Division of Experimental Pathology, Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States; Pittsburgh Liver Research Center, Pittsburgh, PA, United States.
Department of Developmental Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States.
Adv Cancer Res. 2022;156:283-317. doi: 10.1016/bs.acr.2022.02.003. Epub 2022 Mar 9.
Intrahepatic cholangiocarcinoma (iCCA), the second most common primary liver cancer, is a highly lethal epithelial cell malignancy exhibiting features of cholangiocyte differentiation. iCCAs can potentially develop from multiple cell types of origin within liver, including immature or mature cholangiocytes, hepatic stem cells/progenitor cells, and from transdifferentiation of hepatocytes. Understanding the molecular mechanisms and genetic drivers that diversely drive specific cell lineage pathways leading to iCCA has important biological and clinical implications. In this context, activation of the YAP1-TEAD dependent transcription, driven by Hippo-dependent or -independent diverse mechanisms that lead to the stabilization of YAP1 is crucially important to biliary fate commitment in hepatobiliary cancer. In preclinical models, YAP1 activation in hepatocytes or cholangiocytes is sufficient to drive their malignant transformation into iCCA. Moreover, nuclear YAP1/TAZ is highly prevalent in human iCCA irrespective of the varied etiology, and significantly correlates with poor prognosis in iCCA patients. Based on the ubiquitous expression and diverse physiologic roles for YAP1/TAZ in the liver, recent studies have further revealed distinct functions of active YAP1/TAZ in regulating tumor metabolism, as well as the tumor immune microenvironment. In the current review, we discuss our current understanding of the various roles of the Hippo-YAP1 signaling in iCCA pathogenesis, with a specific focus on the roles played by the Hippo-YAP1 pathway in modulating biliary commitment and oncogenicity, iCCA metabolism, and immune microenvironment. We also discuss the therapeutic potential of targeting the YAP1/TAZ-TEAD transcriptional machinery in iCCA, its current limitations, and what future studies are needed to facilitate clinical translation.
肝内胆管癌(iCCA)是第二大常见的原发性肝癌,是一种具有胆管细胞分化特征的高度致命上皮细胞恶性肿瘤。iCCA 可能起源于肝脏内的多种细胞类型,包括未成熟或成熟的胆管细胞、肝干细胞/祖细胞,以及肝细胞的转分化。了解多样化驱动特定细胞谱系途径导致 iCCA 的分子机制和遗传驱动因素具有重要的生物学和临床意义。在这种情况下,YAP1-TEAD 依赖性转录的激活,由 Hippo 依赖性或非依赖性的多种机制驱动,导致 YAP1 的稳定,对于肝胆癌中的胆管命运决定至关重要。在临床前模型中,肝细胞或胆管细胞中 YAP1 的激活足以驱动它们恶性转化为 iCCA。此外,核 YAP1/TAZ 在人类 iCCA 中高度普遍,无论病因如何,并且与 iCCA 患者的预后显著相关。基于 YAP1/TAZ 在肝脏中的普遍表达和多种生理作用,最近的研究进一步揭示了活跃的 YAP1/TAZ 在调节肿瘤代谢以及肿瘤免疫微环境中的不同功能。在当前的综述中,我们讨论了我们对 Hippo-YAP1 信号在 iCCA 发病机制中的各种作用的理解,特别关注 Hippo-YAP1 途径在调节胆管决定和致癌性、iCCA 代谢和免疫微环境方面的作用。我们还讨论了靶向 YAP1/TAZ-TEAD 转录机制治疗 iCCA 的潜力、其当前的局限性,以及需要进行哪些未来研究来促进临床转化。