Integrated single-cell transcriptome analysis reveals heterogeneity of esophageal squamous cell carcinoma microenvironment

The tumor microenvironment is a highly complex ecosystem of diverse cell types, which shape cancer biology and impact the responsiveness to therapy. Here, we analyze the microenvironment of esophageal squamous cell carcinoma (ESCC) using single-cell transcriptome sequencing in 62,161 cells from bloo...

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Published inNature communications Vol. 12; no. 1; pp. 7335 - 15
Main Authors Dinh, Huy Q., Pan, Feng, Wang, Geng, Huang, Qing-Feng, Olingy, Claire E., Wu, Zhi-Yong, Wang, Shao-Hong, Xu, Xin, Xu, Xiu-E, He, Jian-Zhong, Yang, Qian, Orsulic, Sandra, Haro, Marcela, Li, Li-Yan, Huang, Guo-Wei, Breunig, Joshua J., Koeffler, H. Phillip, Hedrick, Catherine C., Xu, Li-Yan, Lin, De-Chen, Li, En-Min
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 17.12.2021
Nature Publishing Group
Nature Portfolio
Subjects
13/51
38/91
631/337/2019
631/67/1504/1477
631/67/2329
631/67/327
631/67/69
Antigen Presentation
Antigens
Biology
Biomarkers, Tumor - metabolism
Cancer
Dendritic Cells - metabolism
Esophageal cancer
Esophageal Neoplasms - genetics
Esophageal Neoplasms - immunology
Esophageal Neoplasms - pathology
Esophageal Squamous Cell Carcinoma - genetics
Esophageal Squamous Cell Carcinoma - immunology
Esophageal Squamous Cell Carcinoma - pathology
Esophagus
Fibroblasts
Gene Expression Profiling
Gene Expression Regulation, Neoplastic
Heterogeneity
Histocompatibility Antigens Class II - metabolism
Humanities and Social Sciences
Humans
Immune checkpoint inhibitors
Immune system
Immunosuppression
Impact response
multidisciplinary
Myeloid Cells - metabolism
Myofibroblasts - pathology
Prognosis
Salivary Cystatins - metabolism
Science
Science (multidisciplinary)
Single-Cell Analysis
Squamous cell carcinoma
Survival Analysis
T-Lymphocytes - metabolism
Transcriptomes
Tumor microenvironment
Tumor Microenvironment - genetics
Tumor Microenvironment - immunology
Tumors
Online AccessGet full text

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Abstract The tumor microenvironment is a highly complex ecosystem of diverse cell types, which shape cancer biology and impact the responsiveness to therapy. Here, we analyze the microenvironment of esophageal squamous cell carcinoma (ESCC) using single-cell transcriptome sequencing in 62,161 cells from blood, adjacent nonmalignant and matched tumor samples from 11 ESCC patients. We uncover heterogeneity in most cell types of the ESCC stroma, particularly in the fibroblast and immune cell compartments. We identify a tumor-specific subset of CST1 + myofibroblasts with prognostic values and potential biological significance. CST1 + myofibroblasts are also highly tumor-specific in other cancer types. Additionally, a subset of antigen-presenting fibroblasts is revealed and validated. Analyses of myeloid and T lymphoid lineages highlight the immunosuppressive nature of the ESCC microenvironment, and identify cancer-specific expression of immune checkpoint inhibitors. This work establishes a rich resource of stromal cell types of the ESCC microenvironment for further understanding of ESCC biology. The microenvironment of oesophageal squamous cell carcinomas (ESCC) is heterogeneous and can strongly impact response to treatment. Here, the authors characterize the ESCC tumour microenvironment with single-cell RNA-seq, finding CST1 + myofibroblasts with potential biological and prognostic significance as well as immunosuppression signatures.
