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

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

doi:10.1080/19490976.2022.2068366

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

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

Department of Biotechnology

Research output: Contribution to journal › Article › peer-review

3 Citations (Scopus)

Abstract

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.

Original language	English
Article number	2068366
Journal	Gut Microbes
Volume	14
Issue number	1
DOIs	https://doi.org/10.1080/19490976.2022.2068366
Publication status	Published - 2022

Bibliographical note

Funding Information:
This study was supported by the Bio & Medical Technology Development Program of the National Research Foundation of Korea (NRF) funded by the Korean government (MSIT) [Ministry of Science and ICT, South Korea NRF-2017M3A9F3043837, NRF-2017M3A9F3043853, and NRF-2021M3A9I4023974]; the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) funded by the Ministry of Health and Welfare [Ministry of Health and Welfare HP20C0082]; the Research Program funded by the Korea Centers for Disease Control and Prevention [2020E670200 and 2020E670201]. We thank D.H. Seo at Seoul National University College of Medicine, S.-Y. Lee at University of Ulsan College of Medicine, K.W. Kim at Yonsei University College of Medicine, Y.H. Sheen at CHA University College of Medicine, and K. Ahn at Sungkyunkwan University School of Medicine for enrolling subjects in the COCOA cohort.

Publisher Copyright:
© 2022 The Author(s). Published with license by Taylor & Francis Group, LLC.

All Science Journal Classification (ASJC) codes

Microbiology
Gastroenterology
Microbiology (medical)
Infectious Diseases

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1080/19490976.2022.2068366

Cite this

Lee, M. J., Park, Y. M., Kim, B., Tae, I. H., Kim, N. E., Pranata, M., Kim, T., Won, S., Kang, N. J., Lee, Y. K., Lee, D. W., Nam, M. H., Hong, S. J., & Kim, B. S. (2022). Disordered development of gut microbiome interferes with the establishment of the gut ecosystem during early childhood with atopic dermatitis. Gut Microbes, 14(1), [2068366]. https://doi.org/10.1080/19490976.2022.2068366

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title = "Disordered development of gut microbiome interferes with the establishment of the gut ecosystem during early childhood with atopic dermatitis",

abstract = "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.",

author = "Lee, {Min Jung} and Park, {Yoon Mee} and Byunghyun Kim and Tae, {in Hwan} and Kim, {Nam Eun} and Marina Pranata and Taewon Kim and Sungho Won and Kang, {Nam Joo} and Lee, {Yun Kyung} and Lee, {Dong Woo} and Nam, {Myung Hee} and Hong, {Soo Jong} and Kim, {Bong Soo}",

note = "Funding Information: This study was supported by the Bio & Medical Technology Development Program of the National Research Foundation of Korea (NRF) funded by the Korean government (MSIT) [Ministry of Science and ICT, South Korea NRF-2017M3A9F3043837, NRF-2017M3A9F3043853, and NRF-2021M3A9I4023974]; the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) funded by the Ministry of Health and Welfare [Ministry of Health and Welfare HP20C0082]; the Research Program funded by the Korea Centers for Disease Control and Prevention [2020E670200 and 2020E670201]. We thank D.H. Seo at Seoul National University College of Medicine, S.-Y. Lee at University of Ulsan College of Medicine, K.W. Kim at Yonsei University College of Medicine, Y.H. Sheen at CHA University College of Medicine, and K. Ahn at Sungkyunkwan University School of Medicine for enrolling subjects in the COCOA cohort. Publisher Copyright: {\textcopyright} 2022 The Author(s). Published with license by Taylor & Francis Group, LLC.",

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doi = "10.1080/19490976.2022.2068366",

language = "English",

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AU - Lee, Min Jung

AU - Park, Yoon Mee

AU - Kim, Byunghyun

AU - Tae, in Hwan

AU - Kim, Nam Eun

AU - Pranata, Marina

AU - Kim, Taewon

AU - Won, Sungho

AU - Kang, Nam Joo

AU - Lee, Yun Kyung

AU - Lee, Dong Woo

AU - Nam, Myung Hee

AU - Hong, Soo Jong

AU - Kim, Bong Soo

N1 - Funding Information: This study was supported by the Bio & Medical Technology Development Program of the National Research Foundation of Korea (NRF) funded by the Korean government (MSIT) [Ministry of Science and ICT, South Korea NRF-2017M3A9F3043837, NRF-2017M3A9F3043853, and NRF-2021M3A9I4023974]; the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) funded by the Ministry of Health and Welfare [Ministry of Health and Welfare HP20C0082]; the Research Program funded by the Korea Centers for Disease Control and Prevention [2020E670200 and 2020E670201]. We thank D.H. Seo at Seoul National University College of Medicine, S.-Y. Lee at University of Ulsan College of Medicine, K.W. Kim at Yonsei University College of Medicine, Y.H. Sheen at CHA University College of Medicine, and K. Ahn at Sungkyunkwan University School of Medicine for enrolling subjects in the COCOA cohort. Publisher Copyright: © 2022 The Author(s). Published with license by Taylor & Francis Group, LLC.

PY - 2022

Y1 - 2022

N2 - 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.

AB - 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.

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

Abstract

Bibliographical note

All Science Journal Classification (ASJC) codes

UN SDGs

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