Distinct skin microbiome community structures in congenital ichthyosis.


Journal

The British journal of dermatology
ISSN: 1365-2133
Titre abrégé: Br J Dermatol
Pays: England
ID NLM: 0004041

Informations de publication

Date de publication:
10 2022
Historique:
revised: 28 03 2022
received: 03 06 2021
accepted: 21 05 2022
pubmed: 29 5 2022
medline: 6 10 2022
entrez: 28 5 2022
Statut: ppublish

Résumé

The ichthyoses are rare genetic keratinizing disorders that share the characteristics of an impaired epidermal barrier and increased risk of microbial infections. Although ichthyotic diseases share a T helper (Th) 17 cell immune signature, including increased expression of antimicrobial peptides, the skin microbiota of ichthyoses is virtually unexplored. To analyse the metagenome profile of skin microbiome for major congenital ichthyosis subtypes. Body site-matched skin surface samples were collected from the scalp, upper arm and upper buttocks of 16 healthy control participants and 22 adult patients with congenital forms of ichthyosis for whole metagenomics sequencing analysis. Taxonomic profiling showed significant shifts in bacteria and fungi abundance and sporadic viral increases across ichthyosis subtypes. Cutibacterium acnes and Malassezia were significantly reduced across body sites, consistent with skin barrier disruption and depletion of lipids. Microbial richness was reduced, with specific increases in Staphylococcus and Corynebacterium genera, as well as shifts in fungal species, including Malassezia. Malassezia globosa was reduced at all body sites, whereas M. sympodialis was reduced in the ichthyotic upper arm and upper buttocks. Malassezia slooffiae, by contrast, was strikingly increased at all body sites in participants with congenital ichthyosiform erythroderma (CIE) and lamellar ichthyosis (LI). A previously undescribed Trichophyton species was also detected as sporadically colonizing the skin of patients with CIE, LI and epidermolytic ichthyosis subtypes. The ichthyosis skin microbiome is significantly altered from healthy skin with specific changes predominating among ichthyosis subtypes. Skewing towards the Th17 pathway may represent a response to the altered microbial colonization in ichthyosis. What is already known about this topic? The skin microbiome of congenital ichthyoses is largely unexplored. Microbes play an important role in pathogenesis, as infections are common. The relative abundances of staphylococci and corynebacteria is increased in the cutaneous microbiome of patients with Netherton syndrome, but extension of these abundances to all congenital ichthyoses is unexplored. What does this study add? A common skin microbiome signature was observed across congenital ichthyoses. Distinct microbiome features were associated with ichthyosis subtypes. Changes in microbiome may contribute to T helper 17 cell immune polarization. What is the translational message? These data provide the basis for comparison of the microbiome with lipidomic and transcriptomic alterations in these forms of ichthyosis and consideration of correcting the dysbiosis as a therapeutic intervention.

Sections du résumé

BACKGROUND
The ichthyoses are rare genetic keratinizing disorders that share the characteristics of an impaired epidermal barrier and increased risk of microbial infections. Although ichthyotic diseases share a T helper (Th) 17 cell immune signature, including increased expression of antimicrobial peptides, the skin microbiota of ichthyoses is virtually unexplored.
OBJECTIVES
To analyse the metagenome profile of skin microbiome for major congenital ichthyosis subtypes.
METHODS
Body site-matched skin surface samples were collected from the scalp, upper arm and upper buttocks of 16 healthy control participants and 22 adult patients with congenital forms of ichthyosis for whole metagenomics sequencing analysis.
RESULTS
Taxonomic profiling showed significant shifts in bacteria and fungi abundance and sporadic viral increases across ichthyosis subtypes. Cutibacterium acnes and Malassezia were significantly reduced across body sites, consistent with skin barrier disruption and depletion of lipids. Microbial richness was reduced, with specific increases in Staphylococcus and Corynebacterium genera, as well as shifts in fungal species, including Malassezia. Malassezia globosa was reduced at all body sites, whereas M. sympodialis was reduced in the ichthyotic upper arm and upper buttocks. Malassezia slooffiae, by contrast, was strikingly increased at all body sites in participants with congenital ichthyosiform erythroderma (CIE) and lamellar ichthyosis (LI). A previously undescribed Trichophyton species was also detected as sporadically colonizing the skin of patients with CIE, LI and epidermolytic ichthyosis subtypes.
CONCLUSIONS
The ichthyosis skin microbiome is significantly altered from healthy skin with specific changes predominating among ichthyosis subtypes. Skewing towards the Th17 pathway may represent a response to the altered microbial colonization in ichthyosis. What is already known about this topic? The skin microbiome of congenital ichthyoses is largely unexplored. Microbes play an important role in pathogenesis, as infections are common. The relative abundances of staphylococci and corynebacteria is increased in the cutaneous microbiome of patients with Netherton syndrome, but extension of these abundances to all congenital ichthyoses is unexplored. What does this study add? A common skin microbiome signature was observed across congenital ichthyoses. Distinct microbiome features were associated with ichthyosis subtypes. Changes in microbiome may contribute to T helper 17 cell immune polarization. What is the translational message? These data provide the basis for comparison of the microbiome with lipidomic and transcriptomic alterations in these forms of ichthyosis and consideration of correcting the dysbiosis as a therapeutic intervention.

Identifiants

pubmed: 35633118
doi: 10.1111/bjd.21687
pmc: PMC10234690
mid: NIHMS1898276
doi:

Substances chimiques

Lipids 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

557-570

Subventions

Organisme : NIAMS NIH HHS
ID : P30 AR075049
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2022 British Association of Dermatologists.

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Auteurs

Khek-Chian Tham (KC)

A*STAR Skin Research Labs, Agency for Science, Technology and Research, 8A Biomedical Grove, #06-10 Immunos, Singapore, 138648, Singapore.

Rachel Lefferdink (R)

Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Kaibo Duan (K)

Singapore Immunology Network, Agency for Science, Technology and Research, 8A Biomedical Grove, #03 Immunos, Singapore, 138648, Singapore.

Seong Soo Lim (SS)

A*STAR Skin Research Labs, Agency for Science, Technology and Research, 8A Biomedical Grove, #06-10 Immunos, Singapore, 138648, Singapore.

X F Colin C Wong (XFCC)

A*STAR Skin Research Labs, Agency for Science, Technology and Research, 8A Biomedical Grove, #06-10 Immunos, Singapore, 138648, Singapore.

Erin Ibler (E)

Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Benedict Wu (B)

Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Hajar Abu-Zayed (H)

Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Stephanie M Rangel (SM)

Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Ester Del Duca (E)

Icahn School of Medicine at Mount Sinai Medical Center, New York, NY, USA.

Mashkura Chowdhury (M)

Icahn School of Medicine at Mount Sinai Medical Center, New York, NY, USA.

Margot Chima (M)

Icahn School of Medicine at Mount Sinai Medical Center, New York, NY, USA.

Hee Jee Kim (HJ)

Icahn School of Medicine at Mount Sinai Medical Center, New York, NY, USA.

Bernett Lee (B)

Singapore Immunology Network, Agency for Science, Technology and Research, 8A Biomedical Grove, #03 Immunos, Singapore, 138648, Singapore.

Emma Guttman-Yassky (E)

Icahn School of Medicine at Mount Sinai Medical Center, New York, NY, USA.

Amy S Paller (AS)

Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

John E A Common (JEA)

A*STAR Skin Research Labs, Agency for Science, Technology and Research, 8A Biomedical Grove, #06-10 Immunos, Singapore, 138648, Singapore.

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