Exploring the Relationship between the Gut Mucosal Virome and Colorectal Cancer: Characteristics and Correlations

The fecal virome has been reported to be associated with CRC. However, little is known about the mucosal virome signature in CRC. This study aimed to determine the viral community within CRC tissues and their contributions to colorectal carcinogenesis. Colonic mucosal biopsies were harvested from pa...

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Main Authors: Gangping Li, Yu Jin, Baolong Chen, Aiqiang Lin, Erchuan Wang, Fenghua Xu, Gengcheng Hu, Chuanxing Xiao, Hongli Liu, Xiaohua Hou, Bangzhou Zhang, Jun Song
Format: Article
Language:English
Published: MDPI AG 2023-07-01
Series:Cancers
Subjects:
Online Access:https://www.mdpi.com/2072-6694/15/14/3555
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author Gangping Li
Yu Jin
Baolong Chen
Aiqiang Lin
Erchuan Wang
Fenghua Xu
Gengcheng Hu
Chuanxing Xiao
Hongli Liu
Xiaohua Hou
Bangzhou Zhang
Jun Song
author_facet Gangping Li
Yu Jin
Baolong Chen
Aiqiang Lin
Erchuan Wang
Fenghua Xu
Gengcheng Hu
Chuanxing Xiao
Hongli Liu
Xiaohua Hou
Bangzhou Zhang
Jun Song
author_sort Gangping Li
collection DOAJ
description The fecal virome has been reported to be associated with CRC. However, little is known about the mucosal virome signature in CRC. This study aimed to determine the viral community within CRC tissues and their contributions to colorectal carcinogenesis. Colonic mucosal biopsies were harvested from patients with CRC (biopsies of both neoplasia and adjacent normal tissue (CRC-A)) and healthy controls (HC). The shot-gun metagenomic sequencing of virus-like particles (VLPs) was performed on the biopsies. Viral community, functional pathways, and their correlations to clinical data were analyzed. Fluorescence in situ hybridizations (FISH) for the localization of viruses in the intestine was performed, as well as quantitative PCR for the detection of Torque teno virus load in human mucosal VLP DNA. A greater number and proportion of core species were found in CRC tissues than in CRC-A and HC tissues. The diversity of the mucosal virome in CRC tissues was significantly increased compared to that in HC and CRC-A tissues. The mucosal virome signature of CRC tissues were significantly different from those of HC and CRC-A tissues at the species level. The abundances of eukaryotic viruses from the Anelloviridae family and its sub-species Torque teno virus (TTV) were significantly higher in CRC patients than in HC. Furthermore, increased levels of TTV in the intestinal lamina propria were found in the CRC group. Multiple viral functions of TTV associated with carcinogenesis were enriched in CRC tissues. We revealed for the first time that the mucosal virobiota signature of CRC is characterized by a higher diversity and more eukaryotic viruses. The enrichment of TTV species in CRC tissues suggests that they may play an oncogenic role in CRC. Targeting eukaryotic viruses in the gut may provide novel strategies for the prevention and treatment of CRC.
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spelling doaj.art-ba91fadf144642dcb076d8f5de2d2a852023-11-18T18:40:43ZengMDPI AGCancers2072-66942023-07-011514355510.3390/cancers15143555Exploring the Relationship between the Gut Mucosal Virome and Colorectal Cancer: Characteristics and CorrelationsGangping Li0Yu Jin1Baolong Chen2Aiqiang Lin3Erchuan Wang4Fenghua Xu5Gengcheng Hu6Chuanxing Xiao7Hongli Liu8Xiaohua Hou9Bangzhou Zhang10Jun Song11Division of Gastroenterology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, ChinaDivision of Gastroenterology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, ChinaXiamen Treatgut Biotechnology Co., Ltd., Xiamen 361115, ChinaXiamen Treatgut Biotechnology Co., Ltd., Xiamen 361115, ChinaDivision of Gastroenterology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, ChinaDivision of Gastroenterology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, ChinaDivision of Gastroenterology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, ChinaXiamen Treatgut Biotechnology Co., Ltd., Xiamen 361115, ChinaCancer Center, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, ChinaDivision of Gastroenterology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, ChinaInstitute for Microbial Ecology, School of Medicine, Xiamen University, Xiamen 361102, ChinaDivision of Gastroenterology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, ChinaThe fecal virome has been reported to be associated with CRC. However, little is known about the mucosal virome signature in CRC. This study aimed to determine the viral community within CRC tissues and their contributions to colorectal carcinogenesis. Colonic mucosal biopsies were harvested from patients with CRC (biopsies of both neoplasia and adjacent normal tissue (CRC-A)) and healthy controls (HC). The shot-gun metagenomic sequencing of virus-like particles (VLPs) was performed on the biopsies. Viral community, functional pathways, and their correlations to clinical data were analyzed. Fluorescence in situ hybridizations (FISH) for the localization of viruses in the intestine was performed, as well as quantitative PCR for the detection of Torque teno virus load in human mucosal VLP DNA. A greater number and proportion of core species were found in CRC tissues than in CRC-A and HC tissues. The diversity of the mucosal virome in CRC tissues was significantly increased compared to that in HC and CRC-A tissues. The mucosal virome signature of CRC tissues were significantly different from those of HC and CRC-A tissues at the species level. The abundances of eukaryotic viruses from the Anelloviridae family and its sub-species Torque teno virus (TTV) were significantly higher in CRC patients than in HC. Furthermore, increased levels of TTV in the intestinal lamina propria were found in the CRC group. Multiple viral functions of TTV associated with carcinogenesis were enriched in CRC tissues. We revealed for the first time that the mucosal virobiota signature of CRC is characterized by a higher diversity and more eukaryotic viruses. The enrichment of TTV species in CRC tissues suggests that they may play an oncogenic role in CRC. Targeting eukaryotic viruses in the gut may provide novel strategies for the prevention and treatment of CRC.https://www.mdpi.com/2072-6694/15/14/3555gut mucosal viromecolorectal cancereukaryotic viruses<i>Anelloviridae</i><i>Torque teno virus</i>
spellingShingle Gangping Li
Yu Jin
Baolong Chen
Aiqiang Lin
Erchuan Wang
Fenghua Xu
Gengcheng Hu
Chuanxing Xiao
Hongli Liu
Xiaohua Hou
Bangzhou Zhang
Jun Song
Exploring the Relationship between the Gut Mucosal Virome and Colorectal Cancer: Characteristics and Correlations
Cancers
gut mucosal virome
colorectal cancer
eukaryotic viruses
<i>Anelloviridae</i>
<i>Torque teno virus</i>
title Exploring the Relationship between the Gut Mucosal Virome and Colorectal Cancer: Characteristics and Correlations
title_full Exploring the Relationship between the Gut Mucosal Virome and Colorectal Cancer: Characteristics and Correlations
title_fullStr Exploring the Relationship between the Gut Mucosal Virome and Colorectal Cancer: Characteristics and Correlations
title_full_unstemmed Exploring the Relationship between the Gut Mucosal Virome and Colorectal Cancer: Characteristics and Correlations
title_short Exploring the Relationship between the Gut Mucosal Virome and Colorectal Cancer: Characteristics and Correlations
title_sort exploring the relationship between the gut mucosal virome and colorectal cancer characteristics and correlations
topic gut mucosal virome
colorectal cancer
eukaryotic viruses
<i>Anelloviridae</i>
<i>Torque teno virus</i>
url https://www.mdpi.com/2072-6694/15/14/3555
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