Chlorogenic Acid Ameliorates Post-Infectious Irritable Bowel Syndrome by Regulating Extracellular Vesicles of Gut Microbes

Overview

Journal Adv Sci (Weinh)

Specialty Biomedical Engineering

Date 2023 Aug 24

PMID 37616338

Authors

Cihua Zheng

Yuchun Zhong

Wenming Zhang

Zhuoya Wang

Haili Xiao

Wenjun Zhang

Jian Xie

Xiaogang Peng

Jun Luo

Wei Xu

Affiliations

Soon will be listed here.

Abstract

Post-infectious irritable bowel syndrome (PI-IBS) occurs after acute infectious diarrhea, and dysbiosis can be involved in its pathogenesis. Here, the role of chlorogenic acid (CGA) is investigated, a natural compound with several pharmacological properties, in alleviating PI-IBS in rats. It is elucidated that the gut microbiota plays a key role in PI-IBS pathogenesis and that rectal administration of CGA alleviated PI-IBS by modulating the gut microbiota and its metabolites. CGA supplementation significantly increased fecal Bacteroides acidifaciens abundance and glycine levels. Glycine structurally altered B. acidifaciens extracellular vesicles (EVs) and enriched functional proteins in the EVs; glycine-induced EVs alleviated PI-IBS by reducing inflammation and hypersensitivity of the intestinal viscera and maintaining mucosal barrier function. Moreover, B. acidifaciens EVs are enriched in the brain tissue. Thus, CGA mediates the mitigation of PI-IBS through the gut microbiota and its metabolites. This study proposes a novel mechanism of signal exchange between the gut microenvironment and the host.

Citing Articles

ScRNA-seq unveils the functional characteristics of glioma-associated macrophages and the regulatory effects of chlorogenic acid on the immune microenvironment-a study based on mouse models and clinical practice.

Wang J, Li S, Chen Y, Chen J, Wang C, Kang Z Front Immunol. 2025; 15:1494806.

PMID: 39867913 PMC: 11757274. DOI: 10.3389/fimmu.2024.1494806.

The Role of Gut Microbiome in Irritable Bowel Syndrome: Implications for Clinical Therapeutics.

Zhao Y, Zhu S, Dong Y, Xie T, Chai Z, Gao X Biomolecules. 2025; 14(12.

PMID: 39766350 PMC: 11674646. DOI: 10.3390/biom14121643.

Insights into Microbiota-Host Crosstalk in the Intestinal Diseases Mediated by Extracellular Vesicles and Their Encapsulated MicroRNAs.

Zeng Y, Yin Y, Zhou X Int J Mol Sci. 2024; 25(23.

PMID: 39684711 PMC: 11641152. DOI: 10.3390/ijms252313001.

Target fishing and mechanistic insights of the natural anticancer drug candidate chlorogenic acid.

Wang Q, Du T, Zhang Z, Zhang Q, Zhang J, Li W Acta Pharm Sin B. 2024; 14(10):4431-4442.

PMID: 39525590 PMC: 11544177. DOI: 10.1016/j.apsb.2024.07.005.

Intranasal administration of and its derived extracellular vesicles alleviate LPS-induced acute lung injury.

Liu L, Zheng C, Xu Z, Wang Z, Zhong Y, He Z Microbiol Spectr. 2024; :e0210824.

PMID: 39472001 PMC: 11619349. DOI: 10.1128/spectrum.02108-24.

References

Grabauskas G, Gao J, Wu X, Zhou S, Turgeon D, Owyang C . WITHDRAWN: Gut Microbiota Alter Visceral Pain Sensation and Inflammation via Modulation of Synthesis of Resolvin D1 in Colonic Tuft Cells. Gastroenterology. 2022; . PMC: 9898459. DOI: 10.1053/j.gastro.2022.07.053. View

Shao Y, Guo Y, Feng X, Liu J, Chang Z, Deng G . Oridonin Attenuates TNBS-induced Post-inflammatory Irritable Bowel Syndrome via PXR/NF-κB Signaling. Inflammation. 2020; 44(2):645-658. DOI: 10.1007/s10753-020-01364-0. View

Xia C, Jiang C, Li W, Wei J, Hong H, Li J . A Phase II Randomized Clinical Trial and Mechanistic Studies Using Improved Probiotics to Prevent Oral Mucositis Induced by Concurrent Radiotherapy and Chemotherapy in Nasopharyngeal Carcinoma. Front Immunol. 2021; 12:618150. PMC: 8024544. DOI: 10.3389/fimmu.2021.618150. View

Deng C, Zheng J, Zhou H, You J, Li G . Dietary glycine supplementation prevents heat stress-induced impairment of antioxidant status and intestinal barrier function in broilers. Poult Sci. 2022; 102(3):102408. PMC: 9827071. DOI: 10.1016/j.psj.2022.102408. View

