Pei Yumeng, Fang Meng, Wu Hong-Kun, Cui Qionghua, Quan Li, Li Xiaochuan, Zhang Keyi, Xie Peng, Jiang Peng, Liu Yuan, Huang Meimei, Lv Fengxiang, Hu Xiaomin, Chen Ye-Guang, Hu Xinli, Xiao Rui-Ping
State Key Laboratory of Membrane Biology, Institute of Molecular Medicine, College of Future Technology, Peking University, 100871, Beijing, China.
Peking-Tsinghua Center for Life Sciences, 100871, Beijing, China.
Signal Transduct Target Ther. 2025 Jun 11;10(1):183. doi: 10.1038/s41392-025-02268-x.
Emerging evidence suggests that priming intestinal stem cells (ISCs) towards secretory progenitor cells is beneficial for maintaining gut homeostasis against inflammatory bowel disease (IBD). However, the mechanism driving such biased lineage commitment remains elusive. Here we show that MG53, also named as TRIM72, prompts ISCs to secretory lineages via upregulating peroxisome proliferator-activated receptor α (PPARα), thus maintaining intestinal epithelium integrity against noxious insults. Using genetic mouse models, we found that MG53 deficiency leads to exacerbated intestinal damage caused by various injuries in mice, whereas MG53 overexpression in ISCs is sufficient to ameliorate such damage. Mechanistically, MG53 promoted asymmetric division of ISCs to generate more progenitor cells of secretory lineages via activating PPARα signaling. Specifically, MG53 overexpression induced PPARα expression at transcriptional level and concomitantly increased PPARα activity by elevating the contents of a panel of unsaturated fatty acids in the intestine that serve as potent endogenous agonists of PPARα. Furthermore, genetic ablation or pharmacological inhibition of PPARα abolished the protective effects of MG53. These findings reveal a crucial role of MG53-PPARα axis in driving the secretory lineage commitment of ISCs, especially during injury response, highlighting the important therapeutic potential of targeting MG53-PPARα signaling for IBD treatment and marking PPARα agonists as novel therapies for IBD caused by various etiologies.
新出现的证据表明,促使肠道干细胞(ISC)向分泌祖细胞分化有利于维持肠道内环境稳定,抵抗炎症性肠病(IBD)。然而,驱动这种偏向性谱系定向的机制仍不清楚。在此,我们表明MG53(也称为TRIM72)通过上调过氧化物酶体增殖物激活受体α(PPARα)促使ISC向分泌谱系分化,从而维持肠道上皮完整性以抵抗有害刺激。利用基因小鼠模型,我们发现MG53缺陷会导致小鼠因各种损伤引起的肠道损伤加剧,而在ISC中过表达MG53足以改善这种损伤。从机制上讲,MG53通过激活PPARα信号通路促进ISC的不对称分裂,以产生更多分泌谱系的祖细胞。具体而言,MG53过表达在转录水平诱导PPARα表达,并通过提高肠道中一组不饱和脂肪酸的含量来增加PPARα活性,这些不饱和脂肪酸是PPARα的有效内源性激动剂。此外,PPARα的基因敲除或药理学抑制消除了MG53的保护作用。这些发现揭示了MG53-PPARα轴在驱动ISC的分泌谱系定向中的关键作用,尤其是在损伤反应期间,突出了靶向MG53-PPARα信号通路治疗IBD的重要治疗潜力,并将PPARα激动剂标记为治疗各种病因引起的IBD的新疗法。