Basic Study
Copyright ©The Author(s) 2024. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Oncol. Oct 15, 2024; 16(10): 4232-4243
Published online Oct 15, 2024. doi: 10.4251/wjgo.v16.i10.4232
Intratumoural microorganism can affect the progression of hepatocellular carcinoma
Bao-Qun Liu, Yi Bai, Da-Peng Chen, Ya-Min Zhang, Tian-Ze Wang, Jing-Rui Chen, Xiang-Yu Liu, Bin Zheng, Zi-Lin Cui
Bao-Qun Liu, Da-Peng Chen, Jing-Rui Chen, First Central Clinical College, Tianjin Medical University, Tianjin 300070, China
Yi Bai, Ya-Min Zhang, Zi-Lin Cui, Department of Hepatobiliary Surgery, Tianjin First Central Hospital, School of Medicine, Nankai University, Tianjin 300192, China
Tian-Ze Wang, Xiang-Yu Liu, Tianjin First Central Hospital Clinic Institute, School of Medicine, Nankai University, Tianjin 300192, China
Bin Zheng, School of Medicine, Tianjin University, Tianjin 300072, China
Co-first authors: Bao-Qun Liu and Yi Bai.
Co-corresponding authors: Bin Zheng and Zi-Lin Cui.
Author contributions: Cui ZL and Zheng B had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis, they serve as co-corresponding authors of this paper; Liu BQ and Bai Y contributed equally to the experimental design, primary literature review, data extraction, data analysis, manuscript drafting and revision as co-first authors of this paper. Cui ZL, Zheng B and Liu BQ designed the research study; Liu BQ, Zheng B and Cui ZL performed the primary literature and data extraction; Liu BQ, Bai Y, Zhang YM, Wang TZ, Chen JR and Liu XY analyzed the data; Liu BQ, Zheng B and Cui ZL wrote the manuscript; Cui ZL, Zheng B, Bai Y and Liu BQ critically revised the manuscript for important intellectual content; and all authors read and approved the final version.
Supported by the Tianjin Health Science and Technology Project Surface Project, No. TJWJ2023MS012.
Institutional animal care and use committee statement: This study was reviewed and approved by Animal Ethics Committee of Tianjin First Central Hospital.
Conflict-of-interest statement: All the Authors have no conflict of interest related to the manuscript.
Data sharing statement: No additional data are available.
ARRIVE guidelines statement: The authors have read the STROBE Statement—checklist of items, and the manuscript was prepared and revised according to the STROBE Statement—checklist of items.
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: Zi-Lin Cui, Doctor, Chief Doctor, Surgeon, Department of Hepatobiliary Surgery, Tianjin First Central Hospital, School of Medicine, Nankai University, No. 24 Fukang Road, Nankai District, Tianjin 300192, China. 13602184643@163.com
Received: June 15, 2024
Revised: July 29, 2024
Accepted: August 12, 2024
Published online: October 15, 2024
Processing time: 102 Days and 21 Hours
Abstract
BACKGROUND

Several recent studies have confirmed that intratumoural microorganisms can affect the occurrence and development of hepatocellular carcinoma (HCC); however, their role in tumor progression remains unclear. Hence, there is a need for further research on the role of intratumoural microorganisms in HCC.

AIM

To investigate the changes in intratumoural microorganisms in HCC and the effect of Propionibacterium on HCC progression.

METHODS

HCC and normal liver tissue specimens were subjected to fluorescence in situ hybridization (FISH). After performing 16S rRNA sequencing on HCC and peritumoral tissues to analyze the differences between the two groups. Propionibacterium was cocultured with HCC cells in vitro. Changes in cell proliferation and migration capacity were evaluated. The expression of NF-κB pathway related proteins in tumor cells was compared. The orthotopic liver implantation model and the subcutaneous xenograft model were constructed. liver tissues and subcutaneous tumors were collected 2 weeks later.

RESULTS

FISH demonstrated the presence of microorganisms in HCC and normal liver tissues. 16S rRNA sequencing revealed an abundance of Lysobacter, Lachnospiraceae, Pseudomonas, and Lactobacillus in HCC tissues. The distribution and abundance of Propionibacterium showed differences between HCC and peritumoral tissues (P < 0.05). In vitro studies demonstrated that Propionibacterium and its metabolite propionic acid (PA) inhibited the proliferation and migration of HCC cells (P < 0.05). The expression of the proteins in NF-κB signaling pathway also decreased in HCC cells (P < 0.05).

CONCLUSION

Microorganisms in HCC and normal liver tissues displayed significant disparities. The PA-producing bacterium Propionibacterium in HCC exerts an effect on the NF-κB pathway, thereby affecting the biological behavior of HCC.

Keywords: Hepatocellular carcinoma; Intratumoural microbiome; 16S rRNA sequencing; Propionibacterium

Core Tip: Significant changes were detected in hepatocellular carcinoma (HCC) microbiomes. Propionibacterium can alter the proliferation and migration of HCC cells, mediate the NF-κB signaling pathway, and impact HCC progression. This study provides useful insights to investigate the microbiome composition of HCC and inhibit its progression.