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The gut microbiome in bullous pemphigoid: implications of the gut-skin axis for disease susceptibility

Bullous pemphigoid (BP) is an autoimmune blistering disease that primarily affects the elderly. An altered skin microbiota in BP was recently revealed. Accumulating evidence points toward a link between the gut microbiota and skin diseases; however, the gut microbiota composition of BP patients rema...

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Autores principales: Liu, Xiaolin, van Beek, Nina, Cepic, Aleksa, Andreani, Nadia A., Chung, Cecilia J., Hermes, Britt M., Yilmaz, Kaan, Benoit, Sandrine, Drenovska, Kossara, Gerdes, Sascha, Gläser, Regine, Goebeler, Matthias, Günther, Claudia, von Georg, Anabelle, Hammers, Christoph M., Holtsche, Maike M., Hübner, Franziska, Kiritsi, Dimitra, Schauer, Franziska, Linnenmann, Beke, Huilaja, Laura, Tasanen-Määttä, Kaisa, Vassileva, Snejina, Zillikens, Detlef, Sadik, Christian D., Schmidt, Enno, Ibrahim, Saleh, Baines, John F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10668026/
https://www.ncbi.nlm.nih.gov/pubmed/38022583
http://dx.doi.org/10.3389/fimmu.2023.1212551
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author Liu, Xiaolin
van Beek, Nina
Cepic, Aleksa
Andreani, Nadia A.
Chung, Cecilia J.
Hermes, Britt M.
Yilmaz, Kaan
Benoit, Sandrine
Drenovska, Kossara
Gerdes, Sascha
Gläser, Regine
Goebeler, Matthias
Günther, Claudia
von Georg, Anabelle
Hammers, Christoph M.
Holtsche, Maike M.
Hübner, Franziska
Kiritsi, Dimitra
Schauer, Franziska
Linnenmann, Beke
Huilaja, Laura
Tasanen-Määttä, Kaisa
Vassileva, Snejina
Zillikens, Detlef
Sadik, Christian D.
Schmidt, Enno
Ibrahim, Saleh
Baines, John F.
author_facet Liu, Xiaolin
van Beek, Nina
Cepic, Aleksa
Andreani, Nadia A.
Chung, Cecilia J.
Hermes, Britt M.
Yilmaz, Kaan
Benoit, Sandrine
Drenovska, Kossara
Gerdes, Sascha
Gläser, Regine
Goebeler, Matthias
Günther, Claudia
von Georg, Anabelle
Hammers, Christoph M.
Holtsche, Maike M.
Hübner, Franziska
Kiritsi, Dimitra
Schauer, Franziska
Linnenmann, Beke
Huilaja, Laura
Tasanen-Määttä, Kaisa
Vassileva, Snejina
Zillikens, Detlef
Sadik, Christian D.
Schmidt, Enno
Ibrahim, Saleh
Baines, John F.
author_sort Liu, Xiaolin
collection PubMed
description Bullous pemphigoid (BP) is an autoimmune blistering disease that primarily affects the elderly. An altered skin microbiota in BP was recently revealed. Accumulating evidence points toward a link between the gut microbiota and skin diseases; however, the gut microbiota composition of BP patients remains largely underexplored, with only one pilot study to date, with a very limited sample size and no functional profiling of gut microbiota. To thoroughly investigate the composition and function of the gut microbiota in BP patients, and explore possible links between skin conditions and gut microbiota, we here investigated the gut microbiota of 66 patients (81.8% firstly diagnosed) suffering from BP and 66 age-, sex-, and study center-matched controls (CL) with non-inflammatory skin diseases (132 total participants), using 16S rRNA gene and shotgun sequencing data. Decreased alpha-diversity and an overall altered gut microbial community is observed in BP patients. Similar trends are observed in subclassifications of BP patients, including first diagnoses and relapsed cases. Furthermore, we observe a set of BP disease-associated gut microbial features, including reduced Faecalibacterium prausnitzii and greater abundance of pathways related to gamma-aminobutyric acid (GABA) metabolism in BP patients. Interestingly, F. prausnitzii is a well-known microbiomarker of inflammatory diseases, which has been reported to be reduced in the gut microbiome of atopic dermatitis and psoriasis patients. Moreover, GABA plays multiple roles in maintaining skin health, including the inhibition of itching by acting as a neurotransmitter, attenuating skin lesions by balancing Th1 and Th2 levels, and maintaining skin elasticity by increasing the expression of type I collagen. These findings thus suggest that gut microbiota alterations present in BP may play a role in the disease, and certain key microbes and functions may contribute to the link between gut dysbiosis and BP disease activity. Further studies to investigate the underlying mechanisms of the gut-skin interaction are thus clearly warranted, which could aid in the development of potential therapeutic interventions.
