Netherton syndrome subtypes share IL-17/IL-36 signature with distinct IFN-α and allergic responses.


Journal

The Journal of allergy and clinical immunology
ISSN: 1097-6825
Titre abrégé: J Allergy Clin Immunol
Pays: United States
ID NLM: 1275002

Informations de publication

Date de publication:
04 2022
Historique:
received: 03 03 2021
revised: 12 08 2021
accepted: 27 08 2021
pubmed: 21 9 2021
medline: 13 4 2022
entrez: 20 9 2021
Statut: ppublish

Résumé

Netherton syndrome (NS) is a rare recessive skin disorder caused by loss-of-function mutations in SPINK5 encoding the protease inhibitor LEKTI (lymphoepithelial Kazal-type-related inhibitor). NS patients experience severe skin barrier defects, display inflammatory skin lesions, and have superficial scaling with atopic manifestations. They present with typical ichthyosis linearis circumflexa (NS-ILC) or scaly erythroderma (NS-SE). We used a combination of several molecular profiling methods to comprehensively characterize the skin, immune cells, and allergic phenotypes of NS-ILC and NS-SE patients. We studied a cohort of 13 patients comprising 9 NS-ILC and 4 NS-SE. Integrated multiomics revealed abnormal epidermal proliferation and differentiation and IL-17/IL-36 signatures in lesion skin and in blood in both NS endotypes. Although the molecular profiles of NS-ILC and NS-SE lesion skin were very similar, nonlesion skin of each disease subtype displayed distinctive molecular features. Nonlesion and lesion NS-SE epidermis showed activation of the type I IFN signaling pathway, while lesion NS-ILC skin differed from nonlesion NS-ILC skin by increased complement activation and neutrophil infiltration. Serum cytokine profiling and immunophenotyping of circulating lymphocytes showed a T This study confirms IL-17/IL-36 as the predominant signaling axes in both NS endotypes and unveils molecular features distinguishing NS-ILC and NS-SE. These results identify new therapeutic targets and could pave the way for precision medicine of NS.

Sections du résumé

BACKGROUND
Netherton syndrome (NS) is a rare recessive skin disorder caused by loss-of-function mutations in SPINK5 encoding the protease inhibitor LEKTI (lymphoepithelial Kazal-type-related inhibitor). NS patients experience severe skin barrier defects, display inflammatory skin lesions, and have superficial scaling with atopic manifestations. They present with typical ichthyosis linearis circumflexa (NS-ILC) or scaly erythroderma (NS-SE).
OBJECTIVE
We used a combination of several molecular profiling methods to comprehensively characterize the skin, immune cells, and allergic phenotypes of NS-ILC and NS-SE patients.
METHODS
We studied a cohort of 13 patients comprising 9 NS-ILC and 4 NS-SE.
RESULTS
Integrated multiomics revealed abnormal epidermal proliferation and differentiation and IL-17/IL-36 signatures in lesion skin and in blood in both NS endotypes. Although the molecular profiles of NS-ILC and NS-SE lesion skin were very similar, nonlesion skin of each disease subtype displayed distinctive molecular features. Nonlesion and lesion NS-SE epidermis showed activation of the type I IFN signaling pathway, while lesion NS-ILC skin differed from nonlesion NS-ILC skin by increased complement activation and neutrophil infiltration. Serum cytokine profiling and immunophenotyping of circulating lymphocytes showed a T
CONCLUSIONS
This study confirms IL-17/IL-36 as the predominant signaling axes in both NS endotypes and unveils molecular features distinguishing NS-ILC and NS-SE. These results identify new therapeutic targets and could pave the way for precision medicine of NS.

Identifiants

pubmed: 34543653
pii: S0091-6749(21)01398-1
doi: 10.1016/j.jaci.2021.08.024
pii:
doi:

Substances chimiques

Interferon-alpha 0
Interleukin-17 0
Proteinase Inhibitory Proteins, Secretory 0
Serine Peptidase Inhibitor Kazal-Type 5 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1358-1372

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Claire Barbieux (C)

INSERM UMR 1163, Laboratory of Genetic Skin Diseases, Imagine Institute, Paris, France.

Mathilde Bonnet des Claustres (M)

INSERM UMR 1163, Laboratory of Genetic Skin Diseases, Imagine Institute, Paris, France.

Matthias Fahrner (M)

Institute for Surgical Pathology, Medical Center, Faculty of Medicine, University of Freiburg, Freiburg, Germany; Spemann Graduate School of Biology and Medicine (SGBM), Albert-Ludwigs-University Freiburg, Freiburg, Germany; Faculty of Biology, Albert-Ludwigs-University Freiburg, Freiburg, Germany.

Evgeniya Petrova (E)

INSERM UMR 1163, Laboratory of Genetic Skin Diseases, Imagine Institute, Paris, France.

Lam C Tsoi (LC)

INSERM UMR 1163, Laboratory of Genetic Skin Diseases, Imagine Institute, Paris, France.

Olivier Gouin (O)

INSERM UMR 1163, Laboratory of Genetic Skin Diseases, Imagine Institute, Paris, France.

Florent Leturcq (F)

INSERM UMR 1163, Laboratory of Genetic Skin Diseases, Imagine Institute, Paris, France.

Pascale Nicaise-Roland (P)

Department of Immunology, Bichat Hospital, AP-HP-Nord, Paris, France; INSERM UMR 1152, Paris, France.

Christine Bole (C)

INSERM UMR 1163, Imagine Institute, Paris, France.

Vivien Béziat (V)

INSERM UMR 1163, Laboratory of Human Genetics of Infectious Diseases, Imagine Institute, Paris, France.

Emmanuelle Bourrat (E)

Department of Dermatology, Saint-Louis Hospital, Paris, France.

Oliver Schilling (O)

Institute for Surgical Pathology, Medical Center, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Johann E Gudjonsson (JE)

Department of Dermatology, University of Michigan, Ann Arbor, Mich.

Alain Hovnanian (A)

University of Paris, Paris, France; Department of Genetics, Necker Hospital for Sick Children (AP-HP), Paris, France; Department of Dermatology, University of Michigan, Ann Arbor, Mich. Electronic address: alain.hovnanian@inserm.fr.

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