Characterizing the cellular and molecular variabilities of peripheral immune cells in healthy recipients of BBIBP-CorV inactivated SARS-CoV-2 vaccine by single-cell RNA sequencing

Over 3 billion doses of inactivated vaccines for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) have been administered globally. However, our understanding of the immune cell functional transcription and T cell receptor (TCR)/B cell receptor (BCR) repertoire dynamics following inactiva...

Full description

Bibliographic Details
Main Authors: Renyang Tong, Lingjie Luo, Yichao Zhao, Mingze Sun, Ronghong Li, Jianmei Zhong, Yifan Chen, Liuhua Hu, Zheng Li, Jianfeng Shi, Yuyan Lyu, Li Hu, Xiao Guo, Qi Liu, Tian Shuang, Chenjie Zhang, Ancai Yuan, Lingyue Sun, Zheng Zhang, Kun Qian, Lei Chen, Wei Lin, Alex F. Chen, Feng Wang, Jun Pu
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Emerging Microbes and Infections
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2023.2187245
_version_ 1826898941959995392
author Renyang Tong
Lingjie Luo
Yichao Zhao
Mingze Sun
Ronghong Li
Jianmei Zhong
Yifan Chen
Liuhua Hu
Zheng Li
Jianfeng Shi
Yuyan Lyu
Li Hu
Xiao Guo
Qi Liu
Tian Shuang
Chenjie Zhang
Ancai Yuan
Lingyue Sun
Zheng Zhang
Kun Qian
Lei Chen
Wei Lin
Alex F. Chen
Feng Wang
Jun Pu
author_facet Renyang Tong
Lingjie Luo
Yichao Zhao
Mingze Sun
Ronghong Li
Jianmei Zhong
Yifan Chen
Liuhua Hu
Zheng Li
Jianfeng Shi
Yuyan Lyu
Li Hu
Xiao Guo
Qi Liu
Tian Shuang
Chenjie Zhang
Ancai Yuan
Lingyue Sun
Zheng Zhang
Kun Qian
Lei Chen
Wei Lin
Alex F. Chen
Feng Wang
Jun Pu
author_sort Renyang Tong
collection DOAJ
description Over 3 billion doses of inactivated vaccines for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) have been administered globally. However, our understanding of the immune cell functional transcription and T cell receptor (TCR)/B cell receptor (BCR) repertoire dynamics following inactivated SARS-CoV-2 vaccination remains poorly understood. Here, we performed single-cell RNA and TCR/BCR sequencing on peripheral blood mononuclear cells at four time points after immunization with the inactivated SARS-CoV-2 vaccine BBIBP-CorV. Our analysis revealed an enrichment of monocytes, central memory CD4+ T cells, type 2 helper T cells and memory B cells following vaccination. Single-cell TCR-seq and RNA-seq comminating analysis identified a clonal expansion of CD4+ T cells (but not CD8+ T cells) following a booster vaccination that corresponded to a decrease in the TCR diversity of central memory CD4+ T cells and type 2 helper T cells. Importantly, these TCR repertoire changes and CD4+ T cell differentiation were correlated with the biased VJ gene usage of BCR and the antibody-producing function of B cells post-vaccination. Finally, we compared the functional transcription and repertoire dynamics in immune cells elicited by vaccination and SARS-CoV-2 infection to explore the immune responses under different stimuli. Our data provide novel molecular and cellular evidence for the CD4+ T cell-dependent antibody response induced by inactivated vaccine BBIBP-CorV. This information is urgently needed to develop new prevention and control strategies for SARS-CoV-2 infection. (ClinicalTrials.gov Identifier: NCT04871932).
first_indexed 2024-03-11T16:35:13Z
format Article
id doaj.art-6942ea9b203e4df1a7d0d43f272ba194
institution Directory Open Access Journal
issn 2222-1751
language English
last_indexed 2025-02-17T06:44:22Z
publishDate 2023-12-01
publisher Taylor & Francis Group
record_format Article
series Emerging Microbes and Infections
spelling doaj.art-6942ea9b203e4df1a7d0d43f272ba1942025-01-06T13:38:29ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512023-12-0112110.1080/22221751.2023.2187245Characterizing the cellular and molecular variabilities of peripheral immune cells in healthy recipients of BBIBP-CorV inactivated SARS-CoV-2 vaccine by single-cell RNA sequencingRenyang Tong0Lingjie Luo1Yichao Zhao2Mingze Sun3Ronghong Li4Jianmei Zhong5Yifan Chen6Liuhua Hu7Zheng Li8Jianfeng Shi9Yuyan Lyu10Li Hu11Xiao Guo12Qi Liu13Tian Shuang14Chenjie Zhang15Ancai Yuan16Lingyue Sun17Zheng Zhang18Kun Qian19Lei Chen20Wei Lin21Alex F. Chen22Feng Wang23Jun Pu24Division of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaShanghai Institute of Immunology, Department of Immunology and Microbiology, State Key Laboratory of Oncogenes and Related Genes, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaInstitute for Hepatology, National Clinical Research Center for Infectious Disease, Shenzhen Third People’s Hospital; The Second Affiliated Hospital, School of Medicine, Southern University of Science and Technology, Shenzhen, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaInstitute for Developmental and Regenerative Cardiovascular Medicine, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, People’s Republic of ChinaShanghai Institute of Immunology, Department of Immunology and Microbiology, State Key Laboratory of Oncogenes and Related Genes, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDivision of Cardiology, Shanghai Immune Therapy Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaOver 3 billion doses of inactivated vaccines for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) have been administered globally. However, our understanding of the immune cell functional transcription and T cell receptor (TCR)/B cell receptor (BCR) repertoire dynamics