Single-Cell RNA Sequencing Identifies New Inflammation-Promoting Cell Subsets in Asian Patients With Chronic Periodontitis

Periodontitis is a highly prevalent chronic inflammatory disease leading to periodontal tissue breakdown and subsequent tooth loss, in which excessive host immune response accounts for most of the tissue damage and disease progression. Despite of the imperative need to develop host modulation therap...

Full description

Bibliographic Details
Main Authors: Shu-jiao Qian, Qian-ru Huang, Rui-ying Chen, Jia-ji Mo, Lin-yi Zhou, Yi Zhao, Bin Li, Hong-chang Lai
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2021.711337/full
id doaj-e1cb9c4d415f46b2acb4cc2ddb7d5197
record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Shu-jiao Qian
Shu-jiao Qian
Shu-jiao Qian
Qian-ru Huang
Rui-ying Chen
Rui-ying Chen
Rui-ying Chen
Jia-ji Mo
Jia-ji Mo
Jia-ji Mo
Lin-yi Zhou
Lin-yi Zhou
Lin-yi Zhou
Yi Zhao
Bin Li
Bin Li
Hong-chang Lai
Hong-chang Lai
Hong-chang Lai
spellingShingle Shu-jiao Qian
Shu-jiao Qian
Shu-jiao Qian
Qian-ru Huang
Rui-ying Chen
Rui-ying Chen
Rui-ying Chen
Jia-ji Mo
Jia-ji Mo
Jia-ji Mo
Lin-yi Zhou
Lin-yi Zhou
Lin-yi Zhou
Yi Zhao
Bin Li
Bin Li
Hong-chang Lai
Hong-chang Lai
Hong-chang Lai
Single-Cell RNA Sequencing Identifies New Inflammation-Promoting Cell Subsets in Asian Patients With Chronic Periodontitis
Frontiers in Immunology
single-cell sequencing
gingiva
periodontitis
inflammatory microenvironment
mucosa
author_facet Shu-jiao Qian
Shu-jiao Qian
Shu-jiao Qian
Qian-ru Huang
Rui-ying Chen
Rui-ying Chen
Rui-ying Chen
Jia-ji Mo
Jia-ji Mo
Jia-ji Mo
Lin-yi Zhou
Lin-yi Zhou
Lin-yi Zhou
Yi Zhao
Bin Li
Bin Li
Hong-chang Lai
Hong-chang Lai
Hong-chang Lai
author_sort Shu-jiao Qian
title Single-Cell RNA Sequencing Identifies New Inflammation-Promoting Cell Subsets in Asian Patients With Chronic Periodontitis
title_short Single-Cell RNA Sequencing Identifies New Inflammation-Promoting Cell Subsets in Asian Patients With Chronic Periodontitis
title_full Single-Cell RNA Sequencing Identifies New Inflammation-Promoting Cell Subsets in Asian Patients With Chronic Periodontitis
title_fullStr Single-Cell RNA Sequencing Identifies New Inflammation-Promoting Cell Subsets in Asian Patients With Chronic Periodontitis
title_full_unstemmed Single-Cell RNA Sequencing Identifies New Inflammation-Promoting Cell Subsets in Asian Patients With Chronic Periodontitis
title_sort single-cell rna sequencing identifies new inflammation-promoting cell subsets in asian patients with chronic periodontitis
publisher Frontiers Media S.A.
series Frontiers in Immunology
issn 1664-3224
publishDate 2021-09-01
description Periodontitis is a highly prevalent chronic inflammatory disease leading to periodontal tissue breakdown and subsequent tooth loss, in which excessive host immune response accounts for most of the tissue damage and disease progression. Despite of the imperative need to develop host modulation therapy, the inflammatory responses and cell population dynamics which are finely tuned by the pathological microenvironment in periodontitis remained unclear. To investigate the local microenvironment of the inflammatory response in periodontitis, 10 periodontitis patients and 10 healthy volunteers were involved in this study. Single-cell transcriptomic profilings of gingival tissues from two patients and two healthy donors were performed. Histology, immunohistochemistry, and flow cytometry analysis were performed to further validate the identified cell subtypes and their involvement in periodontitis. Based on our single-cell resolution analysis, we identified HLA-DR-expressing endothelial cells and CXCL13+ fibroblasts which are highly associated with immune regulation. We also revealed the involvement of the proinflammatory NLRP3+ macrophages in periodontitis. We further showed the increased cell-cell communication between macrophage and T/B cells in the inflammatory periodontal tissues. Our data generated an intriguing catalog of cell types and interaction networks in the human gingiva and identified new inflammation-promoting cell subtypes involved in chronic periodontitis, which will be helpful in advancing host modulation therapy.
topic single-cell sequencing
gingiva
periodontitis
inflammatory microenvironment
mucosa
url https://www.frontiersin.org/articles/10.3389/fimmu.2021.711337/full
