Wen Zhi, Wang Yidan, Fox Kathryn C, Bissonnette Adam M, Moat Luke F, Kitchner Terrie E, Springstroh Kelsey, Kim Sung Hoon, Sheerar Dagna S, Tanawattanacharoen Patcharon, Leon Chady A, Fagbemi Seth O, Katzenellenbogen John A, Hebbring Scott J, Katzenellenbogen Benita S, Janz Siegfried, Onitilo Adedayo A
Center for Precision Medicine Research, Marshfield Clinic Research Institute, Marshfield Clinic Health System, Marshfield, WI, 54449, USA.
McArdle Laboratory for Cancer Research, University of Wisconsin-Madison, Madison, WI, 53705, USA.
Adv Sci (Weinh). 2025 Jul 14:e08822. doi: 10.1002/advs.202508822.
Relapsed and refractory multiple myeloma (RRMM) remains the leading cause of MM mortality. FOXM1 is strongly associated with RRMM, making it a compelling therapeutic target. Through three low-throughput screenings, we have identified nine FDA-approved drugs, including the BH3 mimetic Venetoclax, that synergize with FOXM1 inhibitor NB73 in killing MM cells. Venetoclax has shown effects in 6% of non-t(11;14) and 27% of t(11;14) MM cases. The NB73-Venetoclax combination barely induces acute toxicity in vivo and represses MM cells in vivo and ex vivo. NB73 enhances the ubiquitination and proteasomal degradation of FOXM1, an effect further amplified by Venetoclax. The NB73-Venetoclax combination abolishes FOXM1's binding to promoters of key MYC pathway genes, such as PLK1, leading to significant downregulation of their expression. Furthermore, the PLK1-specific inhibitor GSK461364 synergizes with NB73 to inhibit MM cell growth. Interestingly, NB73 does not sensitize U266 cells, a Venetoclax-resistant t(11;14) MM cell line expressing high FOXM1, to Venetoclax treatment, which is corrected by a new-generation BH3 mimetic Sonrotoclax and ALK inhibitor Ceritinib. Collectively, targeting FOXM1 demonstrates significant potential for enhancing the efficacy of FDA-approved drugs in RRMM. These findings shed new light on the discouraging outcomes of the Phase-III CANOVA study centering Venetoclax with an encouraging molecular clue.
复发难治性多发性骨髓瘤(RRMM)仍然是多发性骨髓瘤死亡的主要原因。叉头框蛋白M1(FOXM1)与RRMM密切相关,使其成为一个极具吸引力的治疗靶点。通过三次低通量筛选,我们确定了九种美国食品药品监督管理局(FDA)批准的药物,包括BH3模拟物维奈克拉,它们与FOXM1抑制剂NB73协同作用以杀死骨髓瘤细胞。维奈克拉在6%的非t(11;14)和27%的t(11;14)骨髓瘤病例中显示出疗效。NB73-维奈克拉组合在体内几乎不诱导急性毒性,并且在体内和体外均能抑制骨髓瘤细胞。NB73增强了FOXM1的泛素化和蛋白酶体降解,维奈克拉进一步放大了这种作用。NB73-维奈克拉组合消除了FOXM1与关键MYC通路基因(如PLK1)启动子的结合,导致其表达显著下调。此外,PLK1特异性抑制剂GSK461364与NB73协同抑制骨髓瘤细胞生长。有趣的是,NB73不能使U266细胞(一种表达高FOXM1的维奈克拉耐药t(11;14)骨髓瘤细胞系)对维奈克拉治疗敏感,新一代BH3模拟物索诺托克拉和ALK抑制剂色瑞替尼可纠正这一情况。总的来说,靶向FOXM1在增强FDA批准药物治疗RRMM的疗效方面显示出巨大潜力。这些发现为以维奈克拉为中心的III期CANOVA研究令人沮丧的结果提供了新的线索,带来了令人鼓舞的分子线索。