Department of Molecular, Cell and Cancer Biology.
Department of Radiation Oncology.
J Clin Invest. 2024 Oct 1;134(22):e181368. doi: 10.1172/JCI181368.
The high rate of recurrence after radiation therapy in triple-negative breast cancer (TNBC) indicates that novel approaches and targets are needed to enhance radiosensitivity. Here, we report that neuropilin-2 (NRP2), a receptor for vascular endothelial growth factor (VEGF) that is enriched on subpopulations of TNBC cells with stem cell properties, is an effective therapeutic target for sensitizing TNBC to radiotherapy. Specifically, VEGF/NRP2 signaling induces nitric oxide synthase 2 (NOS2) transcription by a mechanism dependent on Gli1. NRP2-expressing tumor cells serve as a hub to produce nitric oxide (NO), an autocrine and paracrine signaling metabolite, which promotes cysteine-nitrosylation of Kelch-like ECH-associated protein 1 (KEAP1) and, consequently, nuclear factor erythroid 2-related factor 2-mediated (NFE2L2-mediated) transcription of antioxidant response genes. Inhibiting VEGF binding to NRP2, using a humanized mAb, results in NFE2L2 degradation via KEAP1, rendering cell lines and organoids vulnerable to irradiation. Importantly, treatment of patient-derived xenografts with the NRP2 mAb and radiation resulted in significant tumor necrosis and regression compared with radiation alone. Together, these findings reveal a targetable mechanism of radioresistance, and they support the use of NRP2 mAb as an effective radiosensitizer in TNBC.
在三阴性乳腺癌(TNBC)中,放射治疗后的高复发率表明需要新的方法和靶点来增强放射敏感性。在这里,我们报告神经纤毛蛋白-2(NRP2)是血管内皮生长因子(VEGF)的受体,在具有干细胞特性的 TNBC 细胞亚群中丰富,是一种有效的治疗靶点,可以使 TNBC 对放射治疗敏感。具体而言,VEGF/NRP2 信号通过依赖 Gli1 的机制诱导一氧化氮合酶 2(NOS2)转录。表达 NRP2 的肿瘤细胞充当产生一氧化氮(NO)的中心,NO 是一种自分泌和旁分泌信号代谢物,促进 Kelch 样 ECH 相关蛋白 1(KEAP1)的半胱氨酸-亚硝基化,进而导致核因子红细胞 2 相关因子 2 介导的(NFE2L2 介导的)抗氧化反应基因转录。使用人源化 mAb 抑制 VEGF 与 NRP2 的结合,导致 KEAP1 介导的 NFE2L2 降解,使细胞系和类器官对辐射敏感。重要的是,与单独放疗相比,用 NRP2 mAb 和放疗治疗患者来源的异种移植,导致肿瘤坏死和消退显著。总之,这些发现揭示了一种可靶向的放射抵抗机制,并支持使用 NRP2 mAb 作为 TNBC 的有效放射增敏剂。