Single-Cell RNA-seq Reveals Characteristics of Malignant Cells and Immune Microenvironment in Subcutaneous Panniculitis-Like T-Cell Lymphoma

BackgroundSubcutaneous panniculitis-like T-cell lymphoma (SPTCL) is a malignant primary T-cell lymphoma that is challenging to distinguish from autoimmune disorders and reactive panniculitides. Delay in diagnosis and a high misdiagnosis rate affect the prognosis and survival of patients. The difficu...

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Main Authors: Zifeng Li, Hongsheng Wang, Rui Dong, Jie Man, Li Sun, Xiaowen Qian, Xiaohua Zhu, Ping Cao, Yi Yu, Jun Le, Yang Fu, Ping Wang, Wenjin Jiang, Chen Shen, Yangyang Ma, Lian Chen, Yaochen Xu, Jiantao Shi, Hui Zhang, Maoxiang Qian, Xiaowen Zhai
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Oncology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fonc.2021.611580/full
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language English
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author Zifeng Li
Hongsheng Wang
Rui Dong
Jie Man
Li Sun
Xiaowen Qian
Xiaohua Zhu
Ping Cao
Yi Yu
Jun Le
Yang Fu
Ping Wang
Wenjin Jiang
Chen Shen
Yangyang Ma
Lian Chen
Yaochen Xu
Jiantao Shi
Hui Zhang
Maoxiang Qian
Xiaowen Zhai
spellingShingle Zifeng Li
Hongsheng Wang
Rui Dong
Jie Man
Li Sun
Xiaowen Qian
Xiaohua Zhu
Ping Cao
Yi Yu
Jun Le
Yang Fu
Ping Wang
Wenjin Jiang
Chen Shen
Yangyang Ma
Lian Chen
Yaochen Xu
Jiantao Shi
Hui Zhang
Maoxiang Qian
Xiaowen Zhai
Single-Cell RNA-seq Reveals Characteristics of Malignant Cells and Immune Microenvironment in Subcutaneous Panniculitis-Like T-Cell Lymphoma
Frontiers in Oncology
single-cell RNA-seq (scRNA-seq)
T cell malignancies
pediatric oncology
molecular diagnoses
subcutaneous panniculitis- like T-cell lymphoma
author_facet Zifeng Li
Hongsheng Wang
Rui Dong
Jie Man
Li Sun
Xiaowen Qian
Xiaohua Zhu
Ping Cao
Yi Yu
Jun Le
Yang Fu
Ping Wang
Wenjin Jiang
Chen Shen
Yangyang Ma
Lian Chen
Yaochen Xu
Jiantao Shi
Hui Zhang
Maoxiang Qian
Xiaowen Zhai
author_sort Zifeng Li
title Single-Cell RNA-seq Reveals Characteristics of Malignant Cells and Immune Microenvironment in Subcutaneous Panniculitis-Like T-Cell Lymphoma
title_short Single-Cell RNA-seq Reveals Characteristics of Malignant Cells and Immune Microenvironment in Subcutaneous Panniculitis-Like T-Cell Lymphoma
title_full Single-Cell RNA-seq Reveals Characteristics of Malignant Cells and Immune Microenvironment in Subcutaneous Panniculitis-Like T-Cell Lymphoma
title_fullStr Single-Cell RNA-seq Reveals Characteristics of Malignant Cells and Immune Microenvironment in Subcutaneous Panniculitis-Like T-Cell Lymphoma
title_full_unstemmed Single-Cell RNA-seq Reveals Characteristics of Malignant Cells and Immune Microenvironment in Subcutaneous Panniculitis-Like T-Cell Lymphoma
title_sort single-cell rna-seq reveals characteristics of malignant cells and immune microenvironment in subcutaneous panniculitis-like t-cell lymphoma
publisher Frontiers Media S.A.
