Basic Study
Copyright ©The Author(s) 2022. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Oncol. Oct 15, 2022; 14(10): 1968-1980
Published online Oct 15, 2022. doi: 10.4251/wjgo.v14.i10.1968
Interleukin-34 promotes the proliferation and epithelial-mesenchymal transition of gastric cancer cells
Chuan-Hong Li, Zhang-Ming Chen, Pei-Feng Chen, Lei Meng, Wan-Nian Sui, Song-Cheng Ying, A-Man Xu, Wen-Xiu Han
Chuan-Hong Li, Zhang-Ming Chen, Pei-Feng Chen, Lei Meng, Wan-Nian Sui, A-Man Xu, Wen-Xiu Han, Department of General Surgery, The First Affiliated Hospital of Anhui Medical University, Hefei 230022, Anhui Province, China
Song-Cheng Ying, Department of Immunology, College of Basic Medicine, Anhui Medical University, Hefei 230022, Anhui Province, China
Author contributions: Li CH, Chen ZM, and Chen PF collected the data and wrote the manuscript; Sui WN participated in data analysis; Ying SC participated in discussion and language editing; Xu AM provided funding support; Han WX reviewed the manuscript and provided funding support; All authors contributed to the article and approved the submitted version.
Supported by the Natural Science Project of Anhui Province, No. KJ2021ZD0022; and the Key Research and Development Program of Anhui Province, No. 202104J07020029.
Institutional review board statement: The study was reviewed and approved by the Institutional Review Board of The First Affiliated Hospital of Anhui Medical University (Quick PJ 2019-09-01).
Institutional animal care and use committee statement: All procedures involving animals were reviewed and approved by the Institutional Animal Care and Use Committee of the Anhui Medical University (SC20200513).
Informed consent statement: All study participants, or their legal guardian, provided informed written consent prior to study enrollment.
Conflict-of-interest statement: There is no conflict of interest in this study.
Data sharing statement: Technical appendix, statistical code, and dataset available from the corresponding author at email address hwxhbh@126.com. Participants gave informed consent for data sharing.
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 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: Wen-Xiu Han, MD, PhD, Professor, Department of General Surgery, The First Affiliated Hospital of Anhui Medical University, No. 218 Jixi Avenue, Shushan District, Hefei 230022, Anhui Province, China. hwxhbh@126.com
Received: May 30, 2022
Peer-review started: May 30, 2022
First decision: June 21, 2022
Revised: July 4, 2022
Accepted: August 21, 2022
Article in press: August 21, 2022
Published online: October 15, 2022
Processing time: 136 Days and 22 Hours
Abstract
BACKGROUND

Interleukin (IL)-34 is a pro-inflammatory cytokine involved in tumor development. The role of IL-34 in the proliferation and epithelial-mesenchymal transition (EMT) of gastric cancer (GC) remains to be investigated.

AIM

To investigate whether and how IL-34 affects the proliferation of GC cells and EMT.

METHODS

Using immunohistochemical staining, the expression of IL-34 protein was detected in 60 paired GC and normal paracancerous tissues and the relationship between IL-34 and clinicopathological factors was analyzed. The expression of IL-34 mRNA and protein in normal gastric epithelial cell lines and GC was detected using quantitative real-time polymerase chain reaction (qRT-PCR) and western blotting, respectively. Stable IL-34 knockdown and overexpression in AGS cell lines were established by lentiviral infection and validated by qRT-PCR and western blotting. The cholecystokinin-8 assay, clone formation assay, cell scratch assay, and transwell system were used to detect GC cell proliferation, clone formation, migration, and invasion capacity, respectively. The effects of IL-34 on the growth of GC transplant tumors were assessed using a subcutaneous transplant tumor assay in nude mice. The effects of IL-34 on the expression level of EMT-associated proteins in AGS cells were examined by western blotting.

RESULTS

Expression of IL-34 protein and mRNA was higher in GC cell lines than in GES-1 cells. Compared to matched normal paraneoplastic tissues, the expression of IL-34 protein was higher in 60 GC tissues, which was correlated with tumor size, T-stage, N-stage, tumor, node and metastasis stage, and degree of differentiation. Knockdown of IL-34 expression inhibited the proliferation, clone formation, migration, and invasion of AGS cells, while overexpression of IL-34 promoted cell proliferation, clone formation, migration, and invasion. Furthermore, the reduction of IL-34 promoted the expression of E-cadherin in AGS cells but inhibited the expression of vimentin and N-cadherin. Overexpression of IL-34 inhibited E-cadherin expression but promoted expression of vimentin and N-cadherin in AGS cells. Overexpression of IL-34 promoted the growth of subcutaneous transplanted tumors in nude mice.

CONCLUSION

IL-34 expression is increased in GC tissues and cell lines compared to normal gastric tissues or cell lines. In GC cells, IL-34 promoted proliferation, clone formation, migration, and invasion by regulating EMT-related protein expression cells. Interference with IL-34 may represent a novel strategy for diagnosis and targeted therapy of GC.

Keywords: Gastric cancer; Interleukin-34; Proliferation; Epithelial-mesenchymal transition; Metastasis

Core Tip: Our study provides novel evidence that interleukin (IL)-34 contribute the growth and metastasis of gastric cancer (GC). IL-34 is up-regulated in GC cell lines and tissues, which is correlated with tumor size, grade of differentiation and tumor, node and metastasis stage. IL-34 enhances the ability of proliferation, clone formation, migration and invasion of GC cells and regulates the expression levels of epithelial-mesenchymal transition-associated proteins, suggesting that IL-34 may be an effective target for the therapy of GC.