Martiskainen Henna, Willman Roosa-Maria, Harju Päivi, Heikkinen Sami, Heiskanen Mette, Müller Stephan A, Sinisalo Rosa, Takalo Mari, Mäkinen Petra, Kuulasmaa Teemu, Pekkala Viivi, Galván Del Rey Ana, Juopperi Sini-Pauliina, Jeskanen Heli, Kervinen Inka, Saastamoinen Kirsi, Niiranen Marja, Heikkinen Sami V, Kurki Mitja I, Marttila Jarkko, Mäkinen Petri I, Rostalski Hannah, Hietanen Tomi, Ngandu Tiia, Lehtisalo Jenni, Bellenguez Céline, Lambert Jean-Charles, Haass Christian, Rinne Juha, Hakumäki Juhana, Rauramaa Tuomas, Krüger Johanna, Soininen Hilkka, Haapasalo Annakaisa, Lichtenthaler Stefan F, Leinonen Ville, Solje Eino, Hiltunen Mikko
Institute of Biomedicine, University of Eastern Finland, Kuopio, Finland.
German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Mol Neurodegener. 2025 Apr 29;20(1):50. doi: 10.1186/s13024-025-00830-3.
Biallelic loss-of-function variants in TYROBP and TREM2 cause autosomal recessive presenile dementia with bone cysts known as Nasu-Hakola disease (NHD, alternatively polycystic lipomembranous osteodysplasia with sclerosing leukoencephalopathy, PLOSL). Some other TREM2 variants contribute to the risk of Alzheimer's disease (AD) and frontotemporal dementia, while deleterious TYROBP variants are globally extremely rare and their role in neurodegenerative diseases remains unclear. The population history of Finns has favored the enrichment of deleterious founder mutations, including a 5.2 kb deletion encompassing exons 1-4 of TYROBP and causing NHD in homozygous carriers. We used here a proxy marker to identify monoallelic TYROBP deletion carriers in the Finnish biobank study FinnGen combining genome and health registry data of 520,210 Finns. We show that monoallelic TYROBP deletion associates with an increased risk and earlier onset age of AD and dementia when compared to noncarriers. In addition, we present the first reported case of a monoallelic TYROBP deletion carrier with NHD-type bone cysts. Mechanistically, monoallelic TYROBP deletion leads to decreased levels of DAP12 protein (encoded by TYROBP) in myeloid cells. Using transcriptomic and proteomic analyses of human monocyte-derived microglia-like cells, we show that upon lipopolysaccharide stimulation monoallelic TYROBP deletion leads to the upregulation of the inflammatory response and downregulation of the unfolded protein response when compared to cells with two functional copies of TYROBP. Collectively, our findings indicate TYROBP deletion as a novel risk factor for AD and suggest specific pathways for therapeutic targeting.
TYROBP和TREM2的双等位基因功能丧失变异会导致常染色体隐性早老性痴呆,并伴有骨囊肿,即纳苏 - 哈科拉病(NHD,又称多囊性脂膜性骨发育异常伴硬化性白质脑病,PLOSL)。其他一些TREM2变异会增加患阿尔茨海默病(AD)和额颞叶痴呆的风险,而有害的TYROBP变异在全球极为罕见,其在神经退行性疾病中的作用仍不清楚。芬兰人的群体历史有利于有害奠基者突变的富集,包括一个5.2 kb的缺失,该缺失涵盖TYROBP的外显子1 - 4,导致纯合携带者患NHD。在芬兰生物银行研究FinnGen中,我们结合520,210名芬兰人的基因组和健康登记数据,使用一个替代标记来识别单等位基因TYROBP缺失携带者。我们发现,与非携带者相比,单等位基因TYROBP缺失与AD和痴呆的风险增加及发病年龄提前有关。此外,我们报告了首例患有NHD型骨囊肿的单等位基因TYROBP缺失携带者。从机制上讲,单等位基因TYROBP缺失会导致髓样细胞中DAP12蛋白(由TYROBP编码)水平降低。通过对人单核细胞衍生的小胶质细胞样细胞进行转录组和蛋白质组分析,我们发现与具有两个功能拷贝TYROBP的细胞相比,在脂多糖刺激下,单等位基因TYROBP缺失会导致炎症反应上调和未折叠蛋白反应下调。总的来说,我们的研究结果表明TYROBP缺失是AD的一个新风险因素,并为治疗靶点提供了特定途径。