Lee Donghee, Kozurek Emma C, Abdullah Md, Wong Ethan J, Li Rong, Liu Zhiyan Silvia, Nguyen Hai Dang, Dickerson Erin B, Kim Jong Hyuk
Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL, USA.
Animal Cancer Care and Research Program, University of Minnesota, St Paul, MN, USA.
Cancer Gene Ther. 2025 Feb;32(2):254-267. doi: 10.1038/s41417-024-00867-4. Epub 2024 Dec 21.
Angiosarcomas are a group of vascular cancers that form malignant blood vessels. These malignancies are seemingly inflamed primarily due to their pathognomonic nature, which consists of irregular endothelium and tortuous blood channels. PIK3CA mutations are oncogenic and disrupt the PI3K pathway. In this study, we aimed to define the molecular and functional consequences of oncogenic PIK3CA mutations in angiosarcoma. We first generated two isogenic hemangiosarcoma cell lines harboring the H1047R hotspot mutations in PIK3CA gene using CRISPR/Cas9. We found PIK3CA-mutant cells established distinct molecular signatures in global gene expression and chromatin accessibility, which were associated with enrichment of immune cytokine signaling, including IL-6, IL-8, and MCP-1. These molecular processes were disrupted by the PI3K-α specific inhibitor, alpelisib. We also observed that the molecular distinctions in PIK3CA-mutant cells were linked to metabolic reprogramming in glycolytic activity and mitochondrial respiration. Our multi-omics analysis revealed that activating PIK3CA mutations regulate molecular machinery that contributes to phenotypic alterations and resistance to alpelisib. Furthermore, we identified potential therapeutic vulnerabilities of PIK3CA mutations in response to PI3K-α inhibition mediated by MAPK signaling. In summary, we demonstrate that PIK3CA mutations perpetuate PI3K activation and reinforce immune enrichment to promote drug resistance in vascular cancers.
血管肉瘤是一组形成恶性血管的血管性癌症。这些恶性肿瘤似乎主要因其独特的病理特征而表现出炎症,其病理特征包括不规则的内皮细胞和迂曲的血道。PIK3CA突变具有致癌性,会破坏PI3K信号通路。在本研究中,我们旨在确定血管肉瘤中致癌性PIK3CA突变的分子和功能后果。我们首先使用CRISPR/Cas9技术构建了两个携带PIK3CA基因H1047R热点突变的同基因血管肉瘤细胞系。我们发现PIK3CA突变细胞在整体基因表达和染色质可及性方面建立了独特的分子特征,这与免疫细胞因子信号通路的富集有关,包括IL-6、IL-8和MCP-1。这些分子过程被PI3K-α特异性抑制剂阿培利司破坏。我们还观察到PIK3CA突变细胞中的分子差异与糖酵解活性和线粒体呼吸中的代谢重编程有关。我们的多组学分析表明,激活PIK3CA突变会调节分子机制,导致表型改变和对阿培利司的耐药性。此外,我们确定了PIK3CA突变在应对由MAPK信号介导的PI3K-α抑制时的潜在治疗弱点。总之,我们证明PIK3CA突变使PI3K持续激活并增强免疫富集,从而促进血管性癌症中的耐药性。