AbstractList The tumor microenvironment is a highly complex ecosystem of diverse cell types, which shape cancer biology and impact the responsiveness to therapy. Here, we analyze the microenvironment of esophageal squamous cell carcinoma (ESCC) using single-cell transcriptome sequencing in 62,161 cells from blood, adjacent nonmalignant and matched tumor samples from 11 ESCC patients. We uncover heterogeneity in most cell types of the ESCC stroma, particularly in the fibroblast and immune cell compartments. We identify a tumor-specific subset of CST1+ myofibroblasts with prognostic values and potential biological significance. CST1+ myofibroblasts are also highly tumor-specific in other cancer types. Additionally, a subset of antigen-presenting fibroblasts is revealed and validated. Analyses of myeloid and T lymphoid lineages highlight the immunosuppressive nature of the ESCC microenvironment, and identify cancer-specific expression of immune checkpoint inhibitors. This work establishes a rich resource of stromal cell types of the ESCC microenvironment for further understanding of ESCC biology.The microenvironment of oesophageal squamous cell carcinomas (ESCC) is heterogeneous and can strongly impact response to treatment. Here, the authors characterize the ESCC tumour microenvironment with single-cell RNA-seq, finding CST1 + myofibroblasts with potential biological and prognostic significance as well as immunosuppression signatures.
The tumor microenvironment is a highly complex ecosystem of diverse cell types, which shape cancer biology and impact the responsiveness to therapy. Here, we analyze the microenvironment of esophageal squamous cell carcinoma (ESCC) using single-cell transcriptome sequencing in 62,161 cells from blood, adjacent nonmalignant and matched tumor samples from 11 ESCC patients. We uncover heterogeneity in most cell types of the ESCC stroma, particularly in the fibroblast and immune cell compartments. We identify a tumor-specific subset of CST1+ myofibroblasts with prognostic values and potential biological significance. CST1+ myofibroblasts are also highly tumor-specific in other cancer types. Additionally, a subset of antigen-presenting fibroblasts is revealed and validated. Analyses of myeloid and T lymphoid lineages highlight the immunosuppressive nature of the ESCC microenvironment, and identify cancer-specific expression of immune checkpoint inhibitors. This work establishes a rich resource of stromal cell types of the ESCC microenvironment for further understanding of ESCC biology.The tumor microenvironment is a highly complex ecosystem of diverse cell types, which shape cancer biology and impact the responsiveness to therapy. Here, we analyze the microenvironment of esophageal squamous cell carcinoma (ESCC) using single-cell transcriptome sequencing in 62,161 cells from blood, adjacent nonmalignant and matched tumor samples from 11 ESCC patients. We uncover heterogeneity in most cell types of the ESCC stroma, particularly in the fibroblast and immune cell compartments. We identify a tumor-specific subset of CST1+ myofibroblasts with prognostic values and potential biological significance. CST1+ myofibroblasts are also highly tumor-specific in other cancer types. Additionally, a subset of antigen-presenting fibroblasts is revealed and validated. Analyses of myeloid and T lymphoid lineages highlight the immunosuppressive nature of the ESCC microenvironment, and identify cancer-specific expression of immune checkpoint inhibitors. This work establishes a rich resource of stromal cell types of the ESCC microenvironment for further understanding of ESCC biology.
The tumor microenvironment is a highly complex ecosystem of diverse cell types, which shape cancer biology and impact the responsiveness to therapy. Here, we analyze the microenvironment of esophageal squamous cell carcinoma (ESCC) using single-cell transcriptome sequencing in 62,161 cells from blood, adjacent nonmalignant and matched tumor samples from 11 ESCC patients. We uncover heterogeneity in most cell types of the ESCC stroma, particularly in the fibroblast and immune cell compartments. We identify a tumor-specific subset of CST1 + myofibroblasts with prognostic values and potential biological significance. CST1 + myofibroblasts are also highly tumor-specific in other cancer types. Additionally, a subset of antigen-presenting fibroblasts is revealed and validated. Analyses of myeloid and T lymphoid lineages highlight the immunosuppressive nature of the ESCC microenvironment, and identify cancer-specific expression of immune checkpoint inhibitors. This work establishes a rich resource of stromal cell types of the ESCC microenvironment for further understanding of ESCC biology. The microenvironment of oesophageal squamous cell carcinomas (ESCC) is heterogeneous and can strongly impact response to treatment. Here, the authors characterize the ESCC tumour microenvironment with single-cell RNA-seq, finding CST1 + myofibroblasts with potential biological and prognostic significance as well as immunosuppression signatures.
