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

References

• Krugliak CN, Torres J, Rubin DT. What does disease progression look like in ulcerative colitis, and how might it be prevented? Gastroenterology. 2022;162(5):1396–25. doi:10.1053/j.gastro.2022.01.023.
   PubMed Web of Science ®Google Scholar
• Kobayashi T, Siegmund B, Le Berre C, Wei SC, Ferrante M, Shen B, Bernstein CN, Danese S, Peyrin-Biroulet L, Hibi T. Ulcerative colitis. Nat Rev Dis Primers. 2020;6(1):74. doi:10.1038/s41572-020-0205-x.
   PubMed Web of Science ®Google Scholar
• Wei S, Zhang J, Wu X, Chen M, Huang H, Zeng S, Xiang Z, Li X, Dong W. Fusobacterium nucleatum extracellular vesicles promote experimental colitis by modulating autophagy via the miR-574-5p/CARD3 axis. Inflamm Bowel Dis. 2022;29(1):9–26. doi:10.1093/ibd/izac177.
   Web of Science ®Google Scholar
• Chen Y, Chen Y, Cao P, Su W, Zhan N, Dong W. Fusobacterium nucleatum facilitates ulcerative colitis through activating IL-17F signaling to NF-kappaB via the upregulation of CARD3 expression. J Pathol. 2020;250(2):170–182. doi:10.1002/path.5358.
   PubMed Web of Science ®Google Scholar
• Liu L, Liang L, Yang C, Zhou Y, Chen Y. Extracellular vesicles of Fusobacterium nucleatum compromise intestinal barrier through targeting RIPK1-mediated cell death pathway. Gut Microbes. 2021;13(1):1–20. doi:10.1080/19490976.2021.1902718.
   Web of Science ®Google Scholar
• Pegtel DM, Gould SJ. Exosomes. Annu Rev Biochem. 2019;88:487–514. doi:10.1146/annurev-biochem-013118-111902.
   PubMed Web of Science ®Google Scholar
• Jeppesen DK, Fenix AM, Franklin JL, Higginbotham JN, Zhang Q, Zimmerman LJ, Liebler DC, Ping J, Liu Q, Evans R, et al. Reassessment of exosome composition. Cell. 2019;177(2):428–445.e18. doi:10.1016/j.cell.2019.02.029.
   PubMed Web of Science ®Google Scholar
• Wei S, Peng L, Yang J, Sang H, Jin D, Li X, Chen M, Zhang W, Dang Y, Zhang G. Exosomal transfer of miR-15b-3p enhances tumorigenesis and malignant transformation through the DYNLT1/Caspase-3/Caspase-9 signaling pathway in gastric cancer. J Exp Clin Cancer Res. 2020;39(1):32. doi:10.1186/s13046-019-1511-6.
   PubMed Web of Science ®Google Scholar
• Guo S, Chen J, Chen F, Zeng Q, Liu WL, Zhang G. Exosomes derived from Fusobacterium nucleatum-infected colorectal cancer cells facilitate tumour metastasis by selectively carrying miR-1246/92b-3p/27a-3p and CXCL16. Gut. 2020;70(8):1507–1519. doi:10.1136/gutjnl-2020-321187.
   Web of Science ®Google Scholar
• Cao Y, Wang Z, Yan Y, Ji L, He J, Xuan B, Shen C, Ma Y, Jiang S, Ma D, et al. Enterotoxigenic bacteroidesfragilis promotes intestinal inflammation and malignancy by inhibiting exosome-packaged miR-149-3p. Gastroenterology. 2021;161(5):1552–1566. doi:10.1053/j.gastro.2021.08.003.
   PubMed Web of Science ®Google Scholar
• Yan P, Li Z, Xiong J, Geng Z, Wei W, Zhang Y, Wu G, Zhuang T, Tian X, Liu Z, et al. LARP7 ameliorates cellular senescence and aging by allosterically enhancing SIRT1 deacetylase activity. Cell Rep. 2021;37(8):110038. doi:10.1016/j.celrep.2021.110038.
   PubMed Web of Science ®Google Scholar
• Risques RA, Lai LA, Brentnall TA, Li L, Feng Z, Gallaher J, Mandelson MT, Potter JD, Bronner MP, Rabinovitch PS. Ulcerative colitis is a disease of accelerated colon aging: evidence from telomere attrition and DNA damage. Gastroenterology. 2008;135(2):410–418. doi:10.1053/j.gastro.2008.04.008.
