Association between AHR in EGCs and IBS-D patients: the indole pathway of tryptophan metabolism

BackgroundThe pathophysiological mechanisms of irritable bowel syndrome (IBS) are intricate, and associated with tryptophan metabolites. This study was designed to investigate the relationship between indole metabolites in the feces and intestinal function in patients with IBS.MethodsIn this study,...

Full description

Saved in:
Bibliographic Details
Main Authors: Lianli Wang, Yue Zhang, Yan Ran, Laifu Li, Lin Mei, Fangchen Ye, Yating Sun, Ting Wang, Xiaojing Quan, Haitao Shi, Fei Dai
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-03-01
Series:Frontiers in Nutrition
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnut.2025.1566595/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850066953348055040
author Lianli Wang
Yue Zhang
Yan Ran
Laifu Li
Lin Mei
Fangchen Ye
Yating Sun
Ting Wang
Xiaojing Quan
Haitao Shi
Fei Dai
author_facet Lianli Wang
Yue Zhang
Yan Ran
Laifu Li
Lin Mei
Fangchen Ye
Yating Sun
Ting Wang
Xiaojing Quan
Haitao Shi
Fei Dai
author_sort Lianli Wang
collection DOAJ
description BackgroundThe pathophysiological mechanisms of irritable bowel syndrome (IBS) are intricate, and associated with tryptophan metabolites. This study was designed to investigate the relationship between indole metabolites in the feces and intestinal function in patients with IBS.MethodsIn this study, 42 patients with diarrhea-predominant IBS (IBS-D) and 36 healthy controls were recruited. The symptom severity was evaluated using IBS-quality of life (IBS-QOL) and IBS symptom severity system (IBS-SSS). The levels of indole metabolite in fecal samples were determined by means of mass spectrometry. Colon mucosal tissues were collected during colonoscopy procedures. Immunohistochemistry or immunofluorescence techniques were employed to analyze the expressions of the aryl hydrocarbon receptor (AHR), cytochrome P450 1A1 (CYP1A1), glial fibrillary acidic protein (GFAP), S100 calcium-binding protein B (S100B), zonula occludens-1 (Zo-1), occludin, substance P (SP), nerve growth factor (NGF), NOD-like receptor family pyrin domain containing 3 (NLRP3), and nuclear factor kappa B (NF-κB) in the mucosal tissues.ResultsCompared with healthy controls, the concentrations of the main indole metabolites (p = 0.020), and the expressions of CYP1A1 (p < 0.001), and Zo-1 (p = 0.017) were decreased in patients with IBS-D, but the expressions of S100B (p < 0.001), NF-κB (p = 0.006), and NRLP3 (p = 0.041) were increased. Immunofluorescence analysis demonstrated the co-expression of AHR with GFAP or S100B. Moreover, the ratio of S100B/AHR (p = 0.011) was higher in IBS-D patients than in health controls. This ratio was positively correlated with IBS-SSS score (r = 0.47, p = 0.006), as well as with the expression levels of NRLP3 (r = 0.505, p = 0.019), NF-κB (r = 0.548, p = 0.01), and SP (r = 0.832, p < 0.01).ConclusionPatients with IBS-D exhibited low-grade inflammation in the colon mucosal tissues, compromised intestinal barrier function, and abnormal visceral sensation. This may be attributed to the decreased levels of tryptophan indole metabolites, the heightened activity of enteric glial cells (EGCs), and the inhibition of AHR/CPY1A1 signaling pathway.
format Article
id doaj-art-d2739633be4c4d61ba5a7b718c14b034
institution DOAJ
issn 2296-861X
language English
publishDate 2025-03-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Nutrition
spelling doaj-art-d2739633be4c4d61ba5a7b718c14b0342025-08-20T02:48:33ZengFrontiers Media S.A.Frontiers in Nutrition2296-861X2025-03-011210.3389/fnut.2025.15665951566595Association between AHR in EGCs and IBS-D patients: the indole pathway of tryptophan metabolismLianli Wang0Yue Zhang1Yan Ran2Laifu Li3Lin Mei4Fangchen Ye5Yating Sun6Ting Wang7Xiaojing Quan8Haitao Shi9Fei Dai10Division of Gastroenterology, The Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an, ChinaDivision of Gastroenterology, Honghui Hospital, Xi’an Jiaotong University College of Medicine, Xi’an, ChinaDivision of Gastroenterology, The Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an, ChinaDivision of Gastroenterology, The Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an, ChinaDivision of Gastroenterology, The Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an, ChinaDivision of Gastroenterology, The Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an, ChinaDivision of Gastroenterology, The Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an, ChinaDivision of Gastroenterology, The Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an, ChinaDivision of Gastroenterology, The Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an, ChinaDivision