Distinct immune cell dynamics correlate with the immunogenicity and reactogenicity of SARS-CoV-2 mRNA vaccine
Two doses of Pfizer/BioNTech BNT162b2 mRNA vaccine elicit robust severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-neutralizing antibodies with frequent adverse events. Here, by applying a high-dimensional immune profiling on 92 vaccinees, we identify six vaccine-induced immune dynamics t...
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| Published in | Cell reports. Medicine Vol. 3; no. 5; p. 100631 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
17.05.2022
Elsevier |
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| Abstract | Two doses of Pfizer/BioNTech BNT162b2 mRNA vaccine elicit robust severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-neutralizing antibodies with frequent adverse events. Here, by applying a high-dimensional immune profiling on 92 vaccinees, we identify six vaccine-induced immune dynamics that correlate with the amounts of neutralizing antibodies, the severity of adverse events, or both. The early dynamics of natural killer (NK)/monocyte subsets (CD16+ NK cells, CD56high NK cells, and non-classical monocytes), dendritic cell (DC) subsets (DC3s and CD11c− Axl+ Siglec-6+ [AS]-DCs), and NKT-like cells are revealed as the distinct cell correlates for neutralizing-antibody titers, severity of adverse events, and both, respectively. The cell correlates for neutralizing antibodies or adverse events are consistently associated with elevation of interferon gamma (IFN-γ)-inducible chemokines, but the chemokine receptors CCR2 and CXCR3 are expressed in distinct manners between the two correlates: vaccine-induced expression on the neutralizing-antibody correlate and constitutive expression on the adverse-event correlate. The finding may guide vaccine strategies that balance immunogenicity and reactogenicity.
[Display omitted]
•Immune profiling of mRNA vaccinees reveals dramatic immunological changes•The dynamics of NK/monocyte subsets correlate with neutralizing-antibody response•The dynamics of dendritic cell subsets correlate with severity of adverse events•IFN-γ-inducible chemokines, but not the receptors, are related to these correlates
Takano et al. identify cellular correlates for neutralizing-antibody titers and systemic adverse events following SARS-CoV-2 mRNA vaccination. The involvement of IFN-γ-mediated pathways is proposed. The findings give insights into balancing the immunogenicity and reactogenicity of mRNA vaccine. |
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| AbstractList | Two doses of Pfizer/BioNTech BNT162b2 mRNA vaccine elicit robust severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-neutralizing antibodies with frequent adverse events. Here, by applying a high-dimensional immune profiling on 92 vaccinees, we identify six vaccine-induced immune dynamics that correlate with the amounts of neutralizing antibodies, the severity of adverse events, or both. The early dynamics of natural killer (NK)/monocyte subsets (CD16
NK cells, CD56
NK cells, and non-classical monocytes), dendritic cell (DC) subsets (DC3s and CD11c
Axl
Siglec-6
[AS]-DCs), and NKT-like cells are revealed as the distinct cell correlates for neutralizing-antibody titers, severity of adverse events, and both, respectively. The cell correlates for neutralizing antibodies or adverse events are consistently associated with elevation of interferon gamma (IFN-γ)-inducible chemokines, but the chemokine receptors CCR2 and CXCR3 are expressed in distinct manners between the two correlates: vaccine-induced expression on the neutralizing-antibody correlate and constitutive expression on the adverse-event correlate. The finding may guide vaccine strategies that balance immunogenicity and reactogenicity. Two doses of Pfizer/BioNTech BNT162b2 mRNA vaccine elicit robust severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-neutralizing antibodies with frequent adverse events. Here, by applying a high-dimensional immune profiling on 92 vaccinees, we identify six vaccine-induced immune dynamics that correlate with the amounts of neutralizing antibodies, the severity of adverse events, or both. The early dynamics of natural killer (NK)/monocyte subsets (CD16 + NK cells, CD56 high NK cells, and non-classical monocytes), dendritic cell (DC) subsets (DC3s