Pyrroloquinoline Quinone Regulates Enteric Neurochemical Plasticity of Weaned Rats Challenged With Lipopolysaccharide

The enteric nervous system (ENS) is important for the intestinal barrier to defend and regulate inflammation in the intestine. The aim of this study was to investigate the effect of pyrroloquinoline quinone (PQQ) on regulating neuropeptide secretion by ENS neurons of rats challenged with lipopolysac...

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Main Authors: Chenyu Shi, Song Xu, Caiyun Huang, Zijie Wang, Wenhui Wang, Dongxu Ming, Xindi Yin, Hu Liu, Fenglai Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2022.878541/full
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author Chenyu Shi
Song Xu
Caiyun Huang
Zijie Wang
Wenhui Wang
Dongxu Ming
Xindi Yin
Hu Liu
Fenglai Wang
author_facet Chenyu Shi
Song Xu
Caiyun Huang
Zijie Wang
Wenhui Wang
Dongxu Ming
Xindi Yin
Hu Liu
Fenglai Wang
author_sort Chenyu Shi
collection DOAJ
description The enteric nervous system (ENS) is important for the intestinal barrier to defend and regulate inflammation in the intestine. The aim of this study was to investigate the effect of pyrroloquinoline quinone (PQQ) on regulating neuropeptide secretion by ENS neurons of rats challenged with lipopolysaccharide (LPS) to create enteritis. Thirty Sprague Dawley rats were divided into five groups, namely, basal (CTRL), basal plus LPS challenge (LPS), basal with 2.5 mg/kg b.w./day of PQQ plus challenge with LPS (PQQ 2.5), basal with 5.0 mg/kg b.w./day PQQ plus challenge with LPS (PQQ 5), and basal with 10.0 mg/kg b.w./day PQQ plus challenge with LPS (PQQ 10). After treatment with basal diet or PQQ for 14 days, rats were challenged with LPS except for the CTRL group. Rats were euthanized 6 h after the LPS challenge. Rats showed an increased average daily gain in PQQ treatment groups (P < 0.05). Compared with the LPS group, PQQ 5 and PQQ 10 rats showed increased villus height and villus height/crypt depth of jejunum (P < 0.05). In PQQ treatment groups, concentrations of IL-1β and TNF-α in serum and intestine of rats were decreased, and IL-10 concentration was increased in serum compared with the LPS group (P < 0.05). Compared with the LPS group, the concentration of neuropeptide Y (NPY), nerve growth factor (NGF), vasoactive intestinal peptide (VIP), substance P (SP), calcitonin gene-related peptide (CGRP), and brain-derived neurotropic factor (BDNF) in serum were decreased in PQQ treatment groups (P < 0.05). Compared with the LPS group, ileal mRNA levels of BDNF, NPY, and NGF were decreased in PQQ treatment groups (P < 0.05). Jejunal concentrations of SP, CGRP, VIP, BDNF, NPY, and NGF were decreased in PQQ treatment groups compared with the LPS group (P < 0.05). Compared with the LPS group, phosphor-protein kinase B (p-Akt)/Akt levels in jejunum and colon were decreased in PQQ treatment groups (P < 0.05). In conclusion, daily treatment with PQQ improved daily gain, jejunal morphology, immune responses. PQQ-regulated enteric neurochemical plasticity of ENS via the Akt signaling pathway of weaned rats suffering from enteritis.
