Chronic stress induces hypersensitivity of murine gastric vagal afferents.


Journal

Neurogastroenterology and motility
ISSN: 1365-2982
Titre abrégé: Neurogastroenterol Motil
Pays: England
ID NLM: 9432572

Informations de publication

Date de publication:
12 2019
Historique:
received: 20 02 2019
revised: 22 05 2019
accepted: 18 06 2019
pubmed: 27 6 2019
medline: 1 9 2020
entrez: 27 6 2019
Statut: ppublish

Résumé

Stress exposure is known to trigger and exacerbate functional dyspepsia (FD) symptoms. Increased gastric sensitivity to food-related stimuli is widely observed in FD patients and is associated with stress and psychological disorders. The mechanisms underlying the hypersensitivity are not clear. Gastric vagal afferents (GVAs) play an important role in sensing meal-related mechanical stimulation to modulate gastrointestinal function and food intake. This study aimed to determine whether GVAs display hypersensitivity after chronic stress, and whether its interaction with leptin was altered by stress. Eight-week-old male C57BL/6 mice were exposed to unpredictable chronic mild stress or no stress (control) for 8 weeks. The metabolic rate, gastric emptying rate, and anxiety- and depression-like behaviors were determined. GVA mechanosensitivity, and its modulation by leptin, was determined using an in vitro single fiber recording technique. QRT-PCR was used to establish the levels of leptin and leptin receptor mRNA in the stomach and nodose ganglion, respectively. The stressed mice had lower body weight and food intake, and increased anxiety-like behavior compared to the control mice. The mechanosensitivity of mucosal and tension-sensitive GVAs was higher in the stressed mice. Leptin potentiated mucosal GVA mechanosensitivity in control but not stressed mice. The expression of leptin mRNA in the gastric mucosa was lower in the stressed mice. In conclusion, chronic stress enhances GVA mechanosensitivity, which may contribute to the gastric hypersensitivity in FD. In addition, the modulatory effect of leptin on GVA signaling is lost after chronic stress exposure.

Sections du résumé

BACKGROUND
Stress exposure is known to trigger and exacerbate functional dyspepsia (FD) symptoms. Increased gastric sensitivity to food-related stimuli is widely observed in FD patients and is associated with stress and psychological disorders. The mechanisms underlying the hypersensitivity are not clear. Gastric vagal afferents (GVAs) play an important role in sensing meal-related mechanical stimulation to modulate gastrointestinal function and food intake. This study aimed to determine whether GVAs display hypersensitivity after chronic stress, and whether its interaction with leptin was altered by stress.
METHODS
Eight-week-old male C57BL/6 mice were exposed to unpredictable chronic mild stress or no stress (control) for 8 weeks. The metabolic rate, gastric emptying rate, and anxiety- and depression-like behaviors were determined. GVA mechanosensitivity, and its modulation by leptin, was determined using an in vitro single fiber recording technique. QRT-PCR was used to establish the levels of leptin and leptin receptor mRNA in the stomach and nodose ganglion, respectively.
KEY RESULTS
The stressed mice had lower body weight and food intake, and increased anxiety-like behavior compared to the control mice. The mechanosensitivity of mucosal and tension-sensitive GVAs was higher in the stressed mice. Leptin potentiated mucosal GVA mechanosensitivity in control but not stressed mice. The expression of leptin mRNA in the gastric mucosa was lower in the stressed mice.
CONCLUSIONS AND INFERENCES
In conclusion, chronic stress enhances GVA mechanosensitivity, which may contribute to the gastric hypersensitivity in FD. In addition, the modulatory effect of leptin on GVA signaling is lost after chronic stress exposure.

Identifiants

pubmed: 31241809
doi: 10.1111/nmo.13669
doi:

Substances chimiques

Blood Glucose 0
Leptin 0
Noxae 0
Sucrose 57-50-1
Corticosterone W980KJ009P

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13669

Informations de copyright

© 2019 John Wiley & Sons Ltd.

Références

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Auteurs

Hui Li (H)

Vagal Afferent Research Group, Centre for Nutrition and Gastrointestinal Disease, Adelaide Medical School, University of Adelaide, Adelaide, South Australia, Australia.
Nutrition, Diabetes and Metabolism, South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia.

Femke T A Buisman-Pijlman (FTA)

Behavioural Neuroscience, Adelaide Medical School, University of Adelaide, Adelaide, South Australia, Australia.

Maria Nunez-Salces (M)

Vagal Afferent Research Group, Centre for Nutrition and Gastrointestinal Disease, Adelaide Medical School, University of Adelaide, Adelaide, South Australia, Australia.
Nutrition, Diabetes and Metabolism, South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia.

Stewart Christie (S)

Vagal Afferent Research Group, Centre for Nutrition and Gastrointestinal Disease, Adelaide Medical School, University of Adelaide, Adelaide, South Australia, Australia.
Nutrition, Diabetes and Metabolism, South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia.

Claudine L Frisby (CL)

Vagal Afferent Research Group, Centre for Nutrition and Gastrointestinal Disease, Adelaide Medical School, University of Adelaide, Adelaide, South Australia, Australia.
Nutrition, Diabetes and Metabolism, South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia.

Antonio Inserra (A)

Neuropsychiatric Laboratory of Mental Health Disorder, South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia.

George Hatzinikolas (G)

Vagal Afferent Research Group, Centre for Nutrition and Gastrointestinal Disease, Adelaide Medical School, University of Adelaide, Adelaide, South Australia, Australia.
Nutrition, Diabetes and Metabolism, South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia.

Martin D Lewis (MD)

Neuropsychiatric Laboratory of Mental Health Disorder, South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia.
School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia.
College of Medicine and Public Health, Flinders University, Bedford Park, South Australia, Australia.

Stamatiki Kritas (S)

Women's and Children's Hospital, North Adelaide, South Australia, Australia.

Ma-Li Wong (ML)

Neuropsychiatric Laboratory of Mental Health Disorder, South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia.

Amanda J Page (AJ)

Vagal Afferent Research Group, Centre for Nutrition and Gastrointestinal Disease, Adelaide Medical School, University of Adelaide, Adelaide, South Australia, Australia.
Nutrition, Diabetes and Metabolism, South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia.

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