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Immune response and homeostasis mechanism following administration of BBIBP-CorV SARS-CoV-2 inactivated vaccine

Yin, Jianhua, Zhao, Yingze, Huang, Fubaoqian, Yang, Yunkai, Huang, Yaling, Zhuang, Zhenkun, Wang, Yanxia, Wang, Zhifeng, Lin, Xiumei, Zheng, Yuhui, Zhou, Wenwen, Wang, Shuo, Xu, Ziqian, Ye, Beiwei, Guo, Yaxin, Lei, Wenwen, Li, Lei, Tian, Jinmin, Gan, Jinxian, Wang, Hui, Wang, Wei, Ma, Peiyao, Liu, Chang, Wei, Xiaoyu, Shi, Xuyang, Wang, Zifei, Wang, Yang, Liu, Ying, Yang, Mingming, Yuan, Yue, Song, Yumo, Ma, Wen, Huang, Zhuoli, Liu, Ya, Huang, Yunting, Lu, Haorong, Liu, Peipei, Liang, Hao, Hou, Yong, Xu, Xun, Liu, Longqi, Zhang, Yuntao, Wu, Guizhen, Gao, George F., Jin, Xin, Liu, Chuanyu, Yang, Xiaoming, Liu, William J.·2023·The Innovation
DOI 10.1016/j.xinn.2022.100359PMC PMC9719934
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Graphical abstract CC BY-NC-ND · PubMed Central
Figure 1 Study design and single-cell analysis of PBMC dynamics in vaccine and placebo recipients (A) Flowchart of the study design. Eight participants received three doses of placebo or BBIBP-CorV vaccine, and blood samples were collected from these participants at eight time points divided before and after vaccinations. Then, scRNA-seq and B cell receptor dynamic analysis were conducted. Red dotted lines indicate inoculation days. (B) Uniform manifold approximation and projection (UMAP) plot shows 15 cell types of 672,114 immune cells by unsupervised clustering. Each cell type is indicated by a different color. (C) Bar plots show the number of cells in each sample and the number of cells at each time point. A, B, C, D, E, and G represent vaccine recipients, while F represents a placebo recipient. (D) Violin plots show the normalized expression levels of canonical markers defining cell types in (B). (E) Boxplots show the proportions of selected cells at all time points. p values < 0.05 (Student’s t test) are indicated.
Figure 1 Study design and single-cell analysis of PBMC dynamics in vaccine and placebo recipients (A) Flowchart of the study design. Eight participants received three doses of placebo or BBIBP-CorV vaccine, and blood samples were collected from these participants at eight time points divided before and after vaccinations. Then, scRNA-seq and B cell receptor dynamic analysis were conducted. Red dotted lines indicate inoculation days. (B) Uniform manifold approximation and projection (UMAP) plot shows 15 cell types of 672,114 immune cells by unsupervised clustering. Each cell type is indicated by a different color. (C) Bar plots show the number of cells in each sample and the number of cells at each time point. A, B, C, D, E, and G represent vaccine recipients, while F represents a placebo recipient. (D) Violin plots show the normalized expression levels of canonical markers defining cell types in (B). (E) Boxplots show the proportions of selected cells at all time points. p values < 0.05 (Student’s t test) are indicated.CC BY-NC-ND · PubMed Central
Figure 2 Dynamic changes in innate immune responses among myeloid cell subsets (A) UMAP plot shows the results of sub-clustering involving 25,361 monocytes. (B) Dot plot shows the expression levels of selected genes in the five subsets of myeloid cells. Dot color indicates mean expression level and dot size indicates the percentage of the cell expressing the gene. (C) Violin plot shows the expression levels of MHC-II and MHC-I genes in myeloid cell subsets. (D) Boxplots show the proportions of myeloid cell subsets in vaccine recipients at all time points; bar plots show the proportions of myeloid cell subsets in one placebo recipient at all time points. p values < 0.05 (Student’s t test) are indicated. (E–G) Changes in functional pathways over time in monocyte subsets, the red line indicates the median expression level of vaccine recipients, the blue line indicates the expression level of the placebo recipient, including CD16+ monocytes (E), CD4+ monocytes (F), and DCs (G). p values < 0.05 (Wilcoxon rank-sum test) are indicated. (H) Violin plot shows the dynamic changes in MHC-II expression levels over time in CD16+ monocytes. ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Wilcoxon rank-sum test). (I) Violin plots show dynamic changes in MHC-II and MHC-I expression levels over time in CD14+ monocytes. ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Wilcoxon rank-sum test).
