Article

PRMT5 confers lipid metabolism reprogramming, tumour growth and metastasis depending on the SIRT7-mediated desuccinylation of PRMT5 K387 in tumours

Hong-feng Yuan1,2, Man Zhao1,2, Li-na Zhao2, Hao-lin Yun2, Guang Yang1, Yu Geng2, Yu-fei Wang2, Wei Zheng2, Ying Yuan2, Tian-qiang Song3, Jun-qi Niu4, Xiao-dong Zhang1
1 Department of Gastrointestinal Cancer Biology, Tianjin Cancer Institute, Liver Cancer Center, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, Tianjin 300060, China
2 Department of Cancer Research, College of Life Sciences, Nankai University, Tianjin 300071, China
3 Department of Hepatobiliary Cancer, Liver Cancer Research Center, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin’s Clinical Research Center for Cancer, Tianjin 300060, China
4 Department of Hepatology, the First Hospital, Jilin University, Jilin 130021, China
Correspondence to: Tian-qiang Song: tjmuch@hotmail.com, Jun-qi Niu: junqiniu@aliyun.com, Xiao-dong Zhang: zhangxiaodong@tjmuch.com,
DOI: 10.1038/s41401-021-00841-y
Received: 18 August 2021
Accepted: 9 December 2021
Advance online: 19 January 2022

Abstract

The protein arginine methyltransferase 5 (PRMT5), which is highly expressed in tumour tissues, plays a crucial role in cancer development. However, the mechanism by which PRMT5 promotes cancer growth is poorly understood. Here, we report that PRMT5 contributes to lipid metabolism reprogramming, tumour growth and metastasis depending on the SIRT7-mediated desuccinylation of PRMT5 K387 in tumours. Mass spectrometric analysis identified PRMT5 lysine 387 as its succinylation site. Moreover, the desuccinylation of PRMT5 K387 enhances the methyltransferase activity of PRMT5. SIRT7 catalyses the desuccinylation of PRMT5 in cells. The SIRT7-mediated dessuccinylation of PRMT5 lysine 387 fails to bind to STUB1, decreasing PRMT5 ubiquitination and increasing the interaction between PRMT5 and Mep50, which promotes the formation of the PRMT5- Mep50 octamer. The PRMT5-Mep50 octamer increases PRMT5 methyltransferase activity, leading to arginine methylation of SREBP1a. The symmetric dimethylation of SREBP1a increases the levels of cholesterol, fatty acid, and triglyceride biogenesis in the cells, escaping degradation through the ubiquitin-proteasome pathway. Functionally, the desuccinylation of PRMT5 K387 promotes lipid metabolism reprogramming, tumour growth and metastasis in vitro and in vivo in tumours.
Keywords: PRMT5; methyltransferase activity; desuccinylation; SIRT7; lipid metabolism reprogramming

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