Insights into Keratinocyte and Immunologic Landscape in Cutaneous Graft-Versus-Host Disease through Single-Cell Transcriptomics

Cutaneous manifestations are the most common presenting sign of chronic graft-versus-host disease (GVHD), and the extent of cutaneous involvement is also highly correlated with prognosis. Very little is understood about the underlying pathogenesis underpinning injury at this location, especially the...

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Main Authors: Amy J. Petty, Adela Rambi Cardones, Yingai Jane Jin, Vaibhav Jain, Emily Hocke, Harsh B. Pathak, Amrita Mitra, Simon G. Gregory, M. Angelica Selim, Jennifer Y. Zhang
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:JID Innovations
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Online Access:http://www.sciencedirect.com/science/article/pii/S2667026725000293
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author Amy J. Petty
Adela Rambi Cardones
Yingai Jane Jin
Vaibhav Jain
Emily Hocke
Harsh B. Pathak
Amrita Mitra
Simon G. Gregory
M. Angelica Selim
Jennifer Y. Zhang
author_facet Amy J. Petty
Adela Rambi Cardones
Yingai Jane Jin
Vaibhav Jain
Emily Hocke
Harsh B. Pathak
Amrita Mitra
Simon G. Gregory
M. Angelica Selim
Jennifer Y. Zhang
author_sort Amy J. Petty
collection DOAJ
description Cutaneous manifestations are the most common presenting sign of chronic graft-versus-host disease (GVHD), and the extent of cutaneous involvement is also highly correlated with prognosis. Very little is understood about the underlying pathogenesis underpinning injury at this location, especially the contribution of keratinocytes and other structural skin cells. We performed single-cell RNA sequencing to compare the transcriptome of epidermal and dermal chronic GVHD samples with that of healthy control samples. Our findings reveal unique nonimmunologic and immunologic changes in epidermal keratinocytes and dermal immune cells. Specifically, we observed upregulation of alarmins and inflammatory cytokines and downregulation of anti-reduction–oxidation and activator protein-1 pathway genes in the keratinocyte compartments. In dermal immune cell subsets, we showed increased CD8+ T, CD4+ T, CD4+Foxp3+ regulatory T, and NK cells in chronic GVHD, accompanied by increased signals of leukocyte functions, inflammatory responses, cytolysis, and macrophage M1 polarization. Finally, we also delineated the donor versus recipient cellular origin of nonimmune and immune cell populations in sex-mismatched chronic GVHD. Taken together, these data reveal complex keratinocyte and immune responses in cutaneous chronic GVHD, supporting future studies of skin cell contributions to pathogenesis and potential local treatment strategies.
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spelling doaj-art-43116e8131f74cf18e13acfebc2eb9ee2025-08-20T03:34:00ZengElsevierJID Innovations2667-02672025-07-015410037310.1016/j.xjidi.2025.100373Insights into Keratinocyte and Immunologic Landscape in Cutaneous Graft-Versus-Host Disease through Single-Cell TranscriptomicsAmy J. Petty0Adela Rambi Cardones1Yingai Jane Jin2Vaibhav Jain3Emily Hocke4Harsh B. Pathak5Amrita Mitra6Simon G. Gregory7M. Angelica Selim8Jennifer Y. Zhang9Department of Dermatology, Duke University, Durham, North Carolina, USADepartment of Dermatology, Duke University, Durham, North Carolina, USA; Division of Dermatology, Department of Internal Medicine, University of Kansas Medical Center, Kansas City, Kansas, USADepartment of Dermatology, Duke University, Durham, North Carolina, USAMolecular Genomic Core, Duke University, Durham, North Carolina, USAMolecular Genomic Core, Duke University, Durham, North Carolina, USADepartment of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, Kansas, USADepartment of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, Kansas, USAMolecular Genomic Core, Duke University, Durham, North Carolina, USA; Department of Neurosurgery, Duke University, Durham, North Carolina, USADepartment of Pathology, Duke University, Durham, North Carolina, USADepartment of Dermatology, Duke University, Durham, North Carolina, USA; Department of Pathology, Duke University, Durham, North Carolina, USA; Correspondence: Jennifer Y. Zhang, Department of Dermatology, Duke University, 200 Trent Drive, Durham, North Carolina 27710, USA.Cutaneous manifestations are the most common presenting sign of chronic graft-versus-host disease (GVHD), and the extent of cutaneous involvement is also highly correlated with prognosis. Very little is understood about the underlying pathogenesis underpinning injury at this location, especially the contribution of keratinocytes and other structural skin cells. We performed single-cell RNA sequencing to compare the transcriptome of epidermal and dermal chronic GVHD samples with that of healthy control samples. Our findings reveal unique nonimmunologic and immunologic changes in epidermal keratinocytes and dermal immune cells. Specifically, we observed upregulation of alarmins and inflammatory cytokines and downregulation of anti-reduction–oxidation and activator protein-1 pathway genes in the keratinocyte compartments. In dermal immune cell subsets, we showed increased CD8+ T, CD4+ T, CD4+Foxp3+ regulatory T, and NK cells in chronic GVHD, accompanied by increased signals of leukocyte functions, inflammatory responses, cytolysis, and macrophage M1 polarization. Finally, we also delineated the donor versus recipient cellular origin of nonimmune and immune cell populations in sex-mismatched chronic GVHD. Taken together, these data reveal complex keratinocyte and immune responses in cutaneous chronic GVHD, supporting future studies of skin cell contributions to pathogenesis and potential local treatment strategies.http://www.sciencedirect.com/science/article/pii/S2667026725000293Cutaneous chronic GVHDGraft-versus-host diseaseKeratinocytesM1 and M2 macrophagesT cells
spellingShingle Amy J. Petty
Adela Rambi Cardones
Yingai Jane Jin
Vaibhav Jain
Emily Hocke
Harsh B. Pathak
Amrita Mitra
Simon G. Gregory
M. Angelica Selim
Jennifer Y. Zhang
Insights into Keratinocyte and Immunologic Landscape in Cutaneous Graft-Versus-Host Disease through Single-Cell Transcriptomics
JID Innovations
Cutaneous chronic GVHD
Graft-versus-host disease
Keratinocytes
M1 and M2 macrophages
T cells
title Insights into Keratinocyte and Immunologic Landscape in Cutaneous Graft-Versus-Host Disease through Single-Cell Transcriptomics
title_full Insights into Keratinocyte and Immunologic Landscape in Cutaneous Graft-Versus-Host Disease through Single-Cell Transcriptomics
title_fullStr Insights into Keratinocyte and Immunologic Landscape in Cutaneous Graft-Versus-Host Disease through Single-Cell Transcriptomics
title_full_unstemmed Insights into Keratinocyte and Immunologic Landscape in Cutaneous Graft-Versus-Host Disease through Single-Cell Transcriptomics
title_short Insights into Keratinocyte and Immunologic Landscape in Cutaneous Graft-Versus-Host Disease through Single-Cell Transcriptomics
title_sort insights into keratinocyte and immunologic landscape in cutaneous graft versus host disease through single cell transcriptomics
topic Cutaneous chronic GVHD
Graft-versus-host disease
Keratinocytes
M1 and M2 macrophages
T cells
url http://www.sciencedirect.com/science/article/pii/S2667026725000293
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