and CD11c − Axl + Siglec-6 + [AS]-DCs), and NKT-like cells are revealed as the distinct cell correlates for neutralizing-antibody titers, severity of adverse events, and both, respectively. The cell correlates for neutralizing antibodies or adverse events are consistently associated with elevation of interferon gamma (IFN-γ)-inducible chemokines, but the chemokine receptors CCR2 and CXCR3 are expressed in distinct manners between the two correlates: vaccine-induced expression on the neutralizing-antibody correlate and constitutive expression on the adverse-event correlate. The finding may guide vaccine strategies that balance immunogenicity and reactogenicity. • Immune profiling of mRNA vaccinees reveals dramatic immunological changes • The dynamics of NK/monocyte subsets correlate with neutralizing-antibody response • The dynamics of dendritic cell subsets correlate with severity of adverse events • IFN-γ-inducible chemokines, but not the receptors, are related to these correlates Takano et al. identify cellular correlates for neutralizing-antibody titers and systemic adverse events following SARS-CoV-2 mRNA vaccination. The involvement of IFN-γ-mediated pathways is proposed. The findings give insights into balancing the immunogenicity and reactogenicity of mRNA vaccine. SummaryTwo doses of Pfizer/BioNTech BNT162b2 mRNA vaccine elicit robust severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-neutralizing antibodies with frequent adverse events. Here, by applying a high-dimensional immune profiling on 92 vaccinees, we identify six vaccine-induced immune dynamics that correlate with the amounts of neutralizing antibodies, the severity of adverse events, or both. The early dynamics of natural killer (NK)/monocyte subsets (CD16 + NK cells, CD56 high NK cells, and non-classical monocytes), dendritic cell (DC) subsets (DC3s and CD11c − Axl + Siglec-6 + [AS]-DCs), and NKT-like cells are revealed as the distinct cell correlates for neutralizing-antibody titers, severity of adverse events, and both, respectively. The cell correlates for neutralizing antibodies or adverse events are consistently associated with elevation of interferon gamma (IFN-γ)-inducible chemokines, but the chemokine receptors CCR2 and CXCR3 are expressed in distinct manners between the two correlates: vaccine-induced expression on the neutralizing-antibody correlate and constitutive expression on the adverse-event correlate. The finding may guide vaccine strategies that balance immunogenicity and reactogenicity. Two doses of Pfizer/BioNTech BNT162b2 mRNA vaccine elicit robust severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-neutralizing antibodies with frequent adverse events. Here, by applying a high-dimensional immune profiling on 92 vaccinees, we identify six vaccine-induced immune dynamics that correlate with the amounts of neutralizing antibodies, the severity of adverse events, or both. The early dynamics of natural killer (NK)/monocyte subsets (CD16+ NK cells, CD56high NK cells, and non-classical monocytes), dendritic cell (DC) subsets (DC3s and CD11c- Axl+ Siglec-6+ [AS]-DCs), and NKT-like cells are revealed as the distinct cell correlates for neutralizing-antibody titers, severity of adverse events, and both, respectively. The cell correlates for neutralizing antibodies or adverse events are consistently associated with elevation of interferon gamma (IFN-γ)-inducible chemokines, but the chemokine receptors CCR2 and CXCR3 are expressed in distinct manners between the two correlates: vaccine-induced expression on the neutralizing-antibody correlate and constitutive expression on the adverse-event correlate. The finding may guide vaccine strategies that balance immunogenicity and reactogenicity.Two doses of Pfizer/BioNTech BNT162b2 mRNA vaccine elicit robust severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-neutralizing antibodies with frequent adverse events. Here, by applying a high-dimensional immune profiling on 92 vaccinees, we identify six vaccine-induced immune dynamics that correlate with the amounts of neutralizing antibodies, the severity of adverse events, or both. The early dynamics of natural killer (NK)/monocyte subsets (CD16+ NK cells, CD56high NK cells, and non-classical monocytes), dendritic cell (DC) subsets (DC3s and CD11c- Axl+ Siglec-6+ [AS]-DCs), and NKT-like cells are revealed as