work_keys_str_mv AT shujiaoqian singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT shujiaoqian singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT shujiaoqian singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT qianruhuang singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT ruiyingchen singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT ruiyingchen singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT ruiyingchen singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT jiajimo singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT jiajimo singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT jiajimo singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT linyizhou singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT linyizhou singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT linyizhou singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT yizhao singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT binli singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT binli singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT hongchanglai singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT hongchanglai singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
AT hongchanglai singlecellrnasequencingidentifiesnewinflammationpromotingcellsubsetsinasianpatientswithchronicperiodontitis
_version_ 1717762855192756225
spelling doaj-e1cb9c4d415f46b2acb4cc2ddb7d51972021-09-08T04:35:38ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-09-011210.3389/fimmu.2021.711337711337Single-Cell RNA Sequencing Identifies New Inflammation-Promoting Cell Subsets in Asian Patients With Chronic PeriodontitisShu-jiao Qian0Shu-jiao Qian1Shu-jiao Qian2Qian-ru Huang3Rui-ying Chen4Rui-ying Chen5Rui-ying Chen6Jia-ji Mo7Jia-ji Mo8Jia-ji Mo9Lin-yi Zhou10Lin-yi Zhou11Lin-yi Zhou12Yi Zhao13Bin Li14Bin Li15Hong-chang Lai16Hong-chang Lai17Hong-chang Lai18Department of Oral and Maxillo-facial Dentistry, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaNational Clinical Research Center for Oral Diseases, Shanghai, ChinaShanghai Key Laboratory of Stomatology, Shanghai Research Institute of Stomatology, Shanghai Jiao Tong University, Shanghai, ChinaDepartment of Immunology and Microbiology, Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Oral and Maxillo-facial Dentistry, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaNational Clinical Research Center for Oral Diseases, Shanghai, ChinaShanghai Key Laboratory of Stomatology, Shanghai Research Institute of Stomatology, Shanghai Jiao Tong University, Shanghai, ChinaDepartment of Oral and Maxillo-facial Dentistry, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaNational Clinical Research Center for Oral Diseases, Shanghai, ChinaShanghai Key Laboratory of Stomatology, Shanghai Research Institute of Stomatology, Shanghai Jiao Tong University, Shanghai, ChinaDepartment of Oral and Maxillo-facial Dentistry, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaNational Clinical Research Center for Oral Diseases, Shanghai, ChinaShanghai Key Laboratory of Stomatology, Shanghai Research Institute of Stomatology, Shanghai Jiao Tong University, Shanghai, ChinaDepartment of Immunology and Microbiology, Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Immunology and Microbiology, Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Thoracic Surgery, Shanghai Pulmonary Hospital, Tongji University School of Medicine, Shanghai, ChinaDepartment of Oral and Maxillo-facial Dentistry, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaNational Clinical Research Center for Oral Diseases, Shanghai, ChinaShanghai Key Laboratory of Stomatology, Shanghai Research Institute of Stomatology, Shanghai Jiao Tong University, Shanghai, ChinaPeriodontitis is a highly prevalent chronic inflammatory disease leading to periodontal tissue breakdown and subsequent tooth loss, in which excessive host immune response accounts for most of the tissue damage and disease progression. Despite of the imperative need to develop host modulation therapy, the inflammatory responses and cell population dynamics which are finely tuned by the pathological microenvironment in periodontitis remained unclear. To investigate the local microenvironment of the inflammatory response in periodontitis, 10 periodontitis patients and 10 healthy volunteers were involved in this study. Single-cell transcriptomic profilings of gingival tissues from two patients and two healthy donors were performed. Histology, immunohistochemistry, and flow cytometry analysis were performed to further validate the identified cell subtypes and their involvement in periodontitis. Based on our single-cell resolution analysis, we identified HLA-DR-expressing endothelial cells and CXCL13+ fibroblasts which are highly associated with immune regulation. We also revealed the involvement of the proinflammatory NLRP3+ macrophages in periodontitis. We further showed the increased cell-cell communication between macrophage and T/B cells in the inflammatory periodontal tissues. Our data generated an intriguing catalog of cell types and interaction networks in the human gingiva and identified new inflammation-promoting cell subtypes involved in chronic periodontitis, which will be helpful in advancing host modulation therapy.https://www.frontiersin.org/articles/10.3389/fimmu.2021.711337/fullsingle-cell sequencinggingivaperiodontitisinflammatory microenvironmentmucosa