Department of Medicine IV, Faculty of Medicine, Medical Center-University of Freiburg, 79106 Freiburg, Germany.
Translational and Clinical Research Institute, Faculty of Medical Sciences, Newcastle University, Newcastle upon Tyne NE1 3BZ, UK.
Am J Hum Genet. 2022 May 5;109(5):928-943. doi: 10.1016/j.ajhg.2022.03.015. Epub 2022 Apr 8.
Organ fibrosis is a shared endpoint of many diseases, yet underlying mechanisms are not well understood. Several pathways governed by the primary cilium, a sensory antenna present on most vertebrate cells, have been linked with fibrosis. Ciliopathies usually start early in life and represent a considerable disease burden. We performed massively parallel sequencing by using cohorts of genetically unsolved individuals with unexplained liver and kidney failure and correlated this with clinical, imaging, and histopathological analyses. Mechanistic studies were conducted with a vertebrate model and primary cells. We detected bi-allelic deleterious variants in TULP3, encoding a critical adaptor protein for ciliary trafficking, in a total of 15 mostly adult individuals, originating from eight unrelated families, with progressive degenerative liver fibrosis, fibrocystic kidney disease, and hypertrophic cardiomyopathy with atypical fibrotic patterns on histopathology. We recapitulated the human phenotype in adult zebrafish and confirmed disruption of critical ciliary cargo composition in several primary cell lines derived from affected individuals. Further, we show interaction between TULP3 and the nuclear deacetylase SIRT1, with roles in DNA damage repair and fibrosis, and report increased DNA damage ex vivo. Transcriptomic studies demonstrated upregulation of profibrotic pathways with gene clusters for hypertrophic cardiomyopathy and WNT and TGF-β signaling. These findings identify variants in TULP3 as a monogenic cause for progressive degenerative disease of major organs in which affected individuals benefit from early detection and improved clinical management. Elucidation of mechanisms crucial for DNA damage repair and tissue maintenance will guide novel therapeutic avenues for this and similar genetic and non-genomic diseases.
器官纤维化是许多疾病的共同终点,但潜在机制尚不清楚。初级纤毛(一种存在于大多数脊椎动物细胞上的感觉天线)所调控的几条通路已与纤维化有关。纤毛病通常在生命早期开始,并代表着相当大的疾病负担。我们使用具有未解释的肝和肾功能衰竭的遗传未解决个体的队列进行了大规模平行测序,并将其与临床、影像学和组织病理学分析相关联。我们使用脊椎动物模型和原代细胞进行了机制研究。我们在总共 15 名主要为成年个体中检测到编码关键纤毛运输衔接蛋白的 TULP3 的双等位有害变异,这些个体来自八个无关家庭,具有进行性退行性肝纤维化、纤维囊性肾病和肥厚型心肌病,组织病理学上具有非典型纤维化模式。我们在成年斑马鱼中重现了人类表型,并证实了受影响个体来源的几种原代细胞系中关键纤毛货物组成的破坏。此外,我们还显示了 TULP3 与核去乙酰化酶 SIRT1 之间的相互作用,该基因在 DNA 损伤修复和纤维化中起作用,并报告了体外 DNA 损伤增加。转录组学研究表明,纤维化途径的上调与肥厚型心肌病和 WNT 和 TGF-β信号通路的基因簇有关。这些发现确定了 TULP3 中的变体是主要器官进行性退行性疾病的单基因原因,受影响个体受益于早期检测和改善的临床管理。阐明对 DNA 损伤修复和组织维持至关重要的机制将为这类和类似的遗传和非遗传疾病提供新的治疗途径。