The tumor microenvironment is a highly complex ecosystem of diverse cell types, which shape cancer biology and impact the responsiveness to therapy. Here, we analyze the microenvironment of esophageal squamous cell carcinoma (ESCC) using single-cell transcriptome sequencing in 62,161 cells from blood, adjacent nonmalignant and matched tumor samples from 11 ESCC patients. We uncover heterogeneity in most cell types of the ESCC stroma, particularly in the fibroblast and immune cell compartments. We identify a tumor-specific subset of CST1 + myofibroblasts with prognostic values and potential biological significance. CST1 + myofibroblasts are also highly tumor-specific in other cancer types. Additionally, a subset of antigen-presenting fibroblasts is revealed and validated. Analyses of myeloid and T lymphoid lineages highlight the immunosuppressive nature of the ESCC microenvironment, and identify cancer-specific expression of immune checkpoint inhibitors. This work establishes a rich resource of stromal cell types of the ESCC microenvironment for further understanding of ESCC biology.
The tumor microenvironment is a highly complex ecosystem of diverse cell types, which shape cancer biology and impact the responsiveness to therapy. Here, we analyze the microenvironment of esophageal squamous cell carcinoma (ESCC) using single-cell transcriptome sequencing in 62,161 cells from blood, adjacent nonmalignant and matched tumor samples from 11 ESCC patients. We uncover heterogeneity in most cell types of the ESCC stroma, particularly in the fibroblast and immune cell compartments. We identify a tumor-specific subset of CST1 myofibroblasts with prognostic values and potential biological significance. CST1 myofibroblasts are also highly tumor-specific in other cancer types. Additionally, a subset of antigen-presenting fibroblasts is revealed and validated. Analyses of myeloid and T lymphoid lineages highlight the immunosuppressive nature of the ESCC microenvironment, and identify cancer-specific expression of immune checkpoint inhibitors. This work establishes a rich resource of stromal cell types of the ESCC microenvironment for further understanding of ESCC biology.
The microenvironment of oesophageal squamous cell carcinomas (ESCC) is heterogeneous and can strongly impact response to treatment. Here, the authors characterize the ESCC tumour microenvironment with single-cell RNA-seq, finding CST1 + myofibroblasts with potential biological and prognostic significance as well as immunosuppression signatures.
ArticleNumber 7335
Author Li, Li-Yan
Yang, Qian
Li, En-Min
Wu, Zhi-Yong
He, Jian-Zhong
Koeffler, H. Phillip
Lin, De-Chen
Xu, Li-Yan
Hedrick, Catherine C.
Xu, Xin
Xu, Xiu-E
Wang, Geng
Olingy, Claire E.
Huang, Guo-Wei
Pan, Feng
Orsulic, Sandra
Haro, Marcela
Wang, Shao-Hong
Huang, Qing-Feng
Breunig, Joshua J.
Dinh, Huy Q.
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  surname: Dinh
  fullname: Dinh, Huy Q.
  email: huy.dinh@wisc.edu
  organization: McArdle Laboratory for Cancer Research, University of Wisconsin-Madison School of Medicine and Public Health, Division of Inflammation Biology, La Jolla Institute for Immunology
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  surname: Pan
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  organization: Guangdong Provincial Key Laboratory of Infectious Diseases and Molecular Immunopathology, The Key Laboratory of Molecular Biology for High Cancer Incidence Coastal Chaoshan Area, Shantou University Medical College, Guangdong Esophageal Cancer Research Institute, Shantou Sub-center
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  organization: Guangdong Esophageal Cancer Research Institute, Shantou Sub-center, Department of Thoracic Surgery, Cancer Hospital of Shantou University Medical College
– sequence: 4
  givenname: Qing-Feng
  orcidid: 0000-0003-1594-8884
  surname: Huang
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  organization: Guangdong Provincial Key Laboratory of Infectious Diseases and Molecular Immunopathology, The Key Laboratory of Molecular Biology for High Cancer Incidence Coastal Chaoshan Area, Shantou University Medical College, Guangdong Esophageal Cancer Research Institute, Shantou Sub-center
– sequence: 5
  givenname: Claire E.
