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Commensal microbiota modulate gene expression in the skin

BACKGROUND: The skin harbors complex communities of resident microorganisms, yet little is known of their physiological roles and the molecular mechanisms that mediate cutaneous host-microbe interactions. Here, we profiled skin transcriptomes of mice reared in the presence and absence of microbiota...

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Autores principales: Meisel, Jacquelyn S., Sfyroera, Georgia, Bartow-McKenney, Casey, Gimblet, Ciara, Bugayev, Julia, Horwinski, Joseph, Kim, Brian, Brestoff, Jonathan R., Tyldsley, Amanda S., Zheng, Qi, Hodkinson, Brendan P., Artis, David, Grice, Elizabeth A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5789709/
https://www.ncbi.nlm.nih.gov/pubmed/29378633
http://dx.doi.org/10.1186/s40168-018-0404-9
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author Meisel, Jacquelyn S.
Sfyroera, Georgia
Bartow-McKenney, Casey
Gimblet, Ciara
Bugayev, Julia
Horwinski, Joseph
Kim, Brian
Brestoff, Jonathan R.
Tyldsley, Amanda S.
Zheng, Qi
Hodkinson, Brendan P.
Artis, David
Grice, Elizabeth A.
author_facet Meisel, Jacquelyn S.
Sfyroera, Georgia
Bartow-McKenney, Casey
Gimblet, Ciara
Bugayev, Julia
Horwinski, Joseph
Kim, Brian
Brestoff, Jonathan R.
Tyldsley, Amanda S.
Zheng, Qi
Hodkinson, Brendan P.
Artis, David
Grice, Elizabeth A.
author_sort Meisel, Jacquelyn S.
collection PubMed
description BACKGROUND: The skin harbors complex communities of resident microorganisms, yet little is known of their physiological roles and the molecular mechanisms that mediate cutaneous host-microbe interactions. Here, we profiled skin transcriptomes of mice reared in the presence and absence of microbiota to elucidate the range of pathways and functions modulated in the skin by the microbiota. RESULTS: A total of 2820 genes were differentially regulated in response to microbial colonization and were enriched in gene ontology (GO) terms related to the host-immune response and epidermal differentiation. Innate immune response genes and genes involved in cytokine activity were generally upregulated in response to microbiota and included genes encoding toll-like receptors, antimicrobial peptides, the complement cascade, and genes involved in IL-1 family cytokine signaling and homing of T cells. Our results also reveal a role for the microbiota in modulating epidermal differentiation and development, with differential expression of genes in the epidermal differentiation complex (EDC). Genes with correlated co-expression patterns were enriched in binding sites for the transcription factors Klf4, AP-1, and SP-1, all implicated as regulators of epidermal differentiation. Finally, we identified transcriptional signatures of microbial regulation common to both the skin and the gastrointestinal tract. CONCLUSIONS: With this foundational approach, we establish a critical resource for understanding the genome-wide implications of microbially mediated gene expression in the skin and emphasize prospective ways in which the microbiome contributes to skin health and disease. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0404-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-57897092018-02-08 Commensal microbiota modulate gene expression in the skin Meisel, Jacquelyn S. Sfyroera, Georgia Bartow-McKenney, Casey Gimblet, Ciara Bugayev, Julia Horwinski, Joseph Kim, Brian Brestoff, Jonathan R. Tyldsley, Amanda S. Zheng, Qi Hodkinson, Brendan P. Artis, David Grice, Elizabeth A. Microbiome Research BACKGROUND: The skin harbors complex communities of resident microorganisms, yet little is known of their physiological roles and the molecular mechanisms that mediate cutaneous host-microbe interactions. Here, we profiled skin transcriptomes of mice reared in the presence and absence of microbiota to elucidate the range of pathways and functions modulated in the skin by the microbiota. RESULTS: A total of 2820 genes were differentially regulated in response to microbial colonization and were enriched in gene ontology (GO) terms related to the host-immune response and epidermal differentiation. Innate immune response genes and genes involved in cytokine activity were generally upregulated in response to microbiota and included genes encoding toll-like receptors, antimicrobial peptides, the complement cascade, and genes involved in IL-1 family cytokine signaling and homing of T cells. Our results also reveal a role for the microbiota in modulating epidermal differentiation and development, with differential expression of genes in the epidermal differentiation complex (EDC). Genes with correlated co-expression patterns were enriched in binding sites for the transcription factors Klf4, AP-1, and SP-1, all implicated as regulators of epidermal differentiation. Finally, we identified transcriptional signatures of microbial regulation common to both the skin and the gastrointestinal tract. CONCLUSIONS: With this foundational approach, we establish a critical resource for understanding the genome-wide implications of microbially mediated gene expression in the skin and emphasize prospective ways in which the microbiome contributes to skin health and disease. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0404-9) contains supplementary material, which is available to authorized users. BioMed Central 2018-01-30 /pmc/articles/PMC5789709/ /pubmed/29378633 http://dx.doi.org/10.1186/s40168-018-0404-9 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Meisel, Jacquelyn S.
Sfyroera, Georgia
Bartow-McKenney, Casey
Gimblet, Ciara
Bugayev, Julia
Horwinski, Joseph
Kim, Brian
Brestoff, Jonathan R.
Tyldsley, Amanda S.
Zheng, Qi
Hodkinson, Brendan P.
Artis, David
Grice, Elizabeth A.
Commensal microbiota modulate gene expression in the skin
title Commensal microbiota modulate gene expression in the skin
title_full Commensal microbiota modulate gene expression in the skin
title_fullStr Commensal microbiota modulate gene expression in the skin
title_full_unstemmed Commensal microbiota modulate gene expression in the skin
title_short Commensal microbiota modulate gene expression in the skin
title_sort commensal microbiota modulate gene expression in the skin
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5789709/
https://www.ncbi.nlm.nih.gov/pubmed/29378633
http://dx.doi.org/10.1186/s40168-018-0404-9
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