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Exosomal-miR-129-2-3p derived from <i>Fusobacterium nucleatum</i> -infected intestinal epithelial cells promotes experimental colitis through regulating TIMELESS-mediated cellular senescence pathway

Shuchun Wei, Xiaohan Wu, Meilin Chen, Zixuan Xiang, Xiangyun Li, Jixiang Zhang, Weiguo Dong

2023Gut Microbes44 citationsDOIOpen Access PDF

Abstract

Fusobacterium nucleatum (Fn) infection is known to exacerbate ulcerative colitis (UC). However, the link between Fn-infected intestinal epithelial cell (IEC)-derived exosomes (Fn-Exo) and UC progression has not been investigated. Differentially expressed miRNAs in Fn-Exo and non-infected IECs-derived exosomes (Con-Exo) were identified by miRNA sequencing. Then, the biological role and mechanism of Fn-Exo in UC development were determined in vitro and in vivo. We found that exosomes delivered miR-129-2-3p from Fn-infected IECs into non-infected IECs, exacerbating epithelial barrier dysfunction and experimental colitis. Mechanically, Fn-Exo induces DNA damage via the miR-129-2-3p/TIMELESS axis and subsequently activates the ATM/ATR/p53 pathway, ultimately promoting cellular senescence and colonic inflammation. In conclusion, Exo-miR-129-2-3p/TIMELESS/ATM/ATR/p53 pathway aggravates cellular senescence, barrier damage, and experimental colitis. The current study revealed a previously unknown regulatory pathway in the progression of Fn-infectious UC. Furthermore, Exosomal-miR-129-2-3p in serum and TIMELESS may function as novel potential diagnostic biomarkers for UC and Fn-high-UC.

Topics & Concepts

BiologyFusobacterium nucleatumMicrovesiclesUlcerative colitisColitisSenescencemicroRNAInflammationDNA damageExosomeCancer researchCell biologyMolecular biologyMicrobiologyImmunologyDNAGenePathologyBacteriaGeneticsDiseaseMedicinePorphyromonas gingivalisExtracellular vesicles in diseaseMicroRNA in disease regulationCircular RNAs in diseases