor receptor tyrosine kinase inhibitor (EGFR-TKI) resistance. However, useful predictors of immunotherapy for these patients has not been examined well, although the status of the tumor immune microenvironment (TIME), including programmed death-ligand 1 expression and lymphocyte infiltration, has been generally known to provide predictive markers for the efficacy of immunotherapy. This study aimed to clarify novel predictors of immunotherapy following EGFR-TKI resistance in lung adenocarcinoma, especially regarding micro RNA (miRNA). We evaluated the correlation between EGFR-TKI resistance and lymphocyte infiltration, before and after acquiring EGFR-TKI resistance, in 21 cases of lung adenocarcinoma, and further explored this by in vitro studies, using miRNA PCR arrays. Subsequently, we transfected miRNA-1 (miR-1), the most variable miRNA in this array, into three kinds of lung cancer cells, and examined the effects of miR-1 on EGFR-TKI sensitivity, cytokine expression and lymphocyte migration. Histopathological examination demonstrated that infiltration levels of CD8-positive T cells were significantly decreased after development of EGFR-TKI resistance. In vitro studies revealed that miR-1 significantly inhibited EGFR-TKI effect and induction of cytokines, such as C-C motif chemokine ligand 5 and C-X-C motif chemokine ligand 10, causing inhibition of monocyte migration. These results indicate that the upregulated miR-1 might suppress the TIME, following development of EGFR-TKI resistance. Therefore, miR-1 could be a clinically useful marker to predict therapeutic efficacy of immunotherapy in lung adenocarcinoma patients with EGFR-TKI resistance.
免疫疗法被认为是 EGFR-TKI 耐药后肺腺癌患者最重要的治疗策略之一。然而,尽管肿瘤免疫微环境(TIME)的状态,包括程序性死亡配体 1 表达和淋巴细胞浸润,通常被认为是免疫治疗疗效的预测标志物,但对于这些患者的免疫治疗有用预测因子尚未得到很好的研究。本研究旨在阐明 EGFR-TKI 耐药后肺腺癌免疫治疗的新预测因子,特别是微 RNA(miRNA)。我们评估了 21 例肺腺癌在获得 EGFR-TKI 耐药前后 EGFR-TKI 耐药与淋巴细胞浸润之间的相关性,并通过 miRNA PCR 阵列进行了体外研究进一步探讨了这一点。随后,我们将 miRNA-1(miR-1)转染到三种肺癌细胞中,该 miRNA 在该阵列中变化最大,并检查了 miR-1 对 EGFR-TKI 敏感性、细胞因子表达和淋巴细胞迁移的影响。组织病理学检查表明,EGFR-TKI 耐药后 CD8 阳性 T 细胞浸润水平显著降低。体外研究表明,miR-1 显著抑制了 EGFR-TKI 效应和细胞因子的诱导,如 C-C 基序趋化因子配体 5 和 C-X-C 基序趋化因子配体 10,导致单核细胞迁移受到抑制。这些结果表明,上调的 miR-1 可能抑制 EGFR-TKI 耐药后 TIME。因此,miR-1 可能是预测 EGFR-TKI 耐药的肺腺癌患者免疫治疗疗效的一种有临床意义的标志物。