Disruption of the pro-inflammatory, anti-inflammatory cytokines and tight junction proteins expression, associated with changes of the composition of the gut microbiota in patients with irritable bowel syndrome.
Journal
PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081
Informations de publication
Date de publication:
2021
2021
Historique:
received:
30
09
2020
accepted:
25
05
2021
entrez:
11
6
2021
pubmed:
12
6
2021
medline:
17
11
2021
Statut:
epublish
Résumé
Irritable bowel syndrome (IBS) is a pathologic condition characterized by changes in gut microbiome composition, low-grade inflammation, and disruption of intestinal wall permeability. The interaction between the gut microbiome and the disease manifestation remains unclear. The changing of tight junction proteins and cytokines expression throughout the gastrointestinal tract in IBS patients has not been studied yet. To assess the changes of gut microbiome composition, tight junction proteins, and cytokines expression of intestinal mucosa from the duodenum to the distal part of the colon in IBS patients and healthy volunteers. In 31 IBS patients (16 patients with IBS-D; 15 patients with IBS-C) and 10 healthy volunteers the expression of CLD-2, CLD-3, CLD-5, IL-2, IL-10, and TNF-α in mucosal biopsy specimens was determined by morphological and immune-histochemical methods. The qualitative and quantitative composition of the intestinal microbiota was assessed based on 16S rRNA gene sequencing in both groups of patients. The expression of IL-2 and TNF-α was significantly increased in IBS patients compared with the controls (p<0.001), with a gradual increase from the duodenum to the sigmoid colon. The expression of IL-10, CLD-3, and CLD-5 in mucosal biopsy specimens of these patients was lower than in the control group (p<0.001). Increased ratios of Bacteroidetes and decreased ratios of Firmicutes were noted in IBS patients compared to healthy volunteers (p<0.05). IBS patients have impaired gut permeability and persisting low-grade inflammation throughout the gastrointestinal tract. Changes in the gut microbiota may support or exacerbate these changes.
Sections du résumé
BACKGROUND
Irritable bowel syndrome (IBS) is a pathologic condition characterized by changes in gut microbiome composition, low-grade inflammation, and disruption of intestinal wall permeability. The interaction between the gut microbiome and the disease manifestation remains unclear. The changing of tight junction proteins and cytokines expression throughout the gastrointestinal tract in IBS patients has not been studied yet.
AIM OF THE STUDY
To assess the changes of gut microbiome composition, tight junction proteins, and cytokines expression of intestinal mucosa from the duodenum to the distal part of the colon in IBS patients and healthy volunteers.
METHODS
In 31 IBS patients (16 patients with IBS-D; 15 patients with IBS-C) and 10 healthy volunteers the expression of CLD-2, CLD-3, CLD-5, IL-2, IL-10, and TNF-α in mucosal biopsy specimens was determined by morphological and immune-histochemical methods. The qualitative and quantitative composition of the intestinal microbiota was assessed based on 16S rRNA gene sequencing in both groups of patients.
RESULTS
The expression of IL-2 and TNF-α was significantly increased in IBS patients compared with the controls (p<0.001), with a gradual increase from the duodenum to the sigmoid colon. The expression of IL-10, CLD-3, and CLD-5 in mucosal biopsy specimens of these patients was lower than in the control group (p<0.001). Increased ratios of Bacteroidetes and decreased ratios of Firmicutes were noted in IBS patients compared to healthy volunteers (p<0.05).
CONCLUSION
IBS patients have impaired gut permeability and persisting low-grade inflammation throughout the gastrointestinal tract. Changes in the gut microbiota may support or exacerbate these changes.
Identifiants
pubmed: 34115808
doi: 10.1371/journal.pone.0252930
pii: PONE-D-20-30820
pmc: PMC8195381
doi:
Substances chimiques
Cytokines
0
Inflammation Mediators
0
Tight Junction Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e0252930Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Neurogastroenterol Motil. 2014 Mar;26(3):316-25
pubmed: 24286617
Nat Rev Immunol. 2016 May 27;16(6):341-52
pubmed: 27231050
Expert Rev Gastroenterol Hepatol. 2019 Apr;13(4):345-359
pubmed: 30791775
Am J Physiol Gastrointest Liver Physiol. 2013 Oct 15;305(8):G529-41
pubmed: 23886861
World J Gastroenterol. 2020 Apr 14;26(14):1564-1579
pubmed: 32327906
Scand J Gastroenterol. 2020 May;55(5):537-542
pubmed: 32329383
Mol Med Rep. 2015 Sep;12(3):3257-3264
pubmed: 25998845
Physiol Rev. 2013 Apr;93(2):525-69
pubmed: 23589827
Physiol Rev. 2010 Jul;90(3):859-904
pubmed: 20664075
Curr Gastroenterol Rep. 2014 Apr;16(4):379
pubmed: 24595616
Gastroenterology. 2016 Feb 18;:
pubmed: 27144627
Appl Environ Microbiol. 2005 Nov;71(11):7483-92
pubmed: 16269790
FEMS Microbiol Ecol. 2012 Dec;82(3):666-77
pubmed: 22738186
Behav Res Methods. 2009 Nov;41(4):1149-60
pubmed: 19897823
Clin Transl Gastroenterol. 2019 Feb;10(2):e00012
pubmed: 30829919
Adv Immunol. 2014;121:91-119
pubmed: 24388214
Gastroenterology. 2019 Jul;157(1):97-108
pubmed: 30940523
Lancet Gastroenterol Hepatol. 2016 Oct;1(2):133-146
pubmed: 28404070
J Gen Physiol. 2018 Jul 2;150(7):949-968
pubmed: 29915162
Gut. 2003 Apr;52(4):523-6
pubmed: 12631663
Gut. 2014 May;63(5):744-52
pubmed: 23878165
Gut Liver. 2012 Jul;6(3):305-15
pubmed: 22844557
World J Gastroenterol. 2014 Feb 7;20(5):1165-79
pubmed: 24574793
Scand J Gastroenterol. 2008;43(12):1467-76
pubmed: 18752146
J Clin Invest. 2011 Jun;121(6):2242-53
pubmed: 21606592
ISME J. 2011 Oct;5(10):1571-9
pubmed: 21472016
Am J Gastroenterol. 2012 Feb;107(2):262-72
pubmed: 22158028
Microb Ecol. 2001 Apr;41(3):252-263
pubmed: 11391463
J Inflamm Res. 2018 Sep 21;11:345-349
pubmed: 30288077
J Atheroscler Thromb. 2017 Jul 1;24(7):660-672
pubmed: 28552897
Ann Gastroenterol. 2019 Nov-Dec;32(6):554-564
pubmed: 31700231
Gut. 2014 Feb;63(2):262-71
pubmed: 23474421
Gastroenterology. 2019 Aug;157(2):391-402.e2
pubmed: 31022401
Gut. 2016 Jan;65(1):155-68
pubmed: 26194403
Cytokine. 2017 May;93:34-43
pubmed: 28506572
J Clin Biochem Nutr. 2017 Mar;60(2):146-150
pubmed: 28366996
Nat Commun. 2019 Nov 6;10(1):5029
pubmed: 31695033
Int J Mol Sci. 2019 Mar 25;20(6):
pubmed: 30934533
Behav Res Methods. 2007 May;39(2):175-91
pubmed: 17695343
Physiol Rev. 2019 Oct 1;99(4):1877-2013
pubmed: 31460832
Am J Gastroenterol. 2016 Aug;111(8):1165-76
pubmed: 27272011
Handb Exp Pharmacol. 2017;239:75-113
pubmed: 27995391