the distinct cell correlates for neutralizing-antibody titers, severity of adverse events, and both, respectively. The cell correlates for neutralizing antibodies or adverse events are consistently associated with elevation of interferon gamma (IFN-γ)-inducible chemokines, but the chemokine receptors CCR2 and CXCR3 are expressed in distinct manners between the two correlates: vaccine-induced expression on the neutralizing-antibody correlate and constitutive expression on the adverse-event correlate. The finding may guide vaccine strategies that balance immunogenicity and reactogenicity. Two doses of Pfizer/BioNTech BNT162b2 mRNA vaccine elicit robust severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-neutralizing antibodies with frequent adverse events. Here, by applying a high-dimensional immune profiling on 92 vaccinees, we identify six vaccine-induced immune dynamics that correlate with the amounts of neutralizing antibodies, the severity of adverse events, or both. The early dynamics of natural killer (NK)/monocyte subsets (CD16+ NK cells, CD56high NK cells, and non-classical monocytes), dendritic cell (DC) subsets (DC3s and CD11c− Axl+ Siglec-6+ [AS]-DCs), and NKT-like cells are revealed as the distinct cell correlates for neutralizing-antibody titers, severity of adverse events, and both, respectively. The cell correlates for neutralizing antibodies or adverse events are consistently associated with elevation of interferon gamma (IFN-γ)-inducible chemokines, but the chemokine receptors CCR2 and CXCR3 are expressed in distinct manners between the two correlates: vaccine-induced expression on the neutralizing-antibody correlate and constitutive expression on the adverse-event correlate. The finding may guide vaccine strategies that balance immunogenicity and reactogenicity. [Display omitted] •Immune profiling of mRNA vaccinees reveals dramatic immunological changes•The dynamics of NK/monocyte subsets correlate with neutralizing-antibody response•The dynamics of dendritic cell subsets correlate with severity of adverse events•IFN-γ-inducible chemokines, but not the receptors, are related to these correlates Takano et al. identify cellular correlates for neutralizing-antibody titers and systemic adverse events following SARS-CoV-2 mRNA vaccination. The involvement of IFN-γ-mediated pathways is proposed. The findings give insights into balancing the immunogenicity and reactogenicity of mRNA vaccine. |
| ArticleNumber | 100631 |
| Author | Morikawa, Miwa Shinkai, Masaharu Onodera, Taishi Terahara, Kazutaka Adachi, Yu Tomii, Kentaro Sax, Nicolas Moriyama, Saya Tonouchi, Keisuke Takahashi, Yoshimasa Isogawa, Masanori Yamashita, Kazuo Kabasawa, Kiyomi Nishimura, Masashi Matsumura, Takayuki Sun, Lin Nishiyama, Ayae Takano, Tomohiro |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35545084$$D View this record in MEDLINE/PubMed |
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| Keywords | SARS-CoV-2 immune correlates innate immunity neutralizing antibodies adverse events mRNA vaccine cell dynamics |
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| Snippet | Two doses of Pfizer/BioNTech BNT162b2 mRNA vaccine elicit robust severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-neutralizing antibodies with... SummaryTwo doses of Pfizer/BioNTech BNT162b2 mRNA vaccine elicit robust severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-neutralizing antibodies... |
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| SubjectTerms | Advanced Basic Science adverse events Antibodies, Neutralizing - immunology Antibodies, Viral - immunology BNT162 Vaccine - adverse effects BNT162 Vaccine - immunology BNT162 Vaccine - therapeutic use cell dynamics COVID-19 - immunology COVID-19 - prevention & control COVID-19 Vaccines - adverse effects COVID-19 Vaccines - immunology COVID-19 Vaccines - therapeutic use Humans immune correlates innate immunity mRNA vaccine mRNA Vaccines - adverse effects mRNA Vaccines - immunology mRNA Vaccines - therapeutic use neutralizing antibodies SARS-CoV-2 SARS-CoV-2 - genetics Vaccines, Synthetic - adverse effects Vaccines, Synthetic - immunology Vaccines, Synthetic - therapeutic use |
| Title | Distinct immune cell dynamics correlate with the immunogenicity and reactogenicity of SARS-CoV-2 mRNA vaccine |
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