Yin Bin, Li Mu-Jia, Sun Jia-Lin, You Yue, Zhang Si-Di, Wan Qian-Xue, Yao Mei-Lin, Yang Cheng-Wei, Sun Hua-Qin, Lin Zi-Yuan, Shi Bing, Jia Zhong-Lin
State Key Laboratory of Oral Diseases & National Clinical Research Center for Oral Diseases & Department of cleft lip and palate, West China Hospital of Stomatology, Sichuan University, Chengdu, China.
Department of Oral and Maxillofacial Surgery, Affiliated Stomatology Hospital, Medical School of Nanjing University, No. 30 Zhong Yang's Road, Xuan Wu, Nanjing, 210008, Jiangsu Province, China.
J Hum Genet. 2025 Jun 2. doi: 10.1038/s10038-025-01352-y.
The biological interactions between genetic and environmental modifiers play critical roles in the etiology of non-syndromic orofacial cleft (NSOC), but it is rarely studied. This study selected 47 environmental related genes from the metabolic pathways of smoking, drinking, hypoxia, and vitamins (including vitamin A, vitamin B9 (folic acid), vitamin C (ascorbic acid), vitamin D, and vitamin E), and test their associations with NSOC and its subtypes. We found that a novel gene SLC23A2, the vitamin C transporter gene is significantly associated with non-syndromic cleft palate only (NSCPO) (p = 3.25E-07, OR = 8.45, 95%CI:3.73-19.17). SLC23A2 is expressed in the craniofacial region of zebrafish (24hpf to 120hpf), obvious craniofacial abnormalities appeared in zebrafish (48hpf) when knock down the slc23a2 (slc23a2-MO). Knock down SLC23A2 in human embryonic palatal mesenchymal cell line (HEPM) induced decreased intracellular ascorbic acid (AA), increased reactive oxygen species (ROS), inhibited cell proliferation and triggered apoptosis, activated the PI3K-AKT-mTOR signaling pathway and inhibited autophagy; ROS levels and apoptosis ratio significantly decreased when we supplemented AA to HEPM cells with high ROS levels induced by Sin-1 (an exogenous ROS mimic). Knocked down SLC23A2 in HEPM cells or zebrafish, they became more sensitive to Sin-1, and AA supplementation was ineffective. In conclusion, we identified a novel susceptibility gene SLC23A2 for NSCPO, it may function by decreasing AA level, increasing the ROS levels, inducing apoptosis, and inhibiting autophagy through the activation of the PI3K-AKT-mTOR pathway in etiology of cleft palate.
基因修饰因子与环境修饰因子之间的生物学相互作用在非综合征性口腔颌面部裂隙(NSOC)的病因中起着关键作用,但对此研究甚少。本研究从吸烟、饮酒、缺氧和维生素(包括维生素A、维生素B9(叶酸)、维生素C(抗坏血酸)、维生素D和维生素E)的代谢途径中选择了47个与环境相关的基因,并测试它们与NSOC及其亚型的关联。我们发现一个新基因SLC23A2,即维生素C转运基因,仅与非综合征性腭裂(NSCPO)显著相关(p = 3.25E - 07,OR = 8.45,95%CI:3.73 - 19.17)。SLC23A2在斑马鱼的颅面部区域(24小时胚胎期至120小时胚胎期)表达,当敲低slc23a2(slc23a2 - MO)时,斑马鱼(48小时胚胎期)出现明显的颅面部异常。在人胚胎腭间充质细胞系(HEPM)中敲低SLC23A2会导致细胞内抗坏血酸(AA)减少、活性氧(ROS)增加、细胞增殖受抑制并引发细胞凋亡,激活PI3K - AKT - mTOR信号通路并抑制自噬;当我们用Sin - 1(一种外源性ROS模拟物)诱导产生高ROS水平的HEPM细胞补充AA时,ROS水平和凋亡率显著降低。在HEPM细胞或斑马鱼中敲低SLC23A2后,它们对Sin - 1变得更敏感,补充AA无效。总之,我们鉴定出一个新的NSCPO易感基因SLC23A2,它可能通过降低AA水平、增加ROS水平、诱导细胞凋亡以及通过激活PI3K - AKT - mTOR途径抑制自噬,在腭裂病因中发挥作用。