DOI: 10.1097/cm9.0000000000004123 ISSN: 0366-6999

A selective BRG1 inhibitor targeting bromodomain sensitizes hepatocellular carcinoma to chemoradiotherapy by disrupting the DNA damage response

Qing Tao, Ziqi Zhu, Yuwei Chen, Yuke Shu, Zhenru Wu, Yuting Zeng, Guoqiang Liu, Yongjie Zhou, Wenhao Guo, Yujun Shi

Abstract

Background:

The poor response to ionizing radiation and chemotherapies remains a significant clinical challenge for unresectable hepatocellular carcinoma (HCC). BRG1, the core ATPase subunit of switch/sucrose non-fermentable (SWI/SNF) complex, is often overexpressed in HCC and represents a potential therapeutic target. Mechanistically, BRG1 facilitates DNA damage repair by assisting the assembly of DNA damage response (DDR) complex via its bromodomain (BRD), which selectively binds to acetylated histone H3. Therefore, pharmacological targeting of the BRG1-BRD represents an innovative strategy to sensitize HCC to conventional chemoradiotherapy.

Methods:

To identify specific inhibitors, we employed a high-throughput screening system against a vast library comprising over 2 million bioactive compounds. The binding affinity and selectivity of the leading candidate were comprehensively assessed.  In vitro  assays were conducted to elucidate its mechanism in disrupting DNA double-strand break (DSB) repair. Furthermore,  in vivo  tumor sensitization and systemic biosafety were systematically evaluated using HCC xenograft mouse models treated with combination therapies, supplemented by serological liver enzyme profiling and histopathological analyses of major organs.

Results:

We identified BRGi-39, a novel chemical entity that blocks BRG1-BRD with exceptional selectivity and high affinity. Mechanistically, BRGi-39 profoundly disrupted DNA damage repair by preventing γH2A.X formation and blocking 53BP1 recruitment to DSB sites. At pharmacologically low concentrations, BRGi-39 robustly sensitized HCC cells to both irradiation and chemotherapeutic drugs.  In vivo  studies demonstrated that low-dose BRGi-39 synergistically enhanced the efficacy of chemo-radiotherapy in HCC xenografts. Notably, toxicological assessments, including hematoxylin and eosin staining and serum enzyme analyses, revealed no obvious injuries in main organs (lung, liver, spleen, and kidney), confirming a highly favorable biosafety profile.

Conclusions:

BRGi-39 is identified as a novel and highly selective BRG1-BRD inhibitor that effectively overcomes chemoradioresistance in HCC by dismantling the DDR pathway. Our comprehensive preclinical data highlight BRGi-39 as a promising, safe therapeutic candidate to be combined with chemoradiotherapy for the treatment of unresectable HCC.

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