Institute of Neuropathology, Schmelzbergstr. 12, 8091 Zurich, Switzerland.
Brain. 2011 Sep;134(Pt 9):2595-609. doi: 10.1093/brain/awr201. Epub 2011 Aug 19.
Accumulation of the DNA/RNA binding protein fused in sarcoma as cytoplasmic inclusions in neurons and glial cells is the pathological hallmark of all patients with amyotrophic lateral sclerosis with mutations in FUS as well as in several subtypes of frontotemporal lobar degeneration, which are not associated with FUS mutations. The mechanisms leading to inclusion formation and fused in sarcoma-associated neurodegeneration are only poorly understood. Because fused in sarcoma belongs to a family of proteins known as FET, which also includes Ewing's sarcoma and TATA-binding protein-associated factor 15, we investigated the potential involvement of these other FET protein family members in the pathogenesis of fused in sarcoma proteinopathies. Immunohistochemical analysis of FET proteins revealed a striking difference among the various conditions, with pathology in amyotrophic lateral sclerosis with FUS mutations being labelled exclusively for fused in sarcoma, whereas fused in sarcoma-positive inclusions in subtypes of frontotemporal lobar degeneration also consistently immunostained for TATA-binding protein-associated factor 15 and variably for Ewing's sarcoma. Immunoblot analysis of proteins extracted from post-mortem tissue of frontotemporal lobar degeneration with fused in sarcoma pathology demonstrated a relative shift of all FET proteins towards insoluble protein fractions, while genetic analysis of the TATA-binding protein-associated factor 15 and Ewing's sarcoma gene did not identify any pathogenic variants. Cell culture experiments replicated the findings of amyotrophic lateral sclerosis with FUS mutations by confirming the absence of TATA-binding protein-associated factor 15 and Ewing's sarcoma alterations upon expression of mutant fused in sarcoma. In contrast, all endogenous FET proteins were recruited into cytoplasmic stress granules upon general inhibition of Transportin-mediated nuclear import, mimicking the findings in frontotemporal lobar degeneration with fused in sarcoma pathology. These results allow a separation of fused in sarcoma proteinopathies caused by FUS mutations from those without a known genetic cause based on neuropathological features. More importantly, our data imply different pathological processes underlying inclusion formation and cell death between both conditions; the pathogenesis in amyotrophic lateral sclerosis with FUS mutations appears to be more restricted to dysfunction of fused in sarcoma, while a more global and complex dysregulation of all FET proteins is involved in the subtypes of frontotemporal lobar degeneration with fused in sarcoma pathology.
融合基因 FUS 肉瘤相关蛋白在神经元和神经胶质细胞中的细胞质内包涵体的积累是所有 FUS 突变型肌萎缩侧索硬化症患者以及与 FUS 突变无关的几种额颞叶变性亚型患者的病理标志。导致包涵体形成和融合基因 FUS 相关性神经退行性变的机制尚不完全清楚。由于融合基因 FUS 属于 FET 蛋白家族的一员,该家族还包括尤因肉瘤和 TATA 结合蛋白相关因子 15,因此我们研究了这些其他 FET 蛋白家族成员在融合基因 FUS 蛋白病发病机制中的潜在作用。FET 蛋白的免疫组化分析显示,在各种情况下存在显著差异,FUS 突变型肌萎缩侧索硬化症的病理学仅标记融合基因 FUS,而额颞叶变性亚型的融合基因 FUS 阳性包涵体也始终免疫染色 TATA 结合蛋白相关因子 15,并可变地染色尤因肉瘤。从融合基因 FUS 病理学额颞叶变性的尸检组织中提取的蛋白质进行免疫印迹分析显示,所有 FET 蛋白均向不溶性蛋白部分发生相对转移,而 TATA 结合蛋白相关因子 15 和尤因肉瘤基因的遗传分析并未发现任何致病性变异。细胞培养实验通过确认在表达突变融合基因 FUS 时不存在 TATA 结合蛋白相关因子 15 和尤因肉瘤改变,复制了 FUS 突变型肌萎缩侧索硬化症的发现。相比之下,在一般抑制 Transportin 介导的核输入后,所有内源性 FET 蛋白均被募集到细胞质应激颗粒中,模拟了融合基因 FUS 病理学额颞叶变性的发现。这些结果允许根据神经病理学特征将由 FUS 突变引起的融合基因 FUS 蛋白病与无已知遗传原因的融合基因 FUS 蛋白病区分开来。更重要的是,我们的数据表明,两种情况下包涵体形成和细胞死亡的病理过程不同;FUS 突变型肌萎缩侧索硬化症的发病机制似乎更局限于融合基因 FUS 的功能障碍,而融合基因 FUS 病理学额颞叶变性的所有 FET 蛋白的更广泛和复杂的失调涉及其中。