Dysbiosis of Gut Microbiota Is Associated With the Progression of Radiation-Induced Intestinal Injury and Is Alleviated by Oral Compound Probiotics in Mouse Model

The acute radiation-induced intestinal injury (RIII) has raised much concerns and is influenced by non-cytocidal radiation effects including the perturbations in gut microbiota. Although a number of studies have reported alteration in gut microbiota following radiation, little is known about its dyn...

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Main Authors: Tian-Shu Zhao, Li-Wei Xie, Shang Cai, Jia-Yu Xu, Hao Zhou, Lin-Feng Tang, Chao Yang, Shuguang Fang, Ming Li, Ye Tian
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-10-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2021.717636/full
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author Tian-Shu Zhao
Tian-Shu Zhao
Li-Wei Xie
Li-Wei Xie
Shang Cai
Shang Cai
Jia-Yu Xu
Jia-Yu Xu
Hao Zhou
Lin-Feng Tang
Chao Yang
Shuguang Fang
Ming Li
Ye Tian
Ye Tian
author_facet Tian-Shu Zhao
Tian-Shu Zhao
Li-Wei Xie
Li-Wei Xie
Shang Cai
Shang Cai
Jia-Yu Xu
Jia-Yu Xu
Hao Zhou
Lin-Feng Tang
Chao Yang
Shuguang Fang
Ming Li
Ye Tian
Ye Tian
author_sort Tian-Shu Zhao
collection DOAJ
description The acute radiation-induced intestinal injury (RIII) has raised much concerns and is influenced by non-cytocidal radiation effects including the perturbations in gut microbiota. Although a number of studies have reported alteration in gut microbiota following radiation, little is known about its dynamic variation in the progression of acute RIII. In this study, mouse model were treated with total body irradiation (TBI) of 0, 4, 8 and 12 Gy, and the intestinal tissues and fecal samples were collected at 6 h, 3.5 d and 7 d post radiation. We found that the intestinal injuries were manifested in a radiation dose-dependent manner. Results from 16S rRNA gene sequencing demonstrated that the diversity of gut microbiota was not significantly affected at the prodromal stage of acute RIII, after 6 h of radiation. At the critical stage of acute RIII, after 3.5 d of radiation, the composition of gut microbiota was correlated with the radiation dose. The Pearson’s correlation analysis showed that the relative abundances of phylum Proteobacteria, genera Escherichia-Shigella and Eubacterium xylanophilum_group, and species Lactobacillus murinus exhibited linear correlations with radiation dose. At the recovery stage of acute RIII, after 7 d of radiation, the diversity of gut microbiota decreased as a whole, among which the relative abundance of phyla Proteobacteria and Bacteroides increased, while that of phylum Tenericutes and genus Roseburia decreased. The intra-gastric administration of compound probiotics for 14 days improved the survival duration of mice exposed to 9 Gy TBI, alleviated the intestinal epithelial injury and partially restored the diversity of gut microbiota. Our findings suggest that acute RIII is accompanied by the dysbiosis of gut microbiota, including its decreased diversity, reduced abundance of beneficial bacteria and increased abundance of pathogens. The gut microbiota cannot be used as sensitive biomarkers at the prodromal stage in acute RIII, but are potential biomarkers at the critical stage of acute RIII. The dysbiosis is persistent until the recovery stage of acute RIII, and interventions are needed to restore it. The administration of probiotics is an effective strategy to protect against acute RIII and subsequent dysbiosis.
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spelling doaj.art-2d192d67216c4a5d8ab1ccab98c1d6892022-12-21T19:15:19ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882021-10-011110.3389/fcimb.2021.717636717636Dysbiosis of Gut Microbiota Is Associated With the Progression of Radiation-Induced Intestinal Injury and Is Alleviated by Oral Compound Probiotics in Mouse ModelTian-Shu Zhao0Tian-Shu Zhao1Li-Wei Xie2Li-Wei Xie3Shang Cai4Shang Cai5Jia-Yu Xu6Jia-Yu Xu7Hao Zhou8Lin-Feng Tang9Chao Yang10Shuguang Fang11Ming Li12Ye Tian13Ye Tian14Department of Radiotherapy and Oncology, The Second Affiliated Hospital of Soochow University, Suzhou, ChinaInstitute of Radiotherapy and Oncology, Soochow University, Suzhou, ChinaDepartment of Radiotherapy and Oncology, The Second Affiliated Hospital of Soochow University, Suzhou, ChinaInstitute of Radiotherapy and Oncology, Soochow University, Suzhou, ChinaDepartment of Radiotherapy and Oncology, The Second Affiliated Hospital of Soochow University, Suzhou, ChinaInstitute of Radiotherapy and Oncology, Soochow University, Suzhou, ChinaDepartment of Radiotherapy and Oncology, The Second Affiliated Hospital of Soochow University, Suzhou, ChinaInstitute of Radiotherapy and Oncology, Soochow University, Suzhou, ChinaState Key Laboratory of Radiation Medicine and Protection, School of Radiation Medicine and Protection, Medical College of Soochow University; Collaborative Innovation Center of Radiation Medicine of Jiangsu Higher Education Institutions, Soochow