Single-cell transcriptome analysis of human skin identifies novel fibroblast subpopulation and enrichment of immune subsets in atopic dermatitis
Atopic dermatitis (AD) is a prevalent inflammatory skin disease with a complex pathogenesis involving immune cell and epidermal abnormalities. Despite whole tissue biopsy studies that have advanced the mechanistic understanding of AD, single cell–based molecular alterations are largely unknown. Our...
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| Published in | Journal of allergy and clinical immunology Vol. 145; no. 6; pp. 1615 - 1628 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.06.2020
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0091-6749 1097-6825 1097-6825 |
| DOI | 10.1016/j.jaci.2020.01.042 |
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| Abstract | Atopic dermatitis (AD) is a prevalent inflammatory skin disease with a complex pathogenesis involving immune cell and epidermal abnormalities. Despite whole tissue biopsy studies that have advanced the mechanistic understanding of AD, single cell–based molecular alterations are largely unknown.
Our aims were to construct a detailed, high-resolution atlas of cell populations and assess variability in cell composition and cell-specific gene expression in the skin of patients with AD versus in controls.
We performed single-cell RNA sequencing on skin biopsy specimens from 5 patients with AD (4 lesional samples and 5 nonlesional samples) and 7 healthy control subjects, using 10× Genomics.
We created transcriptomic profiles for 39,042 AD (lesional and nonlesional) and healthy skin cells. Fibroblasts demonstrated a novel COL6A5+COL18A1+ subpopulation that was unique to lesional AD and expressed CCL2 and CCL19 cytokines. A corresponding LAMP3+ dendritic cell (DC) population that expressed the CCL19 receptor CCR7 was also unique to AD lesions, illustrating a potential role for fibroblast signaling to immune cells. The lesional AD samples were characterized by expansion of inflammatory DCs (CD1A+FCER1A+) and tissue-resident memory T cells (CD69+CD103+). The frequencies of type 2 (IL13+)/type 22 (IL22+) T cells were higher than those of type 1 (IFNG+) in lesional AD, whereas this ratio was slightly diminished in nonlesional AD and further diminished in controls.
AD lesions were characterized by expanded type 2/type 22 T cells and inflammatory DCs, and by a unique inflammatory fibroblast that may interact with immune cells to regulate lymphoid cell organization and type 2 inflammation.
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| AbstractList | Atopic dermatitis (AD) is a prevalent inflammatory skin disease with a complex pathogenesis involving immune cell and epidermal abnormalities. Despite whole tissue biopsy studies that have advanced the mechanistic understanding of AD, single cell-based molecular alterations are largely unknown.BACKGROUNDAtopic dermatitis (AD) is a prevalent inflammatory skin disease with a complex pathogenesis involving immune cell and epidermal abnormalities. Despite whole tissue biopsy studies that have advanced the mechanistic understanding of AD, single cell-based molecular alterations are largely unknown.Our aims were to construct a detailed, high-resolution atlas of cell populations and assess variability in cell composition and cell-specific gene expression in the skin of patients with AD versus in controls.OBJECTIVEOur aims were to construct a detailed, high-resolution atlas of cell populations and assess variability in cell composition and cell-specific gene expression in the skin of patients with AD versus in controls.We performed single-cell RNA sequencing on skin biopsy specimens from 5 patients with AD (4 lesional samples and 5 nonlesional samples) and 7 healthy control subjects, using 10× Genomics.METHODSWe performed single-cell RNA sequencing on skin biopsy specimens from 5 patients with AD (4 lesional samples and 5 nonlesional samples) and 7 healthy control subjects, using 10× Genomics.We created transcriptomic profiles for 39,042 AD (lesional and nonlesional) and healthy skin cells. Fibroblasts demonstrated a novel COL6A5+COL18A1+ subpopulation that was unique to lesional AD and expressed CCL2 and CCL19 cytokines. A corresponding LAMP3+ dendritic cell (DC) population that expressed the CCL19 receptor CCR7 was also unique to AD lesions, illustrating a potential role for fibroblast signaling to immune cells. The lesional AD samples were characterized by expansion of inflammatory DCs (CD1A+FCER1A+) and tissue-resident memory T cells (CD69+CD103+). The frequencies of type 2 (IL13+)/type 22 (IL22+) T cells were higher than those of type 1 (IFNG+) in lesional AD, whereas this ratio was slightly diminished in nonlesional AD and further diminished in controls.RESULTSWe created transcriptomic profiles for 39,042 AD (lesional and nonlesional) and healthy skin cells. Fibroblasts demonstrated a novel COL6A5+COL18A1+ subpopulation that was unique to lesional AD and expressed CCL2 and CCL19 cytokines. A corresponding LAMP3+ dendritic cell (DC) population that expressed the CCL19 receptor CCR7 was also unique to AD lesions, illustrating a potential role for fibroblast signaling to immune cells. The lesional AD samples were characterized by expansion of inflammatory DCs (CD1A+FCER1A+) and tissue-resident memory T cells (CD69+CD103+). The frequencies of type 2 (IL13+)/type 22 (IL22+) T cells were higher than those of type 1 (IFNG+) in lesional AD, whereas this ratio was slightly diminished in nonlesional AD and further diminished in controls.AD lesions were characterized by expanded type 2/type 22 T cells and inflammatory DCs, and by a unique inflammatory fibroblast that may interact with immune cells to regulate lymphoid cell organization and type 2 inflammation.CONCLUSIONAD lesions were characterized by expanded type 2/type 22 T cells and inflammatory DCs, and by a unique inflammatory fibroblast that may interact with immune cells to regulate lymphoid cell organization and type 2 inflammation. Atopic dermatitis (AD) is a prevalent inflammatory skin disease with a complex pathogenesis involving immune cell and epidermal abnormalities. Despite whole tissue biopsy studies that have advanced the mechanistic understanding of AD, single cell-based molecular alterations are largely unknown. Our aims were to construct a detailed, high-resolution atlas of cell populations and assess variability in cell composition and cell-specific gene expression in the skin of patients with AD versus in controls. We performed single-cell RNA sequencing on skin biopsy specimens from 5 patients with AD (4 lesional samples and 5 nonlesional samples) and 7 healthy control subjects, using 10× Genomics. We created transcriptomic profiles for 39,042 AD (lesional and nonlesional) and healthy skin cells. Fibroblasts demonstrated a novel COL6A5 COL18A1 subpopulation that was unique to lesional AD and expressed CCL2 and CCL19 cytokines. A corresponding LAMP3 dendritic cell (DC) population that expressed the CCL19 receptor CCR7 was also unique to AD lesions, illustrating a potential role for fibroblast signaling to immune cells. The lesional AD samples were characterized by expansion of inflammatory DCs (CD1A FCER1A ) and tissue-resident memory T cells (CD69 CD103 ). The frequencies of type 2 (IL13 )/type 22 (IL22 ) T cells were higher than those of type 1 (IFNG ) in lesional AD, whereas this ratio was slightly diminished in nonlesional AD and further diminished in controls. AD lesions were characterized by expanded type 2/type 22 T cells and inflammatory DCs, and by a unique inflammatory fibroblast that may interact with immune cells to regulate lymphoid cell organization and type 2 inflammation. Atopic dermatitis (AD) is a prevalent inflammatory skin disease with a complex pathogenesis involving immune cell and epidermal abnormalities. Despite whole tissue biopsy studies that have advanced the mechanistic understanding of AD, single cell–based molecular alterations are largely unknown. Our aims were to construct a detailed, high-resolution atlas of cell populations and assess variability in cell composition and cell-specific gene expression in the skin of patients with AD versus in controls. We performed single-cell RNA sequencing on skin biopsy specimens from 5 patients with