Wu Chia-Hao, Yuen Kit L, Molony Ryan D, Silvers Christopher R, Akash Md Mahmudul Hasan, Messing Edward M, Lee Yi-Fen
Department of Pathology & Laboratory Medicine, University of Rochester Medical Center, Rochester, NY14642, USA.
Department of Urology, University of Rochester Medical Center, Rochester, NY14642, USA.
Oncogene. 2025 Apr 11. doi: 10.1038/s41388-025-03380-6.
Bladder cancer (BC) patients face high rates of disease recurrence, partially driven by the cancer field effect. This effect is mediated in part by the release of pro-tumorigenic cargos in membrane-enclosed extracellular vesicles (EVs), but the specific underlying mechanisms remain poorly understood. Protein disulfide isomerase (PDIA1) catalyze disulfide bond formation and can help mitigate endoplasmic reticulum (ER) stress, potentially supporting tumor survival. Here, BC cells were found to exhibit better survival under ER stress when PDIA1 was downregulated. These cells maintained homeostatic PDIA1 levels through the EV-mediated release of PDIA1. Chronic exposure of urothelial cells to these PDIA1-enriched BCEVs induced oxidative stress and DNA damage, ultimately leading to the malignant transformation of recipient cells. The EV-transformed cells exhibited DNA damage patterns potentially attributable to oxidative damage, and PDIA1 was found to be a key tumorigenic cargo within EVs. Tissue microarray analyses of BC recurrence confirmed a significant correlation between tumor recurrence and the levels of both PDIA1 and ER stress. Together, these data suggest that cancer cells selectively sort oxidized PDIA1 into EVs for removal, and these EVs can, in turn, induce oxidative stress in recipient urothelial cells, predisposing them to malignant transformation and thereby increasing the risk of recurrence.
膀胱癌(BC)患者面临着较高的疾病复发率,部分原因是癌症场效应。这种效应部分是由膜包裹的细胞外囊泡(EVs)中促肿瘤物质的释放介导的,但具体的潜在机制仍知之甚少。蛋白质二硫键异构酶(PDIA1)催化二硫键的形成,并有助于减轻内质网(ER)应激,可能支持肿瘤存活。在这里,研究发现当PDIA1下调时,BC细胞在ER应激下表现出更好的存活率。这些细胞通过EV介导的PDIA1释放来维持PDIA1水平的稳态。尿路上皮细胞长期暴露于这些富含PDIA1的BCEVs会诱导氧化应激和DNA损伤,最终导致受体细胞的恶性转化。经EV转化的细胞表现出可能归因于氧化损伤的DNA损伤模式,并且发现PDIA1是EVs中的关键致瘤物质。对BC复发的组织芯片分析证实,肿瘤复发与PDIA1水平和ER应激之间存在显著相关性。总之,这些数据表明癌细胞选择性地将氧化的PDIA1分选到EVs中以进行清除,而这些EVs反过来又可以在受体尿路上皮细胞中诱导氧化应激,使它们易于发生恶性转化,从而增加复发风险。