Basic Study
Copyright ©The Author(s) 2016. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Pharmacol Ther. Nov 6, 2016; 7(4): 540-549
Published online Nov 6, 2016. doi: 10.4292/wjgpt.v7.i4.540
A20 inhibits lipopolysaccharide-induced inflammation in enterocytes
Cui-Fang Zheng, Jie-Ru Shi, Ying Huang, Sheng-Nan Wang
Cui-Fang Zheng, Jie-Ru Shi, Ying Huang, Sheng-Nan Wang, Department of Gastroenterology, Children’s Hospital of Fudan University, Shanghai 201102, China
Author contributions: Zheng CF and Huang Y designed the study; Zheng CF and Wang SN performed the research; Zheng CF and Shi JR analysed the data; Zheng CF, Shi JR and Huang Y wrote the paper.
Supported by The National Natural Science Foundation of China, No. 81300291.
Institutional review board statement: The publication of this manuscript has been reviewed and approved by the Children’s Hospital of Fudan University Review Board.
Conflict-of-interest statement: All authors declare no conflicts of interest.
Data sharing statement: The technical appendix, statistical code, and dataset are available from the corresponding author at yhuang815@163.com. The study participants provided their informed consent for data sharing. 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: Ying Huang, MD, PhD, Department of Gastroenterology, Children’s Hospital of Fudan University, No. 399 Wan-Yuan Road, Minhang District, Shanghai 201102, China. yhuang815@163.com
Telephone: +86-21-64931727 Fax: +86-21-64931901
Received: May 1, 2016
Peer-review started: May 2, 2016
First decision: July 4, 2016
Revised: July 14, 2016
Accepted: August 15, 2016
Article in press: August 17, 2016
Published online: November 6, 2016
Processing time: 182 Days and 17.7 Hours
Abstract
AIM

To examine the role of A20 in the regulation of intestinal epithelial cells (IECs) inflammation.

METHODS

Using gene transfection, both stable overexpression and knockdown A20-expressed HT-29 cell lines were established. Accordingly, the cells were divided into the following groups: The control group, the A20 overexpression group, the A20 knockdown group and the respective controls. A20 was stimulated with lipopolysaccharide (LPS) in a dose- and time-dependent manner and was detected using western blotting and real-time polymerase chain reaction (PCR) analyses. Immunofluorescence and western blotting analyses were performed to investigate the role of A20 in the regulation of nuclear factor (NF)-κB activation and translocation into the nucleus. ELISA and real-time PCR were performed to examine A20 in regulating the release of the following inflammatory cytokines: Tumor necrosis factor (TNF)-α, interleukin (IL)-1β, IL-6 and IL-8.

RESULTS

The expression of A20 in IECs was inducible. When intestinal epithelial cells were subjected to the stimulation of LPS, the expression of A20 was increased, and the expression of A20 was induced in a dose- and time-dependent manner. The expression of A20 was very low in HT-29 cells without LPS stimulation but rapidly increased and was maintained at a high level 2-4 h after stimulation with LPS. These levels gradually declined with a change in time-course, and the expression of A20 increased with increasing LPS stimulation. Western blotting and immunofluorescence revealed that overexpression of A20 can inhibit NF-κB activation and its translocation to the nucleus. The overexpression of A20 can reduce the levels of proinflammatory cytokines involved in the pathophysiology of inflammatory bowel disease. There was no significant difference in the expression of IL-8 mRNA in the control group, A20 overexpression group or A20 knockdown group without LPS stimulation (P > 0.05); however, while after 2 h, 4 h and 8 h stimulation with LPS, the expression of IL-8 in the A20 overexpression group was lower than the control group and the A20 knockdown group (P < 0.05 or P < 0.01). The expression of TNF-α was different at different time points after 8 h of LPS stimulation (F = 31.33, DF = 5, P < 0.001), and the expression of TNF-α increased as the LPS stimulation time increased. Upon LPS stimulation, lower levels of TNF-α were detected in the A20 overexpression cell lines (P < 0.05). There were no significant differences in the induction of IL-6 and IL-1β among the control group, A20 overexpression group and A20 knockdown group (P > 0.05).

CONCLUSION

A20 plays an important role in limiting inflammation by inhibiting LPS-induced NF-κB responses in the gut luminal. A20 may be a potential therapeutic tool for inflammatory diseases.

Keywords: A20 (TNFAIP3); Lipopolysaccharide; Nuclear factor-κB; Inflammatory bowel disease

Core tip: The use of A20-deficient mice and RNA interference technologies has revealed that mice or enterocytes lacking A20 showed hyper-responsiveness to stimulation. However, studies on whether the overexpression of A20 can extenuate enterocyte inflammation are limited. Our present results demonstrated that the expression of A20 was increased in a dose- and time-dependent manner upon lipopolysaccharide (LPS) stimulation in intestinal epithelial cells. More importantly, the overexpression of A20 suppressed the activation of nuclear factor-κB and the induction of pro-inflammatory molecules, such as Tumor necrosis factor-α and IL-8. Taken together, these findings indicate that A20 plays a critical role in limiting LPS-induced inflammation in the gut luminal and may be a potential therapeutic tool for immune and inflammatory diseases.