Basic Study
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World J Gastroenterol. Mar 21, 2022; 28(11): 1139-1158
Published online Mar 21, 2022. doi: 10.3748/wjg.v28.i11.1139
Quercetin exerts anti-inflammatory effects via inhibiting tumor necrosis factor-α-induced matrix metalloproteinase-9 expression in normal human gastric epithelial cells
Hsi-Lung Hsieh, Ming-Chin Yu, Li-Ching Cheng, Mei-Yi Chu, Tzu-Hao Huang, Ta-Sen Yeh, Ming-Ming Tsai
Hsi-Lung Hsieh, Li-Ching Cheng, Tzu-Hao Huang, Ming-Ming Tsai, Department of Nursing, Division of Basic Medical Sciences, Chang-Gung University of Science and Technology, Taoyuan 333, Taiwan
Hsi-Lung Hsieh, Mei-Yi Chu, Ming-Ming Tsai, Research Center for Chinese Herbal Medicine, College of Human Ecology, Chang Gung University of Science and Technology, Taoyuan 333, Taiwan
Hsi-Lung Hsieh, Department of Neurology, Chang Gung Memorial Hospital, Taoyuan 333, Taiwan
Ming-Chin Yu, Ming-Ming Tsai, Department of General Surgery, New Taipei Municipal TuCheng Hospital, New Taipei 236, Taiwan
Ming-Chin Yu, Ta-Sen Yeh, College of Medicine, Chang Gung University, Taoyuan 333, Taiwan
Ming-Chin Yu, Li-Ching Cheng, Ta-Sen Yeh, Ming-Ming Tsai, Department of General Surgery, Chang Gung Memorial Hospital, Taoyuan 333, Taiwan
Author contributions: Hsieh HL, Yu MC, and Cheng LC contributed equally to this work; all authors contributed to this paper with conception and design of the study, literature review and analysis, manuscript drafting, critical revision, and editing, and approval of the final version.
Supported by Ministry of Science and Technology, Taiwan, No. MOST 108-2320-B-255-002-MY3 and No. MOST 110-2635-B-255-001; Chang Gung Medical Research Foundation, Taoyuan, Taiwan, No. CMRPF1I0031, No. CMRPF1L0081, No. CMRPF1L0021, No. CMRPF1L0041, and No. CMRPF1I0042; and Chang Gung University of Science and Technology, Taoyuan, Taiwan, No. ZRRPF3K0111 and No. ZRRPF3L0091.
Institutional review board statement: No human specimens were involved in this study.
Conflict-of-interest statement: All authors have nothing to disclose.
Data sharing statement: No additional data are available.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (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: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Ming-Ming Tsai, PhD, Associate Professor, Department of Nursing, Division of Basic Medical Sciences, Chang-Gung University of Science and Technology, No. 261 Wenhua 1st Road, Guishan District, Taoyuan 333, Taiwan. mmtsai@mail.cgust.edu.tw
Received: September 2, 2021
Peer-review started: September 2, 2021
First decision: November 7, 2021
Revised: December 23, 2021
Accepted: February 12, 2022
Article in press: February 12, 2022
Published online: March 21, 2022
Processing time: 195 Days and 17 Hours
ARTICLE HIGHLIGHTS
Research background

Gastric injury involving inflammation is one of the most common diseases of the digestive system worldwide and is associated with gastric ulcers and gastric cancer (GC). Matrix metallopeptidase-9 (MMP-9) plays an important role in the inflammation and progression of GC. Quercetin exhibits anti-inflammatory activities, but its effects and mechanism of action on human chronic gastritis remain unclear.

Research motivation

To assess whether tumor necrosis factor-α (TNF-α)-induced MMP-9 expression is involved in the anti-inflammatory effects of quercetin in normal human gastric mucosa epithelial cell line GES-1.

Research objectives

The objective of this study was to evaluate the anti- inflammatory effects and mechanisms of quercetin in GES-1 cells.

Research methods

A GES-1 cell model was established to evaluate the anti-inflammatory effects of quercetin on TNF-α-induced overexpression of the proinflammatory MMP-9 protein. The cell counting Kit-8 assay was used to examine the effects of quercetin dose on GES-1 cell viability. Cell migration was measured using the Transwell assay. The expression of c-Src, phospho (p)-c-Src, p- extracellular-signal-regulated kinase (ERK) 1/2, ERK2, p-c-Fos, c-Fos, p-p65, and nuclear factor kappa B (NF-κB)/p65 and the effects of their inhibitors were examined using Western blot analysis and the measurement of luciferase activity. p65 expression was detected by immunofluorescence. MMP-9 mRNA and protein expression levels were determined by quantitative reverse transcription polymerase chain reaction (qRT–PCR) and gelatin zymography, respectively.

Research results

qRT–PCR and gelatin zymography showed that TNF-α induced MMP-9 mRNA and protein expression in a dose- and time-dependent manner. These effects were reduced by pretreatment of GES-1 cells with quercetin or TNF-α antagonist in a dose- and time-dependent manner. Quercetin decreased the TNF-α-induced phosphorylation of c-Src, ERK1/2, c-Fos, and p65 in a dose- and time-dependent manner. Quercetin, PP1, U0126, TSIIA, and a TNF-α antagonist reduced TNF-α-induced c-Fos phosphorylation and AP-1–Luc activity in a dose- and time-dependent manner. Pretreatment with quercetin, PP1, U0126, Bay 11-7082, or TNF-α antagonist reduced TNF-α-induced p65 phosphorylation and translocation and p65–Luc activity in a dose- and time-dependent manner. TNF-α significantly increased GES-1 cell migration, and this effect was reduced by pretreatment with quercetin and a TNF-α antagonist.

Research conclusions

Quercetin significantly downregulates TNF-α-induced MMP-9 expression in GES-1 cells via the TNFR-c-Src–ERK1/2–c-Fos and NF-κB pathways.

Research perspectives

We propose that quercetin potentially represents a new approach for reducing reliance on nonsteroidal anti-inflammatory drugs and an effective therapeutic agent for protecting gastric mucosal epithelial cells. Quercetin and quercetin-rich diets may exhibit potential as food supplements for the prevention of early pathological changes associated with gastric inflammation.