Article

SNS-023 sensitizes hepatocellular carcinoma to sorafenib by inducing degradation of cancer drivers SIX1 and RPS16

Yuan Liu1,2, Wei-yao Kong1,2, Cui-fu Yu2, Zhen-long Shao2, Qiu-cheng Lei3, Yuan-fei Deng4, Geng-xi Cai5, Xue-fen Zhuang2, Wen-shuang Sun2, Shi-gang Wu6, Rong Wang1, Xiang Chen1, Guo-xing Chen1, Hong-biao Huang1,2, Yu-ning Liao1,2
1 Department of General Surgery, The Sixth Affiliated Hospital of Guangzhou Medical University, Qingyuan People’s Hospital, Qingyuan 511500, China
2 Affiliated Cancer Hospital & Institute of Guangzhou Medical University, Guangzhou Municipal and Guangdong Provincial Key Laboratory of Protein Modification and Degradation, School of Basic Medical Sciences, Guangzhou Medical University, Guangzhou 511436, China
3 Department of Hepatopancreatic Surgery, The First People’s Hospital of Foshan, Foshan 528000, China
4 Department of Pathology, The First People’s Hospital of Foshan, Foshan 528000, China
5 Department of Breast Surgery, The First People’s Hospital of Foshan, Foshan 528000, China
6 Department of Pathology, The Sixth Affiliated Hospital of Guangzhou Medical University, Qingyuan People’s Hospital, Qingyuan 511500, China
Correspondence to: Guo-xing Chen: chenguoxing1981@163.com, Hong-biao Huang: hhb800616@126.com, Yu-ning Liao: liaoyuningm1@126.com,
DOI: 10.1038/s41401-022-01003-4
Received: 25 May 2022
Accepted: 20 September 2022
Advance online: 19 October 2022

Abstract

Hepatocellular carcinoma (HCC) remains challenging due to the lack of efficient therapy. Promoting degradation of certain cancer drivers has become an innovative therapy. The nuclear transcription factor sine oculis homeobox 1 (SIX1) is a key driver for the progression of HCC. Here, we explored the molecular mechanisms of ubiquitination of SIX1 and whether targeting SIX1 degradation might represent a potential strategy for HCC therapy. Through detecting the ubiquitination level of SIX1 in clinical HCC tissues and analyzing TCGA and GEPIA databases, we found that ubiquitin specific peptidase 1 (USP1), a deubiquitinating enzyme, contributed to the lower ubiquitination and high protein level of SIX1 in HCC tissues. In HepG2 and Hep3B cells, activation of EGFR-AKT signaling pathway promoted the expression of USP1 and the stability of its substrates, including SIX1 and ribosomal protein S16 (RPS16). In contrast, suppression of EGFR with gefitinib or knockdown of USP1 restrained EGF-elevated levels of SIX1 and RPS16. We further revealed that SNS-023 (formerly known as BMS-387032) induced degradation of SIX1 and RPS16, whereas this process was reversed by reactivation of EGFR-AKT pathway or overexpression of USP1. Consequently, inactivation of the EGFR-AKT-USP1 axis with SNS-032 led to cell cycle arrest, apoptosis, and suppression of cell proliferation and migration in HCC. Moreover, we showed that sorafenib combined with SNS-032 or gefitinib synergistically inhibited the growth of Hep3B xenografts in vivo. Overall, we identify that both SIX1 and RPS16 are crucial substrates for the EGFR-AKT-USP1 axis-driven growth of HCC, suggesting a potential anti-HCC strategy from a novel perspective.
Keywords: SNS-023; ML323; sorafenib; gefitinib; MK2206

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