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spelling doaj.art-cb2d5fe43550463ea5c0aedd22a72c1e2022-12-22T02:35:19ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2022-05-011610.3389/fnins.2022.878541878541Pyrroloquinoline Quinone Regulates Enteric Neurochemical Plasticity of Weaned Rats Challenged With LipopolysaccharideChenyu Shi0Song Xu1Caiyun Huang2Zijie Wang3Wenhui Wang4Dongxu Ming5Xindi Yin6Hu Liu7Fenglai Wang8State Key Lab of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, ChinaState Key Lab of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, ChinaCollege of Animal Science, Fujian Agriculture and Forestry University, Fuzhou, ChinaState Key Lab of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, ChinaState Key Lab of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, ChinaState Key Lab of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, ChinaDepartment of Nutrition and Health, China Agricultural University, Beijing, ChinaState Key Lab of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, ChinaState Key Lab of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, ChinaThe enteric nervous system (ENS) is important for the intestinal barrier to defend and regulate inflammation in the intestine. The aim of this study was to investigate the effect of pyrroloquinoline quinone (PQQ) on regulating neuropeptide secretion by ENS neurons of rats challenged with lipopolysaccharide (LPS) to create enteritis. Thirty Sprague Dawley rats were divided into five groups, namely, basal (CTRL), basal plus LPS challenge (LPS), basal with 2.5 mg/kg b.w./day of PQQ plus challenge with LPS (PQQ 2.5), basal with 5.0 mg/kg b.w./day PQQ plus challenge with LPS (PQQ 5), and basal with 10.0 mg/kg b.w./day PQQ plus challenge with LPS (PQQ 10). After treatment with basal diet or PQQ for 14 days, rats were challenged with LPS except for the CTRL group. Rats were euthanized 6 h after the LPS challenge. Rats showed an increased average daily gain in PQQ treatment groups (P < 0.05). Compared with the LPS group, PQQ 5 and PQQ 10 rats showed increased villus height and villus height/crypt depth of jejunum (P < 0.05). In PQQ treatment groups, concentrations of IL-1β and TNF-α in serum and intestine of rats were decreased, and IL-10 concentration was increased in serum compared with the LPS group (P < 0.05). Compared with the LPS group, the concentration of neuropeptide Y (NPY), nerve growth factor (NGF), vasoactive intestinal peptide (VIP), substance P (SP), calcitonin gene-related peptide (CGRP), and brain-derived neurotropic factor (BDNF) in serum were decreased in PQQ treatment groups (P < 0.05). Compared with the LPS group, ileal mRNA levels of BDNF, NPY, and NGF were decreased in PQQ treatment groups (P < 0.05). Jejunal concentrations of SP, CGRP, VIP, BDNF, NPY, and NGF were decreased in PQQ treatment groups compared with the LPS group (P < 0.05). Compared with the LPS group, phosphor-protein kinase B (p-Akt)/Akt levels in jejunum and colon were decreased in PQQ treatment groups (P < 0.05). In conclusion, daily treatment with PQQ improved daily gain, jejunal morphology, immune responses. PQQ-regulated enteric neurochemical plasticity of ENS via the Akt signaling pathway of weaned rats suffering from enteritis.https://www.frontiersin.org/articles/10.3389/fnins.2022.878541/fullpyrroloquinoline quinoneenteric nervous systemneurochemical plasticityAkt signaling pathwayenteritis rats
spellingShingle Chenyu Shi
Song Xu
Caiyun Huang
Zijie Wang
Wenhui Wang
Dongxu Ming
Xindi Yin
Hu Liu
Fenglai Wang
Pyrroloquinoline Quinone Regulates Enteric Neurochemical Plasticity of Weaned Rats Challenged With Lipopolysaccharide
Frontiers in Neuroscience
pyrroloquinoline quinone
enteric nervous system
neurochemical plasticity
Akt signaling pathway
enteritis rats
title Pyrroloquinoline Quinone Regulates Enteric Neurochemical Plasticity of Weaned Rats Challenged With Lipopolysaccharide
title_full Pyrroloquinoline Quinone Regulates Enteric Neurochemical Plasticity of Weaned Rats Challenged With Lipopolysaccharide
title_fullStr Pyrroloquinoline Quinone Regulates Enteric Neurochemical Plasticity of Weaned Rats Challenged With Lipopolysaccharide
title_full_unstemmed Pyrroloquinoline Quinone Regulates Enteric Neurochemical Plasticity of Weaned Rats Challenged With Lipopolysaccharide
title_short Pyrroloquinoline Quinone Regulates Enteric Neurochemical Plasticity of Weaned Rats Challenged With Lipopolysaccharide
title_sort pyrroloquinoline quinone regulates enteric neurochemical plasticity of weaned rats challenged with lipopolysaccharide
topic pyrroloquinoline quinone
enteric nervous system
neurochemical plasticity
Akt signaling pathway
enteritis rats
url https://www.frontiersin.org/articles/10.3389/fnins.2022.878541/full
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