Carvalho Laura Machado Lara, Rzasa Jessica, Kerkhof Jennifer, McConkey Haley, Fishman Veniamin, Koksharova Galina, de Lima Jorge Alexander Augusto, Branco Elisa Varella, de Oliveira Danyllo Felipe, Martinez-Delgado Beatriz, Barrero Maria J, Kleefstra Tjitske, Sadikovic Bekim, Haddad Luciana Amaral, Bertola Débora Romeo, Rosenberg Carla, Krepischi Ana Cristina Victorino
Department of Genetics and Evolutionary Biology, Institute of Biosciences, Human Genome and Stem Cell Research Center, University of Sao Paulo (USP), Sao Paulo, SP, Brazil.
Verspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON, Canada.
Mol Neurobiol. 2025 May;62(5):5977-5989. doi: 10.1007/s12035-024-04655-x. Epub 2024 Dec 15.
Neurodevelopmental disorders (NDD) comprise clinical conditions with high genetic heterogeneity and a notable enrichment of genes involved in regulating chromatin structure and function. The EHMT1/2 epigenetic complex plays a crucial role in repression of gene transcription in a highly tissue- and temporal-specific manner. Mutations resulting in heterozygous loss-of-function (LoF) of EHMT1 are implicated in Kleefstra syndrome 1 (KS1). EHMT2 is a gene acting in epigenetic regulation; however, the involvement of mutations in this gene in the etiology of NDDs has not been established thus far. A homozygous EHMT2 LoF variant [(NM_006709.5):c.328 + 2 T > G] was identified by exome sequencing in an adult female patient with a phenotype resembling KS1, presenting with intellectual disability, aggressive behavior, facial dysmorphisms, fused C2-C3 vertebrae, ventricular septal defect, supernumerary nipple, umbilical hernia, and fingers and toes abnormalities. The absence of homozygous LoF EHMT2 variants in population databases underscores the significant negative selection pressure exerted on these variants. In silico evaluation of the effect of the EHMT2(NM_006709.5):c.328 + 2 T > G variant predicted the abolishment of intron 3 splice donor site. However, manual inspection revealed potential cryptic donor splice sites at this EHMT2 region. To directly access the impact of this splice site variant, RNAseq analysis was employed and disclosed the usage of two cryptic donor sites within exon 3 in the patient's blood, which are predicted to result in either an out-of-frame or in-frame effect on the protein. Methylation analysis was conducted on DNA from blood samples using the clinically validated EpiSign assay, which revealed that the patient with the homozygous EHMT2(NM_006709.5):c.328 + 2 T > G splice site variant is conclusively positive for the KS1 episignature. Taken together, clinical, genetic, and epigenetic data pointed to a LoF mechanism for the EHMT2 splice variant and support this gene as a novel candidate for an autosomal recessive Kleefstra-like syndrome. The identification of additional cases with deleterious EHMT2 variants, alongside further functional validation studies, is required to substantiate EHMT2 as a novel NDD gene.
神经发育障碍(NDD)包括具有高度遗传异质性的临床病症,且参与调节染色质结构和功能的基因显著富集。EHMT1/2表观遗传复合体在以高度组织和时间特异性方式抑制基因转录中起关键作用。导致EHMT1杂合功能丧失(LoF)的突变与克莱夫斯特拉综合征1型(KS1)有关。EHMT2是一个在表观遗传调控中起作用的基因;然而,该基因突变在NDD病因学中的作用迄今尚未明确。通过外显子组测序在一名成年女性患者中鉴定出一个纯合的EHMT2 LoF变体[(NM_006709.5):c.328+2 T>G],该患者具有类似KS1的表型,表现为智力残疾、攻击性行为、面部畸形、C2-C3椎体融合、室间隔缺损、多乳头、脐疝以及手指和脚趾异常。人群数据库中不存在纯合的EHMT2 LoF变体,这突出了对这些变体施加的显著负选择压力。对EHMT2(NM_006709.5):c.328+2 T>G变体的影响进行的计算机模拟评估预测内含子3剪接供体位点将被废除。然而,人工检查发现在该EHMT2区域存在潜在的隐蔽供体剪接位点。为了直接评估这种剪接位点变体的影响,采用了RNAseq分析,结果显示患者血液中外显子3内有两个隐蔽供体位点被使用,预计这会对蛋白质产生移码或框内效应。使用经过临床验证的EpiSign检测法对血液样本中的DNA进行甲基化分析,结果显示具有纯合EHMT2(NM_006709.5):c.328+2 T>G剪接位点变体的患者KS1表观特征呈阳性。综合来看,临床、遗传和表观遗传数据表明EHMT2剪接变体存在功能丧失机制,并支持该基因作为常染色体隐性克莱夫斯特拉样综合征的一个新候选基因。需要鉴定更多携带有害EHMT2变体的病例,并进行进一步的功能验证研究,以证实EHMT2是一种新的NDD基因。