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Discovery of a novel BTK inhibitor S-016 and identification of a new strategy for the treatment of lymphomas including BTK inhibitor-resistant lymphomas

Pei-ran Song1, Zhi-peng Wan2,3, Ge-ge Huang2,3, Zi-lan Song4, Tao Zhang1, Lin-jiang Tong1, Yan Fang1, Hao-tian Tang1,3, Yu Xue1, Zheng-sheng Zhan1, Fang Feng1, Yan Li1, Wen-hao Shi3,5, Yu-qing Huang3,6, Yi Chen1, Wen-hu Duan1, Jian Ding1, Ao Zhang4, Hua Xie1,2,3
1 Division of Antitumor Pharmacology & Small-Molecule Drug Research Center, State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China
2 School of Pharmaceutical Sciences, Southern Medical University, Guangzhou 510515, China
3 Zhongshan Institute for Drug Discovery, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Zhongshan 528400, China
4 Shanghai Frontiers Science Center of Drug Target Identification and Delivery, School of Pharmacy, Shanghai Jiao Tong University, Shanghai 200240, China
5 School of Pharmacy, Zunyi Medical University, Zunyi 563006, China
6 School of Pharmacy, Guizhou Medical University, Guiyang 561113, China
Correspondence to: Wen-hu Duan: whduan@simm.ac.cn, Jian Ding: jding@simm.ac.cn, Ao Zhang: ao6919zhang@sjtu.edu.cn, Hua Xie: hxie@simm.ac.cn,
DOI: 10.1038/s41401-024-01311-x
Received: 3 March 2024
Accepted: 13 May 2024
Advance online: 4 June 2024

Abstract

Bruton’s tyrosine kinase (BTK) has emerged as a therapeutic target for B-cell malignancies, which is substantiated by the efficacy of various irreversible or reversible BTK inhibitors. However, on-target BTK mutations facilitating evasion from BTK inhibition lead to resistance that limits the therapeutic efficacy of BTK inhibitors. In this study we employed structure-based drug design strategies based on established BTK inhibitors and yielded a series of BTK targeting compounds. Among them, compound S-016 bearing a unique tricyclic structure exhibited potent BTK kinase inhibitory activity with an IC50 value of 0.5 nM, comparable to a commercially available BTK inhibitor ibrutinib (IC50 = 0.4 nM). S-016, as a novel irreversible BTK inhibitor, displayed superior kinase selectivity compared to ibrutinib and significant therapeutic effects against B-cell lymphoma both in vitro and in vivo. Furthermore, we generated BTK inhibitor-resistant lymphoma cells harboring BTK C481F or A428D to explore strategies for overcoming resistance. Co-culture of these DLBCL cells with M0 macrophages led to the polarization of M0 macrophages toward the M2 phenotype, a process known to support tumor progression. Intriguingly, we demonstrated that SYHA1813, a compound targeting both VEGFR and CSF1R, effectively reshaped the tumor microenvironment (TME) and significantly overcame the acquired resistance to BTK inhibitors in both BTK-mutated and wild-type BTK DLBCL models by inhibiting angiogenesis and modulating macrophage polarization. Overall, this study not only promotes the development of new BTK inhibitors but also offers innovative treatment strategies for B-cell lymphomas, including those with BTK mutations.

Keywords: diffuse large B-cell lymphoma; BTK inhibitors; drug resistance; BTK C481F; BTK A428D; SYHA1813

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