Investigation of Campylobacter concisus gastric epithelial pathogenicity using AGS cells

Christopher Yau Man Luk; Seul A Lee; Nicholas Naidovski; Fang Liu; Alfred Chin Yen Tay; Liang Wang; Stephen Riordan; Li Zhang

doi:10.3389/fmicb.2023.1289549

Investigation of Campylobacter concisus gastric epithelial pathogenicity using AGS cells

Front Microbiol. 2024 Jan 11:14:1289549. doi: 10.3389/fmicb.2023.1289549. eCollection 2023.

Authors

Christopher Yau Man Luk¹, Seul A Lee¹, Nicholas Naidovski¹, Fang Liu¹, Alfred Chin Yen Tay², Liang Wang^{3

4

5}, Stephen Riordan⁶, Li Zhang¹

Affiliations

¹ School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia.
² Helicobacter Research Laboratory, School of Pathology and Laboratory Medicine, Marshall Centre for Infectious Diseases Research and Training, University of Western Australia, Perth, WA, Australia.
³ Laboratory Medicine, Guangdong Provincial People's Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong, China.
⁴ The Center for Precision Health, School of Medical and Health Sciences, Edith Cowan University, Perth, WA, Australia.
⁵ Department of Medical Informatics, School of Medical Informatics and Engineering, Xuzhou Medical University, Xuzhou, Jiangsu, China.
⁶ Gastrointestinal and Liver Unit, Prince of Wales Hospital, University of New South Wales, Sydney, NSW, Australia.

Abstract

Campylobacter concisus is an oral bacterium. Recent studies suggest that C. concisus may be involved in human gastric diseases. The mechanisms, however, by which C. concisus causes human gastric diseases have not been investigated. Here we examined the gastric epithelial pathogenicity of C. concisus using a cell culture model. Six C. concisus strains and the human gastric epithelial cell line AGS cells were used. IL-8 produced by AGS cells after incubation with C. concisus was measured using enzyme-linked immunosorbent assay (ELISA), and AGS cell apoptosis was determined by caspase 3/7 activities. The effects of C. concisus on actin arrangement in AGS cells was determined using fluorescence staining. The effects of C. concisus on global gene expression in AGS cells was determined by transcriptomic analysis and quantitative real-time PCR (qRT-PCR). The role of the upregulated CYP1A1 gene in gastric cancer survival was assessed using the Kaplan-Meier method. C. concisus induced production of IL-8 by AGS cells with strain variation. Significantly increased caspase 3/7 activities were observed in AGS cells incubated with C. concisus strains when compared to AGS cells without bacteria. C. concisus induced actin re-arrangement in AGS cells. C. concisus upregulated 30 genes in AGS cells and the upregulation of CYP1A1 gene was confirmed by qRT-PCR. The Kaplan-Meier analysis showed that upregulation of CYP1A1 gene is associated with worse survival in gastric cancer patients. Our findings suggest that C. concisus may play a role in gastric inflammation and the progression of gastric cancer. Further investigation in clinical studies is warranted.

Keywords: CYP1A1; Campylobacter; Campylobacter concisus; gastritis; oral Campylobacter.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This project was supported by the Xuzhou Medical University Open Research Grant (XYKF202102) and the Faculty Research Grant (Grant no. PS46772) of the University of New South Wales awarded to Associate Professor LZ.