Du Danyu, Qin Mengyao, Shi Li, Liu Chan, Jiang Jingwei, Liao Zhengguang, Wang Hongxv, Zhang Zhibo, Sun Li, Fan Hui, Liu Zhengrui, Yu Hong, Li Hongyang, Peng Jun, Yuan Shengtao, Yang Mei, Xiong Jing
Department of Pharmacology, School of Pharmacy, China Pharmaceutical University, Nanjing, 210009, China.
Institute of Pharmaceutical Sciences, China Pharmaceutical University, Nanjing, 210009, China.
Oncogene. 2023 Oct;42(42):3127-3141. doi: 10.1038/s41388-023-02795-3. Epub 2023 Sep 1.
Targeting metabolic remodeling represents a potentially promising strategy for hepatocellular carcinoma (HCC) therapy. In-depth understanding on the regulation of the glutamine transporter alanine-serine-cysteine transporter 2 (ASCT2) contributes to the development of novel promising therapeutics. As a developmentally regulated RNA binding protein, RBM45 is capable to shuttle between nucleus and cytoplasm, and directly interacts with proteins. By bioinformatics analysis, we screened out that RBM45 was elevated in the HCC patient specimens and positively correlated with poor prognosis. RBM45 promoted cell proliferation, boosted xenograft tumorigenicity and accelerated HCC progression. Using untargeted metabolomics, it was found that RBM45 interfered with glutamine metabolism. Further results demonstrated that RBM45 positively associated with ASCT2 in human and mouse specimens. Moreover, RBM45 enhanced ASCT2 protein stability by counteracting autophagy-independent lysosomal degradation. Significantly, wild-type ASCT2, instead of phospho-defective mutants, rescued siRBM45-suppressed HCC cell proliferation. Using molecular docking approaches, we found AG-221, a mutant isocitrate dehydrogenase 2 (mIDH2) inhibitor for acute myeloid leukemia therapy, pharmacologically perturbed RBM45-ASCT2 interaction, decreased ASCT2 stability and suppressed HCC progression. These findings provide evidence that RBM45 plays a crucial role in HCC progression via interacting with and counteracting the degradation of ASCT2. Our findings suggest a novel alternative structural sites for the design of ASCT2 inhibitors and the agents interfering with RBM45-ASCT2 interaction may be a potential direction for HCC drug development.
靶向代谢重塑是肝细胞癌(HCC)治疗中一种颇具潜力的策略。深入了解谷氨酰胺转运体丙氨酸 - 丝氨酸 - 半胱氨酸转运体2(ASCT2)的调控机制有助于开发新的有前景的治疗方法。作为一种受发育调控的RNA结合蛋白,RBM45能够在细胞核和细胞质之间穿梭,并直接与蛋白质相互作用。通过生物信息学分析,我们筛选出RBM45在HCC患者标本中升高,且与不良预后呈正相关。RBM45促进细胞增殖,增强异种移植瘤形成能力并加速HCC进展。通过非靶向代谢组学发现,RBM45干扰谷氨酰胺代谢。进一步结果表明,在人和小鼠标本中RBM45与ASCT2呈正相关。此外,RBM45通过对抗非自噬依赖性溶酶体降解来增强ASCT2蛋白稳定性。值得注意的是,野生型ASCT2而非磷酸化缺陷突变体可挽救siRBM45抑制的HCC细胞增殖。使用分子对接方法,我们发现AG - 221,一种用于急性髓细胞白血病治疗的突变异柠檬酸脱氢酶2(mIDH2)抑制剂,在药理学上扰乱了RBM45 - ASCT2相互作用,降低了ASCT2稳定性并抑制了HCC进展。这些发现提供了证据,表明RBM45通过与ASCT2相互作用并对抗其降解在HCC进展中起关键作用。我们的发现为ASCT2抑制剂的设计提出了新的替代结构位点,干扰RBM45 - ASCT2相互作用的药物可能是HCC药物开发的一个潜在方向。