Disordered development of gut microbiome interferes with the establishment of the gut ecosystem during early childhood with atopic dermatitis

The gut microbiome influences the development of allergic diseases during early childhood. However, there is a lack of comprehensive understanding of microbiome-host crosstalk. Here, we analyzed the influence of gut microbiome dynamics in early childhood on atopic dermatitis (AD) and the potential i...

Full description

Saved in:
Bibliographic Details
Main Authors: Min-Jung Lee, Yoon Mee Park, Byunghyun Kim, in Hwan Tae, Nam-Eun Kim, Marina Pranata, Taewon Kim, Sungho Won, Nam Joo Kang, Yun Kyung Lee, Dong-Woo Lee, Myung Hee Nam, Soo-Jong Hong, Bong-Soo Kim
Format: Article
Language:English
Published: Taylor & Francis Group 2022-12-01
Series:Gut Microbes
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2022.2068366
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849687638579085312
author Min-Jung Lee
Yoon Mee Park
Byunghyun Kim
in Hwan Tae
Nam-Eun Kim
Marina Pranata
Taewon Kim
Sungho Won
Nam Joo Kang
Yun Kyung Lee
Dong-Woo Lee
Myung Hee Nam
Soo-Jong Hong
Bong-Soo Kim
author_facet Min-Jung Lee
Yoon Mee Park
Byunghyun Kim
in Hwan Tae
Nam-Eun Kim
Marina Pranata
Taewon Kim
Sungho Won
Nam Joo Kang
Yun Kyung Lee
Dong-Woo Lee
Myung Hee Nam
Soo-Jong Hong
Bong-Soo Kim
author_sort Min-Jung Lee
collection DOAJ
description The gut microbiome influences the development of allergic diseases during early childhood. However, there is a lack of comprehensive understanding of microbiome-host crosstalk. Here, we analyzed the influence of gut microbiome dynamics in early childhood on atopic dermatitis (AD) and the potential interactions between host and microbiome that control this homeostasis. We analyzed the gut microbiome in 346 fecal samples (6–36 months; 112 non-AD, 110 mild AD, and 124 moderate to severe AD) from the Longitudinal Cohort for Childhood Origin of Asthma and Allergic Disease birth cohort. The microbiome-host interactions were analyzed in animal and in vitro cell assays. Although the gut microbiome maturated with age in both AD and non-AD groups, its development was disordered in the AD group. Disordered colonization of short-chain fatty acids (SCFA) producers along with age led to abnormal SCFA production and increased IgE levels. A butyrate deficiency and downregulation of GPR109A and PPAR-γ genes were detected in AD-induced mice. Insufficient butyrate decreases the oxygen consumption rate of host cells, which can release oxygen to the gut and perturb the gut microbiome. The disordered gut microbiome development could aggravate balanced microbiome-host interactions, including immune responses during early childhood with AD.
format Article
id doaj-art-f9f052eb18cd4fcc95d5071928c5c8d3
institution DOAJ
issn 1949-0976
1949-0984
language English
publishDate 2022-12-01
publisher Taylor & Francis Group
record_format Article
series Gut Microbes
spelling doaj-art-f9f052eb18cd4fcc95d5071928c5c8d32025-08-20T03:22:16ZengTaylor & Francis GroupGut Microbes1949-09761949-09842022-12-0114110.1080/19490976.2022.2068366Disordered development of gut microbiome interferes with the establishment of the gut ecosystem during early childhood with atopic dermatitisMin-Jung Lee0Yoon Mee Park1Byunghyun Kim2in Hwan Tae3Nam-Eun Kim4Marina Pranata5Taewon Kim6Sungho Won7Nam Joo Kang8Yun Kyung Lee9Dong-Woo Lee10Myung Hee Nam11Soo-Jong Hong12Bong-Soo Kim13Department of Life Science, Multidisciplinary Genome Institute, Hallym University, Chuncheon, Republic of KoreaAsan Institute for Life Sciences, Asan Medical Center, Seoul, Republic of KoreaSeoul Center, Korea Basic Science Institute, Seoul, Republic of KoreaSeoul Center, Korea Basic Science Institute, Seoul, Republic of KoreaDepartment of Public Health Sciences, Graduate School of Public Health, Seoul National University, Seoul, Republic of KoreaDepartment of Integrated Biomedical Science, Soonchunhyang Institute of Medi-Bioscience, Soonchunhyang University, Cheonan, Republic of KoreaSchool of Food Science and Biotechnology, Kyungpook National University, Daegu, Republic of KoreaDepartment of Public Health Sciences, Graduate School of Public Health, Seoul National University, Seoul, Republic of KoreaSchool of Food Science and Biotechnology, Kyungpook National University, Daegu, Republic of KoreaDepartment of Integrated Biomedical Science, Soonchunhyang Institute of Medi-Bioscience, Soonchunhyang