Figure 2 Dynamic changes in innate immune responses among myeloid cell subsets (A) UMAP plot shows the results of sub-clustering involving 25,361 monocytes. (B) Dot plot shows the expression levels of selected genes in the five subsets of myeloid cells. Dot color indicates mean expression level and dot size indicates the percentage of the cell expressing the gene. (C) Violin plot shows the expression levels of MHC-II and MHC-I genes in myeloid cell subsets. (D) Boxplots show the proportions of myeloid cell subsets in vaccine recipients at all time points; bar plots show the proportions of myeloid cell subsets in one placebo recipient at all time points. p values < 0.05 (Student’s t test) are indicated. (E–G) Changes in functional pathways over time in monocyte subsets, the red line indicates the median expression level of vaccine recipients, the blue line indicates the expression level of the placebo recipient, including CD16+ monocytes (E), CD4+ monocytes (F), and DCs (G). p values < 0.05 (Wilcoxon rank-sum test) are indicated. (H) Violin plot shows the dynamic changes in MHC-II expression levels over time in CD16+ monocytes. ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Wilcoxon rank-sum test). (I) Violin plots show dynamic changes in MHC-II and MHC-I expression levels over time in CD14+ monocytes. ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Wilcoxon rank-sum test).CC BY-NC-ND · PubMed Central
Figure 3 Vaccine-mediated induction of T cell responses in T and NK cell subsets (A) UMAP plot shows the results of sub-clustering involving 557,551 T and NK cells. (B) Dot plot shows the expression levels of selected genes in the nine subsets of T and NK cells. Dot color indicates mean expression level and dot size indicates the proportion of cells expressing the gene. (C) Boxplots show the proportions of T and NK cell subsets in vaccine recipients at all time points; bar plots show the proportions of T and NK cell subsets in one placebo recipient at all time points. p values < 0.05 (Student’s t test) are indicated. (D–G) Changes in T cell activation and positive regulation of T cell activation pathways over time in T cell subsets; the red line indicates the median expression level of vaccine recipients, including activated CD4+ T cells (D), GZMK+ cytotoxic T cells (E), GZMH+ cytotoxic T cells (F), and Treg cells (G). p values < 0.05 (Wilcoxon rank-sum test) are indicated. (H–K) Violin plots show dynamic changes in the expression levels of selected genes over time in T cell subsets, including activated CD4+ T cells (H), GZMK+ cytotoxic T cells (I), GZMH+ cytotoxic T cells (J), and Treg cells (K). ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Wilcoxon rank-sum test).
Figure 3 Vaccine-mediated induction of T cell responses in T and NK cell subsets (A) UMAP plot shows the results of sub-clustering involving 557,551 T and NK cells. (B) Dot plot shows the expression levels of selected genes in the nine subsets of T and NK cells. Dot color indicates mean expression level and dot size indicates the proportion of cells expressing the gene. (C) Boxplots show the proportions of T and NK cell subsets in vaccine recipients at all time points; bar plots show the proportions of T and NK cell subsets in one placebo recipient at all time points. p values < 0.05 (Student’s t test) are indicated. (D–G) Changes in T cell activation and positive regulation of T cell activation pathways over time in T cell subsets; the red line indicates the median expression level of vaccine recipients, including activated CD4+ T cells (D), GZMK+ cytotoxic T cells (E), GZMH+ cytotoxic T cells (F), and Treg cells (G). p values < 0.05 (Wilcoxon rank-sum test) are indicated. (H–K) Violin plots show dynamic changes in the expression levels of selected genes over time in T cell subsets, including activated CD4+ T cells (H), GZMK+ cytotoxic T cells (I), GZMH+ cytotoxic T cells (J), and Treg cells (K). ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Wilcoxon rank-sum test).CC BY-NC-ND · PubMed Central
Figure 4 Dynamic changes in functional status among B cell subsets (A) UMAP plot shows the results of sub-clustering involving 75,204 B cells. (B) Dot plot shows the expression level of selected genes in four subsets of B cells. Dot color indicates mean expression level and dot size indicates the proportion of cells expressing the gene. (C) Boxplots show the proportions of memory B and plasma cells in six vaccine recipients at all time points; bar plots show the proportions of memory B and plasma cells in one placebo recipient at all time points. p values < 0.05 (Student’s t test) are indicated. (D) Line chart shows the dynamic changes in anti-receptor-binding domain IgG levels in six vaccine recipients and two placebo recipients, as determined by enzyme-linked immunosorbent assays. (E) Bar plot shows the proportion of IGHV3-23-IGHJ4 pairs in six vaccine recipients and two placebo recipients. The proportion of IGHV3-23-IGHJ4 pairs in each time point is minus the proportion on day 0. (F and G) Changes in pathways regulating B cell receptor signaling over time in memory B cells (F) and plasma cells (G); the red line indicates the median expression level of vaccine recipients, the blue line indicates the expression level of the placebo recipient. p values < 0.05 (Wilcoxon rank-sum test) are indicated. (H) Violin plot shows the expression level CD81 at dynamic time points in naive B cells. ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Wilcoxon rank-sum test). (I) Violin plots show dynamic changes in the expression levels of IGHA1, XBP1, and SSR3 over time in plasma cells. ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Wilcoxon rank-sum test).
