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Upregulation of wild-type p53 by small molecule-induced elevation of NQO1 in non-small cell lung cancer cells

Hong Yu1,2, Hong-ying Gao3, Hua Guo2, Gui-zhen Wang2, Yi-qing Yang3, Qian Hu1, Li-jun Liang2, Qun Zhao2,4, Da-wei Xie2, Yu Rao3, Guang-biao Zhou1,2
1 School of Chinese Materia Medica, Beijing University of Chinese Medicine, Beijing 100029, China
2 State Key Laboratory of Molecular Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
3 MOE Key Laboratory of Protein Sciences, School of Pharmaceutical Sciences, MOE Key Laboratory of Bioorganic Phosphorus Chemistry & Chemical Biology, and School of Medicine and Collaborative Innovation Center of Biotherapy, Tsinghua University, Beijing 100084, China
4 Hubei University of Medicine, Shiyan 442000, China
Correspondence to: Yu Rao: yrao@tsinghua.edu.cn, Guang-biao Zhou: gbzhou@ioz.ac.cn,
DOI: 10.1038/s41401-021-00691-8
Received: 9 February 2021
Accepted: 28 April 2021
Advance online: 25 May 2021

Abstract

The tumor suppressor p53 is usually inactivated by somatic mutations in malignant neoplasms, and its reactivation represents an attractive therapeutic strategy for cancers. Here, we reported that a new quinolone compound RYL-687 significantly inhibited non- small cell lung cancer (NSCLC) cells which express wild type (wt) p53, in contract to its much weaker cytotoxicity on cells with mutant p53. RYL-687 upregulated p53 in cells with wt but not mutant p53, and ectopic expression of wt p53 significantly enhanced the anti-NSCLC activity of this compound. RYL-687 induced production of reactive oxygen species (ROS) and upregulation of Nrf2, leading to an elevation of the NAD(P)H:quinoneoxidoreductase-1 (NQO1) that can protect p53 by inhibiting its degradation by 20S proteasome. RYL-687 bound NQO1, facilitating the physical interaction between NQO1 and p53. NQO1 was required for RYL-687- induced p53 accumulation, because silencing of NQO1 by specific siRNA or an NQO1 inhibitor uridine, drastically suppressed RYL- 687-induced p53 upregulation. Moreover, a RYL-687-related prodrug significantly inhibited tumor growth in NOD-SCID mice inoculated with NSCLC cells and in a wt p53-NSCLC patient-derived xenograft mouse model. These data indicate that targeting NQO1 is a rational strategy to reactivate p53, and RYL-687 as a p53 stabilizer bears therapeutic potentials in NSCLCs with wt p53.
Keywords: NQO1; p53; RYL-687; non-small cell lung cancer

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