University, Cheonan, Republic of KoreaDepartment of Biotechnology, Yonsei University, Seoul, Republic of KoreaSeoul Center, Korea Basic Science Institute, Seoul, Republic of KoreaDepartment of Pediatrics, Childhood Asthma Atopy Center, Humidifier Disinfectant Health Center, University of Ulsan College of Medicine, Seoul, Republic of KoreaDepartment of Life Science, Multidisciplinary Genome Institute, Hallym University, Chuncheon, Republic of KoreaThe gut microbiome influences the development of allergic diseases during early childhood. However, there is a lack of comprehensive understanding of microbiome-host crosstalk. Here, we analyzed the influence of gut microbiome dynamics in early childhood on atopic dermatitis (AD) and the potential interactions between host and microbiome that control this homeostasis. We analyzed the gut microbiome in 346 fecal samples (6–36 months; 112 non-AD, 110 mild AD, and 124 moderate to severe AD) from the Longitudinal Cohort for Childhood Origin of Asthma and Allergic Disease birth cohort. The microbiome-host interactions were analyzed in animal and in vitro cell assays. Although the gut microbiome maturated with age in both AD and non-AD groups, its development was disordered in the AD group. Disordered colonization of short-chain fatty acids (SCFA) producers along with age led to abnormal SCFA production and increased IgE levels. A butyrate deficiency and downregulation of GPR109A and PPAR-γ genes were detected in AD-induced mice. Insufficient butyrate decreases the oxygen consumption rate of host cells, which can release oxygen to the gut and perturb the gut microbiome. The disordered gut microbiome development could aggravate balanced microbiome-host interactions, including immune responses during early childhood with AD.https://www.tandfonline.com/doi/10.1080/19490976.2022.2068366Gutmicrobiomeatopic dermatitisdevelopmenthomeostasis
spellingShingle Min-Jung Lee
Yoon Mee Park
Byunghyun Kim
in Hwan Tae
Nam-Eun Kim
Marina Pranata
Taewon Kim
Sungho Won
Nam Joo Kang
Yun Kyung Lee
Dong-Woo Lee
Myung Hee Nam
Soo-Jong Hong
Bong-Soo Kim
Disordered development of gut microbiome interferes with the establishment of the gut ecosystem during early childhood with atopic dermatitis
Gut Microbes
Gut
microbiome
atopic dermatitis
development
homeostasis
title Disordered development of gut microbiome interferes with the establishment of the gut ecosystem during early childhood with atopic dermatitis
title_full Disordered development of gut microbiome interferes with the establishment of the gut ecosystem during early childhood with atopic dermatitis
title_fullStr Disordered development of gut microbiome interferes with the establishment of the gut ecosystem during early childhood with atopic dermatitis
title_full_unstemmed Disordered development of gut microbiome interferes with the establishment of the gut ecosystem during early childhood with atopic dermatitis
title_short Disordered development of gut microbiome interferes with the establishment of the gut ecosystem during early childhood with atopic dermatitis
title_sort disordered development of gut microbiome interferes with the establishment of the gut ecosystem during early childhood with atopic dermatitis
topic Gut
microbiome
atopic dermatitis
development
homeostasis
url https://www.tandfonline.com/doi/10.1080/19490976.2022.2068366
work_keys_str_mv AT minjunglee disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT yoonmeepark disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT byunghyunkim disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT inhwantae disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT nameunkim disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT marinapranata disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT taewonkim disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT sunghowon disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT namjookang disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT yunkyunglee disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT dongwoolee disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT myungheenam disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT soojonghong disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis
AT bongsookim disordereddevelopmentofgutmicrobiomeinterfereswiththeestablishmentofthegutecosystemduringearlychildhoodwithatopicdermatitis