Weber Jonasz J, Czisch Leah, Pereira Sena Priscila, Fath Florian, Huridou Chrisovalantou, Schwarz Natasa, Incebacak Eltemur Rana D, Würth Anna, Weishäupl Daniel, Döcker Miriam, Blumenstock Gunnar, Martins Sandra, Sequeiros Jorge, Rouleau Guy A, Jardim Laura Bannach, Saraiva-Pereira Maria-Luiza, França Marcondes C, Gordon Carlos R, Zaltzman Roy, Cornejo-Olivas Mario R, van de Warrenburg Bart P C, Durr Alexandra, Brice Alexis, Bauer Peter, Klockgether Thomas, Schöls Ludger, Riess Olaf, Schmidt Thorsten
Institute of Medical Genetics and Applied Genomics, University of Tübingen, 72076, Tübingen, Germany.
Department of Human Genetics, Ruhr University Bochum, 44801, Bochum, Germany.
Acta Neuropathol. 2024 Aug 1;148(1):14. doi: 10.1007/s00401-024-02762-6.
Machado-Joseph disease (MJD) is an autosomal dominant neurodegenerative spinocerebellar ataxia caused by a polyglutamine-coding CAG repeat expansion in the ATXN3 gene. While the CAG length correlates negatively with the age at onset, it accounts for approximately 50% of its variability only. Despite larger efforts in identifying contributing genetic factors, candidate genes with a robust and plausible impact on the molecular pathogenesis of MJD are scarce. Therefore, we analysed missense single nucleotide polymorphism variants in the PRKN gene encoding the Parkinson's disease-associated E3 ubiquitin ligase parkin, which is a well-described interaction partner of the MJD protein ataxin-3, a deubiquitinase. By performing a correlation analysis in the to-date largest MJD cohort of more than 900 individuals, we identified the V380L variant as a relevant factor, decreasing the age at onset by 3 years in homozygous carriers. Functional analysis in an MJD cell model demonstrated that parkin V380L did not modulate soluble or aggregate levels of ataxin-3 but reduced the interaction of the two proteins. Moreover, the presence of parkin V380L interfered with the execution of mitophagy-the autophagic removal of surplus or damaged mitochondria-thereby compromising cell viability. In summary, we identified the V380L variant in parkin as a genetic modifier of MJD, with negative repercussions on its molecular pathogenesis and disease age at onset.
马查多-约瑟夫病(MJD)是一种常染色体显性神经退行性脊髓小脑共济失调,由ATXN3基因中编码多聚谷氨酰胺的CAG重复序列扩增引起。虽然CAG长度与发病年龄呈负相关,但它仅占其变异性的约50%。尽管在确定相关遗传因素方面付出了更大努力,但对MJD分子发病机制有强大且合理影响的候选基因却很稀少。因此,我们分析了编码帕金森病相关E3泛素连接酶帕金的PRKN基因中的错义单核苷酸多态性变体,帕金是MJD蛋白ataxin-3(一种去泛素化酶)的一个广为人知的相互作用伙伴。通过在迄今最大的900多名个体的MJD队列中进行相关性分析,我们确定V380L变体是一个相关因素,纯合携带者的发病年龄降低了3岁。在MJD细胞模型中的功能分析表明,帕金V380L并未调节ataxin-3的可溶性或聚集水平,但减少了这两种蛋白的相互作用。此外,帕金V380L的存在干扰了线粒体自噬(对多余或受损线粒体的自噬清除)的执行,从而损害细胞活力。总之,我们确定帕金中的V380L变体是MJD的一种遗传修饰因子,对其分子发病机制和疾病发病年龄有负面影响。