Article

Oncoprotein LAMTOR5-mediated CHOP silence via DNA hypermethylation and miR-182/miR-769 in promotion of liver cancer growth

Xue Wang1, Qian-qian Li1, Yan-xin Tang1, Ye Li1, Lu Zhang1,2, Fei-fei Xu1,3, Xue-li Fu1, Kai Ye1, Jia-qi Ma1, Shi-man Guo1, Fang-yuan Ma1, Zhi-yu Liu1, Xu-he Shi1, Xian-meng Li1, Hui-min Sun1, Yue Wu1,4, Wei-ying Zhang1, Li-hong Ye1
1 State Key Laboratory of Medicinal Chemical Biology, Tianjin Key Laboratory of Protein Sciences, Department of Biochemistry and Molecular Biology, College of Life Sciences, Nankai University, Tianjin 300071, China
2 Chinese Academy of Medical Sciences & Peking Union Medical College Institute of Biomedical Engineering, Tianjin 300192, China
3 Institute of Radiation Medicine, Peking Union Medical College & Chinese Academy of Medical Sciences, Tianjin 300192, China
4 Center for Cell Structure and Function, Shandong Provincial Key Laboratory of Animal Resistance Biology, Collaborative Innovation Center of Cell Biology in Universities of Shandong, College of Life Sciences, Shandong Normal University, Jinan 250014, China
Correspondence to: Wei-ying Zhang: zhwybao@nankai.edu.cn, Li-hong Ye: yelihong@nankai.edu.cn,
DOI: 10.1038/s41401-024-01310-y
Received: 17 January 2024
Accepted: 8 May 2024
Advance online: 28 June 2024

Abstract

C/EBP homologous protein (CHOP) triggers the death of multiple cancers via endoplasmic reticulum (ER) stress. However, the function and regulatory mechanism of CHOP in liver cancer remain elusive. We have reported that late endosomal/lysosomal adapter, mitogen-activated protein kinase and mTOR activator 5 (LAMTOR5) suppresses apoptosis in various cancers. Here, we show that the transcriptional and posttranscriptional inactivation of CHOP mediated by LAMTOR5 accelerates liver cancer growth. Clinical bioinformatic analysis revealed that the expression of CHOP was low in liver cancer tissues and that its increased expression predicted a good prognosis. Elevated CHOP contributed to destruction of LAMTOR5-induced apoptotic suppression and proliferation. Mechanistically, LAMTOR5-recruited DNA methyltransferase 1 (DNMT1) to the CpG3 region (−559/−429) of the CHOP promoter and potentiated its hypermethylation to block its interaction with general transcription factor IIi (TFII-I), resulting in its inactivation. Moreover, LAMTOR5-enhanced miR-182/miR-769 reduced CHOP expression by targeting its 3’UTR. Notably, lenvatinib, a first-line targeted therapy for liver cancer, could target the LAMTOR5/CHOP axis to prevent liver cancer progression. Accordingly, LAMTOR5-mediated silencing of CHOP via the regulation of ER stress-related apoptosis promotes liver cancer growth, providing a theoretical basis for the use of lenvatinib for the treatment of liver cancer.

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