Guguin Justine, Chen Ting-Yu, Cuinat Silvestre, Besson Alicia, Bertiaux Eloïse, Boutaud Lucile, Ardito Nolan, Imaz Murguiondo Miren, Cabet Sara, Hamel Virginie, Thomas Sophie, Pain Bertrand, Edery Patrick, Putoux Audrey, Tang Tang K, Mazoyer Sylvie, Delous Marion
Université Claude Bernard Lyon 1, CNRS, INSERM, Centre de Recherche en Neurosciences de Lyon CRNL U1028 UMR5292, GENDEV, Bron, France.
Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan.
PLoS Genet. 2024 Dec 16;20(12):e1011517. doi: 10.1371/journal.pgen.1011517. eCollection 2024 Dec.
Taybi-Linder syndrome (TALS) is a rare autosomal recessive disorder characterized by severe microcephaly with abnormal gyral pattern, severe growth retardation and bone abnormalities. It is caused by pathogenic variants in the RNU4ATAC gene. Its transcript, the small nuclear RNA U4atac, is involved in the excision of ~850 minor introns. Here, we report a patient presenting with TALS features but no pathogenic variants were found in RNU4ATAC, instead the homozygous RTTN c.2953A>G variant was detected by whole-exome sequencing. After deciphering the impact of the variant on the RTTN protein function at centrosome in engineered RTTN-depleted RPE1 cells and patient fibroblasts, we analysed neural stem cells (NSC) derived from CRISPR/Cas9-edited induced pluripotent stem cells and revealed major cell cycle and mitotic abnormalities, leading to aneuploidy, cell cycle arrest and cell death. In cortical organoids, we discovered an additional function of RTTN in the self-organisation of NSC into neural rosettes, by observing delayed apico-basal polarization of NSC. Altogether, these defects contributed to a marked delay of rosette formation in RTTN-mutated organoids, thus impeding their overall growth and shedding light on mechanisms leading to microcephaly.
泰比-林德综合征(TALS)是一种罕见的常染色体隐性疾病,其特征为严重小头畸形伴脑回模式异常、严重生长发育迟缓及骨骼异常。它由RNU4ATAC基因的致病性变异引起。其转录本,即小核RNA U4atac,参与约850个小内含子的切除。在此,我们报告一名表现出TALS特征的患者,但在RNU4ATAC基因中未发现致病性变异,相反,通过全外显子组测序检测到纯合的RTTN基因c.2953A>G变异。在解析该变异对工程化缺失RTTN的RPE1细胞和患者成纤维细胞中心体处RTTN蛋白功能的影响后,我们分析了源自CRISPR/Cas9编辑的诱导多能干细胞的神经干细胞(NSC),并揭示了主要的细胞周期和有丝分裂异常,导致非整倍体、细胞周期停滞和细胞死亡。在皮质类器官中,通过观察NSC顶-基极化延迟,我们发现RTTN在NSC自我组织形成神经玫瑰花结方面具有额外功能。总之,这些缺陷导致RTTN突变的类器官中玫瑰花结形成明显延迟,从而阻碍其整体生长,并揭示了导致小头畸形的机制。