Figure 4 Dynamic changes in functional status among B cell subsets (A) UMAP plot shows the results of sub-clustering involving 75,204 B cells. (B) Dot plot shows the expression level of selected genes in four subsets of B cells. Dot color indicates mean expression level and dot size indicates the proportion of cells expressing the gene. (C) Boxplots show the proportions of memory B and plasma cells in six vaccine recipients at all time points; bar plots show the proportions of memory B and plasma cells in one placebo recipient at all time points. p values < 0.05 (Student’s t test) are indicated. (D) Line chart shows the dynamic changes in anti-receptor-binding domain IgG levels in six vaccine recipients and two placebo recipients, as determined by enzyme-linked immunosorbent assays. (E) Bar plot shows the proportion of IGHV3-23-IGHJ4 pairs in six vaccine recipients and two placebo recipients. The proportion of IGHV3-23-IGHJ4 pairs in each time point is minus the proportion on day 0. (F and G) Changes in pathways regulating B cell receptor signaling over time in memory B cells (F) and plasma cells (G); the red line indicates the median expression level of vaccine recipients, the blue line indicates the expression level of the placebo recipient. p values < 0.05 (Wilcoxon rank-sum test) are indicated. (H) Violin plot shows the expression level CD81 at dynamic time points in naive B cells. ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Wilcoxon rank-sum test). (I) Violin plots show dynamic changes in the expression levels of IGHA1, XBP1, and SSR3 over time in plasma cells. ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Wilcoxon rank-sum test).CC BY-NC-ND · PubMed Central
Figure 5 Dynamic changes in interactions between innate and adaptive immunity (A) Boxplots show the numbers of interaction pairs among overall immune cells over time in six vaccine recipients; sample points from the same recipient are connected via lines in the same color. p values < 0.05 (Student' s t test) are indicated. (B) Bar and line plots show the numbers of interaction pairs in selected cell subsets over time in six vaccine recipients; sample points from the same recipient are connected via lines in the same color. p values < 0.05 (Student' s t test) are indicated. (C–F) Dot plots show the potential ligand-receptor pairs among innate immune cell subsets and adaptive immune cell subsets over time, including chemokine-receptor pairs indicative of interactions between monocyte and T cell subsets (C), co-stimulatory ligand-receptor pairs indicative of interactions between T cell and APC subsets (D), co-inhibitory ligand-receptor pairs indicative of interactions between T cell and APCs subsets (E), and IFNG-type II IFNR and CSF1-CSR1R pairs (F). Dot colors show the interaction scores calculated using the CellPhoneDB, while dot sizes indicate p values.
