Basic Study
Copyright ©The Author(s) 2019. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Jul 21, 2019; 25(27): 3572-3589
Published online Jul 21, 2019. doi: 10.3748/wjg.v25.i27.3572
Mucosal healing progression after acute colitis in mice
Sandra Vidal-Lletjós, Mireille Andriamihaja, Anne Blais, Marta Grauso, Patricia Lepage, Anne-Marie Davila, Claire Gaudichon, Marion Leclerc, François Blachier, Annaïg Lan
Sandra Vidal-Lletjós, Mireille Andriamihaja, Anne Blais, Marta Grauso, Anne-Marie Davila, Claire Gaudichon, François Blachier, Annaïg Lan, UMR PNCA, AgroParisTech, INRA, Université Paris-Saclay, Paris 75005, France
Patricia Lepage, Marion Leclerc, UMR MICALIS, INRA, Université Paris-Saclay, Jouy-en-Josas 78350, France
Author contributions: Vidal-Lletjós S, Andriamihaja M, Blais A, Grauso M, and Lan A performed experiments; Vidal-Lletjós S, Lepage P, Davila AM, and Lan A analyzed the data; Lan A, Leclerc M, and Blachier F conceived and supervised the study; Vidal-Lletjós S and Lan A drafted the manuscript; All authors have read and approved the final manuscript as submitted and are accountable for all aspects of the research.
Supported by grants from the Société Française de Nutrition and the Association François Aupetit. Vidal-Lletjós S was a recipient of a PhD grant from INRA-Université Paris-Saclay (ALIAS program).
Institutional review board statement: The study was reviewed and approved by the AgroParisTech/ INRA Institutional Review Board.
Institutional animal care and use committee statement: All procedures involving animals were reviewed and approved by the local Institutional Animal Care and Use Committee of AgroParisTech/ INRA (Comethea) and received the approval of the ministerial committee for animal experimentation (registration number: APAFIS#3987-2016012214388658), according to the European directive for the use and care of laboratory animals (2010/63/UE).
Conflict-of-interest statement: The authors have nothing to disclose.
ARRIVE guidelines statement: The authors have read the ARRIVE guidelines, and the manuscript was prepared and revised according to the ARRIVE guidelines.
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/
Corresponding author: Annaïg Lan, PhD, Associate Professor, UMR PNCA, AgroParisTech, INRA, Université Paris-Saclay, 16 rue Claude Bernard, Paris 75005, France. annaig.lan@agroparistech.fr
Telephone: +33-1-44087242 Fax: +33-1-44081858
Received: April 9, 2019
Peer-review started: April 10, 2019
First decision: May 9, 2019
Revised: May 27, 2019
Accepted: June 8, 2019
Article in press: June 8, 2019
Published online: July 21, 2019
Processing time: 101 Days and 21.1 Hours
Abstract
BACKGROUND

Mucosal healing has become a therapeutic goal to achieve stable remission in patients with inflammatory bowel diseases. To achieve this objective, overlapping actions of complex cellular processes, such as migration, proliferation, and differentiation, are required. These events are longitudinally and tightly controlled by numerous factors including a wide range of distinct regulatory proteins. However, the sequence of events associated with colon mucosal repair after colitis and the evolution of the luminal content characteristics during this process have been little studied.

AIM

To document the evolution of colon mucosal characteristics during mucosal healing using a mouse model with chemically-induced colitis.

METHODS

C57BL/6 male mice were given 3.5% dextran sodium sulfate (DSS) in drinking water for 5 d. They were euthanized 2 (day 7), 5 (day 10), 8 (day 13), and 23 (day 28) d after DSS removal. The colonic luminal environment and epithelial repair processes during the inflammatory flare and colitis resolution were analyzed with reference to a non-DSS treated control group, euthanized at day 0. Epithelial repair events were assessed histo-morphologically in combination with functional permeability tests, expression of key inflammatory and repairing factors, and evaluation of colon mucosa-adherent microbiota composition by 16S rRNA sequencing.

RESULTS

The maximal intensity of colitis was concomitant with maximal alterations of intestinal barrier function and histological damage associated with goblet cell depletion in colon mucosa. It was recorded 2 d after termination of the DSS-treatment, followed by a progressive return to values similar to those of control mice. Although signs of colitis were severe (inflammatory cell infiltrate, crypt disarray, increased permeability) and associated with colonic luminal alterations (hyperosmolarity, dysbiosis, decrease in short-chain fatty acid content), epithelial healing processes were launched early during the inflammatory flare with increased gene expression of certain key epithelial repair modulators, including transforming growth factor-β, interleukin (Il)-15, Il-22, Il-33, and serum amyloid A. Whereas signs of inflammation progressively diminished, luminal colonic environment alterations and microscopic abnormalities of colon mucosa persisted long after colitis induction.

CONCLUSION

This study shows that colon repair can be initiated in the context of inflamed mucosa associated with alterations of the luminal environment and highlights the longitudinal involvement of key modulators.

Keywords: Colon luminal environment; Dextran sodium sulfate-induced colitis; Dysbiosis; Epithelial repair; Acute colitis

Core tip: When colitis was chemically induced with dextran sodium sulfate, 2 d after the end of the treatment, mice showed unequivocal sign of colitis, changes in the luminal environment of the large intestine, epithelial permeability loss, and dysbiosis. These inflammation-induced alterations progressively and partly resolved in the period of time following colitis induction. Early and long-term evaluation of the epithelial repairing process showed overlapping action of inflammatory and repairing markers, rather than successive actions.