Basic Study
Copyright ©The Author(s) 2017. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Nov 14, 2017; 23(42): 7594-7608
Published online Nov 14, 2017. doi: 10.3748/wjg.v23.i42.7594
Potential rat model of anxiety-like gastric hypersensitivity induced by sequential stress
Fu-Chun Jing, Jun Zhang, Chen Feng, Yuan-Yuan Nian, Jin-Hai Wang, Hao Hu, Bao-De Yang, Xiao-Ming Sun, Jian-Yun Zheng, Xiao-Ran Yin
Fu-Chun Jing, Jun Zhang, Chen Feng, Yuan-Yuan Nian, Jin-Hai Wang, Xiao-Ran Yin, Department of Gastroenterology, Second Hospital Affiliated to the Medical School of Xi’an Jiao Tong University, Xi’an 710004, Shaanxi Province, China
Fu-Chun Jing, Department of Digestive Diseases, Baoji People’s Hospital Affiliated to the Medical School of Yan’an University, Baoji 721000, Shaanxi Province, China
Hao Hu, Bao-De Yang, Xiao-Ming Sun, Department of Pharmacology, Health Science Center, Xi’an Jiao Tong University, Xi’an 710061, Shaanxi Province, China
Hao Hu, Bao-De Yang, Xiao-Ming Sun, Basic Medical Experiment Teaching Center, Health Science Center, Xi’an Jiao Tong University, Xi’an 710061, Shaanxi Province, China
Jian-Yun Zheng, Department of Pathology, the First Affiliated Hospital of Xi’an Medical University, Xi’an 710077, Shaanxi Province, China
Author contributions: Jing FC designed and performed the experiments and wrote the manuscript; Zhang J put forward the conceptualization of the experiments; Feng C, Nian YY, Wang JH, Hu H, Yang BD, Sun XM and Zheng JY performed part of the experiments and collected data; Jing FC and Yin XR were responsible for the analysis of data.
Institutional review board statement: The study was reviewed and approved by the Institutional Review Board of Baoji People’s Hospital Affiliated to the Medical School of Yan’an University.
Institutional animal care and use committee statement: All procedures involving animals were reviewed and approved by the Experimental Animal Care and Use Committee of Baoji People’s Hospital Affiliated to the Medical School of Yan’an University (EACUC Protocol no. 2016-0001).
Conflict-of-interest statement: All authors declare that there are no conflicts of interest.
Data sharing statement: All authors declare that no additional data are available.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Jun Zhang, PhD, Professor, Department of Gastroenterology, Second Hospital Affiliated to the Medical School of Xi’an Jiao Tong University, No. 157, West Road 5, Xi’an 710004, Shaanxi Province, China. jun3z@163.com
Telephone: +86-29-87679272 Fax: +86-29-87679272
Received: July 27, 2017
Peer-review started: July 28, 2017
First decision: September 26, 2017
Revised: October 4, 2017
Accepted: October 18, 2017
Article in press: October 19, 2017
Published online: November 14, 2017
Processing time: 107 Days and 16.9 Hours
Abstract
AIM

To establish a rat model of anxiety-like gastric hypersensitivity (GHS) of functional dyspepsia (FD) induced by novel sequential stress.

METHODS

Animal pups were divided into two groups from postnatal day 2: controls and the sequential-stress-treated. The sequential-stress-treated group received maternal separation and acute gastric irritation early in life and restraint stress in adulthood; controls were reared undisturbed with their mothers. Rats in both groups were followed to adulthood (8 wk) at which point the anxiety-like behaviors and visceromotor responses to gastric distention (20-100 mmHg) and gastric emptying were tested. Meanwhile, alterations in several anxiety-related brain-stomach modulators including 5-hydroxytryptamine (5-HT), γ-aminobutyric acid (GABA), brain-derived neurotrophic factor (BDNF) and nesfatin-1 in the rat hippocampus, plasma and gastric fundus and the 5-HT1A receptor (5-HT1AR) in the hippocampal CA1 subfield and the mucosa of the gastric fundus were examined.

RESULTS

Sequential-stress-treated rats simultaneously demonstrated anxiety-like behaviors and GHS in dose-dependent manner compared with the control group. Although rats in both groups consumed similar amount of solid food, the rate of gastric emptying was lower in the sequential-stress-treated rats than in the control group. Sequential stress significantly decreased the levels of 5-HT (51.91 ± 1.88 vs 104.21 ± 2.88, P < 0.01), GABA (2.38 ± 0.16 vs 5.01 ± 0.13, P < 0.01) and BDNF (304.40 ± 10.16 vs 698.17 ± 27.91, P < 0.01) in the hippocampus but increased the content of nesfatin-1 (1961.38 ± 56.89 vs 1007.50 ± 33.05, P < 0.01) in the same site; significantly decreased the levels of 5-HT (47.82 ± 2.29 vs 89.45 ± 2.61, P < 0.01) and BDNF (257.05 ± 12.89 vs 536.71 ± 20.73, P < 0.01) in the plasma but increased the content of nesfatin-1 in it (1391.75 ± 42.77 vs 737.88 ± 33.15, P < 0.01); significantly decreased the levels of 5-HT (41.15 ± 1.81 vs 89.17 ± 2.31, P < 0.01) and BDNF (226.49 ± 12.10 vs 551.36 ± 16.47, P < 0.01) in the gastric fundus but increased the content of nesfatin-1 in the same site (1534.75 ± 38.52 vs 819.63 ± 38.04, P < 0.01). The expressions of 5-HT1AR in the hippocampal CA1 subfield and the mucosa of the gastric fundus were down-regulated measured by IHC (Optical Density value: Hippocampus 15253.50 ± 760.35 vs 21149.75 ± 834.13; gastric fundus 15865.25 ± 521.24 vs 23865.75 ± 1868.60; P < 0.05, respectively) and WB (0.38 ± 0.01 vs 0.57 ± 0.03, P < 0.01) (n = 8 in each group).

CONCLUSION

Sequential stress could induce a potential rat model of anxiety-like GHS of FD, which could be used to research the mechanisms of this intractable disease.

Keywords: Gastric hypersensitivity; Anxiety; Functional dyspepsia; 5-hydroxytryptamine; γ-aminobutyric acid; Brain-derived neurotrophic factor; Nesfatin-1; Rat model

Core tip: Functional dyspepsia (FD) is a common gastrointestinal disorder in clinic. Gastric hypersensitivity (GHS) and anxiety are important factors triggering or aggravating it, however, the mechanisms by which affect the development of FD are still unknown. In part, this is due to a lack of suitable animal models of FD with anxiety and GHS. Our study provided such a newly developed rat model induced by sequential stress. It demonstrated the complex behavioral characteristics of anxiety and GHS, and the complicated alterations in some anxiety-related neurobiochemical modulators such as 5-hydroxytryptamine, γ-aminobutyric acid, brain-derived neurotrophic factor and nesfatin-1 in the hippocampus, plasma and gastric fundus.