AD (4 lesional samples and 5 nonlesional samples) and 7 healthy control subjects, using 10× Genomics. We created transcriptomic profiles for 39,042 AD (lesional and nonlesional) and healthy skin cells. Fibroblasts demonstrated a novel COL6A5+COL18A1+ subpopulation that was unique to lesional AD and expressed CCL2 and CCL19 cytokines. A corresponding LAMP3+ dendritic cell (DC) population that expressed the CCL19 receptor CCR7 was also unique to AD lesions, illustrating a potential role for fibroblast signaling to immune cells. The lesional AD samples were characterized by expansion of inflammatory DCs (CD1A+FCER1A+) and tissue-resident memory T cells (CD69+CD103+). The frequencies of type 2 (IL13+)/type 22 (IL22+) T cells were higher than those of type 1 (IFNG+) in lesional AD, whereas this ratio was slightly diminished in nonlesional AD and further diminished in controls. AD lesions were characterized by expanded type 2/type 22 T cells and inflammatory DCs, and by a unique inflammatory fibroblast that may interact with immune cells to regulate lymphoid cell organization and type 2 inflammation. [Display omitted] |
| Author | Der, Evan Suryawanshi, Hemant Kim, Hyun Je He, Helen Guttman-Yassky, Emma Estrada, Yeriel Morozov, Pavel Tuschl, Thomas Del Duca, Ester Ruano, Juan Gay-Mimbrera, Jesús Kameyama, Naoya Krueger, James G. |
| Author_xml | – sequence: 1 givenname: Helen surname: He fullname: He, Helen organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 2 givenname: Hemant surname: Suryawanshi fullname: Suryawanshi, Hemant email: hsuryawans@mail.rockefeller.edu organization: Laboratory of RNA Molecular Biology, The Rockefeller University, New York, NY – sequence: 3 givenname: Pavel surname: Morozov fullname: Morozov, Pavel organization: Laboratory of RNA Molecular Biology, The Rockefeller University, New York, NY – sequence: 4 givenname: Jesús surname: Gay-Mimbrera fullname: Gay-Mimbrera, Jesús organization: Department of Dermatology, Reina Sofía University Hospital, Córdoba, Spain – sequence: 5 givenname: Ester surname: Del Duca fullname: Del Duca, Ester organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 6 givenname: Hyun Je surname: Kim fullname: Kim, Hyun Je organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 7 givenname: Naoya surname: Kameyama fullname: Kameyama, Naoya organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 8 givenname: Yeriel surname: Estrada fullname: Estrada, Yeriel organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 9 givenname: Evan surname: Der fullname: Der, Evan organization: Division of Rheumatology and Department of Microbiology and Immunology, Albert Einstein College of Medicine, New York, NY – sequence: 10 givenname: James G. surname: Krueger fullname: Krueger, James G. organization: Laboratory of Investigative Dermatology, The Rockefeller University, New York, NY – sequence: 11 givenname: Juan surname: Ruano fullname: Ruano, Juan organization: Department of Dermatology, Reina Sofía University Hospital, Córdoba, Spain – sequence: 12 givenname: Thomas surname: Tuschl fullname: Tuschl, Thomas email: ttuschl@rockefeller.edu organization: Laboratory of RNA Molecular Biology, The Rockefeller University, New York, NY – sequence: 13 givenname: Emma orcidid: 0000-0002-9363-324X surname: Guttman-Yassky fullname: Guttman-Yassky, Emma email: emma.guttman@mountsinai.org organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32035984$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Atopic dermatitis Case-Control Studies cytokines Cytokines - immunology dendritic cells Dendritic Cells - immunology Dermatitis, Atopic - immunology fibroblasts Fibroblasts - immunology Gene Expression Profiling - methods Humans Immunologic Memory - immunology Inflammation - immunology Sequence Analysis, RNA - methods Single-Cell Analysis - methods single-cell RNA sequencing Skin - immunology T cells T-Lymphocytes - immunology Transcriptome - immunology |
| Title | Single-cell transcriptome analysis of human skin identifies novel fibroblast subpopulation and enrichment of immune subsets in atopic dermatitis |
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