Lien Sally, Whitbread Thomas P, Shastri Shiva O, Contreras Jamie A, Zhao Ruiying, Zhu Yan
Department of Biological Sciences, St. John's University Queens, NY 11439, USA.
Department of Integrative Biology and Pharmacology, McGovern Medical School, The University of Texas Health Science Center at Houston Houston, TX 77030, USA.
Am J Cancer Res. 2024 May 15;14(5):2141-2156. doi: 10.62347/QIFC4021. eCollection 2024.
Although amplification/overexpression is the predominant mechanism for the oncogenic properties of MDM2, an increasing number of MDM2 somatic missense mutations were identified in cancer patients with the recent advances in sequencing technology. Here, we characterized an MDM2 cancer-associated mutant variant W329G identified from a patient sample that contains a wild-type p53 gene. Trp329 is one of residues that were reported to be critical to MDM2's binding to ribosomal protein L11 (RPL11). We found that the MDM2 W329G mutant was resistant to the inhibitory effect of RPL11 on MDM2-mediated p53 ubiquitination and degradation, in line with its defect on RPL11 binding. Using isogenic U2OS cells with or without endogenous MDM2 W329G mutation, we demonstrated that the expression of classic p53 targets induced by ribosomal stress signals was reduced in mutant cells. RNA-seq analysis revealed that upon 5-FU treatment, the p53 response was significantly impaired. Also, the 5-FU-mediated repression of genes in cell cycle progression and DNA replication was diminished in W329G mutant-containing cells. Physiologically, U2OS W329G cells were more resistant to cell growth inhibition induced by ribosomal stress and exhibited higher glycolytic rates upon 5-FU treatment. Together, our data indicated that cancer-associated MDM2 W329G mutant attenuates ribosomal stress-mediated p53 responses to promote cell survival and glycolysis.
尽管扩增/过表达是MDM2致癌特性的主要机制,但随着测序技术的最新进展,在癌症患者中发现了越来越多的MDM2体细胞错义突变。在此,我们对从一名含有野生型p53基因的患者样本中鉴定出的与癌症相关的MDM2突变体变体W329G进行了表征。色氨酸329是据报道对MDM2与核糖体蛋白L11(RPL11)结合至关重要的残基之一。我们发现MDM2 W329G突变体对RPL11对MDM2介导的p53泛素化和降解的抑制作用具有抗性,这与其在RPL11结合上的缺陷一致。使用具有或不具有内源性MDM2 W329G突变的同基因U2OS细胞,我们证明在突变细胞中核糖体应激信号诱导的经典p53靶标的表达降低。RNA测序分析表明,在5-氟尿嘧啶处理后,p53反应明显受损。此外,在含有W329G突变体的细胞中,5-氟尿嘧啶对细胞周期进程和DNA复制中基因表达的抑制作用减弱。在生理上,U2OS W329G细胞对核糖体应激诱导的细胞生长抑制更具抗性,并且在5-氟尿嘧啶处理后表现出更高的糖酵解速率。总之,我们的数据表明,与癌症相关的MDM2 W329G突变体减弱核糖体应激介导的p53反应以促进细胞存活和糖酵解。