Microbe-host interplay in atopic dermatitis and psoriasis

Nanna Fyhrquist; Gareth Muirhead; Stefanie Prast-Nielsen; Marine Jeanmougin; Peter Olah; Tiina Skoog; Gerome Jules-Clement; Micha Feld; Mauricio Barrientos-Somarribas; Hanna Sinkko; Ellen H. van den Bogaard; Patrick L.J.M. Zeeuwen; Gijs Rikken; Joost Schalkwijk; Hanna Niehues; Walter Däubener; Silvia Kathrin Eller; Helen Alexander; Davide Pennino; Sari Suomela; Ioannis Tessas; Emilia Lybeck; Anna M. Baran; Hamid Darban; Roopesh Singh Gangwar; Ulrich Gerstel; Katharina Jahn; Piia Karisola; Lee Yan; Britta Hansmann; Shintaro Katayama; Stephan Meller; Max Bylesjö; Philippe Hupé; Francesca Levi-Schaffer; Dario Greco; Annamari Ranki; Jens M. Schröder; Jonathan Barker; Juha Kere; Sophia Tsoka; Antti Lauerma; Vassili Soumelis; Frank O. Nestle; Bernhard Homey; Björn Andersson; Harri Alenius

doi:10.1038/s41467-019-12253-y

Microbe-host interplay in atopic dermatitis and psoriasis

Nanna Fyhrquist, Gareth Muirhead, Stefanie Prast-Nielsen, Marine Jeanmougin, Peter Olah, Tiina Skoog, Gerome Jules-Clement, Micha Feld, Mauricio Barrientos-Somarribas, Hanna Sinkko, Ellen H. van den Bogaard, Patrick L.J.M. Zeeuwen, Gijs Rikken, Joost Schalkwijk, Hanna Niehues, Walter Däubener, Silvia Kathrin Eller, Helen Alexander, Davide Pennino, Sari SuomelaIoannis Tessas, Emilia Lybeck, Anna M. Baran, Hamid Darban, Roopesh Singh Gangwar, Ulrich Gerstel, Katharina Jahn, Piia Karisola, Lee Yan, Britta Hansmann, Shintaro Katayama, Stephan Meller, Max Bylesjö, Philippe Hupé, Francesca Levi-Schaffer, Dario Greco, Annamari Ranki, Jens M. Schröder, Jonathan Barker, Juha Kere, Sophia Tsoka, Antti Lauerma, Vassili Soumelis, Frank O. Nestle, Bernhard Homey, Björn Andersson, Harri Alenius^*

^*Corresponding author for this work

School of Pharmacy

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

170 Scopus citations

Abstract

Despite recent advances in understanding microbial diversity in skin homeostasis, the relevance of microbial dysbiosis in inflammatory disease is poorly understood. Here we perform a comparative analysis of skin microbial communities coupled to global patterns of cutaneous gene expression in patients with atopic dermatitis or psoriasis. The skin microbiota is analysed by 16S amplicon or whole genome sequencing and the skin transcriptome by microarrays, followed by integration of the data layers. We find that atopic dermatitis and psoriasis can be classified by distinct microbes, which differ from healthy volunteers microbiome composition. Atopic dermatitis is dominated by a single microbe (Staphylococcus aureus), and associated with a disease relevant host transcriptomic signature enriched for skin barrier function, tryptophan metabolism and immune activation. In contrast, psoriasis is characterized by co-occurring communities of microbes with weak associations with disease related gene expression. Our work provides a basis for biomarker discovery and targeted therapies in skin dysbiosis.

