Shuang Ge, Meiling Sun, Jiaqi He, Yu Pan, Yi Xu, Lei Wang, Rongrong Luo, Yanyao Zhong, Yuqing Wang, Jun Huang, Mengyao Hu, Zhenhe Huang, Guangyan Wu, Yu Wan, Lijun Mo, Fan Wu, Chengtao Nie, Hongwei Zhou, Yan He, Zhenchao Ma, Xiaolong He, Jie Gao
Chronic alcohol consumption disrupts gut-liver homeostasis not only by inducing direct hepatotoxic injury, but also by perturbing host-microbial defense mechanisms that normally protect the liver from metabolic and inflammatory stress. We show that hepatocyte-specific deletion of Nod2 exacerbates ethanol-induced steatosis, oxidative stress, and mitochondrial dysfunction, establishing NOD2 as a critical protective factor in alcohol-associated liver disease (ALD). Importantly, beyond its direct hepatotoxic effects, ethanol exposure simultaneously diminishes this protective NOD2 pathway by limiting microbiota-derived ligand availability. Guided by this functional deficit, clinical metagenomic analysis (n = 1516) revealed that alcohol consumption is associated with a selective depletion of gut microbial DL-endopeptidase, a rate-limiting enzyme for NOD2 ligand generation, which inversely correlated with liver injury severity. Mice receiving fecal microbiota from donors with low DL-endopeptidase activity showed increased susceptibility to ALD. Importantly, supplementation with a NOD2 ligand or its clinical analogue, mifamurtide, restored mitochondrial homeostasis and alleviated liver injury. Together, these findings identify the gut microbial DL-endopeptidase-NOD2 axis as a key protective mechanism against ethanol-induced liver injury and a promising therapeutic target in alcohol-associated liver disease.