Department of Oncology, Renmin Hospital of Wuhan University, Wuhan, China.
Division of Experimental Pathology, Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.
Am J Pathol. 2019 May;189(5):1091-1104. doi: 10.1016/j.ajpath.2019.02.002. Epub 2019 Feb 19.
Hepatoblastoma (HB), the most common pediatric primary liver neoplasm, shows nuclear localization of β-catenin and yes-associated protein 1 (YAP1) in almost 80% of the cases. Co-expression of constitutively active S127A-YAP1 and ΔN90 deletion-mutant β-catenin (YAP1-ΔN90-β-catenin) causes HB in mice. Because heterogeneity in downstream signaling is being identified owing to mutational differences even in the β-catenin gene alone, we investigated if co-expression of point mutants of β-catenin (S33Y or S45Y) with S127A-YAP1 led to similar tumors as YAP1-ΔN90-β-catenin. Co-expression of S33Y/S45Y-β-catenin and S127A-YAP1 led to activation of Yap and Wnt signaling and development of HB, with 100% mortality by 13 to 14 weeks. Co-expression with YAP1-S45Y/S33Y-β-catenin of the dominant-negative T-cell factor 4 or dominant-negative transcriptional enhanced associate domain 2, the respective surrogate transcription factors, prevented HB development. Although histologically similar, HB in YAP1-S45Y/S33Y-β-catenin, unlike YAP1-ΔN90-β-catenin HB, was glutamine synthetase (GS) positive. However, both ΔN90-β-catenin and point-mutant β-catenin comparably induced GS-luciferase reporter in vitro. Finally, using a previously reported 16-gene signature, it was shown that YAP1-ΔN90-β-catenin HB tumors exhibited genetic similarities with more proliferative, less differentiated, GS-negative HB patient tumors, whereas YAP1-S33Y/S45Y-β-catenin HB exhibited heterogeneity and clustered with both well-differentiated GS-positive and proliferative GS-negative patient tumors. Thus, we demonstrate that β-catenin point mutants can also collaborate with YAP1 in HB development, albeit with a distinct molecular profile from the deletion mutant, which may have implications in both biology and therapy.
肝母细胞瘤 (HB) 是最常见的小儿原发性肝脏肿瘤,近 80%的病例中β-catenin 和 yes 相关蛋白 1 (YAP1) 呈核定位。在小鼠中,组成性激活 S127A-YAP1 和 ΔN90 缺失突变β-catenin (YAP1-ΔN90-β-catenin) 的共表达导致 HB 的发生。由于仅在β-catenin 基因中就存在突变差异导致下游信号的异质性,因此我们研究了 S127A-YAP1 与β-catenin 点突变 (S33Y 或 S45Y) 的共表达是否会导致类似的肿瘤,就像 YAP1-ΔN90-β-catenin 一样。S33Y/S45Y-β-catenin 和 S127A-YAP1 的共表达导致 Yap 和 Wnt 信号的激活,并发展为 HB,在 13 到 14 周时死亡率达到 100%。与 YAP1-S45Y/S33Y-β-catenin 共表达显性 T 细胞因子 4 或显性转录增强相关域 2,即各自的替代转录因子,可防止 HB 的发展。虽然组织学上相似,但 YAP1-S45Y/S33Y-β-catenin 中的 HB 与 YAP1-ΔN90-β-catenin HB 不同,它是谷氨酰胺合成酶 (GS) 阳性的。然而,ΔN90-β-catenin 和点突变β-catenin 在体外均可诱导 GS-荧光素酶报告基因。最后,使用之前报道的 16 基因特征,表明 YAP1-ΔN90-β-catenin HB 肿瘤与更具增殖性、分化程度更低、GS 阴性的 HB 患者肿瘤具有遗传相似性,而 YAP1-S33Y/S45Y-β-catenin HB 表现出异质性,与分化良好的 GS 阳性和增殖性 GS 阴性患者肿瘤聚类。因此,我们证明β-catenin 点突变也可以与 YAP1 合作在 HB 发育中发挥作用,尽管与缺失突变体具有不同的分子特征,这可能对生物学和治疗都有意义。