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

被引:7
作者
Liu, Xiaolin [1 ,2 ]
van Beek, Nina [3 ]
Cepic, Aleksa [1 ,2 ]
Andreani, Nadia A. [1 ,2 ]
Chung, Cecilia J. [1 ,2 ]
Hermes, Britt M. [1 ,2 ]
Yilmaz, Kaan [3 ]
Benoit, Sandrine [4 ]
Drenovska, Kossara [5 ]
Gerdes, Sascha [6 ]
Glaeser, Regine [6 ]
Goebeler, Matthias [4 ]
Guenther, Claudia [7 ]
von Georg, Anabelle [3 ]
Hammers, Christoph M. [3 ]
Holtsche, Maike M. [3 ]
Huebner, Franziska [3 ]
Kiritsi, Dimitra [8 ]
Schauer, Franziska [8 ]
Linnenmann, Beke [3 ]
Huilaja, Laura [9 ,10 ,11 ]
Tasanen-Maatta, Kaisa [9 ,10 ,11 ]
Vassileva, Snejina [5 ]
Zillikens, Detlef [3 ,12 ]
Sadik, Christian D. [3 ,12 ]
Schmidt, Enno [3 ,12 ,13 ]
Ibrahim, Saleh [13 ,14 ]
Baines, John F. [1 ,2 ]
机构
[1] Max Planck Inst Evolutionary Biol, Dept Evolutionary Genet, Plon, Germany
[2] Univ Kiel, Inst Expt Med, Sect Evolutionary Med, Kiel, Germany
[3] Univ Lubeck, Dept Dermatol Allergy & Venereol, Lubeck, Germany
[4] Univ Hosp Wurzburg, Dept Dermatol Venereol & Allergol, Wurzburg, Germany
[5] Med Univ Sofia, Dept Dermatol & Venereol, Sofia, Bulgaria
[6] Univ Kiel, Dept Dermatol Venereol & Allergol, Kiel, Germany
[7] Tech Univ TU Dresden, Univ Hosp, Dept Dermatol, Dresden, Germany
[8] Univ Freiburg, Fac Med, Med Ctr, Dept Dermatol, Freiburg, Germany
[9] Univ Oulu, Res Unit Clin Med, Oulu, Finland
[10] Oulu Univ Hosp, Dept Dermatol, Oulu, Finland
[11] Oulu Univ Hosp, Med Res Ctr Oulu, Oulu, Finland
[12] Univ Lubeck, Ctr Res Inflammat Skin CRIS, Lubeck, Germany
[13] Univ Lubeck, Lubeck Inst Expt Dermatol LIED, Lubeck, Germany
[14] Khalifa Univ, Coll Med & Hlth Sci, Abu Dhabi, U Arab Emirates
关键词
bullous pemphigoid; skin; inflammation; gut microbiome; 16S rRNA gene; metagenome; GAMMA-AMINOBUTYRIC-ACID; ATOPIC-DERMATITIS; DIVERSITY; DYSBIOSIS; GABA;
D O I
10.3389/fimmu.2023.1212551
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
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.
引用
收藏
页数:11
相关论文
共 84 条
[1]   Low diversity of the gut microbiota in infants with atopic eczema [J].
Abrahamsson, Thomas R. ;
Jakobsson, Hedvig E. ;
Andersson, Anders F. ;
Bjorksten, Bengt ;
Engstrand, Lars ;
Jenmalm, Maria C. .
JOURNAL OF ALLERGY AND CLINICAL IMMUNOLOGY, 2012, 129 (02) :434-U244
[2]   Community differentiation of the cutaneous microbiota in psoriasis [J].
Alekseyenko, Alexander V. ;
Perez-Perez, Guillermo I. ;
De Souza, Aieska ;
Strober, Bruce ;
Gao, Zhan ;
Bihan, Monika ;
Li, Kelvin ;
Methe, Barbara A. ;
Blaser, Martin J. .
MICROBIOME, 2013, 1
[3]   Autoimmune Subepidermal Bullous Diseases of the Skin and Mucosae: Clinical Features, Diagnosis, and Management [J].
Amber, Kyle T. ;
Murrell, Dedee F. ;
Schmidt, Enno ;
Joly, Pascal ;
Borradori, Luca .
CLINICAL REVIEWS IN ALLERGY & IMMUNOLOGY, 2018, 54 (01) :26-51
[4]  
Anderson M.J., 2017, WILEY STATSREF STAT, P1, DOI [10.1002/9781118445112.stat07841, DOI 10.1002/9781118445112.STAT07841]
[5]   Skin and gut microbiota dysbiosis in autoimmune and inflammatory skin diseases [J].
Baglama, Spela Suler ;
Trcko, Katarina .
ACTA DERMATOVENEROLOGICA ALPINA PANNONICA ET ADRIATICA, 2022, 31 (03) :105-109
[6]   Gut microbiome of multiple sclerosis patients and paired household healthy controls reveal associations with disease risk and course [J].
Baranzini, Sergio E. ;
iMSMS Consortium .
CELL, 2022, 185 (19) :3467-+
[7]   Integrating taxonomic, functional, and strain-level profiling of diverse microbial communities with bioBakery 3 [J].
Beghini, Francesco ;
McIver, Lauren J. ;
Blanco-Miguez, Aitor ;
Dubois, Leonard ;
Asnicar, Francesco ;
Maharjan, Sagun ;
Mailyan, Ana ;
Manghi, Paolo ;
Scholz, Matthias ;
Thomas, Andrew Maltez ;
Valles-Colomer, Mireia ;
Weingart, George ;
Zhang, Yancong ;
Zolfo, Moreno ;
Huttenhower, Curtis ;
Franzosa, Eric A. ;
Segata, Nicola .
ELIFE, 2021, 10
[8]   Characterization of the skin microbiota in bullous pemphigoid patients and controls reveals novel microbial indicators of disease [J].
Belheouane, Meriem ;
Hermes, Britt M. ;
Van Beek, Nina ;
Benoit, Sandrine ;
Bernard, Philippe ;
Drenovska, Kossara ;
Gerdes, Sascha ;
Glaeser, Regine ;
Goebeler, Matthias ;
Guenther, Claudia ;
von Georg, Anabelle ;
Hammers, Christoph M. ;
Holtsche, Maike M. ;
Homey, Bernhard ;
Horvath, Orsolya N. ;
Huebner, Franziska ;
Linnemann, Beke ;
Joly, Pascal ;
Marton, Dalma ;
Patsatsi, Aikaterini ;
Pfoehler, Claudia ;
Sardy, Miklos ;
Huilaja, Laura ;
Vassileva, Snejina ;
Zillikens, Detlef ;
Ibrahim, Saleh ;
Sadik, Christian D. ;
Schmidt, Enno ;
Baines, John F. .
JOURNAL OF ADVANCED RESEARCH, 2023, 44 :71-79
[9]   Mining the microbiota to identify gut commensals modulating neuroinflammation in a mouse model of multiple sclerosis [J].
Bianchimano, Paola ;
Britton, Graham J. ;
Wallach, David S. ;
Smith, Emma M. ;
Cox, Laura M. ;
Liu, Shirong ;
Iwanowski, Kacper ;
Weiner, Howard L. ;
Faith, Jeremiah J. ;
Clemente, Jose C. ;
Tankou, Stephanie K. .
MICROBIOME, 2022, 10 (01)
[10]   Trimmomatic: a flexible trimmer for Illumina sequence data [J].
Bolger, Anthony M. ;
Lohse, Marc ;
Usadel, Bjoern .
BIOINFORMATICS, 2014, 30 (15) :2114-2120