University, Suzhou, ChinaState Key Laboratory of Radiation Medicine and Protection, School of Radiation Medicine and Protection, Medical College of Soochow University; Collaborative Innovation Center of Radiation Medicine of Jiangsu Higher Education Institutions, Soochow University, Suzhou, ChinaDepartment of Nucleus Radiation-Related Injury Treatment, PLA Rocket Force Characteristic Medical Center, Beijing, ChinaWecare Probiotics (Suzhou) Co., Ltd, Suzhou, ChinaState Key Laboratory of Radiation Medicine and Protection, School of Radiation Medicine and Protection, Medical College of Soochow University; Collaborative Innovation Center of Radiation Medicine of Jiangsu Higher Education Institutions, Soochow University, Suzhou, ChinaDepartment of Radiotherapy and Oncology, The Second Affiliated Hospital of Soochow University, Suzhou, ChinaInstitute of Radiotherapy and Oncology, Soochow University, Suzhou, ChinaThe acute radiation-induced intestinal injury (RIII) has raised much concerns and is influenced by non-cytocidal radiation effects including the perturbations in gut microbiota. Although a number of studies have reported alteration in gut microbiota following radiation, little is known about its dynamic variation in the progression of acute RIII. In this study, mouse model were treated with total body irradiation (TBI) of 0, 4, 8 and 12 Gy, and the intestinal tissues and fecal samples were collected at 6 h, 3.5 d and 7 d post radiation. We found that the intestinal injuries were manifested in a radiation dose-dependent manner. Results from 16S rRNA gene sequencing demonstrated that the diversity of gut microbiota was not significantly affected at the prodromal stage of acute RIII, after 6 h of radiation. At the critical stage of acute RIII, after 3.5 d of radiation, the composition of gut microbiota was correlated with the radiation dose. The Pearson’s correlation analysis showed that the relative abundances of phylum Proteobacteria, genera Escherichia-Shigella and Eubacterium xylanophilum_group, and species Lactobacillus murinus exhibited linear correlations with radiation dose. At the recovery stage of acute RIII, after 7 d of radiation, the diversity of gut microbiota decreased as a whole, among which the relative abundance of phyla Proteobacteria and Bacteroides increased, while that of phylum Tenericutes and genus Roseburia decreased. The intra-gastric administration of compound probiotics for 14 days improved the survival duration of mice exposed to 9 Gy TBI, alleviated the intestinal epithelial injury and partially restored the diversity of gut microbiota. Our findings suggest that acute RIII is accompanied by the dysbiosis of gut microbiota, including its decreased diversity, reduced abundance of beneficial bacteria and increased abundance of pathogens. The gut microbiota cannot be used as sensitive biomarkers at the prodromal stage in acute RIII, but are potential biomarkers at the critical stage of acute RIII. The dysbiosis is persistent until the recovery stage of acute RIII, and interventions are needed to restore it. The administration of probiotics is an effective strategy to protect against acute RIII and subsequent dysbiosis.https://www.frontiersin.org/articles/10.3389/fcimb.2021.717636/fullionizing radiationintestinal injurydysbiosisbiomarkerprobiotics
spellingShingle Tian-Shu Zhao
Tian-Shu Zhao
Li-Wei Xie
Li-Wei Xie
Shang Cai
Shang Cai
Jia-Yu Xu
Jia-Yu Xu
Hao Zhou
Lin-Feng Tang
Chao Yang
Shuguang Fang
Ming Li
Ye Tian
Ye Tian
Dysbiosis of Gut Microbiota Is Associated With the Progression of Radiation-Induced Intestinal Injury and Is Alleviated by Oral Compound Probiotics in Mouse Model
Frontiers in Cellular and Infection Microbiology
ionizing radiation
intestinal injury
dysbiosis
biomarker
probiotics
title Dysbiosis of Gut Microbiota Is Associated With the Progression of Radiation-Induced Intestinal Injury and Is Alleviated by Oral Compound Probiotics in Mouse Model
title_full Dysbiosis of Gut Microbiota Is Associated With the Progression of Radiation-Induced Intestinal Injury and Is Alleviated by Oral Compound Probiotics in Mouse Model
title_fullStr Dysbiosis of Gut Microbiota Is Associated With the Progression of Radiation-Induced Intestinal Injury and Is Alleviated by Oral Compound Probiotics in Mouse Model
title_full_unstemmed Dysbiosis of Gut Microbiota Is Associated With the Progression of Radiation-Induced Intestinal Injury and Is Alleviated by Oral Compound Probiotics in Mouse Model
title_short Dysbiosis of Gut Microbiota Is Associated With the Progression of Radiation-Induced Intestinal Injury and Is Alleviated by Oral Compound Probiotics in Mouse Model
title_sort dysbiosis of gut microbiota is associated with the progression of radiation induced intestinal injury and is alleviated by oral compound probiotics in mouse model
topic ionizing radiation
intestinal injury
dysbiosis
biomarker
probiotics
url https://www.frontiersin.org/articles/10.3389/fcimb.2021.717636/full
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