   PubMed Web of Science ®Google Scholar
• Martin O, Bergonzini A, Lopez CM, Paparouna E, Butter D, Theodorou S, Haykal MM, Boutet-Robinet E, Tebaldi T, Wakeham A, et al. Influence of the microenvironment on modulation of the host response by typhoid toxin. Cell Rep. 2021;35(1):108931. doi:10.1016/j.celrep.2021.108931.
   PubMed Web of Science ®Google Scholar
• Peng L, Sang H, Wei S, Li Y, Jin D, Zhu X, Li X, Dang Y, Zhang G. circCUL2 regulates gastric cancer malignant transformation and cisplatin resistance by modulating autophagy activation via miR-142-3p/ROCK2. Mol Cancer. 2020;19(1):156. doi:10.1186/s12943-020-01270-x.
   PubMed Web of Science ®Google Scholar
• Sang H, Zhang W, Peng L, Wei S, Zhu X, Huang K, Yang J, Chen M, Dang Y, Zhang G. Exosomal circRELL1 serves as a miR-637 sponge to modulate gastric cancer progression via regulating autophagy activation. Cell Death Disease. 2022;13(1):56. doi:10.1038/s41419-021-04364-6.
   PubMed Web of Science ®Google Scholar
• Mosna K, Janega P, Sedlak J, Babal P. Complex changes of circadian proteins expression in inflammatory bowel disease. Bratisl Lek Listy. 2021;122(4):235–241. doi:10.4149/BLL_2021_038.
   PubMed Web of Science ®Google Scholar
• D’Adda DFF. Living on a break: cellular senescence as a DNA-damage response. Nat Rev Cancer. 2008;8(7):512–522. doi:10.1038/nrc2440.
   PubMed Web of Science ®Google Scholar
• Ahn SH, Cho SH, Song JE, Kim S, Oh SS, Jung S, Cho KA, Lee TH. Caveolin-1 serves as a negative effector in senescent human gingival fibroblasts during Fusobacterium nucleatum infection. Mol Oral Microbiol. 2017;32(3):236–249. doi:10.1111/omi.12167.
   PubMed Web of Science ®Google Scholar
• Smith-Roe SL, Patel SS, Zhou Y, Simpson DA, Rao S, Ibrahim JG, Cordeiro-Stone M, Kaufmann WK. Separation of intra-S checkpoint protein contributions to DNA replication fork protection and genomic stability in normal human fibroblasts. Cell Cycle. 2013;12(2):332–345. doi:10.4161/cc.23177.
   PubMed Web of Science ®Google Scholar
• Kondratov RV, Antoch MP. Circadian proteins in the regulation of cell cycle and genotoxic stress responses. Trends Cell Biol. 2007;17(7):311–317. doi:10.1016/j.tcb.2007.07.001.
   PubMed Web of Science ®Google Scholar
• Li G, Lin J, Zhang C, Gao H, Lu H, Gao X, Zhu R, Li Z, Li M, Liu Z. Microbiota metabolite butyrate constrains neutrophil functions and ameliorates mucosal inflammation in inflammatory bowel disease. Gut Microbes. 2021;13(1):1968257. doi:10.1080/19490976.2021.1968257.
   PubMed Web of Science ®Google Scholar
• Su W, Chen Y, Cao P, Chen Y, Guo Y, Wang S, Dong W. Fusobacterium nucleatum promotes the development of ulcerative colitis by inducing the autophagic cell death of intestinal epithelial. Front Cell Infect Microbiol. 2020;10:594806. doi:10.3389/fcimb.2020.594806.
   PubMed Web of Science ®Google Scholar
• Engevik MA, Danhof HA, Ruan W, Engevik AC, Chang-Graham AL, Engevik KA, Shi Z, Zhao Y, Brand CK, Krystofiak ES, et al. Fusobacterium nucleatum secretes outer membrane vesicles and promotes intestinal inflammation. Mbio. 2021;12(2). doi:10.1128/mBio.02706-20
   PubMed Web of Science ®Google Scholar
• Yang C, Zhang M, Sung J, Wang L, Jung Y, Merlin D. Autologous exosome transfer: A new personalised treatment concept to prevent colitis in a murine model. J Crohns Colitis. 2020;14(6):841–855. doi:10.1093/ecco-jcc/jjz184.
   PubMed Web of Science ®Google Scholar
• Liu C, Yan X, Zhang Y, Yang M, Ma Y, Zhang Y, Xu Q, Tu K, Zhang M. Oral administration of turmeric-derived exosome-like nanovesicles with anti-inflammatory and pro-resolving bioactions for murine colitis therapy. J Nanobiotechnology. 2022;20(1):206. doi:10.1186/s12951-022-01421-w.
