Salivary Exosomes Exacerbate Colitis by Bridging the Oral Cavity and Intestine

Overview

Journal iScience

Publisher Cell Press

Date 2025 Jan 6

PMID 39759079

Authors

Congyi Yang

Jingyi Chen

Yuzheng Zhao

Jushan Wu

Yalan Xu

Jun Xu

Feng Chen

Yang Chen

Ning Chen

Affiliations

Soon will be listed here.

Abstract

Inflammatory bowel disease (IBD) presents a range of extraintestinal manifestations, notably including oral cavity involvement. The mechanisms underlying oral-gut crosstalk in IBD are not fully understood. Exosomes, found in various body fluids such as saliva, play an unclear role in IBD that requires further exploration. In the dextran sulfate sodium (DSS) mouse model, salivary exosomes from patients with active IBD (active IBD-Sexos) exacerbated colitis, while those from IBD patients in remission (remission IBD-Sexos) did not. Possible reasons may include the regulation of macrophage polarization, disruption of intestinal epithelial function, and alteration of the intestinal flora. During co-culture with active IBD-Sexos, THP-1 cells exhibited inflammatory responses, while Caco-2 cells showed reduced tight junction protein expression. Additionally, 35 differentially expressed miRNAs were identified in active IBD-Sexos. In brief, our findings substantiate an intriguing phenomenon whereby active IBD-Sexos exacerbate colitis by bridging the oral cavity and intestine.

References

Qian J, Lu J, Huang Y, Wang M, Chen B, Bao J . Periodontitis Salivary Microbiota Worsens Colitis. J Dent Res. 2021; 101(5):559-568. DOI: 10.1177/00220345211049781. View

Greenhill C . IBD: Modified Lactobacillus acidophilus may regulate intestinal inflammation. Nat Rev Gastroenterol Hepatol. 2011; 8(4):182. DOI: 10.1038/nrgastro.2011.26. View

Bao J, Li L, Zhang Y, Wang M, Chen F, Ge S . Periodontitis may induce gut microbiota dysbiosis via salivary microbiota. Int J Oral Sci. 2022; 14(1):32. PMC: 9217941. DOI: 10.1038/s41368-022-00183-3. View

Cheshmi B, Cheshomi H . Salivary exosomes: properties, medical applications, and isolation methods. Mol Biol Rep. 2020; 47(8):6295-6307. DOI: 10.1007/s11033-020-05659-1. View

Zhou T, Xu W, Wang Q, Jiang C, Li H, Chao Y . The effect of the "Oral-Gut" axis on periodontitis in inflammatory bowel disease: A review of microbe and immune mechanism associations. Front Cell Infect Microbiol. 2023; 13:1132420. PMC: 10008960. DOI: 10.3389/fcimb.2023.1132420. View

Han P, Lai A, Salomon C, Ivanovski S . Detection of Salivary Small Extracellular Vesicles Associated Inflammatory Cytokines Gene Methylation in Gingivitis. Int J Mol Sci. 2020; 21(15). PMC: 7432462. DOI: 10.3390/ijms21155273. View

Jarmalaviciute A, Pivoriunas A . Exosomes as a potential novel therapeutic tools against neurodegenerative diseases. Pharmacol Res. 2016; 113(Pt B):816-822. DOI: 10.1016/j.phrs.2016.02.002. View

Kobayashi R, Ogawa Y, Hashizume-Takizawa T, Kurita-Ochiai T . Oral bacteria affect the gut microbiome and intestinal immunity. Pathog Dis. 2020; 78(3). DOI: 10.1093/femspd/ftaa024. View

Lin Y, Dong H, Deng W, Lin W, Li K, Xiong X . Evaluation of Salivary Exosomal Chimeric RNA as a Potential Biomarker in Esophageal Carcinoma. Clin Cancer Res. 2019; 25(10):3035-3045. DOI: 10.1158/1078-0432.CCR-18-3169. View

10.

Gao X, Jiang S, Koh D, Stephen Hsu C . Salivary biomarkers for dental caries. Periodontol 2000. 2015; 70(1):128-41. DOI: 10.1111/prd.12100. View

11.

Nell S, Suerbaum S, Josenhans C . The impact of the microbiota on the pathogenesis of IBD: lessons from mouse infection models. Nat Rev Microbiol. 2010; 8(8):564-77. DOI: 10.1038/nrmicro2403. View

12.

Zheng X, Chen F, Zhang Q, Liu Y, You P, Sun S . Salivary exosomal PSMA7: a promising biomarker of inflammatory bowel disease. Protein Cell. 2017; 8(9):686-695. PMC: 5563283. DOI: 10.1007/s13238-017-0413-7. View

13.

Fizanne L, Villard A, Benabbou N, Recoquillon S, Soleti R, Delage E . Faeces-derived extracellular vesicles participate in the onset of barrier dysfunction leading to liver diseases. J Extracell Vesicles. 2023; 12(2):e12303. PMC: 9883837. DOI: 10.1002/jev2.12303. View

14.

Wang H, Chao K, Ng S, Bai A, Yu Q, Yu J . Pro-inflammatory miR-223 mediates the cross-talk between the IL23 pathway and the intestinal barrier in inflammatory bowel disease. Genome Biol. 2016; 17:58. PMC: 4815271. DOI: 10.1186/s13059-016-0901-8. View

15.

He L, Ping F, Fan Z, Zhang C, Deng M, Cheng B . Salivary exosomal miR-24-3p serves as a potential detective biomarker for oral squamous cell carcinoma screening. Biomed Pharmacother. 2019; 121:109553. DOI: 10.1016/j.biopha.2019.109553. View

16.

Park S, Hwang B, Lim M, Ok S, Lee S, Chun K . Oral-Gut Microbiome Axis in Gastrointestinal Disease and Cancer. Cancers (Basel). 2021; 13(9). PMC: 8125773. DOI: 10.3390/cancers13092124. View

17.

von Schillde M, Hormannsperger G, Weiher M, Alpert C, Hahne H, Bauerl C . Lactocepin secreted by Lactobacillus exerts anti-inflammatory effects by selectively degrading proinflammatory chemokines. Cell Host Microbe. 2012; 11(4):387-96. DOI: 10.1016/j.chom.2012.02.006. View

18.

Rogler G, Singh A, Kavanaugh A, Rubin D . Extraintestinal Manifestations of Inflammatory Bowel Disease: Current Concepts, Treatment, and Implications for Disease Management. Gastroenterology. 2021; 161(4):1118-1132. PMC: 8564770. DOI: 10.1053/j.gastro.2021.07.042. View

19.

Shah N, Ishii M, Brandon C, Ablonczy Z, Cai J, Liu Y . Extracellular vesicle-mediated long-range communication in stressed retinal pigment epithelial cell monolayers. Biochim Biophys Acta Mol Basis Dis. 2018; 1864(8):2610-2622. PMC: 6545903. DOI: 10.1016/j.bbadis.2018.04.016. View

20.

Sun Y, Huo C, Qiao Z, Shang Z, Uzzaman A, Liu S . Comparative Proteomic Analysis of Exosomes and Microvesicles in Human Saliva for Lung Cancer. J Proteome Res. 2018; 17(3):1101-1107. DOI: 10.1021/acs.jproteome.7b00770. View