He S, Guo Y, Zhao J, Xu X, Wang N, Liu Q . Ferulic Acid Ameliorates Lipopolysaccharide-Induced Barrier Dysfunction MicroRNA-200c-3p-Mediated Activation of PI3K/AKT Pathway in Caco-2 Cells. Front Pharmacol. 2020; 11:376. PMC: 7145943. DOI: 10.3389/fphar.2020.00376. View

Ghoshal U . Postinfection Irritable Bowel Syndrome. Gut Liver. 2021; 16(3):331-340. PMC: 9099396. DOI: 10.5009/gnl210208. View

Lee T, Kang I, Kim B, Sim H, Kim D, Ahn J . Experimental Pretreatment with Chlorogenic Acid Prevents Transient Ischemia-Induced Cognitive Decline and Neuronal Damage in the Hippocampus through Anti-Oxidative and Anti-Inflammatory Effects. Molecules. 2020; 25(16). PMC: 7463954. DOI: 10.3390/molecules25163578. View

Liu Y, Hu P, Zheng Z, Zhong D, Xie W, Tang Z . Photoresponsive Vaccine-Like CAR-M System with High-Efficiency Central Immune Regulation for Inflammation-Related Depression. Adv Mater. 2021; 34(11):e2108525. DOI: 10.1002/adma.202108525. View

Zhou X, Lu J, Wei K, Wei J, Tian P, Yue M . Neuroprotective Effect of Ceftriaxone on MPTP-Induced Parkinson's Disease Mouse Model by Regulating Inflammation and Intestinal Microbiota. Oxid Med Cell Longev. 2021; 2021:9424582. PMC: 8687851. DOI: 10.1155/2021/9424582. View

10.

Black C, Ford A . Global burden of irritable bowel syndrome: trends, predictions and risk factors. Nat Rev Gastroenterol Hepatol. 2020; 17(8):473-486. DOI: 10.1038/s41575-020-0286-8. View

11.

Yang Z, Gao Z, Yang Z, Zhang Y, Chen H, Yang X . Lactobacillus plantarum-derived extracellular vesicles protect against ischemic brain injury via the microRNA-101a-3p/c-Fos/TGF-β axis. Pharmacol Res. 2022; 182:106332. DOI: 10.1016/j.phrs.2022.106332. View

12.

Chen C, Rao S, Yue T, Tan Y, Yin H, Chen L . Glucocorticoid-induced loss of beneficial gut bacterial extracellular vesicles is associated with the pathogenesis of osteonecrosis. Sci Adv. 2022; 8(15):eabg8335. PMC: 9007505. DOI: 10.1126/sciadv.abg8335. View

13.

Zheng C, Chen T, Lu J, Wei K, Tian H, Liu W . Adjuvant treatment and molecular mechanism of probiotic compounds in patients with gastric cancer after gastrectomy. Food Funct. 2021; 12(14):6294-6308. DOI: 10.1039/d1fo01375k. View

14.

Xie M, Fei Y, Wang Y, Wang W, Wang Z . Chlorogenic Acid Alleviates Colon Mucosal Damage Induced by a High-Fat Diet via Gut Microflora Adjustment to Increase Short-Chain Fatty Acid Accumulation in Rats. Oxid Med Cell Longev. 2021; 2021:3456542. PMC: 7889347. DOI: 10.1155/2021/3456542. View

15.

Gwee K, Collins S, Read N, Rajnakova A, Deng Y, GRAHAM J . Increased rectal mucosal expression of interleukin 1beta in recently acquired post-infectious irritable bowel syndrome. Gut. 2003; 52(4):523-6. PMC: 1773606. DOI: 10.1136/gut.52.4.523. View

16.

Browne H, Forster S, Anonye B, Kumar N, Neville B, Stares M . Culturing of 'unculturable' human microbiota reveals novel taxa and extensive sporulation. Nature. 2016; 533(7604):543-546. PMC: 4890681. DOI: 10.1038/nature17645. View

17.

Ruan Z, Yang Y, Zhou Y, Wen Y, Ding S, Liu G . Metabolomic analysis of amino acid and energy metabolism in rats supplemented with chlorogenic acid. Amino Acids. 2014; 46(9):2219-29. PMC: 5013734. DOI: 10.1007/s00726-014-1762-7. View

18.

Sumiyoshi T, Anil A, Jin D, Jayathilake K, Lee M, Meltzer H . Plasma glycine and serine levels in schizophrenia compared to normal controls and major depression: relation to negative symptoms. Int J Neuropsychopharmacol. 2004; 7(1):1-8. DOI: 10.1017/S1461145703003900. View

19.

Gonthier M, Verny M, Besson C, Remesy C, Scalbert A . Chlorogenic acid bioavailability largely depends on its metabolism by the gut microflora in rats. J Nutr. 2003; 133(6):1853-9. DOI: 10.1093/jn/133.6.1853. View

20.

Wang F, Su M, Zheng Y, Wang X, Kang N, Chen T . Herbal prescription Chang'an II repairs intestinal mucosal barrier in rats with post-inflammation irritable bowel syndrome. Acta Pharmacol Sin. 2015; 36(6):708-15. PMC: 4594184. DOI: 10.1038/aps.2014.170. View