Department of Organ Anatomy, Tohoku University Graduate School of Medicine, Sendai, Japan.
Department of Neurosurgery, Tohoku University Graduate School of Medicine, Sendai, Japan.
Mol Oncol. 2022 Jan;16(1):289-306. doi: 10.1002/1878-0261.13130. Epub 2021 Nov 9.
Isocitrate dehydrogenase 1 (IDH1) is a key enzyme in cellular metabolism. IDH1 mutation (IDH1mut) is the most important genetic alteration in lower grade glioma, whereas glioblastoma (GB), the most common malignant brain tumor, often has wild-type IDH1 (IDH1wt). Although there is no effective treatment yet for neither IDH1wt nor IDHmut GB, it is important to note that the survival span of IDH1wt GB patients is significantly shorter than those with IDH1mut GB. Thus, understanding IDH1wt GB biology and developing effective molecular-targeted therapies is of paramount importance. Fatty acid-binding protein 7 (FABP7) is highly expressed in GB, and its expression level is negatively correlated with survival in malignant glioma patients; however, the underlying mechanisms of FABP7 involvement in tumor proliferation are still unknown. In this study, we demonstrate that FABP7 is highly expressed and localized in nuclei in IDH1wt glioma. Wild-type FABP7 (FABP7wt) overexpression in IDH1wt U87 cells increased cell proliferation rate, caveolin-1 expression, and caveolae/caveosome formation. In addition, FABP7wt overexpression increased the levels of H3K27ac on the caveolin-1 promoter through controlling the nuclear acetyl-CoA level via the interaction with ACLY. Consistent results were obtained using a xenograft model transplanted with U87 cells overexpressing FABP7. Interestingly, in U87 cells with mutant FABP7 overexpression, both in vitro and in vivo phenotypes shown by FABP7wt overexpression were disrupted. Furthermore, IDH1wt patient GB showed upregulated caveolin-1 expression, increased levels of histone acetylation, and increased levels of acetyl-CoA compared with IDH1mut patient GB. Taken together, these data suggest that nuclear FABP7 is involved in cell proliferation of GB through caveolae function/formation regulated via epigenetic regulation of caveolin-1, and this mechanism is critically important for IDH1wt tumor biology.
异柠檬酸脱氢酶 1(IDH1)是细胞代谢中的关键酶。IDH1 突变(IDH1mut)是低级别胶质瘤中最重要的遗传改变,而胶质母细胞瘤(GB)是最常见的恶性脑肿瘤,通常具有野生型 IDH1(IDH1wt)。尽管目前对于 IDH1wt 或 IDHmutGB 都没有有效的治疗方法,但需要注意的是,IDH1wtGB 患者的生存时间明显短于 IDH1mutGB 患者。因此,了解 IDH1wtGB 的生物学特性并开发有效的分子靶向治疗方法至关重要。脂肪酸结合蛋白 7(FABP7)在 GB 中高度表达,其表达水平与恶性胶质瘤患者的生存呈负相关;然而,FABP7 参与肿瘤增殖的潜在机制尚不清楚。在这项研究中,我们证明 FABP7 在 IDH1wt 神经胶质瘤中高度表达并定位于核内。在 IDH1wtU87 细胞中过表达野生型 FABP7(FABP7wt)会增加细胞增殖率、窖蛋白-1 的表达和小窝/小窝体的形成。此外,FABP7wt 通过与 ACLY 相互作用控制核乙酰辅酶 A 水平,从而增加窖蛋白-1 启动子上的 H3K27ac 水平。在移植了过表达 FABP7 的 U87 细胞的异种移植模型中获得了一致的结果。有趣的是,在过表达突变型 FABP7 的 U87 细胞中,FABP7wt 过表达所表现出的体外和体内表型都被破坏。此外,与 IDH1mut 患者的 GB 相比,IDH1wt 患者的 GB 显示窖蛋白-1 表达上调、组蛋白乙酰化水平升高和乙酰辅酶 A 水平升高。总之,这些数据表明,核 FABP7 通过 caveolin-1 的表观遗传调控参与 GB 细胞的增殖,通过调节小窝/小窝体的形成来发挥作用,而这种机制对于 IDH1wt 肿瘤生物学至关重要。