Powell Reid T, Rinkenbaugh Amanda L, Guo Lei, Cai Shirong, Shao Jiansu, Zhou Xinhui, Zhang Xiaomei, Jeter-Jones Sabrina, Fu Chunxiao, Qi Yuan, Baameur Hancock Faiza, White Jason B, Stephan Clifford, Davies Peter J, Moulder Stacy, Symmans W Fraser, Chang Jeffrey T, Piwnica-Worms Helen
Center for Translational Cancer Research, Institute of Bioscience and Technology Texas A&M Health Science Center, Houston, TX, USA.
Department of Experimental Radiation Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
NPJ Breast Cancer. 2024 May 27;10(1):37. doi: 10.1038/s41523-024-00644-4.
Triple negative breast cancer (TNBC) accounts for 15-20% of breast cancer cases in the United States. Systemic neoadjuvant chemotherapy (NACT), with or without immunotherapy, is the current standard of care for patients with early-stage TNBC. However, up to 70% of TNBC patients have significant residual disease once NACT is completed, which is associated with a high risk of developing recurrence within two to three years of surgical resection. To identify targetable vulnerabilities in chemoresistant TNBC, we generated longitudinal patient-derived xenograft (PDX) models from TNBC tumors before and after patients received NACT. We then compiled transcriptomes and drug response profiles for all models. Transcriptomic analysis identified the enrichment of aberrant protein homeostasis pathways in models from post-NACT tumors relative to pre-NACT tumors. This observation correlated with increased sensitivity in vitro to inhibitors targeting the proteasome, heat shock proteins, and neddylation pathways. Pevonedistat, a drug annotated as a NEDD8-activating enzyme (NAE) inhibitor, was prioritized for validation in vivo and demonstrated efficacy as a single agent in multiple PDX models of TNBC. Pharmacotranscriptomic analysis identified a pathway-level correlation between pevonedistat activity and post-translational modification (PTM) machinery, particularly involving neddylation and sumoylation targets. Elevated levels of both NEDD8 and SUMO1 were observed in models exhibiting a favorable response to pevonedistat compared to those with a less favorable response in vivo. Moreover, a correlation emerged between the expression of neddylation-regulated pathways and tumor response to pevonedistat, indicating that targeting these PTM pathways may prove effective in combating chemoresistant TNBC.
三阴性乳腺癌(TNBC)在美国乳腺癌病例中占15%-20%。全身新辅助化疗(NACT),无论是否联合免疫治疗,是早期TNBC患者目前的标准治疗方法。然而,高达70%的TNBC患者在完成NACT后仍有显著残留病灶,这与手术切除后两到三年内复发的高风险相关。为了确定化疗耐药性TNBC中可靶向的脆弱点,我们从TNBC患者接受NACT前后的肿瘤中生成了纵向患者来源的异种移植(PDX)模型。然后,我们编制了所有模型的转录组和药物反应谱。转录组分析发现,相对于NACT前肿瘤,NACT后肿瘤模型中异常蛋白质稳态途径富集。这一观察结果与体外对靶向蛋白酶体、热休克蛋白和NEDD化途径的抑制剂的敏感性增加相关。pevonedistat是一种被标注为NEDD8激活酶(NAE)抑制剂的药物,被优先用于体内验证,并在多个TNBC的PDX模型中显示出单药疗效。药物转录组学分析确定了pevonedistat活性与翻译后修饰(PTM)机制之间的途径水平相关性,特别是涉及NEDD化和SUMO化靶点。与体内反应较差的模型相比,在对pevonedistat有良好反应的模型中观察到NEDD8和SUMO1水平均升高。此外,NEDD化调节途径的表达与肿瘤对pevonedistat的反应之间出现了相关性,表明靶向这些PTM途径可能对对抗化疗耐药性TNBC有效。