   PubMed Web of Science ®Google Scholar
• Deng F, Yan J, Lu J, Luo M, Xia P, Liu S, Wang X, Zhi F, Liu D. M2 macrophage-derived exosomal miR-590-3p attenuates DSS-Induced mucosal damage and promotes epithelial repair via the LATS1/YAP/beta-catenin signalling axis. J Crohns Colitis. 2021;15(4):665–677. doi:10.1093/ecco-jcc/jjaa214.
   PubMed Web of Science ®Google Scholar
• Tian Y, Xu J, Li Y, Zhao R, Du S, Lv C, Wu W, Liu R, Sheng X, Song Y, et al. MicroRNA-31 reduces inflammatory signaling and promotes regeneration in colon epithelium, and delivery of mimics in microspheres reduces colitis in mice. Gastroenterology. 2019;156(8):2281–2296. doi:10.1053/j.gastro.2019.02.023.
   PubMed Web of Science ®Google Scholar
• Sun Y, Zhou Y, Shi Y, Zhang Y, Liu K, Liang R, Sun P, Chang X, Tang W, Zhang Y, et al. Expression of miRNA-29 in pancreatic beta cells promotes inflammation and diabetes via TRAF3. Cell Rep. 2021;34(1):108576. doi:10.1016/j.celrep.2020.108576.
   PubMed Web of Science ®Google Scholar
• Umehara T, Mori R, Mace KA, Murase T, Abe Y, Yamamoto T, Ikematsu K. Identification of specific miRNAs in neutrophils of type 2 diabetic mice: Overexpression of miRNA-129-2-3p accelerates diabetic wound healing. Diabetes. 2019;68(3):617–630. doi:10.2337/db18-0313.
   PubMed Web of Science ®Google Scholar
• Zhu M, Liang Q, Chen T, Kong Q, Ye G, Yu S, Li X, He Q, Liu H, Hu Y, et al. Identification and validation of methylated differentially expressed miRnas and immune infiltrate profile in EBV-associated gastric cancer. Clin Epigenetics. 2021;13(1):22. doi:10.1186/s13148-020-00989-0.
   PubMed Web of Science ®Google Scholar
• Yu X, Luo L, Wu Y, Yu X, Liu Y, Yu X, Zhao X, Zhang X, Cui L, Ye G, et al. Gastric juice miR-129 as a potential biomarker for screening gastric cancer. Med Oncol. 2013;30(1):365. doi:10.1007/s12032-012-0365-y.
   PubMed Web of Science ®Google Scholar
• Liu X, Zhang G, Yu T, He J, Liu J, Chai X, Zhao G, Yin D, Zhang C. Exosomes deliver lncRNA DARS-AS1 siRNA to inhibit chronic unpredictable mild stress-induced TNBC metastasis. Cancer Lett. 2022;543:215781. doi:10.1016/j.canlet.2022.215781.
   PubMed Web of Science ®Google Scholar
• Young LM, Marzio A, Perez-Duran P, Reid DA, Meredith DN, Roberti D, Star A, Rothenberg E, Ueberheide B, Pagano M. TIMELESS forms a complex with PARP1 distinct from its complex with TIPIN and plays a role in the DNA damage response. Cell Rep. 2015;13(3):451–459. doi:10.1016/j.celrep.2015.09.017.
   PubMed Web of Science ®Google Scholar
• Barnes JW, Tischkau SA, Barnes JA, Mitchell JW, Burgoon PW, Hickok JR, Gillette MU. Requirement of mammalian Timeless for circadian rhythmicity. Science. 2003;302(5644):439–442. doi:10.1126/science.1086593.
   PubMed Web of Science ®Google Scholar
• Leman AR, Dheekollu J, Deng Z, Lee SW, Das MM, Lieberman PM, Noguchi E. Timeless preserves telomere length by promoting efficient DNA replication through human telomeres. Cell Cycle. 2012;11(12):2337–2347. doi:10.4161/cc.20810.
   PubMed Web of Science ®Google Scholar
• Paulsen RD, Soni DV, Wollman R, Hahn AT, Yee MC, Guan A, Hesley JA, Miller SC, Cromwell EF, Solow-Cordero DE, et al. A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol Cell. 2009;35(2):228–239. doi:10.1016/j.molcel.2009.06.021.
   PubMed Web of Science ®Google Scholar
• Faye AS, Colombel JF. Aging and IBD: A new challenge for clinicians and researchers. Inflamm Bowel Dis. 2022;28(1):126–132. doi:10.1093/ibd/izab039.
