Single cell sequencing delineates T-cell clonality and pathogenesis of the parapsoriasis disease group.

Atopic dermatitis fingerprint dermatitis innate lymphoid cells mycosis fungoides parapsoriasis single-cell RNA sequencing

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:
13 Sep 2024
Historique:
received: 27 03 2024
revised: 30 07 2024
accepted: 10 09 2024
medline: 16 9 2024
pubmed: 16 9 2024
entrez: 15 9 2024
Statut: aheadofprint

Résumé

Mycosis fungoides (MF), the most common cutaneous T-cell lymphoma, is often underdiagnosed in early stages due to similarities with benign dermatoses such as atopic dermatitis (AD). Furthermore, the delineation from so-called "parapsoriasis en plaque," a disease that can appear either in a small- or large-plaque form, is still controversial. To characterize the parapsoriasis disease spectrum. We performed single-cell RNA sequencing of skin biopsies from patients within the parapsoriasis-to-early-stage MF spectrum, stratified for small and large plaques, and compared them to AD, psoriasis and healthy control skin. 6 out of 8 large-plaque lesions harbored either an expanded alpha/beta or gamma/delta T-cell clone with downregulation of CD7 expression, consistent with a diagnosis of early-stage MF. By contrast, 6 out of 7 small-plaque lesions were polyclonal in nature thereby lacking a lymphomatous phenotype, and also revealed a less inflammatory microenvironment than early-stage MF or AD. Of note, polyclonal small- and large-plaque lesions characteristically harbored a population of NPY+ innate lymphoid cells and displayed a stromal signature of complement upregulation and antimicrobial hyperresponsiveness in fibroblasts and sweat gland cells, respectively. These conditions were clearly distinct from AD or psoriasis, which uniquely harbored CD3+CRTH2+ IL13-expressing "Th2A" cells or strong type 17 inflammation, respectively. These data position polyclonal small- and large-plaque dermatitis lesions as a separate disease entity, that characteristically harbors a so far undescribed ILC population. We thus propose the new term "polyclonal parapsoriasis en plaque" to this kind of lesions, as they can be clearly differentiated from early and advanced-stage MF, psoriasis and AD on several cellular and molecular levels.

Sections du résumé

BACKGROUND BACKGROUND
Mycosis fungoides (MF), the most common cutaneous T-cell lymphoma, is often underdiagnosed in early stages due to similarities with benign dermatoses such as atopic dermatitis (AD). Furthermore, the delineation from so-called "parapsoriasis en plaque," a disease that can appear either in a small- or large-plaque form, is still controversial.
OBJECTIVE OBJECTIVE
To characterize the parapsoriasis disease spectrum.
METHODS METHODS
We performed single-cell RNA sequencing of skin biopsies from patients within the parapsoriasis-to-early-stage MF spectrum, stratified for small and large plaques, and compared them to AD, psoriasis and healthy control skin.
RESULTS RESULTS
6 out of 8 large-plaque lesions harbored either an expanded alpha/beta or gamma/delta T-cell clone with downregulation of CD7 expression, consistent with a diagnosis of early-stage MF. By contrast, 6 out of 7 small-plaque lesions were polyclonal in nature thereby lacking a lymphomatous phenotype, and also revealed a less inflammatory microenvironment than early-stage MF or AD. Of note, polyclonal small- and large-plaque lesions characteristically harbored a population of NPY+ innate lymphoid cells and displayed a stromal signature of complement upregulation and antimicrobial hyperresponsiveness in fibroblasts and sweat gland cells, respectively. These conditions were clearly distinct from AD or psoriasis, which uniquely harbored CD3+CRTH2+ IL13-expressing "Th2A" cells or strong type 17 inflammation, respectively.
CONCLUSION CONCLUSIONS
These data position polyclonal small- and large-plaque dermatitis lesions as a separate disease entity, that characteristically harbors a so far undescribed ILC population. We thus propose the new term "polyclonal parapsoriasis en plaque" to this kind of lesions, as they can be clearly differentiated from early and advanced-stage MF, psoriasis and AD on several cellular and molecular levels.

Identifiants

pubmed: 39278361
pii: S0091-6749(24)00942-4
doi: 10.1016/j.jaci.2024.09.004
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024. Published by Elsevier Inc.

Auteurs

Natalia Alkon (N)

Department of Dermatology, Medical University of Vienna, Austria.

Sumanth Chennareddy (S)

Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Emry R Cohenour (ER)

Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

John R Ruggiero (JR)

Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Georg Stingl (G)

Department of Dermatology, Medical University of Vienna, Austria.

Christine Bangert (C)

Department of Dermatology, Medical University of Vienna, Austria.

Katharina Rindler (K)

Department of Dermatology, Medical University of Vienna, Austria.

Wolfgang M Bauer (WM)

Department of Dermatology, Medical University of Vienna, Austria.

Wolfgang Weninger (W)

Department of Dermatology, Medical University of Vienna, Austria.

Johannes Griss (J)

Department of Dermatology, Medical University of Vienna, Austria.

Constanze Jonak (C)

Department of Dermatology, Medical University of Vienna, Austria. Electronic address: constanze.jonak@meduniwien.ac.at.

Patrick M Brunner (PM)

Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY, USA. Electronic address: patrick.brunner@mountsinai.org.

Classifications MeSH