Original language	American English
Article number	4703
Journal	Nature Communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-12253-y
State	Published - 1 Dec 2019

Bibliographical note

Funding Information:
The authors want to thank Prof. A. Andersson (KTH Royal Institute of Technology and Science for Life Laboratory (SciLifeLab)) for providing the 16S primer designs and acknowledge support from SciLifeLab, the national infrastructure SNISS, and Uppmax for assistance in massive parallel sequencing and computational infrastructure. Technical support by D. Lundin, BILS (Bioinformatics Infrastructure for Life Sciences) and T. Keyvanfar is also acknowledged. The research has received funding from the FP7/ 2007–2013 (Grant 261366). The study was partially funded by the Knut and Alice Wallenberg Foundation, the Department of Health via the National Institute for Health Research (NIHR) comprehensive Biomedical Research Centre award to Guy’s & St Thomas’ NHS Foundation Trust in partnership with King’s College London and King’s College Hospital NHS Foundation (guysbrc-2012-1) Trust, and Dunhill Medical Trust, the Association pour la Recherche contre le Cancer (ARC), the European Research Council (Grant IT-DC 281987), Institute National de la Santé et de la Recherche Médicale (BIO2012-02 and BIO2014-08), INCA (2011-1-PL BIO-12-IC-1), Fondation ARSEP (R12023JJ), ANR (ANR-13-BSV1-0024-02, ANR-10-IDEX-0001-02 PSL*, ANR-11-LABX-0043 and ZonMw MKMD grant 114021503) and BIOMAP IMI2 (Grant 821511).

Publisher Copyright:
© 2019, The Author(s).

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10.1038/s41467-019-12253-y

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Fyhrquist, N., Muirhead, G., Prast-Nielsen, S., Jeanmougin, M., Olah, P., Skoog, T., Jules-Clement, G., Feld, M., Barrientos-Somarribas, M., Sinkko, H., van den Bogaard, E. H., Zeeuwen, P. L. J. M., Rikken, G., Schalkwijk, J., Niehues, H., Däubener, W., Eller, S. K., Alexander, H., Pennino, D., ... Alenius, H. (2019). Microbe-host interplay in atopic dermatitis and psoriasis. Nature Communications, 10(1), Article 4703. https://doi.org/10.1038/s41467-019-12253-y

@article{8533499c334d4fa78d0da299ae03c96e,

title = "Microbe-host interplay in atopic dermatitis and psoriasis",

abstract = "Despite recent advances in understanding microbial diversity in skin homeostasis, the relevance of microbial dysbiosis in inflammatory disease is poorly understood. Here we perform a comparative analysis of skin microbial communities coupled to global patterns of cutaneous gene expression in patients with atopic dermatitis or psoriasis. The skin microbiota is analysed by 16S amplicon or whole genome sequencing and the skin transcriptome by microarrays, followed by integration of the data layers. We find that atopic dermatitis and psoriasis can be classified by distinct microbes, which differ from healthy volunteers microbiome composition. Atopic dermatitis is dominated by a single microbe (Staphylococcus aureus), and associated with a disease relevant host transcriptomic signature enriched for skin barrier function, tryptophan metabolism and immune activation. In contrast, psoriasis is characterized by co-occurring communities of microbes with weak associations with disease related gene expression. Our work provides a basis for biomarker discovery and targeted therapies in skin dysbiosis.",

author = "Nanna Fyhrquist and Gareth Muirhead and Stefanie Prast-Nielsen and Marine Jeanmougin and Peter Olah and Tiina Skoog and Gerome Jules-Clement and Micha Feld and Mauricio Barrientos-Somarribas and Hanna Sinkko and {van den Bogaard}, {Ellen H.} and Zeeuwen, {Patrick L.J.M.} and Gijs Rikken and Joost Schalkwijk and Hanna Niehues and Walter D{\"a}ubener and Eller, {Silvia Kathrin} and Helen Alexander and Davide Pennino and Sari Suomela and Ioannis Tessas and Emilia Lybeck and Baran, {Anna M.} and Hamid Darban and Gangwar, {Roopesh Singh} and Ulrich Gerstel and Katharina Jahn and Piia Karisola and Lee Yan and Britta Hansmann and Shintaro Katayama and Stephan Meller and Max Bylesj{\"o} and Philippe Hup{\'e} and Francesca Levi-Schaffer and Dario Greco and Annamari Ranki and Schr{\"o}der, {Jens M.} and Jonathan Barker and Juha Kere and Sophia Tsoka and Antti Lauerma and Vassili Soumelis and Nestle, {Frank O.} and Bernhard Homey and Bj{\"o}rn Andersson and Harri Alenius",