   PubMed Web of Science ®Google Scholar
• Shen X, Li M, Mao Z, Yu W. Loss of circadian protein TIMELESS accelerates the progression of cellular senescence. Biochem Biophys Res Commun. 2018;503(4):2784–2791. doi:10.1016/j.bbrc.2018.08.040.
   PubMed Web of Science ®Google Scholar
• Kang C, Xu Q, Martin TD, Li MZ, Demaria M, Aron L, Lu T, Yankner BA, Campisi J, Elledge SJ. The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4. Science. 2015;349(6255):a5612. doi:10.1126/science.aaa5612.
   Web of Science ®Google Scholar
• Yan S, Sorrell M, Berman Z. Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress. Cell Mol Life Sci. 2014;71(20):3951–3967. doi:10.1007/s00018-014-1666-4.
   PubMed Web of Science ®Google Scholar
• Barnes RP, de Rosa M, Thosar SA, Detwiler AC, Roginskaya V, Van Houten B, Bruchez MP, Stewart-Ornstein J, Opresko PL. Telomeric 8-oxo-guanine drives rapid premature senescence in the absence of telomere shortening. Nature Structural & Molecular Biology. 2022;29(7):639–652. doi:10.1038/s41594-022-00790-y.
   PubMed Web of Science ®Google Scholar
• Chen TY, Huang BM, Tang TK, Chao YY, Xiao XY, Lee PR, Yang LY, Wang CY. Genotoxic stress-activated DNA-PK-p53 cascade and autophagy cooperatively induce ciliogenesis to maintain the DNA damage response. Cell Death Differ. 2021;28(6):1865–1879. doi:10.1038/s41418-020-00713-8.
   PubMed Web of Science ®Google Scholar
• Lee J, Mo JH, Katakura K, Alkalay I, Rucker AN, Liu YT, Lee HK, Shen C, Cojocaru G, Shenouda S, et al. Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat Cell Biol. 2006;8(12):1327–1336. doi:10.1038/ncb1500.
   PubMed Web of Science ®Google Scholar
• Dawson PA, Huxley S, Gardiner B, Tran T, McAuley JL, Grimmond S, McGuckin MA, Markovich D. Reduced mucin sulfonation and impaired intestinal barrier function in the hyposulfataemic NaS1 null mouse. Gut. 2009;58(7):910–919. doi:10.1136/gut.2007.147595.
   PubMed Web of Science ®Google Scholar
• Gross KM, Zhou W, Breindel JL, Ouyang J, Jin DX, Sokol ES, Gupta PB, Huber K, Zou L, Kuperwasser C. Loss of slug compromises DNA damage repair and accelerates stem cell aging in mammary epithelium. Cell Rep. 2019;28(2):394–407. doi:10.1016/j.celrep.2019.06.043.
   PubMed Web of Science ®Google Scholar
• Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. doi:10.1186/s13059-014-0550-8.
   PubMed Web of Science ®Google Scholar
• Qian Y, Arellano G, Ifergan I, Lin J, Snowden C, Kim T, Thomas JJ, Law C, Guan T, Balabanov RD, et al. ZEB1 promotes pathogenic Th1 and Th17 cell differentiation in multiple sclerosis. Cell Rep. 2021;36(8):109602. doi:10.1016/j.celrep.2021.109602.
   PubMed Web of Science ®Google Scholar
• Liu X, Liu Y, Liu Z, Lin C, Meng F, Xu L, Zhang X, Zhang C, Zhang P, Gong S, et al. CircMYH9 drives colorectal cancer growth by regulating serine metabolism and redox homeostasis in a p53-dependent manner. Mol Cancer. 2021;20(1):114. doi:10.1186/s12943-021-01412-9.
   PubMed Web of Science ®Google Scholar
• Guo P, Tian Z, Kong X, Yang L, Shan X, Dong B, Ding X, Jing X, Jiang C, Jiang N, et al. FadA promotes DNA damage and progression of Fusobacterium nucleatum-induced colorectal cancer through up-regulation of chk2. J Exp Clin Cancer Res. 2020;39(1):202. doi:10.1186/s13046-020-01677-w.
   PubMed Web of Science ®Google Scholar
• Youden WJ. Index for rating diagnostic tests. Cancer-Am Cancer Soc. 1950;3(1):32–35. doi:10.1002/1097-0142(1950)3:1<32:aid-cncr2820030106>3.0.co;2-3.
   Google Scholar