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Exploring the alterations and function of skin microbiome mediated by ionizing radiation injury

BACKGROUND: Radiation-induced skin injury (RISI) is still the most common and severe side effect of radiotherapy. The role of the skin’s microbial barrier in the pathogenesis and progression of RISI needs to be fully investigated. METHODS: This study aimed to explore the alterations in and functions...

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Autores principales: Huang, Biao, An, Lu, Su, Wenxing, Yan, Tao, Zhang, Haifang, Yu, Dao-Jiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9702067/
https://www.ncbi.nlm.nih.gov/pubmed/36452293
http://dx.doi.org/10.3389/fcimb.2022.1029592
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author Huang, Biao
An, Lu
Su, Wenxing
Yan, Tao
Zhang, Haifang
Yu, Dao-Jiang
author_facet Huang, Biao
An, Lu
Su, Wenxing
Yan, Tao
Zhang, Haifang
Yu, Dao-Jiang
author_sort Huang, Biao
collection PubMed
description BACKGROUND: Radiation-induced skin injury (RISI) is still the most common and severe side effect of radiotherapy. The role of the skin’s microbial barrier in the pathogenesis and progression of RISI needs to be fully investigated. METHODS: This study aimed to explore the alterations in and functions of the skin microbiota in RISI. We applied the unculturable approach to characterize the cutaneous microbiomes of a radiation-induced animal model by sequencing the V1–V3 regions of the 16S ribosomal RNA (rRNA) gene. Combined with the downloaded clinical data of patients, a comprehensive analysis was performed to identify potential radioprotective species and metabolic pathways. RESULTS: There were no significant differences in the alpha diversity indices (Sobs, Shannon, Simpson, Ace, and Chao) between the acute radiation injury and control groups. Phylum-level analysis of the RISI microbiomes exhibited significant predominance of Firmicutes (mean abundance = 67%, corrected p = 0.0035). The high abundance of Firmicutes was significantly associated with rapid healing of RISI (average relative abundance = 52%; Kruskal–Wallis: p = 5.7E−4). Among its members, Streptococcus, Staphylococcus, Acetivibrio ethanolgignens group, Peptostreptococcus, Anaerofilum, and UCG-002 [linear discriminant analysis (LDA) > 3, p < 0.05] were identified as the core genera of Firmicutes. In addition, Lachnosiraceae and Lactobacillus occupied an important position in the interaction network (r > 0.6, p < 0.05). The differential metabolic pathways of RISI were mainly associated with carbohydrate metabolism (butanoate and propanoate metabolism), amino acid metabolism (tryptophan and histidine metabolism), energy metabolism, and lipid metabolism (fatty acid degradation and biosynthesis). CONCLUSION: This study provides new insights into the potential mechanism and skin microbial changes in the progression of RISI. The overwhelming predominance of members of Firmicutes, including Streptococcaceae, Staphylococcaceae, Lachnospiraceae, and Lactobacillus, is potentially related to rapid healing of RISI. The microbiota–metabolite axis plays a critical role in RISI and provides promising therapeutic targets for the treatment of adverse side effects.
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spelling pubmed-97020672022-11-29 Exploring the alterations and function of skin microbiome mediated by ionizing radiation injury Huang, Biao An, Lu Su, Wenxing Yan, Tao Zhang, Haifang Yu, Dao-Jiang Front Cell Infect Microbiol Cellular and Infection Microbiology BACKGROUND: Radiation-induced skin injury (RISI) is still the most common and severe side effect of radiotherapy. The role of the skin’s microbial barrier in the pathogenesis and progression of RISI needs to be fully investigated. METHODS: This study aimed to explore the alterations in and functions of the skin microbiota in RISI. We applied the unculturable approach to characterize the cutaneous microbiomes of a radiation-induced animal model by sequencing the V1–V3 regions of the 16S ribosomal RNA (rRNA) gene. Combined with the downloaded clinical data of patients, a comprehensive analysis was performed to identify potential radioprotective species and metabolic pathways. RESULTS: There were no significant differences in the alpha diversity indices (Sobs, Shannon, Simpson, Ace, and Chao) between the acute radiation injury and control groups. Phylum-level analysis of the RISI microbiomes exhibited significant predominance of Firmicutes (mean abundance = 67%, corrected p = 0.0035). The high abundance of Firmicutes was significantly associated with rapid healing of RISI (average relative abundance = 52%; Kruskal–Wallis: p = 5.7E−4). Among its members, Streptococcus, Staphylococcus, Acetivibrio ethanolgignens group, Peptostreptococcus, Anaerofilum, and UCG-002 [linear discriminant analysis (LDA) > 3, p < 0.05] were identified as the core genera of Firmicutes. In addition, Lachnosiraceae and Lactobacillus occupied an important position in the interaction network (r > 0.6, p < 0.05). The differential metabolic pathways of RISI were mainly associated with carbohydrate metabolism (butanoate and propanoate metabolism), amino acid metabolism (tryptophan and histidine metabolism), energy metabolism, and lipid metabolism (fatty acid degradation and biosynthesis). CONCLUSION: This study provides new insights into the potential mechanism and skin microbial changes in the progression of RISI. The overwhelming predominance of members of Firmicutes, including Streptococcaceae, Staphylococcaceae, Lachnospiraceae, and Lactobacillus, is potentially related to rapid healing of RISI. The microbiota–metabolite axis plays a critical role in RISI and provides promising therapeutic targets for the treatment of adverse side effects. Frontiers Media S.A. 2022-11-14 /pmc/articles/PMC9702067/ /pubmed/36452293 http://dx.doi.org/10.3389/fcimb.2022.1029592 Text en Copyright © 2022 Huang, An, Su, Yan, Zhang and Yu https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular and Infection Microbiology
Huang, Biao
An, Lu
Su, Wenxing
Yan, Tao
Zhang, Haifang
Yu, Dao-Jiang
Exploring the alterations and function of skin microbiome mediated by ionizing radiation injury
title Exploring the alterations and function of skin microbiome mediated by ionizing radiation injury
title_full Exploring the alterations and function of skin microbiome mediated by ionizing radiation injury
title_fullStr Exploring the alterations and function of skin microbiome mediated by ionizing radiation injury
title_full_unstemmed Exploring the alterations and function of skin microbiome mediated by ionizing radiation injury
title_short Exploring the alterations and function of skin microbiome mediated by ionizing radiation injury
title_sort exploring the alterations and function of skin microbiome mediated by ionizing radiation injury
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9702067/
https://www.ncbi.nlm.nih.gov/pubmed/36452293
http://dx.doi.org/10.3389/fcimb.2022.1029592
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