note = "Funding Information: The authors want to thank Prof. A. Andersson (KTH Royal Institute of Technology and Science for Life Laboratory (SciLifeLab)) for providing the 16S primer designs and acknowledge support from SciLifeLab, the national infrastructure SNISS, and Uppmax for assistance in massive parallel sequencing and computational infrastructure. Technical support by D. Lundin, BILS (Bioinformatics Infrastructure for Life Sciences) and T. Keyvanfar is also acknowledged. The research has received funding from the FP7/ 2007–2013 (Grant 261366). The study was partially funded by the Knut and Alice Wallenberg Foundation, the Department of Health via the National Institute for Health Research (NIHR) comprehensive Biomedical Research Centre award to Guy{\textquoteright}s & St Thomas{\textquoteright} NHS Foundation Trust in partnership with King{\textquoteright}s College London and King{\textquoteright}s College Hospital NHS Foundation (guysbrc-2012-1) Trust, and Dunhill Medical Trust, the Association pour la Recherche contre le Cancer (ARC), the European Research Council (Grant IT-DC 281987), Institute National de la Sant{\'e} et de la Recherche M{\'e}dicale (BIO2012-02 and BIO2014-08), INCA (2011-1-PL BIO-12-IC-1), Fondation ARSEP (R12023JJ), ANR (ANR-13-BSV1-0024-02, ANR-10-IDEX-0001-02 PSL*, ANR-11-LABX-0043 and ZonMw MKMD grant 114021503) and BIOMAP IMI2 (Grant 821511). Publisher Copyright: {\textcopyright} 2019, The Author(s).",

year = "2019",

month = dec,

day = "1",

doi = "10.1038/s41467-019-12253-y",

language = "American English",

volume = "10",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

number = "1",

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Fyhrquist, N, Muirhead, G, Prast-Nielsen, S, Jeanmougin, M, Olah, P, Skoog, T, Jules-Clement, G, Feld, M, Barrientos-Somarribas, M, Sinkko, H, van den Bogaard, EH, Zeeuwen, PLJM, Rikken, G, Schalkwijk, J, Niehues, H, Däubener, W, Eller, SK, Alexander, H, Pennino, D, Suomela, S, Tessas, I, Lybeck, E, Baran, AM, Darban, H, Gangwar, RS, Gerstel, U, Jahn, K, Karisola, P, Yan, L, Hansmann, B, Katayama, S, Meller, S, Bylesjö, M, Hupé, P, Levi-Schaffer, F, Greco, D, Ranki, A, Schröder, JM, Barker, J, Kere, J, Tsoka, S, Lauerma, A, Soumelis, V, Nestle, FO, Homey, B, Andersson, B & Alenius, H 2019, 'Microbe-host interplay in atopic dermatitis and psoriasis', Nature Communications, vol. 10, no. 1, 4703. https://doi.org/10.1038/s41467-019-12253-y

TY - JOUR

T1 - Microbe-host interplay in atopic dermatitis and psoriasis

AU - Fyhrquist, Nanna

AU - Muirhead, Gareth

AU - Prast-Nielsen, Stefanie

AU - Jeanmougin, Marine

AU - Olah, Peter

AU - Skoog, Tiina

AU - Jules-Clement, Gerome

AU - Feld, Micha

AU - Barrientos-Somarribas, Mauricio

AU - Sinkko, Hanna

AU - van den Bogaard, Ellen H.

AU - Zeeuwen, Patrick L.J.M.

AU - Rikken, Gijs

AU - Schalkwijk, Joost

AU - Niehues, Hanna

AU - Däubener, Walter

AU - Eller, Silvia Kathrin

AU - Alexander, Helen

AU - Pennino, Davide

AU - Suomela, Sari

AU - Tessas, Ioannis

AU - Lybeck, Emilia

AU - Baran, Anna M.

AU - Darban, Hamid

AU - Gangwar, Roopesh Singh

AU - Gerstel, Ulrich

AU - Jahn, Katharina

AU - Karisola, Piia

AU - Yan, Lee

AU - Hansmann, Britta

AU - Katayama, Shintaro

AU - Meller, Stephan

AU - Bylesjö, Max

AU - Hupé, Philippe

AU - Levi-Schaffer, Francesca

AU - Greco, Dario

AU - Ranki, Annamari

AU - Schröder, Jens M.

