The Ph.D. Program for Neural Regenerative Medicine, College of Medical Science and Technology, Taipei Medical University and National Health Research Institutes, Taipei, Taiwan.
Graduate Institute of Medical Sciences, Taipei Medical University, Taipei, Taiwan.
Mol Neurobiol. 2018 Apr;55(4):3211-3223. doi: 10.1007/s12035-017-0569-4. Epub 2017 May 6.
Glioblastoma multiforme (GBM) is the most fatal of all brain cancers, and the standard care protocol for GBM patients is surgical tumor resection followed by radiotherapy and temozolomide (TMZ)-mediated chemotherapy. However, tumor recurrence frequently occurs, and recurrent GBM exhibits more malignancy and less sensitivity in response to chemotherapy. The malignancy and drug resistance primarily reflect the small population of glioma stem-like cells (GSC). Therefore, understanding the mechanism that controls GSC enrichment is important to benefit the prognosis of GBM patients. Nucleolin (NCL), which is responsible for ribosome biogenesis and RNA maturation, is overexpressed in gliomas. However, the role of NCL in GSC development and drug resistance is still unclear. In this study, we demonstrate that NCL attenuated GSC enrichment to enhance the sensitivity of GBM cells in response to TMZ. In GSC enrichment, NCL was significantly reduced at the protein level as a result of decreased protein stability. In particular, the inhibition of HDAC activity by suberoylanilide hydroxamic acid rescued NCL acetylation accompanied by the loss of mouse double minute 2 homolog (MDM2)-mediated ubiquitination. In addition, we found that NCL ubiquitination resulted from the activation of STAT3- and JNK-mediated signaling in GSC. Moreover, NCL inhibited the formation of stem-like spheres by attenuating the expression of Sox2, Oct4, and Bmi1. Furthermore, NCL sensitized the response of GBM cells to TMZ. Based on these findings, NCL expression is a potential indicator to predict chemotherapeutic efficiency in GBM patients.
多形性胶质母细胞瘤(GBM)是所有脑癌中最致命的一种,GBM 患者的标准治疗方案是手术切除肿瘤,然后进行放疗和替莫唑胺(TMZ)介导的化疗。然而,肿瘤经常复发,复发性 GBM 表现出更高的恶性程度和对化疗的较低敏感性。这种恶性程度和耐药性主要反映了少量胶质瘤干细胞(GSC)的存在。因此,了解控制 GSC 富集的机制对于改善 GBM 患者的预后非常重要。核仁素(NCL)负责核糖体的生物发生和 RNA 的成熟,在神经胶质瘤中过表达。然而,NCL 在 GSC 发育和耐药性中的作用尚不清楚。在这项研究中,我们证明 NCL 减弱了 GSC 的富集,从而增强了 GBM 细胞对 TMZ 的敏感性。在 GSC 富集过程中,由于蛋白质稳定性降低,NCL 的蛋白质水平显著降低。特别是,通过抑制 HDAC 活性的 suberoylanilide hydroxamic acid 挽救了 NCL 的乙酰化,同时伴随着鼠双微体 2 同源物(MDM2)介导的泛素化的丢失。此外,我们发现 NCL 泛素化是由 GSC 中 STAT3 和 JNK 介导的信号通路激活引起的。此外,NCL 通过减弱 Sox2、Oct4 和 Bmi1 的表达来抑制类干细胞球体的形成。此外,NCL 使 GBM 细胞对 TMZ 的反应更加敏感。基于这些发现,NCL 的表达是预测 GBM 患者化疗效果的一个潜在指标。