Psychiatric Genetics Group, McGill University, 6875 LaSalle Boulevard, Frank Common Building, Room 2101.2, Verdun, Montreal, QC H4H 1R3, Canada.
Department of Psychiatry, McGill University and Douglas Hospital Research Institute, Montreal, QC H4H 1R3, Canada.
Hum Mol Genet. 2022 Oct 28;31(21):3715-3728. doi: 10.1093/hmg/ddac121.
Kabuki syndrome is frequently caused by loss-of-function mutations in one allele of histone 3 lysine 4 (H3K4) methyltransferase KMT2D and is associated with problems in neurological, immunological and skeletal system development. We generated heterozygous KMT2D knockout and Kabuki patient-derived cell models to investigate the role of reduced dosage of KMT2D in stem cells. We discovered chromosomal locus-specific alterations in gene expression, specifically a 110 Kb region containing Synaptotagmin 3 (SYT3), C-Type Lectin Domain Containing 11A (CLEC11A), Chromosome 19 Open Reading Frame 81 (C19ORF81) and SH3 And Multiple Ankyrin Repeat Domains 1 (SHANK1), suggesting locus-specific targeting of KMT2D. Using whole genome histone methylation mapping, we confirmed locus-specific changes in H3K4 methylation patterning coincident with regional decreases in gene expression in Kabuki cell models. Significantly reduced H3K4 peaks aligned with regions of stem cell maps of H3K27 and H3K4 methylation suggesting KMT2D haploinsufficiency impact bivalent enhancers in stem cells. Preparing the genome for subsequent differentiation cues may be of significant importance for Kabuki-related genes. This work provides a new insight into the mechanism of action of an important gene in bone and brain development and may increase our understanding of a specific function of a human disease-relevant H3K4 methyltransferase family member.
歌舞伎综合征通常由组蛋白 3 赖氨酸 4(H3K4)甲基转移酶 KMT2D 一个等位基因的功能丧失突变引起,与神经系统、免疫系统和骨骼系统发育问题有关。我们生成了杂合 KMT2D 敲除和歌舞伎患者来源的细胞模型,以研究 KMT2D 剂量降低在干细胞中的作用。我们发现了基因表达的染色体位置特异性改变,特别是一个包含突触结合蛋白 3(SYT3)、C 型凝集素结构域蛋白 11A(CLEC11A)、染色体 19 开放阅读框 81(C19ORF81)和 SH3 和多个锚蛋白重复结构域 1(SHANK1)的 110kb 区域,提示 KMT2D 的位置特异性靶向。使用全基因组组蛋白甲基化图谱,我们证实了 Kabuki 细胞模型中 H3K4 甲基化模式的位置特异性变化与基因表达的区域减少一致。H3K4 峰的显著减少与 H3K27 和 H3K4 甲基化的干细胞图谱区域一致,表明 KMT2D 杂合不足影响干细胞中的双价增强子。为随后的分化线索准备基因组可能对与歌舞伎相关的基因非常重要。这项工作为骨和脑发育中一个重要基因的作用机制提供了新的见解,并可能增加我们对人类疾病相关 H3K4 甲基转移酶家族成员特定功能的理解。