Kotani Hiroshi, Yamano Tomoyoshi, Boucher Justin C, Sato Shigeki, Sakaguchi Hiroyuki, Fukuda Koji, Nishiyama Akihiro, Yamashita Kaname, Ohtsubo Koushiro, Takeuchi Shinji, Nishiuchi Takumi, Oshima Hiroko, Oshima Masanobu, Davila Marco L, Yano Seiji
Division of Medical Oncology, Cancer Research Institute, Kanazawa University, 13-1 Takara-Machi, Kanazawa, Ishikawa, 920-0934, Japan.
Department of Immunology, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Japan.
Exp Hematol Oncol. 2024 Sep 27;13(1):94. doi: 10.1186/s40164-024-00563-x.
Precision medicine has drastically changed cancer treatment strategies including KRAS-mutant cancers which have been undruggable for decades. While intrinsic or acquired treatment resistance remains unresolved in many cases, epigenome-targeted therapy may be an option to overcome. We recently discovered the effectiveness of blocking small ubiquitin-like modifier (SUMO) signaling cascade (SUMOylation) in MYC-expressing KRAS-mutant cancer cells using a SUMO-activating enzyme E inhibitor TAK-981 that results in SUMOylation inhibition. Interestingly, TAK-981 promoted the degradation of MYC via the ubiquitin-proteasome system. Moreover, combination therapy with TAK-981 and MEK inhibitor trametinib remarkably regressed xenografted KRAS-mutant tumors by accumulating DNA damage and inducing apoptosis. Whereas our recent study revealed immune-independent antitumor efficacy, we evaluated the immune responses of cancer cells and immune cells in this study. We found that TAK-981-induced MYC downregulation promoted the activation of STING followed by Stat1 and MHC class I in KRAS-mutant cancer cells. Activation of dendritic cells or T cells treated with TAK-981 was also verified by upregulated activation markers in dendritic cells or skew-toward effector-like phenotypes in T cells. Furthermore, the enhanced immune-dependent antitumor efficacy of the combination therapy with TAK-981 and trametinib was confirmed by infiltration of immune cells into tumor tissues and immunodepleting-test using immunodepleting antibodies in syngeneic immunocompetent mouse models. Together with our recent study and here, the findings support that combination inhibition of SUMOylation and MEK comprehensively conquers MYC-expressing KRAS-mutant cancers by both immune-dependent and immune-independent antitumor responses.
精准医学已经彻底改变了癌症治疗策略,包括几十年来一直无法用药的KRAS突变型癌症。虽然在许多情况下,内在或获得性治疗耐药性仍未得到解决,但表观基因组靶向治疗可能是一种克服方法。我们最近发现,使用SUMO激活酶E抑制剂TAK-981阻断小泛素样修饰物(SUMO)信号级联反应(SUMO化)在表达MYC的KRAS突变癌细胞中具有有效性,这会导致SUMO化抑制。有趣的是,TAK-981通过泛素-蛋白酶体系统促进了MYC的降解。此外,TAK-981与MEK抑制剂曲美替尼的联合治疗通过积累DNA损伤和诱导凋亡,使异种移植的KRAS突变肿瘤显著消退。虽然我们最近的研究揭示了免疫非依赖性抗肿瘤疗效,但在本研究中我们评估了癌细胞和免疫细胞的免疫反应。我们发现,TAK-981诱导的MYC下调促进了STING的激活,随后在KRAS突变癌细胞中激活了Stat1和MHC I类分子。用TAK-981处理的树突状细胞或T细胞的激活也通过树突状细胞中激活标志物的上调或T细胞向效应样表型的倾斜得到了验证。此外,在同基因免疫活性小鼠模型中,通过免疫细胞浸润到肿瘤组织以及使用免疫耗竭抗体进行免疫耗竭试验,证实了TAK-981与曲美替尼联合治疗增强的免疫依赖性抗肿瘤疗效。结合我们最近的研究以及本研究结果,这些发现支持SUMO化和MEK的联合抑制通过免疫依赖性和免疫非依赖性抗肿瘤反应全面攻克表达MYC的KRAS突变癌症。