of Gastroenterology, The Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an, ChinaDivision of Gastroenterology, The Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an, ChinaBackgroundThe pathophysiological mechanisms of irritable bowel syndrome (IBS) are intricate, and associated with tryptophan metabolites. This study was designed to investigate the relationship between indole metabolites in the feces and intestinal function in patients with IBS.MethodsIn this study, 42 patients with diarrhea-predominant IBS (IBS-D) and 36 healthy controls were recruited. The symptom severity was evaluated using IBS-quality of life (IBS-QOL) and IBS symptom severity system (IBS-SSS). The levels of indole metabolite in fecal samples were determined by means of mass spectrometry. Colon mucosal tissues were collected during colonoscopy procedures. Immunohistochemistry or immunofluorescence techniques were employed to analyze the expressions of the aryl hydrocarbon receptor (AHR), cytochrome P450 1A1 (CYP1A1), glial fibrillary acidic protein (GFAP), S100 calcium-binding protein B (S100B), zonula occludens-1 (Zo-1), occludin, substance P (SP), nerve growth factor (NGF), NOD-like receptor family pyrin domain containing 3 (NLRP3), and nuclear factor kappa B (NF-κB) in the mucosal tissues.ResultsCompared with healthy controls, the concentrations of the main indole metabolites (p = 0.020), and the expressions of CYP1A1 (p < 0.001), and Zo-1 (p = 0.017) were decreased in patients with IBS-D, but the expressions of S100B (p < 0.001), NF-κB (p = 0.006), and NRLP3 (p = 0.041) were increased. Immunofluorescence analysis demonstrated the co-expression of AHR with GFAP or S100B. Moreover, the ratio of S100B/AHR (p = 0.011) was higher in IBS-D patients than in health controls. This ratio was positively correlated with IBS-SSS score (r = 0.47, p = 0.006), as well as with the expression levels of NRLP3 (r = 0.505, p = 0.019), NF-κB (r = 0.548, p = 0.01), and SP (r = 0.832, p < 0.01).ConclusionPatients with IBS-D exhibited low-grade inflammation in the colon mucosal tissues, compromised intestinal barrier function, and abnormal visceral sensation. This may be attributed to the decreased levels of tryptophan indole metabolites, the heightened activity of enteric glial cells (EGCs), and the inhibition of AHR/CPY1A1 signaling pathway.https://www.frontiersin.org/articles/10.3389/fnut.2025.1566595/fulltryptophanaryl hydrocarbon receptorinflammationenteric glial cellsIBS-D
spellingShingle Lianli Wang
Yue Zhang
Yan Ran
Laifu Li
Lin Mei
Fangchen Ye
Yating Sun
Ting Wang
Xiaojing Quan
Haitao Shi
Fei Dai
Association between AHR in EGCs and IBS-D patients: the indole pathway of tryptophan metabolism
Frontiers in Nutrition
tryptophan
aryl hydrocarbon receptor
inflammation
enteric glial cells
IBS-D
title Association between AHR in EGCs and IBS-D patients: the indole pathway of tryptophan metabolism
title_full Association between AHR in EGCs and IBS-D patients: the indole pathway of tryptophan metabolism
title_fullStr Association between AHR in EGCs and IBS-D patients: the indole pathway of tryptophan metabolism
title_full_unstemmed Association between AHR in EGCs and IBS-D patients: the indole pathway of tryptophan metabolism
title_short Association between AHR in EGCs and IBS-D patients: the indole pathway of tryptophan metabolism
title_sort association between ahr in egcs and ibs d patients the indole pathway of tryptophan metabolism
topic tryptophan
aryl hydrocarbon receptor
inflammation
enteric glial cells
IBS-D
url https://www.frontiersin.org/articles/10.3389/fnut.2025.1566595/full
work_keys_str_mv AT lianliwang associationbetweenahrinegcsandibsdpatientstheindolepathwayoftryptophanmetabolism
AT yuezhang associationbetweenahrinegcsandibsdpatientstheindolepathwayoftryptophanmetabolism
AT yanran associationbetweenahrinegcsandibsdpatientstheindolepathwayoftryptophanmetabolism
AT laifuli associationbetweenahrinegcsandibsdpatientstheindolepathwayoftryptophanmetabolism
AT linmei associationbetweenahrinegcsandibsdpatientstheindolepathwayoftryptophanmetabolism
AT fangchenye associationbetweenahrinegcsandibsdpatientstheindolepathwayoftryptophanmetabolism
AT yatingsun associationbetweenahrinegcsandibsdpatientstheindolepathwayoftryptophanmetabolism
AT tingwang associationbetweenahrinegcsandibsdpatientstheindolepathwayoftryptophanmetabolism
AT xiaojingquan associationbetweenahrinegcsandibsdpatientstheindolepathwayoftryptophanmetabolism
AT haitaoshi associationbetweenahrinegcsandibsdpatientstheindolepathwayoftryptophanmetabolism
AT feidai associationbetweenahrinegcsandibsdpatientstheindolepathwayoftryptophanmetabolism