Chen Shengkai, Dai Zhenlin, Shi Jianbo, Rui Mengyu, Zhang Zhiyuan, Xu Qin
Department of Oral and Maxillofacial-Head and Neck Oncology, Ninth People's Hospital, Shanghai Jiao Tong University, School of Medicine, Shanghai, China.
Shanghai Key Laboratory of Stomatology & Shanghai Research Institute of Stomatology, Shanghai, China.
Int J Oral Sci. 2025 Sep 12;17(1):64. doi: 10.1038/s41368-025-00396-2.
Hypoxia and aberrant activation of epidermal growth factor receptor (EGFR) are considered important features of various malignancies. However, whether hypoxia can directly trigger EGFR activation and its clinical implications remain unclear. In this study, we demonstrated that in oral cancer, a typical hypoxic tumor, hypoxia can induce chronic but constitutive phosphorylation of wild-type EGFR in the absence of ligands. Oral cancer cell lines exhibit different EGFR phosphorylation responses to hypoxia. In hypoxic HN4 and HN6 cells, ubiquitination-mediated endocytosis, lysosomal sorting, and degradation lead to low levels of EGFR phosphorylation. However, in CAL-27 and HN30 cells, a novel HIF-1α-induced long noncoding RNA (lncRNA), EUDAL, can compete with the E3 ligase/adaptor complex c-Cbl/Grb2 for binding to EGFR, stabilizing phosphorylated EGFR (pEGFR) and resulting in sustained activation of EGFR and its downstream STAT3/BNIP3 signaling. STAT3/BNIP3-mediated autophagy leads to antitumor drug resistance. A high EUDAL/EGFR/STAT3/autophagy pathway activation predicts poor response to chemotherapy in oral cancer patients. Collectively, hypoxia can induce noncanonical ligand-independent EGFR phosphorylation. High EUDAL expression facilitates sustained EGFR phosphorylation in hypoxic tumor cells and leads to autophagy-related drug resistance.
缺氧和表皮生长因子受体(EGFR)的异常激活被认为是各种恶性肿瘤的重要特征。然而,缺氧是否能直接触发EGFR激活及其临床意义仍不清楚。在本研究中,我们证明在口腔癌(一种典型的缺氧肿瘤)中,缺氧可在无配体的情况下诱导野生型EGFR的慢性但持续性磷酸化。口腔癌细胞系对缺氧表现出不同的EGFR磷酸化反应。在缺氧的HN4和HN6细胞中,泛素化介导的内吞作用、溶酶体分选和降解导致EGFR磷酸化水平较低。然而,在CAL-27和HN30细胞中,一种新的HIF-1α诱导的长链非编码RNA(lncRNA),即EUDAL,可与E3连接酶/衔接子复合物c-Cbl/Grb2竞争结合EGFR,稳定磷酸化的EGFR(pEGFR),并导致EGFR及其下游STAT3/BNIP3信号的持续激活。STAT3/BNIP3介导的自噬导致抗肿瘤药物耐药性。EUDAL/EGFR/STAT3/自噬途径的高激活预示着口腔癌患者对化疗反应不佳。总之,缺氧可诱导非经典的非配体依赖性EGFR磷酸化。高EUDAL表达促进缺氧肿瘤细胞中EGFR的持续磷酸化,并导致自噬相关的耐药性。