Cuinat Silvestre, Chatron Nicolas, Petit Florence, Brunelle Perrine, Dincuff Etienne, Aubert Mucca Marion, Bieth Eric, Schmetz Ariane, Rieder Harald, Wollnik Bernd, Kaulfuß Silke, Yigit Gökhan, McKeown Colina, Savage Tim, Mulligan Meghan R, Bicknell Louise S, Corsten-Janssen Nicole, Edery Patrick, Lesca Gaetan, de Villartay Jean-Pierre, Putoux Audrey
Hospices Civils de Lyon, Service de Génétique, Centre Labélisé Anomalies du Développement CLAD Sud-Est, Lyon, France.
Centre de Recherche en Neurosciences de Lyon, équipe GENDEV, INSERM U1028 CNRS UMR5292, Université Claude Bernard Lyon 1, Lyon, France.
Eur J Hum Genet. 2025 Mar 20. doi: 10.1038/s41431-025-01821-0.
The non-homologous end joining (NHEJ) pathway is essential to repair DNA double-strand breaks. XRCC4 acts as a stabilizer of the DNA ligase LIG4 in the NHEJ process. In humans, XRCC4 pathogenic variants are responsible for a microcephalic primordial dwarfism syndrome (MPD). Currently, 17 patients have been reported with XRCC4-related MPD and we report 7 new patients from 6 different families, including one fetus. The patients present with short stature, severe microcephaly, neurodevelopmental disorder and additional features, such as transient increase in nuchal translucency, congenital glaucoma, thumb anomalies, hepatic steatosis, seizures, essential tremor and oligodontia which have not been previously described. Hyper- and hypopigmented skin macules, dermatofibrosarcoma, mandibular osteoid osteoma and pancytopenia are also new features, reminiscent of cancer susceptibility syndromes. Functional studies were performed on two patients carrying the known pathogenic p.(Trp43Arg) variant in homozygous state, using a fast, cost-effective and non-invasive approach on PBMCs: (1) Survival analyses after ionizing radiation confirm important radiosensitivity. (2) Flow cytometry showed the lack of TCR-Va7+ T-lymphocytes, suggesting recombination defect of V(D)J coding segments. (3) This was confirmed by multiplexed RT-PCR (PROMIDISα biomarker), analyzing the diversity of V(D)J coding segments in a subset of the TCRα repertoire. We therefore extend the phenotype of XRCC4-related MPD and suggest a combination of three functional assays, based on radiosensitivity and V(D)J recombination defect, to improve the interpretation of XRCC4 variants in fast, cost-effective and non-invasive manner. These findings will improve the diagnosis, genetic counselling, follow-up and management of these patients.
非同源末端连接(NHEJ)途径对于修复DNA双链断裂至关重要。XRCC4在NHEJ过程中作为DNA连接酶LIG4的稳定剂发挥作用。在人类中,XRCC4致病变体导致小头原发性侏儒综合征(MPD)。目前,已有17例与XRCC4相关的MPD患者被报道,我们报告了来自6个不同家庭的7例新患者,包括1例胎儿。这些患者表现为身材矮小、严重小头畸形、神经发育障碍以及其他特征,如颈部半透明厚度短暂增加、先天性青光眼、拇指异常、肝脂肪变性、癫痫发作、特发性震颤和少牙症,这些特征此前未曾被描述过。皮肤色素沉着过多和过少斑、皮肤纤维肉瘤、下颌骨骨样骨瘤和全血细胞减少也是新特征,让人联想到癌症易感性综合征。我们使用一种快速、经济高效且非侵入性的方法,对两名纯合携带已知致病p.(Trp43Arg)变体的患者的外周血单核细胞进行了功能研究:(1)电离辐射后的生存分析证实了重要的放射敏感性。(2)流式细胞术显示缺乏TCR-Va7 + T淋巴细胞,提示V(D)J编码片段的重组缺陷。(3)通过多重逆转录聚合酶链反应(PROMIDISα生物标志物)分析TCRα库子集中V(D)J编码片段的多样性,证实了这一点。因此,我们扩展了与XRCC4相关的MPD的表型,并建议基于放射敏感性和V(D)J重组缺陷的三种功能检测方法相结合,以快速、经济高效且非侵入性的方式改进对XRCC4变体的解读。这些发现将改善这些患者的诊断、遗传咨询、随访和管理。