Department of Experimental Radiation Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas.
Department of Pathology and Helen Diller Cancer Center, University of California, San Francisco, California.
Mol Cancer Ther. 2024 Apr 2;23(4):492-506. doi: 10.1158/1535-7163.MCT-23-0414.
Metastatic disease remains the leading cause of death due to cancer, yet the mechanism(s) of metastasis and its timely detection remain to be elucidated. Neutrophil elastase (NE), a serine protease secreted by neutrophils, is a crucial mediator of chronic inflammation and tumor progression. In this study, we used the PyMT model (NE+/+ and NE-/-) of breast cancer to interrogate the tumor-intrinsic and -extrinsic mechanisms by which NE can promote metastasis. Our results showed that genetic ablation of NE significantly reduced lung metastasis and improved metastasis-free survival. RNA-sequencing analysis of primary tumors indicated differential regulation of tumor-intrinsic actin cytoskeleton signaling pathways by NE. These NE-regulated pathways are critical for cell-to-cell contact and motility and consistent with the delay in metastasis in NE-/- mice. To evaluate whether pharmacologic inhibition of NE inhibited pulmonary metastasis and phenotypically mimicked PyMT NE-/- mice, we utilized AZD9668, a clinically available and specific NE inhibitor. We found AZD9668 treated PyMT-NE+/+ mice showed significantly reduced lung metastases, improved recurrence-free, metastasis-free and overall survival, and their tumors showed similar molecular alterations as those observed in PyMT-NE-/- tumors. Finally, we identified a NE-specific signature that predicts recurrence and metastasis in patients with breast cancer. Collectively, our studies suggest that genetic ablation and pharmacologic inhibition of NE reduces metastasis and extends survival of mouse models of breast cancer, providing rationale to examine NE inhibitors as a treatment strategy for the clinical management of patients with metastatic breast cancer.
转移性疾病仍然是癌症死亡的主要原因,但转移的机制及其及时检测仍有待阐明。中性粒细胞弹性蛋白酶(NE),一种由中性粒细胞分泌的丝氨酸蛋白酶,是慢性炎症和肿瘤进展的关键介质。在这项研究中,我们使用 PyMT 乳腺癌模型(NE+/+ 和 NE-/-)来探究 NE 促进转移的肿瘤内在和外在机制。我们的结果表明,NE 的基因缺失显著减少了肺转移并提高了无转移生存率。对原发肿瘤的 RNA 测序分析表明,NE 对肿瘤内在肌动蛋白细胞骨架信号通路进行了差异调节。这些由 NE 调节的通路对于细胞间接触和运动至关重要,与 NE-/- 小鼠转移延迟一致。为了评估 NE 的药理学抑制是否抑制了肺转移并在表型上模拟 PyMT NE-/- 小鼠,我们利用了 AZD9668,一种临床可用的特异性 NE 抑制剂。我们发现,AZD9668 处理的 PyMT-NE+/+ 小鼠的肺转移明显减少,复发无、转移无和总生存率提高,其肿瘤显示出与 PyMT-NE-/- 肿瘤中观察到的类似的分子改变。最后,我们确定了一个预测乳腺癌患者复发和转移的 NE 特异性特征。总之,我们的研究表明,NE 的基因缺失和药理学抑制可减少乳腺癌小鼠模型的转移并延长其生存,为研究 NE 抑制剂作为转移性乳腺癌患者临床治疗策略提供了依据。