AU - Barker, Jonathan

AU - Kere, Juha

AU - Tsoka, Sophia

AU - Lauerma, Antti

AU - Soumelis, Vassili

AU - Nestle, Frank O.

AU - Homey, Bernhard

AU - Andersson, Björn

AU - Alenius, Harri

N1 - Funding Information: The authors want to thank Prof. A. Andersson (KTH Royal Institute of Technology and Science for Life Laboratory (SciLifeLab)) for providing the 16S primer designs and acknowledge support from SciLifeLab, the national infrastructure SNISS, and Uppmax for assistance in massive parallel sequencing and computational infrastructure. Technical support by D. Lundin, BILS (Bioinformatics Infrastructure for Life Sciences) and T. Keyvanfar is also acknowledged. The research has received funding from the FP7/ 2007–2013 (Grant 261366). The study was partially funded by the Knut and Alice Wallenberg Foundation, the Department of Health via the National Institute for Health Research (NIHR) comprehensive Biomedical Research Centre award to Guy’s & St Thomas’ NHS Foundation Trust in partnership with King’s College London and King’s College Hospital NHS Foundation (guysbrc-2012-1) Trust, and Dunhill Medical Trust, the Association pour la Recherche contre le Cancer (ARC), the European Research Council (Grant IT-DC 281987), Institute National de la Santé et de la Recherche Médicale (BIO2012-02 and BIO2014-08), INCA (2011-1-PL BIO-12-IC-1), Fondation ARSEP (R12023JJ), ANR (ANR-13-BSV1-0024-02, ANR-10-IDEX-0001-02 PSL*, ANR-11-LABX-0043 and ZonMw MKMD grant 114021503) and BIOMAP IMI2 (Grant 821511). Publisher Copyright: © 2019, The Author(s).

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Despite recent advances in understanding microbial diversity in skin homeostasis, the relevance of microbial dysbiosis in inflammatory disease is poorly understood. Here we perform a comparative analysis of skin microbial communities coupled to global patterns of cutaneous gene expression in patients with atopic dermatitis or psoriasis. The skin microbiota is analysed by 16S amplicon or whole genome sequencing and the skin transcriptome by microarrays, followed by integration of the data layers. We find that atopic dermatitis and psoriasis can be classified by distinct microbes, which differ from healthy volunteers microbiome composition. Atopic dermatitis is dominated by a single microbe (Staphylococcus aureus), and associated with a disease relevant host transcriptomic signature enriched for skin barrier function, tryptophan metabolism and immune activation. In contrast, psoriasis is characterized by co-occurring communities of microbes with weak associations with disease related gene expression. Our work provides a basis for biomarker discovery and targeted therapies in skin dysbiosis.

AB - Despite recent advances in understanding microbial diversity in skin homeostasis, the relevance of microbial dysbiosis in inflammatory disease is poorly understood. Here we perform a comparative analysis of skin microbial communities coupled to global patterns of cutaneous gene expression in patients with atopic dermatitis or psoriasis. The skin microbiota is analysed by 16S amplicon or whole genome sequencing and the skin transcriptome by microarrays, followed by integration of the data layers. We find that atopic dermatitis and psoriasis can be classified by distinct microbes, which differ from healthy volunteers microbiome composition. Atopic dermatitis is dominated by a single microbe (Staphylococcus aureus), and associated with a disease relevant host transcriptomic signature enriched for skin barrier function, tryptophan metabolism and immune activation. In contrast, psoriasis is characterized by co-occurring communities of microbes with weak associations with disease related gene expression. Our work provides a basis for biomarker discovery and targeted therapies in skin dysbiosis.

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U2 - 10.1038/s41467-019-12253-y

DO - 10.1038/s41467-019-12253-y

M3 - Article

C2 - 31619666

AN - SCOPUS:85073475919

SN - 2041-1723

VL - 10

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 4703

ER -

Microbe-host interplay in atopic dermatitis and psoriasis

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