Zhao Kai, Sun Tifan, Sun Qiruo, Chen Zhenzhong, Wang Tiepeng, Yang Jinming, Li Lei, Zhu Yanan, Liu Xinye, Yang Dawei, Lin Binyan, Lu Na
State Key Laboratory of Natural Medicines, Jiangsu Key Laboratory of Carcinogenesis and Intervention, Department of Physiology, School of Basic Medicine and Clinical Pharmacy, China Pharmaceutical University, 24 Tongjiaxiang, Nanjing, 210009, China.
School of Pharmacy, Nanjing University of Chinese Medicine, 138 Xianlin Rd., Nanjing, 210023, China.
Adv Sci (Weinh). 2025 Feb;12(7):e2414437. doi: 10.1002/advs.202414437. Epub 2024 Dec 24.
Tumor necrosis factor receptor-associated factor 4 (TRAF4), an E3 ubiquitin ligase, is frequently overexpressed in tumors. Although its cytoplasmic role in tumor progression is well-documented, the precise mechanisms underlying its nuclear localization and functional contributions in tumor cells remain elusive. This study demonstrated a positive correlation between the expression of nuclear TRAF4 and both tumor grades and stemness signatures in human cancer tissues. Notably, reduced nuclear TRAF4 led to decreased stemness properties and metastatic dormancy of tumor cells. Conversely, restoring nuclear TRAF4 in TRAF4-knockout (TRAF4-KO) cells augmented these cellular capabilities. Within the nucleus, the TRAF domain of TRAF4 interacted with c-Jun, thereby stimulating its transcriptional activity. This interaction subsequently led to an enhancement of the promoter activity of interleukin-8 (IL-8), which is identified as a mediator of nuclear TRAF4-induced tumor dormancy. Additionally, activation of AKT signaling by nerve growth factor facilitated TRAF4 phosphorylation at Ser242, enhancing its interaction with 14-3-3θ and promoting its nuclear translocation. Importantly, pharmacological modulation of TRAF4 nuclear translocation is found to suppress tumor tumorigenicity and metastasis in tumor models. This study highlights the critical role of nuclear TRAF4 in regulating tumor stemness and dormancy, positioning it as a potential therapeutic target for metastatic and refractory cancers.
肿瘤坏死因子受体相关因子4(TRAF4)是一种E3泛素连接酶,在肿瘤中经常过度表达。尽管其在肿瘤进展中的细胞质作用已有充分记录,但其在肿瘤细胞核定位及功能贡献的精确机制仍不清楚。本研究表明,在人类癌症组织中,细胞核TRAF4的表达与肿瘤分级和干性特征呈正相关。值得注意的是,细胞核TRAF4减少导致肿瘤细胞干性特性和转移休眠降低。相反,在TRAF4基因敲除(TRAF4-KO)细胞中恢复细胞核TRAF4可增强这些细胞能力。在细胞核内,TRAF4的TRAF结构域与c-Jun相互作用,从而刺激其转录活性。这种相互作用随后导致白细胞介素8(IL-8)启动子活性增强,IL-8被确定为细胞核TRAF4诱导肿瘤休眠的介质。此外,神经生长因子激活AKT信号通路促进TRAF4在Ser242位点磷酸化,增强其与14-3-3θ的相互作用并促进其核转位。重要的是,在肿瘤模型中发现对TRAF4核转位进行药理调节可抑制肿瘤的致瘤性和转移。本研究强调了细胞核TRAF4在调节肿瘤干性和休眠中的关键作用,使其成为转移性和难治性癌症的潜在治疗靶点。