Neurogastroenterol Motil. 2017;e13069. wileyonlinelibrary.com/journal/nmo
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1 of 12
https://doi.org/10.1111/nmo.13069
© 2017 John Wiley & Sons Ltd
Received: 21 November 2016
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Accepted: 21 February 2017
DOI: 10.1111/nmo.13069
ORIGINAL ARTICLE
L. fermentum CECT 5716 prevents stress-induced intestinal
barrier dysfunction in newborn rats
T. Vanhaecke
1,2,3,6
| P. Aubert
1,2,3
| P.-A. Grohard
1,2,3
| T. Durand
1,2,3
| P. Hulin
2,4
|
P. Paul-Gilloteaux
2,4
| A. Fournier
5
| F. Docagne
5
| A. Ligneul
6
| C. Fressange-Mazda
7
|
P. Naveilhan
1,2,3
| H. Boudin
1,2,3
| P. Le Ruyet
6
| M. Neunlist
1,2,3
Abbreviations: CMC, carboxymethylcellulose; EPM, Elevated plus maze; FSA, Fluorescein–5.6
sulfonic acid; GI, Gastrointestinal; HPS, hemalun-phloxine-saffron; HRP, Horse radish perox-
idase; IEB, Intestinal epithelial barrierMS, Maternal separation; NEC, Necrotizing enterocoli-
tis; TJ, Tight junctions; WAS, Water avoidance stress
Philippe Aubert and Pierre-Antoine Grohard contributed equally to the work.
1
INSERM U1235, Nantes, France
2
Université de Nantes, Nantes, France
3
Institut des Maladies de l’Appareil Digestif,
Nantes, France
4
MicroPICell - Cellular and Tissular Imaging
Core Facility of Nantes, SFR Santé F. Bonamy-
FED 4203/Inserm UMS016/CNRS UMS3556,
Nantes, France
5
Normandie Univ, UNICAEN, INSERM,
Physiopathology and Imaging of Neurological
Disorders (PhIND), Centre Cyceron, Caen,
France
6
Lactalis Recherche et Développement,
Retiers, France
7
Lactalis Nutrition Europe, Torcé, France
Correspondence
Michel Neunlist, Inserm U1235; Faculté de
Médecine, Nantes, France.
Email: michel.neunlist@univ-nantes.fr
Funding information
This work was supported by a grant from the
Association Nationale de la Recherche et de
la Technologie (ANRT) and Lactalis Nutrition
Europe (Torcé, France) (n°2013/1189)
Abstract
Background: Intestinal epithelial barrier (IEB) dysfunction plays a critical role in various
intestinal disorders affecting infants and children, including the development of food
allergies and colitis. Recent studies highlighted the role of probiotics in regulating IEB
functions and behavior in adults, but their effects in the newborn remain largely un-
known. We therefore characterized in rat pups, the impact of Lactobacillus fermentum
CECT 5716 (L. fermentum) on stress-induced IEB dysfunction, systemic immune re-
sponse and exploratory behavior.
Methods: Newborn rats received daily by gavage either L. fermentum or water.
Intestinal permeability to fluorescein sulfonic acid (FSA) and horseradish peroxidase
(HRP) was measured following maternal separation (MS) and water avoidance stress
(WAS). Immunohistochemical, transcriptomic, and Western blot analysis of zonula
occludens-1 (ZO-1) distribution and expression were performed. Anxiety-like and
exploratory behavior was assessed using the elevated plus maze test. Cytokine
secretion of activated splenocytes was also evaluated.
Key Results: L. fermentum prevented MS and WAS-induced IEB dysfunction in vivo. L.
fermentum reduced permeability to both FSA and HRP in the small intestine but not in
the colon. L. fermentum increased expression of ZO-1 and prevented WAS-induced
ZO-1 disorganization in ileal epithelial cells. L. fermentum also significantly reduced
stress-induced increase in plasma corticosteronemia. In activated splenocytes, L. fer-
mentum enhanced IFNγ secretion while it prevented IL-4 secretion. Finally, L. fermen-
tum increased exploratory behavior.
Conclusions & Inferences: These results suggest that L. fermentum could provide a
novel tool for the prevention and/or treatment of gastrointestinal disorders associated
with altered IEB functions in the newborn.
KEYWORDS
corticosterone, Intestinal epithelial permeability, newborn, probiotic, ZO-1
1 | INTRODUCTION
The postnatal period is a critical developmental window of the gastro-
intestinal (GI) tract.
1,2
Various GI functions, such as intestinal epithelial