Zhang Kaihui, Sun Wenxing, Liu Yi, Lv Yuqiang, Hou Daisen, Lin Yan, Xu Wei, Zhao Jianyuan, Gai Zhongtao, Zhao Shimin, Yuan Yiyuan
The Obstetrics and Gynecology Hospital, Fudan University, Shanghai, China.
Pediatric Research Institute, Qilu Children's Hospital of Shandong University, Ji'nan, China.
Front Cell Dev Biol. 2021 Mar 4;9:619475. doi: 10.3389/fcell.2021.619475. eCollection 2021.
Nonsense variants in KIDINS220/ARMS were identified as the main cause of spastic paraplegia, intellectual disability, nystagmus, and obesity (SINO) syndrome, a rare disease with birth defects in brachycephaly, neurological disorder, and obesity. The cause of neural cell dysfunction by KIDINS220/ARMS were extensively studied while the cause of obesity in SINO syndrome remains elusive. Here, we identified KIDINS220/ARMS as an adipocyte differentiation-regulating gene. A Chinese family, mother and her two sons, all showed severe symptoms of SINO syndrome. G-banding karyotyping, chromosome microarray analysis, and whole exome sequencing revealed a novel amber mutation, c.3934G>T (p. E1312X), which was close to the C-terminal region of KIDINS220/ARMS and resulted in the premature of the protein. Both the mRNA and protein levels of KIDINS220/ARMS gradually decreased during adipocyte differentiation. Knockdown of KINDINS220/ARMS could prompt adipocyte differentiation and lipid accumulation while overexpression of KIDINS220/ARMS decrease the rate of matured adipocytes. Furthermore, we demonstrated that KIDINS220/ARMS inhibits adipocyte maturation through sustained extracellular signal-regulated kinase signaling. In conclusion, this is the first report about a vertical heredity of severe dominant pathogenic mutation of KIDINS220/ARMS, suggested that KIDINS220/ARMS played a negative role in adipocyte maturation, explained the cause of obesity in SINO syndrome and could highlight the importance of adipocyte differentiation in neuron functions.
KIDINS220/ARMS基因中的无义变异被确定为痉挛性截瘫、智力残疾、眼球震颤和肥胖(SINO)综合征的主要病因,这是一种罕见疾病,具有短头畸形、神经障碍和肥胖等出生缺陷。KIDINS220/ARMS导致神经细胞功能障碍的原因已得到广泛研究,而SINO综合征中肥胖的病因仍不清楚。在此,我们确定KIDINS220/ARMS是一种调节脂肪细胞分化的基因。一个中国家庭,母亲及其两个儿子,均表现出严重的SINO综合征症状。G显带核型分析、染色体微阵列分析和全外显子测序揭示了一个新的琥珀突变,即c.3934G>T(p.E1312X),该突变靠近KIDINS220/ARMS的C末端区域,导致蛋白质提前终止。在脂肪细胞分化过程中,KIDINS220/ARMS的mRNA和蛋白质水平均逐渐下降。敲低KINDINS220/ARMS可促进脂肪细胞分化和脂质积累,而KIDINS220/ARMS的过表达则降低成熟脂肪细胞的比例。此外,我们证明KIDINS220/ARMS通过持续的细胞外信号调节激酶信号传导抑制脂肪细胞成熟。总之,这是关于KIDINS220/ARMS严重显性致病突变垂直遗传的首次报道,表明KIDINS220/ARMS在脂肪细胞成熟中起负性作用,解释了SINO综合征中肥胖的病因,并凸显了脂肪细胞分化在神经元功能中的重要性。