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Deep learning enables the discovery of a novel cuproptosis- inducing molecule for the inhibition of hepatocellular carcinoma

Fan Yang1,2,3, Lin Jia4, Hong-chao Zhou1,2, Jing-nan Huang1,2, Meng-yun Hou1,2, Feng-ting Liu1,2, Nayana Prabhu5, Zhi-jie Li1,2, Chuan-bin Yang1,2, Chang Zou1,2,6, Pär Nordlund5,7, Ji-gang Wang1,2,8, Ling-yun Dai1,2,5
1 Department of Geriatrics, and Shenzhen Clinical Research Centre for Geriatrics, Shenzhen People’s Hospital (the Second Clinical Medical College of Jinan University
2 the First Affiliated Hospital of Southern University of Science and Technology), Shenzhen 518020, China
3 Integrated Chinese and Western Medicine Postdoctoral Research Station, Jinan University, Guangzhou 510632, China
4 College of Pharmacy, Shenzhen Technology University, Shenzhen 518118, China
5 Institute of Molecular and Cell Biology, Agency for Science, Technology and Research (A*STAR), Singapore 138673, Singapore
6 Department of Clinical Medical Research Center, The First Affiliated Hospital, School of Medicine, Southern University of Science and Technology, Shenzhen 518020, China
7 Department of Oncology and Pathology, Karolinska Institutet, 17177 Stockholm, Sweden
8 Artemisinin Research Center, and Institute of Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China
Correspondence to: Ji-gang Wang: jgwang@icmm.ac.cn, Ling-yun Dai: lingyun.dai@outlook.com,
DOI: 10.1038/s41401-023-01167-7
Received: 17 April 2023
Accepted: 5 September 2023
Advance online: 6 October 2023

Abstract

Hepatocellular carcinoma (HCC) is one of the most common and deadly cancers in the world. The therapeutic outlook for HCC patients has significantly improved with the advent and development of systematic and targeted therapies such as sorafenib and lenvatinib; however, the rise of drug resistance and the high mortality rate necessitate the continuous discovery of effective targeting agents. To discover novel anti-HCC compounds, we first constructed a deep learning-based chemical representation model to screen more than 6 million compounds in the ZINC15 drug-like library. We successfully identified LGOd1 as a novel anticancer agent with a characteristic levoglucosenone (LGO) scaffold. The mechanistic studies revealed that LGOd1 treatment leads to HCC cell death by interfering with cellular copper homeostasis, which is similar to a recently reported copper-dependent cell death named cuproptosis. While the prototypical cuproptosis is brought on by copper ionophore-induced copper overload, mechanistic studies indicated that LGOd1 does not act as a copper ionophore, but most likely by interacting with the copper chaperone protein CCS, thus LGOd1 represents a potentially new class of compounds with unique cuproptosis-inducing property. In summary, our findings highlight the critical role of bioavailable copper in the regulation of cell death and represent a novel route of cuproptosis induction.

Keywords: hepatocellular carcinoma; cuproptosis; deep learning; levoglucosenone; copper homeostasis; cell death

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