Department of Medical Oncology, The First Hospital of China Medical University, Shenyang, China.
Key Laboratory of Anticancer Drugs and Biotherapy of Liaoning Province, The First Hospital of China Medical University, Shenyang, China.
Oncogene. 2024 Sep;43(37):2768-2780. doi: 10.1038/s41388-024-03124-y. Epub 2024 Aug 13.
Peritoneal metastasis is one of the most common risk factors contributing to the poor prognosis of gastric cancer. We previously reported that extracellular vesicles from gastric cancer cells could facilitate peritoneal metastasis. However, their impact on gastric cancer-induced peritoneal metastasis under hypoxic conditions remains unclear. This study aims to elucidate how hypoxia-resistant gastric cancer cell-derived extracellular vesicles affect the peritoneal metastasis of normoxic gastric cancer cells. Proteomic analysis revealed elevated levels of Caveolin1 and Laminin β2 in hypoxia-resistant gastric cancer cells and their corresponding extracellular vesicles. Importantly, Caveolin1 was found to play a central role in mediating Laminin β2 sorting into extracellular vesicles derived from hypoxia-resistant gastric cancer cells, and subsequently, extracellular vesicle-associated Laminin β2 promoted peritoneal metastasis in normoxic gastric cancer cells by activating the AKT pathway. Further investigation confirmed that Caveolin1 activation by Rho-related Coiled-coil kinase 1-mediated phosphorylation of Y14 residue is a key factor facilitating Laminin β2 sorting into extracellular vesicles. Moreover, Y14 phosphorylated- Caveolin1 enhanced Laminin β2 sorting by activating Rab11. Finally, our study demonstrated that a combined assessment of plasma extracellular vesicle-associated Caveolin1 and extracellular vesicle-associated Laminin β2 could provide an accurate predictive tool for peritoneal metastasis occurrence in gastric cancer.
腹膜转移是导致胃癌预后不良的最常见危险因素之一。我们之前报道过,胃癌细胞来源的细胞外囊泡可促进腹膜转移。然而,它们在缺氧条件下对胃癌诱导的腹膜转移的影响尚不清楚。本研究旨在阐明耐缺氧胃癌细胞来源的细胞外囊泡如何影响常氧胃癌细胞的腹膜转移。蛋白质组学分析显示,耐缺氧胃癌细胞及其相应的细胞外囊泡中 Caveolin1 和 Laminin β2 的水平升高。重要的是,发现 Caveolin1 在介导耐缺氧胃癌细胞来源的细胞外囊泡中 Laminin β2 的分拣中起核心作用,并且随后,细胞外囊泡相关的 Laminin β2 通过激活 AKT 通路促进常氧胃癌细胞的腹膜转移。进一步的研究证实,Rho 相关卷曲螺旋激酶 1 介导的 Y14 残基磷酸化激活 Caveolin1 是促进 Laminin β2 分拣到细胞外囊泡中的关键因素。此外,Y14 磷酸化的 Caveolin1 通过激活 Rab11 增强了 Laminin β2 的分拣。最后,我们的研究表明,联合评估血浆细胞外囊泡相关 Caveolin1 和细胞外囊泡相关 Laminin β2 可提供一种用于预测胃癌腹膜转移发生的准确工具。