series Frontiers in Oncology
issn 2234-943X
publishDate 2021-03-01
description BackgroundSubcutaneous panniculitis-like T-cell lymphoma (SPTCL) is a malignant primary T-cell lymphoma that is challenging to distinguish from autoimmune disorders and reactive panniculitides. Delay in diagnosis and a high misdiagnosis rate affect the prognosis and survival of patients. The difficulty of diagnosis is mainly due to an incomplete understanding of disease pathogenesis.MethodsWe performed single-cell RNA sequencing of matched subcutaneous lesion tissue, peripheral blood, and bone marrow from a patient with SPTCL, as well as peripheral blood, bone marrow, lymph node, and lung tissue samples from healthy donors as normal controls. We conducted cell clustering, gene expression program identification, gene differential expression analysis, and cell-cell interaction analysis to investigate the ecosystem of SPTCL.ResultsBased on gene expression profiles in a single-cell resolution, we identified and characterized the malignant cells and immune subsets from a patient with SPTCL. Our analysis showed that SPTCL malignant cells expressed a distinct gene signature, including chemokines families, cytotoxic proteins, T cell immune checkpoint molecules, and the immunoglobulin family. By comparing with normal T cells, we identified potential novel markers for SPTCL (e.g., CYTOR, CXCL13, VCAM1, and TIMD4) specifically differentially expressed in the malignant cells. We also found that macrophages and fibroblasts dominated the cell-cell communication landscape with the SPTCL malignant cells.ConclusionsThis work offers insight into the heterogeneity of subcutaneous panniculitis-like T-cell lymphoma, providing a better understanding of the transcription characteristics and immune microenvironment of this rare tumor.
topic single-cell RNA-seq (scRNA-seq)
T cell malignancies
pediatric oncology
molecular diagnoses
subcutaneous panniculitis- like T-cell lymphoma
url https://www.frontiersin.org/articles/10.3389/fonc.2021.611580/full
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spelling doaj-010951e6ad594a84a2b5a704fbe881b62021-03-18T08:40:16ZengFrontiers Media S.A.Frontiers in Oncology2234-943X2021-03-011110.3389/fonc.2021.611580611580Single-Cell RNA-seq Reveals Characteristics of Malignant Cells and Immune Microenvironment in Subcutaneous Panniculitis-Like T-Cell LymphomaZifeng Li0Hongsheng Wang1Rui Dong2Jie Man3Li Sun4Xiaowen Qian5Xiaohua Zhu6Ping Cao7Yi Yu8Jun Le9Yang Fu10Ping Wang11Wenjin Jiang12Chen Shen13Yangyang Ma14Lian Chen15Yaochen Xu16Jiantao Shi17Hui Zhang18Maoxiang Qian19Xiaowen Zhai20Department of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Pediatric Surgery, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Rheumatism and Immunology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Pathology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaDepartment of Pathology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaShanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences, Shanghai, ChinaShanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences, Shanghai, ChinaDepartment of Hematology/Oncology, Guangzhou Women and Children’s Medical Center, Guangzhou, ChinaInstitute of Pediatrics, Children’s Hospital of Fudan University, National Children's Medical Center, and the Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, Fudan University, Shanghai, ChinaDepartment of Hematology and Oncology, Children’s Hospital of Fudan University, National Children's Medical Center, Shanghai, ChinaBackgroundSubcutaneous panniculitis-like T-cell lymphoma (SPTCL) is a malignant primary T-cell lymphoma that is challenging to distinguish from autoimmune disorders and reactive panniculitides. Delay in diagnosis and a high misdiagnosis rate affect the prognosis and survival of patients. The difficulty of diagnosis is mainly due to an incomplete understanding of disease pathogenesis.MethodsWe performed single-cell RNA sequencing of matched subcutaneous lesion tissue, peripheral blood, and bone marrow from a patient with SPTCL, as well as peripheral blood, bone marrow, lymph node, and lung tissue samples from healthy donors as normal controls. We conducted cell clustering, gene expression program identification, gene differential expression analysis, and cell-cell interaction analysis to investigate the ecosystem of SPTCL.ResultsBased on gene expression profiles in a single-cell resolution, we identified and characterized the malignant cells and immune subsets from a patient with SPTCL. Our analysis showed that SPTCL malignant cells expressed a distinct gene signature, including chemokines families, cytotoxic proteins, T cell immune checkpoint molecules, and the immunoglobulin family. By comparing with normal T cells, we identified potential novel markers for SPTCL (e.g., CYTOR, CXCL13, VCAM1, and TIMD4) specifically differentially expressed in the malignant cells. We also found that macrophages and fibroblasts dominated the cell-cell communication landscape with the SPTCL malignant cells.ConclusionsThis work offers insight into the heterogeneity of subcutaneous panniculitis-like T-cell lymphoma, providing a better understanding of the transcription characteristics and immune microenvironment of this rare tumor.https://www.frontiersin.org/articles/10.3389/fonc.2021.611580/fullsingle-cell RNA-seq (scRNA-seq)T cell malignanciespediatric oncologymolecular diagnosessubcutaneous panniculitis- like T-cell lymphoma