Article

Skullcapflavone II, a novel NQO1 inhibitor, alleviates aristolochic acid I-induced liver and kidney injury in mice

Ya-ping Dong1, Shu-zhen Chen2,3, Hui-si He2,3, Zhuo-ran Sun4, Li-xuan Jiang2,3, Yan-qiu Gu5, Ying Zhang4, Fei Feng4, Chun Chen6, Zhe-cai Fan2,3, Xiao-fei Chen4, Wen Wen2,3, Hong-yang Wang1,2,3,7
1 Fudan University Shanghai Cancer Center, Department of Oncology, Shanghai Medical College, Fudan University, Shanghai 200032, China
2 National Center for Liver Cancer, Naval Medical University (Second Military Medical University), Shanghai 200438, China
3 International Cooperation Laboratory on Signal Transduction, Eastern Hepatobiliary Surgery Hospital, Naval Medical University (Second Military Medical University), Shanghai 200438, China
4 School of Pharmacy, Naval Medical University (Second Military Medical University), Shanghai 200433, China
5 Department of Pharmacy, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, China
6 Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
7 State Key Laboratory of Oncogenes and Related Genes, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200032, China
Correspondence to: Xiao-fei Chen: xfchen2010@163.com, Wen Wen: wenwen_smmu@163.com, Hong-yang Wang: hywangk@vip.sina.com,
DOI: 10.1038/s41401-023-01052-3
Received: 19 August 2022
Accepted: 8 January 2023
Advance online: 25 January 2023

Abstract

Aristolochic acid I (AAI) is a well established nephrotoxin and human carcinogen. Cytosolic NAD(P)H quinone oxidoreductase 1 (NQO1) plays an important role in the nitro reduction of aristolochic acids, leading to production of aristoloactam and AA-DNA adduct. Application of a potent NQO1 inhibitor dicoumarol is limited by its life-threatening side effect as an anticoagulant and the subsequent hemorrhagic complications. As traditional medicines containing AAI remain available in the market, novel NQO1 inhibitors are urgently needed to attenuate the toxicity of AAI exposure. In this study, we employed comprehensive 2D NQO1 biochromatography to screen candidate compounds that could bind with NQO1 protein. Four compounds, i.e., skullcapflavone II (SFII), oroxylin A, wogonin and tectochrysin were screened out from Scutellaria baicalensis. Among them, SFII was the most promising NQO1 inhibitor with a binding affinity (KD = 4.198 μmol/L) and inhibitory activity (IC50 = 2.87 μmol/L). In human normal liver cell line (L02) and human renal proximal tubular epithelial cell line (HK-2), SFII significantly alleviated AAI-induced DNA damage and apoptosis. In adult mice, oral administration of SFII dose-dependently ameliorated AAI-induced renal fibrosis and dysfunction. In infant mice, oral administration of SFII suppressed AAI-induced hepatocellular carcinoma initiation. Moreover, administration of SFII did not affect the coagulation function in short term in adult mice. In conclusion, SFII has been identified as a novel NQO1 inhibitor that might impede the risk of AAI to kidney and liver without obvious side effect.

Keywords: aristolochic acids; skullcapflavone II; NAD(P)H quinone oxidoreductase 1 (NQO1); hepatorenal toxicity; DNA damage; dicoumarol

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