following inactivated SARS-CoV-2 vaccination remains poorly understood. Here, we performed single-cell RNA and TCR/BCR sequencing on peripheral blood mononuclear cells at four time points after immunization with the inactivated SARS-CoV-2 vaccine BBIBP-CorV. Our analysis revealed an enrichment of monocytes, central memory CD4+ T cells, type 2 helper T cells and memory B cells following vaccination. Single-cell TCR-seq and RNA-seq comminating analysis identified a clonal expansion of CD4+ T cells (but not CD8+ T cells) following a booster vaccination that corresponded to a decrease in the TCR diversity of central memory CD4+ T cells and type 2 helper T cells. Importantly, these TCR repertoire changes and CD4+ T cell differentiation were correlated with the biased VJ gene usage of BCR and the antibody-producing function of B cells post-vaccination. Finally, we compared the functional transcription and repertoire dynamics in immune cells elicited by vaccination and SARS-CoV-2 infection to explore the immune responses under different stimuli. Our data provide novel molecular and cellular evidence for the CD4+ T cell-dependent antibody response induced by inactivated vaccine BBIBP-CorV. This information is urgently needed to develop new prevention and control strategies for SARS-CoV-2 infection. (ClinicalTrials.gov Identifier: NCT04871932).https://www.tandfonline.com/doi/10.1080/22221751.2023.2187245Inactivated SARS-CoV-2 vaccineBBIBP-CorVsingle-cell RNA sequencingsingle-cell TCR/BCR sequencingperipheral blood mononuclear cells
spellingShingle Renyang Tong
Lingjie Luo
Yichao Zhao
Mingze Sun
Ronghong Li
Jianmei Zhong
Yifan Chen
Liuhua Hu
Zheng Li
Jianfeng Shi
Yuyan Lyu
Li Hu
Xiao Guo
Qi Liu
Tian Shuang
Chenjie Zhang
Ancai Yuan
Lingyue Sun
Zheng Zhang
Kun Qian
Lei Chen
Wei Lin
Alex F. Chen
Feng Wang
Jun Pu
Characterizing the cellular and molecular variabilities of peripheral immune cells in healthy recipients of BBIBP-CorV inactivated SARS-CoV-2 vaccine by single-cell RNA sequencing
Emerging Microbes and Infections
Inactivated SARS-CoV-2 vaccine
BBIBP-CorV
single-cell RNA sequencing
single-cell TCR/BCR sequencing
peripheral blood mononuclear cells
title Characterizing the cellular and molecular variabilities of peripheral immune cells in healthy recipients of BBIBP-CorV inactivated SARS-CoV-2 vaccine by single-cell RNA sequencing
title_full Characterizing the cellular and molecular variabilities of peripheral immune cells in healthy recipients of BBIBP-CorV inactivated SARS-CoV-2 vaccine by single-cell RNA sequencing
title_fullStr Characterizing the cellular and molecular variabilities of peripheral immune cells in healthy recipients of BBIBP-CorV inactivated SARS-CoV-2 vaccine by single-cell RNA sequencing
title_full_unstemmed Characterizing the cellular and molecular variabilities of peripheral immune cells in healthy recipients of BBIBP-CorV inactivated SARS-CoV-2 vaccine by single-cell RNA sequencing
title_short Characterizing the cellular and molecular variabilities of peripheral immune cells in healthy recipients of BBIBP-CorV inactivated SARS-CoV-2 vaccine by single-cell RNA sequencing
title_sort characterizing the cellular and molecular variabilities of peripheral immune cells in healthy recipients of bbibp corv inactivated sars cov 2 vaccine by single cell rna sequencing
topic Inactivated SARS-CoV-2 vaccine
BBIBP-CorV
single-cell RNA sequencing
single-cell TCR/BCR sequencing
peripheral blood mononuclear cells
url https://www.tandfonline.com/doi/10.1080/22221751.2023.2187245
work_keys_str_mv AT renyangtong characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT lingjieluo characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT yichaozhao characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT mingzesun characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT ronghongli characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT jianmeizhong characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT yifanchen characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT liuhuahu characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT zhengli characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT jianfengshi characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT yuyanlyu characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT lihu characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT xiaoguo characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT qiliu characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT tianshuang characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT chenjiezhang characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT ancaiyuan characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT lingyuesun characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT zhengzhang characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT kunqian characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT leichen characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT weilin characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT alexfchen characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT fengwang characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing
AT junpu characterizingthecellularandmolecularvariabilitiesofperipheralimmunecellsinhealthyrecipientsofbbibpcorvinactivatedsarscov2vaccinebysinglecellrnasequencing