Mallin Mikaela M, Rolle Louis T A, Schmidt Michael J, Priyadarsini Nair Shilpa, Zurita Amado J, Kuhn Peter, Hicks James, Pienta Kenneth J, Amend Sarah R
Cancer Ecology Center, James Buchanan Brady Urological Institute, Johns Hopkins Medical Institute, Baltimore, Maryland.
Cellular and Molecular Medicine Graduate Training Program, Johns Hopkins School of Medicine, Baltimore, Maryland.
Mol Cancer Res. 2025 Mar 3;23(3):219-235. doi: 10.1158/1541-7786.MCR-24-0689.
Our research aims to understand the adaptive-ergo potentially metastatic-responses of prostate cancer to changing microenvironments. Emerging evidence implicates a role of the polyaneuploid cancer cell (PACC) state in metastasis, positing the PACC state as capable of conferring metastatic competency. Mounting in vitro evidence supports increased metastatic potential of cells in the PACC state. Additionally, our recent retrospective study revealed that PACC presence in patient prostate tumors at the time of radical prostatectomy was predictive of future metastasis. To test for a causative relationship between PACC state biology and metastasis in prostate cancer, we leveraged a novel method designed for flow cytometric detection of circulating tumor cells (CTC) and disseminated tumor cells (DTC) from animal models. This approach provides both quantitative and qualitative information about the number and PACC status of recovered CTCs and DTCs. Specifically, we applied this approach to the analysis of subcutaneous, caudal artery, and intracardiac murine models. Collating data from all models, we found that 74% of recovered CTCs and DTCs were in the PACC state. Furthermore, in vivo colonization assays proved that PACC populations can regain proliferative capacity at metastatic sites. Additional in vitro analyses revealed a PACC-specific partial epithelial-to-mesenchymal transition phenotype and a prometastatic secretory profile, together providing preliminary evidence of prometastatic mechanisms specific to the PACC state. Implications: Considering that many anticancer agents induce the PACC state, our data position the increased metastatic competency of PACC state cells as an important unforeseen ramification of neoadjuvant regimens, which may help explain clinical correlations between chemotherapy and metastatic progression.
我们的研究旨在了解前列腺癌对不断变化的微环境的适应性——即潜在的转移反应。新出现的证据表明多倍体癌细胞(PACC)状态在转移中起作用,认为PACC状态能够赋予转移能力。越来越多的体外证据支持处于PACC状态的细胞具有更高的转移潜力。此外,我们最近的回顾性研究表明,在根治性前列腺切除术时患者前列腺肿瘤中存在PACC可预测未来转移。为了测试PACC状态生物学与前列腺癌转移之间的因果关系,我们利用了一种设计用于从动物模型中进行流式细胞术检测循环肿瘤细胞(CTC)和播散肿瘤细胞(DTC)的新方法。这种方法提供了有关回收的CTC和DTC的数量和PACC状态的定量和定性信息。具体而言,我们将这种方法应用于皮下、尾动脉和心脏内小鼠模型的分析。整理所有模型的数据后,我们发现74%回收的CTC和DTC处于PACC状态。此外,体内定植试验证明PACC群体可在转移部位恢复增殖能力。额外的体外分析揭示了一种PACC特异性的部分上皮-间质转化表型和一种促转移分泌谱,共同提供了PACC状态特异性促转移机制的初步证据。启示:考虑到许多抗癌药物会诱导PACC状态,我们的数据表明PACC状态细胞转移能力的增强是新辅助治疗方案一个重要的意外后果,这可能有助于解释化疗与转移进展之间的临床相关性。