Figure 5 Dynamic changes in interactions between innate and adaptive immunity (A) Boxplots show the numbers of interaction pairs among overall immune cells over time in six vaccine recipients; sample points from the same recipient are connected via lines in the same color. p values < 0.05 (Student' s t test) are indicated. (B) Bar and line plots show the numbers of interaction pairs in selected cell subsets over time in six vaccine recipients; sample points from the same recipient are connected via lines in the same color. p values < 0.05 (Student' s t test) are indicated. (C–F) Dot plots show the potential ligand-receptor pairs among innate immune cell subsets and adaptive immune cell subsets over time, including chemokine-receptor pairs indicative of interactions between monocyte and T cell subsets (C), co-stimulatory ligand-receptor pairs indicative of interactions between T cell and APC subsets (D), co-inhibitory ligand-receptor pairs indicative of interactions between T cell and APCs subsets (E), and IFNG-type II IFNR and CSF1-CSR1R pairs (F). Dot colors show the interaction scores calculated using the CellPhoneDB, while dot sizes indicate p values.CC BY-NC-ND · PubMed Central
Figure 6 Changes in the immune response after the third dose vaccination using different booster dosing strategies (A) Flowchart of the sampling design for validation cohort 2 (n = 6, who received the third dose more than 9 months after the second injection). (B) UMAP plots show immune cells of the discovery cohort (n = 6) and validation cohort 2 (n = 5) before and after the third dose vaccination, including subsets of T and NK cells, B cells and myeloid cells by unsupervised clustering. Each cell type is indicated by a different color. (C) Comparison of neutralizing antibody titers before and after the third dose vaccination with 1 month or more than 9 month intervals between the second and third vaccinations, blue dots show the neutralizing antibody titers of vaccine recipients before the third dose vaccination, and red squares show the neutralizing antibody titers 14 days after the third injections. Median titers of groups at each time point are indicated. p values < 0.05 (paired t test and Student’s t test) are indicated. (D) Boxplots show the proportions of T cell subsets for the discovery cohort and validation cohort 2 before and after the third dose vaccination. p values < 0.05 are indicated; ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Student’s t test). (E) Violin plot shows the expression levels of selected genes in selected cell types before and after the third dose vaccination in the discovery cohort and validation cohort 2. ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Wilcoxon rank-sum test). (F) Dot plots show the potential ligand-receptor pairs among APCs and T cell subsets before and after the third dose vaccination in the discovery cohort and validation cohort 2. Dot colors show the interaction scores calculated using the CellPhoneDB, while dot sizes indicate the p values.
Figure 6 Changes in the immune response after the third dose vaccination using different booster dosing strategies (A) Flowchart of the sampling design for validation cohort 2 (n = 6, who received the third dose more than 9 months after the second injection). (B) UMAP plots show immune cells of the discovery cohort (n = 6) and validation cohort 2 (n = 5) before and after the third dose vaccination, including subsets of T and NK cells, B cells and myeloid cells by unsupervised clustering. Each cell type is indicated by a different color. (C) Comparison of neutralizing antibody titers before and after the third dose vaccination with 1 month or more than 9 month intervals between the second and third vaccinations, blue dots show the neutralizing antibody titers of vaccine recipients before the third dose vaccination, and red squares show the neutralizing antibody titers 14 days after the third injections. Median titers of groups at each time point are indicated. p values < 0.05 (paired t test and Student’s t test) are indicated. (D) Boxplots show the proportions of T cell subsets for the discovery cohort and validation cohort 2 before and after the third dose vaccination. p values < 0.05 are indicated; ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Student’s t test). (E) Violin plot shows the expression levels of selected genes in selected cell types before and after the third dose vaccination in the discovery cohort and validation cohort 2. ∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001 (Wilcoxon rank-sum test). (F) Dot plots show the potential ligand-receptor pairs among APCs and T cell subsets before and after the third dose vaccination in the discovery cohort and validation cohort 2. Dot colors show the interaction scores calculated using the CellPhoneDB, while dot sizes indicate the p values.CC BY-NC-ND · PubMed Central

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Metadata

Authors
Yin, J., Zhao, Y., Huang, F., Yang, Y., Huang, Y., Zhuang, Z., Wang, Y., Wang, Z., Lin, X., Zheng, Y., Zhou, W., Wang, S., Xu, Z., Ye, B., Guo, Y., Lei, W., Li, L., Tian, J., Gan, J., Wang, H., Wang, W., Ma, P., Liu, C., Wei, X., Shi, X., Wang, Z., Wang, Y., Liu, Y., Yang, M., Yuan, Y., Song, Y., Ma, W., Huang, Z., Liu, Y., Huang, Y., Lu, H., Liu, P., Liang, H., Hou, Y., Xu, X., Liu, L., Zhang, Y., Wu, G., Gao, G. F., Jin, X., Liu, C., Yang, X., & Liu, W. J.
Venue
The Innovation
Publisher
Elsevier BV
Published
2023-01
Volume
4
Issue
1
Pages
100359
ISSN
2666-6758
DOI
10.1016/j.xinn.2022.100359
PMC
PMC9719934
Cited by
9
References
4
Language
en
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