Hildonen Mathis, Ciolfi Andrea, Ferilli Marco, Cappelletti Camilla, Al Alam Chadi, Amor David J, Barakat Tahsin Stefan, Benoit Valérie, Birk Ohad Shmuel, Callewaert Bert, Cazurro-Gutiérrez Ana, De Wachter Matthias, Doco-Fenzy Martine, Gómez-Puertas Paulino, Hammer Trine Bjørg, Jamra Rami Abou, Kaiyrzhanov Rauan, Kameyama Shinichi, Keren Boris, Kresge Christina, Krey Ilona, Lederer Damien, Marcos-Alcalde Iñigo, Maroofian Reza, Matsumoto Naomichi, Mizuguchi Takeshi, Moey Lip-Hen, Morgan Angela, Munell Francina, Platzer Konrad, Pletcher Beth A, Ros-Pardo David, Rumping Lynne, Szakszon Katalin, Van Schil Kristof, Verdura Edgard, Vogt Julie, Wassmer Evangeline, Zamani Mina, Tümer Zeynep, Tartaglia Marco
Department of Clinical Genetics, Copenhagen University Hospital, Rigshospitalet, 2100, Copenhagen, Denmark.
Molecular Genetics and Functional Genomics, Bambino Gesù Children's Hospital, IRCCS, 00146, Rome, Italy.
Eur J Hum Genet. 2025 May 23. doi: 10.1038/s41431-025-01876-z.
Biallelic inactivating variants in ZNF142 underlie a clinically variable neurodevelopmental disorder. ZNF142 is a zinc-finger transcription factor with potential roles on chromatin organization, implying a possible association of ZNF142 loss of function with perturbed genome-wide DNA methylation (DNAm) pattern. We performed EPIC array-based methylation profiling of peripheral blood-derived DNA samples from 27 individuals with biallelic ZNF142 inactivating variants, together with 6 heterozygous carriers and 40 controls. A DNAm signature discovery pipeline was applied by using 440 controls for discovery and validation analyses, and a machine-learning model was trained to classify 8 individuals carrying ZNF142 variants of uncertain clinical significance. Analyses directed to explore the genome-wide DNAm landscape in affected individuals revealed 88 differentially methylated probes constituting the minimal informative set specific to ZNF142 loss of function. This reproducible pattern of DNAm changes involved regulatory regions of a small number of genes. The DNAm signature derived from peripheral blood allowed us to diagnose individuals carrying biallelic inactivating ZNF142 variants when applied to fibroblasts. Our findings provide evidence that biallelic loss-of-function ZNF142 variants result in a specific and robust DNAm signature. The identified DNAm pattern suggests occurrence of a methylation disturbance involving a small number of loci that appears to be shared by different cell lineages.
ZNF142基因的双等位基因失活变异是一种临床症状多样的神经发育障碍的病因。ZNF142是一种锌指转录因子,在染色质组织中具有潜在作用,这意味着ZNF142功能丧失可能与全基因组DNA甲基化(DNAm)模式紊乱有关。我们对27名携带ZNF142双等位基因失活变异的个体、6名杂合携带者和40名对照者的外周血来源DNA样本进行了基于EPIC阵列的甲基化分析。通过使用440名对照者进行发现和验证分析,应用了一种DNAm特征发现流程,并训练了一个机器学习模型来对8名携带临床意义不确定的ZNF142变异的个体进行分类。针对受影响个体全基因组DNAm图谱的分析揭示了88个差异甲基化探针,它们构成了ZNF142功能丧失特有的最小信息集。这种可重复的DNAm变化模式涉及少数基因的调控区域。当应用于成纤维细胞时,源自外周血的DNAm特征使我们能够诊断携带ZNF142双等位基因失活变异的个体。我们的研究结果提供了证据,表明ZNF142双等位基因功能丧失变异会导致一种特定且稳定的DNAm特征。所确定的DNAm模式表明存在一种涉及少数位点的甲基化干扰,这种干扰似乎在不同细胞谱系中都存在。