  surname: Olingy
  fullname: Olingy, Claire E.
  organization: Division of Inflammation Biology, La Jolla Institute for Immunology
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  givenname: Zhi-Yong
  surname: Wu
  fullname: Wu, Zhi-Yong
  organization: Shantou Central Hospital
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  givenname: Shao-Hong
  surname: Wang
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  organization: Shantou Central Hospital
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  givenname: Xin
  surname: Xu
  fullname: Xu, Xin
  organization: Guangdong Provincial Key Laboratory of Infectious Diseases and Molecular Immunopathology, The Key Laboratory of Molecular Biology for High Cancer Incidence Coastal Chaoshan Area, Shantou University Medical College, Guangdong Esophageal Cancer Research Institute, Shantou Sub-center
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  organization: Department of Medicine, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center
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  orcidid: 0000-0001-5119-8721
  surname: Orsulic
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  organization: Department of Obstetrics and Gynecology and Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, David Geffen School of Medicine at UCLA
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  email: nmli@stu.edu.cn
  organization: Guangdong Provincial Key Laboratory of Infectious Diseases and Molecular Immunopathology, The Key Laboratory of Molecular Biology for High Cancer Incidence Coastal Chaoshan Area, Shantou University Medical College, Guangdong Esophageal Cancer Research Institute, Shantou Sub-center
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34921160$$D View this record in MEDLINE/PubMed
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SSID ssj0000391844
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Snippet The tumor microenvironment is a highly complex ecosystem of diverse cell types, which shape cancer biology and impact the responsiveness to therapy. Here, we...
The microenvironment of oesophageal squamous cell carcinomas (ESCC) is heterogeneous and can strongly impact response to treatment. Here, the authors...
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pubmedcentral
proquest
pubmed
crossref
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SourceType Open Website
Open Access Repository
Aggregation Database
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Enrichment Source
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StartPage 7335
SubjectTerms 13/51
38/91
631/337/2019
631/67/1504/1477
631/67/2329
631/67/327
631/67/69
Antigen Presentation
Antigens
Biology
Biomarkers, Tumor - metabolism
Cancer
Dendritic Cells - metabolism
Esophageal cancer
Esophageal Neoplasms - genetics
Esophageal Neoplasms - immunology
Esophageal Neoplasms - pathology
Esophageal Squamous Cell Carcinoma - genetics
Esophageal Squamous Cell Carcinoma - immunology
Esophageal Squamous Cell Carcinoma - pathology
Esophagus
Fibroblasts
Gene Expression Profiling
Gene Expression Regulation, Neoplastic
Heterogeneity
Histocompatibility Antigens Class II - metabolism
Humanities and Social Sciences
Humans
Immune checkpoint inhibitors
Immune system
Immunosuppression
Impact response
multidisciplinary
Myeloid Cells - metabolism
Myofibroblasts - pathology
Prognosis
Salivary Cystatins - metabolism
Science
Science (multidisciplinary)
Single-Cell Analysis
Squamous cell carcinoma
Survival Analysis
T-Lymphocytes - metabolism
Transcriptomes
Tumor microenvironment
Tumor Microenvironment - genetics
Tumor Microenvironment - immunology
Tumors
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Title Integrated single-cell transcriptome analysis reveals heterogeneity of esophageal squamous cell carcinoma microenvironment
URI https://link.springer.com/article/10.1038/s41467-021-27599-5
https://www.ncbi.nlm.nih.gov/pubmed/34921160
https://www.proquest.com/docview/2611009585
https://www.proquest.com/docview/2611652497
https://pubmed.ncbi.nlm.nih.gov/PMC8683407
https://doaj.org/article/2e80dc52b5e14a5c9cab19a0f4a82e35
Volume 12
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