Wang Jingjing, Wang Xiaoxin, Jiang Mingjie, Lang Tao, Wan Leilei, Dai Juanjuan
Shanghai Key Laboratory of Pancreatic Diseases, Institute of Translational Medicine, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
Department of Head and Neck Surgery, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, 510060, P.R. China.
Naunyn Schmiedebergs Arch Pharmacol. 2025 Apr;398(4):3681-3695. doi: 10.1007/s00210-024-03485-x. Epub 2024 Oct 1.
5-aminosalicylic acid (5-ASA) is widely used in the treatment of ulcerative colitis (UC), but its anti-inflammatory mechanism is complex and has not been fully understood. DSS model was used to test the effect of 5-ASA. Tight junction and Ki-67 were detected by western blot, immunofluorescence, and immunohistochemistry or qPCR. 16S rRNA gene sequencing of gut microbiota and subsequent bioinformatics and statistical analysis were performed to identify the specific bacteria which were associated with the treatment effect of 5-ASA. GC-MS was performed to test short-chain fatty acids (SCFAs). Antibiotic-treated mice were used to demonstrate the key role of endogenous gut microbiota. Here, we found that 5-ASA alleviated dextran sulfate sodium (DSS)-induced colitis in mice. Moreover, 5-ASA significantly repaired the intestinal barrier. At the molecular level, 5-ASA markedly raised the expression of tight junction proteins including JAM-A and occludin and cell proliferation marker Ki-67 in mice. In addition, bacterial 16S rRNA gene sequencing and bioinformatics analysis showed that 5-ASA significantly modulated the DSS-induced gut bacterial dysbiosis. In detail, it stimulated the growth of protective bacteria belonging to Faecalibaculum and Dubosiella, which were negatively correlated with colitis parameters, and blocked the expansion of pro-inflammatory bacteria such as Escherichia-Shigella and Oscillibacter, which were positively correlated with colitis in mice. Meanwhile, 5-ASA increased the cecal acetate level. Most notably, 5-ASA was no longer able to treat colitis and reverse gut barrier dysfunction in antibiotic-treated mice that lacked endogenous gut microbiota. Our data suggested that the anti-inflammatory activity of 5-ASA required the inherent intestinal flora, and the gut microbiota was a potential and effective target for the treatment of ulcerative colitis.
5-氨基水杨酸(5-ASA)广泛用于治疗溃疡性结肠炎(UC),但其抗炎机制复杂,尚未完全明确。采用葡聚糖硫酸钠(DSS)模型来检测5-ASA的作用效果。通过蛋白质免疫印迹法、免疫荧光法、免疫组织化学法或定量聚合酶链反应(qPCR)检测紧密连接蛋白和增殖细胞核抗原(Ki-67)。进行肠道微生物群的16S核糖体RNA(rRNA)基因测序以及后续的生物信息学和统计分析,以鉴定与5-ASA治疗效果相关的特定细菌。采用气相色谱-质谱联用仪(GC-MS)检测短链脂肪酸(SCFA)。利用抗生素处理的小鼠来证明内源性肠道微生物群的关键作用。在此,我们发现5-ASA可减轻DSS诱导的小鼠结肠炎。此外,5-ASA可显著修复肠道屏障。在分子水平上,5-ASA可显著提高小鼠体内紧密连接蛋白(包括连接粘附分子A(JAM-A)和闭合蛋白)和细胞增殖标志物Ki-67的表达。此外,细菌16S rRNA基因测序和生物信息学分析表明,5-ASA可显著调节DSS诱导的肠道细菌失调。具体而言,它可促进属于粪杆菌属和杜氏菌属的保护性细菌生长,这些细菌与结肠炎参数呈负相关,并可抑制诸如埃希氏菌-志贺氏菌属和颤杆菌属等促炎细菌的扩增,这些细菌与小鼠结肠炎呈正相关。同时,5-ASA可提高盲肠乙酸盐水平。最值得注意的是,在缺乏内源性肠道微生物群的抗生素处理小鼠中,5-ASA不再能够治疗结肠炎并逆转肠道屏障功能障碍。我们的数据表明,5-ASA的抗炎活性需要肠道固有菌群,肠道微生物群是治疗溃疡性结肠炎的一个潜在有效靶点。