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spelling pubmed-106680262023-01-01 The gut microbiome in bullous pemphigoid: implications of the gut-skin axis for disease susceptibility Liu, Xiaolin van Beek, Nina Cepic, Aleksa Andreani, Nadia A. Chung, Cecilia J. Hermes, Britt M. Yilmaz, Kaan Benoit, Sandrine Drenovska, Kossara Gerdes, Sascha Gläser, Regine Goebeler, Matthias Günther, Claudia von Georg, Anabelle Hammers, Christoph M. Holtsche, Maike M. Hübner, Franziska Kiritsi, Dimitra Schauer, Franziska Linnenmann, Beke Huilaja, Laura Tasanen-Määttä, Kaisa Vassileva, Snejina Zillikens, Detlef Sadik, Christian D. Schmidt, Enno Ibrahim, Saleh Baines, John F. Front Immunol Immunology Bullous pemphigoid (BP) is an autoimmune blistering disease that primarily affects the elderly. An altered skin microbiota in BP was recently revealed. Accumulating evidence points toward a link between the gut microbiota and skin diseases; however, the gut microbiota composition of BP patients remains largely underexplored, with only one pilot study to date, with a very limited sample size and no functional profiling of gut microbiota. To thoroughly investigate the composition and function of the gut microbiota in BP patients, and explore possible links between skin conditions and gut microbiota, we here investigated the gut microbiota of 66 patients (81.8% firstly diagnosed) suffering from BP and 66 age-, sex-, and study center-matched controls (CL) with non-inflammatory skin diseases (132 total participants), using 16S rRNA gene and shotgun sequencing data. Decreased alpha-diversity and an overall altered gut microbial community is observed in BP patients. Similar trends are observed in subclassifications of BP patients, including first diagnoses and relapsed cases. Furthermore, we observe a set of BP disease-associated gut microbial features, including reduced Faecalibacterium prausnitzii and greater abundance of pathways related to gamma-aminobutyric acid (GABA) metabolism in BP patients. Interestingly, F. prausnitzii is a well-known microbiomarker of inflammatory diseases, which has been reported to be reduced in the gut microbiome of atopic dermatitis and psoriasis patients. Moreover, GABA plays multiple roles in maintaining skin health, including the inhibition of itching by acting as a neurotransmitter, attenuating skin lesions by balancing Th1 and Th2 levels, and maintaining skin elasticity by increasing the expression of type I collagen. These findings thus suggest that gut microbiota alterations present in BP may play a role in the disease, and certain key microbes and functions may contribute to the link between gut dysbiosis and BP disease activity. Further studies to investigate the underlying mechanisms of the gut-skin interaction are thus clearly warranted, which could aid in the development of potential therapeutic interventions. Frontiers Media S.A. 2023-11-10 /pmc/articles/PMC10668026/ /pubmed/38022583 http://dx.doi.org/10.3389/fimmu.2023.1212551 Text en Copyright © 2023 Liu, van Beek, Cepic, Andreani, Chung, Hermes, Yilmaz, Benoit, Drenovska, Gerdes, Gläser, Goebeler, Günther, von Georg, Hammers, Holtsche, Hübner, Kiritsi, Schauer, Linnenmann, Huilaja, Tasanen-Määttä, Vassileva, Zillikens, Sadik, Schmidt, Ibrahim and Baines 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 Immunology
Liu, Xiaolin
van Beek, Nina
Cepic, Aleksa
Andreani, Nadia A.
Chung, Cecilia J.
Hermes, Britt M.
Yilmaz, Kaan
Benoit, Sandrine
Drenovska, Kossara
Gerdes, Sascha
Gläser, Regine
Goebeler, Matthias
Günther, Claudia
von Georg, Anabelle
Hammers, Christoph M.
Holtsche, Maike M.
Hübner, Franziska
Kiritsi, Dimitra
Schauer, Franziska
Linnenmann, Beke
Huilaja, Laura
Tasanen-Määttä, Kaisa
Vassileva, Snejina
Zillikens, Detlef
Sadik, Christian D.
Schmidt, Enno
Ibrahim, Saleh
Baines, John F.
The gut microbiome in bullous pemphigoid: implications of the gut-skin axis for disease susceptibility
title The gut microbiome in bullous pemphigoid: implications of the gut-skin axis for disease susceptibility
title_full The gut microbiome in bullous pemphigoid: implications of the gut-skin axis for disease susceptibility
title_fullStr The gut microbiome in bullous pemphigoid: implications of the gut-skin axis for disease susceptibility
title_full_unstemmed The gut microbiome in bullous pemphigoid: implications of the gut-skin axis for disease susceptibility
title_short The gut microbiome in bullous pemphigoid: implications of the gut-skin axis for disease susceptibility
title_sort gut microbiome in bullous pemphigoid: implications of the gut-skin axis for disease susceptibility
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10668026/
https://www.ncbi.nlm.nih.gov/pubmed/38022583
http://dx.doi.org/10.3389/fimmu.2023.1212551
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