SARS-CoV-2 mRNA Vaccines Foster Potent Antigen-Specific Germinal Center Responses Associated with Neutralizing Antibody Generation
Open accessAbstract
The deployment of effective vaccines against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is critical to eradicate the coronavirus disease 2019 (COVID-19) pandemic. Many licensed vaccines confer protection by inducing long-lived plasma cells (LLPCs) and memory B cells (MBCs), cell types canonically generated during germinal center (GC) reactions. Here, we directly compared two vaccine platforms-mRNA vaccines and a recombinant protein formulated with an MF59-like adjuvant-looking for their abilities to quantitatively and qualitatively shape SARS-CoV-2-specific primary GC responses over time. We demonstrated that a single immunization with SARS-CoV-2 mRNA, but not with the recombinant protein vaccine, elicited potent SARS-CoV-2-specific GC B and T follicular helper (Tfh) cell responses as well as LLPCs and MBCs. Importantly, GC responses strongly correlated with neutralizing antibody production. mRNA vaccines more efficiently induced key regulators of the Tfh cell program and influenced the functional properties of Tfh cells. Overall, this study identifies SARS-CoV-2 mRNA vaccines as strong candidates for promoting robust GC-derived immune responses.
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Human data corroborate reports that demonstrate the induction of potent germinal centre responses by SARS-CoV-2 mRNA-based vaccines in mice.
“Our data in humans corroborate reports that demonstrate the induction of potent germinal centre responses by SARS-CoV-2 mRNA-based vaccines in mice22,23.”
From SARS-CoV-2 mRNA vaccines induce persistent human germinal centre responses (2021) · cites this paper as [23]
A persistent antigen-specific germinal center B cell response and plasmablast response in blood and draining lymph nodes are elicited after vaccination with SARS-CoV-2 LNP-mRNA in humans, leading to robust and prolonged humoral immunity.
“Indeed, a persistent antigen-specific germinal center B cell response and plasmablast response in blood and draining lymph nodes are elicited after vaccination with SARS-CoV-2 LNP-mRNA in humans, leading to the development of a robust and prolonged humoral immunity.53,58”
From COVID-19 mRNA vaccines: Platforms and current developments (2022) · cites this paper as [53]
The germinal center B cell response and its regulation by CD4+ T follicular helper (Tfh) cells are of key importance for high-affinity neutralization antibody titers and long-lasting B cell responses.
“The germinal center B cell response and its regulation by CD4+ T follicular helper (Tfh) cells are of key importance for high-affinity neutralization antibody titers and long-lasting B cell responses.53,54”
From COVID-19 mRNA vaccines: Platforms and current developments (2022) · cites this paper as [53]
Absolute numbers of S-specific GC B cells and Tfh cells correlated with levels of neutralizing antibodies in mice immunized with 1mΨ-modified mRNA LNP vaccines.
“in which their absolute numbers correlated with the levels of neutralizing antibodies [74].”
From The dawn of mRNA vaccines: the COVID-19 case (2021) · cites this paper as [74]
A single immunization of mice with 1mΨ-modified mRNA LNP vaccines elicits potent S-specific GC B cells and Tfh cells.
“Pardi and colleagues recently demonstrated that a single immunization of mice with 1mΨ-modified mRNA LNP vaccines could elicit potent S-specific GC B cells and Tfh cells”
From The dawn of mRNA vaccines: the COVID-19 case (2021) · cites this paper as [74]
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“Knowing that Tfh cell responses normally peak between days 7 and 9 in mice (Baumjohann et al., 2011; Botta et al., 2017), we determined the frequencies and absolute numbers of Tfh cells induced by the mRNA vaccines and rRBDAddaVax in draining LNs 7 days post-immunization.”
Suan, D., Kräutler, N. J., Mååg, J. L. V., Butt, D., Bourne, K., Hermes, J. R., Avery, D. T., Young, C., Statham, A. L., Elliott, M., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.11.022 · Cited by 230 · see citing works
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“A previously published study also described small GC formation by microscopy after one immunization with a protein antigen inMF59 (Liang et al., 2017).”
MEK inhibitors activate Wnt signalling and induce stem cell plasticity in colorectal cancer
Zhan, T., Ambrosi, G., Wandmacher, A. M., Rauscher, B., Betge, J., Rindtorff, N., Häussler, R. S., Hinsenkamp, I., Bamberg, L., Hessling, B., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09898-0 · Cited by 189 · see citing works
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“The notion that effective nAb formation deeply relies on GC reactions has been widely studied in the HIV field (Havenar-Daughton et al., 2017).”
SARS-CoV-2 mRNA Vaccine Development Enabled by Prototype Pathogen PreparednessPreprint
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“Published work has shown that mRNA vaccines can induce GC B cells (Lindgren et al., 2017; Pardi et al., 2018a), but the kinetics of GC responses upon immunization with mRNA vaccines was not previously investigated.”
Pandemic Preparedness: Developing Vaccines and Therapeutic Antibodies For COVID-19
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“A large number of different vaccine strategies for SARS-CoV-2 are being simultaneously pursued by multiple pharmaceutical companies and laboratories around the world (Amanat and Krammer, 2020; Graham, 2020; Sempowski et al., 2020).”
Self-citationGerminal Center Selection and the Antibody Response to Influenza
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“Nevertheless, studies on other viruses such as influenza virus revealed that most human Abs to influenza are heavily mutated, and these mutations are likely critical to mediate broad protection against the virus (Victora and Wilson, 2015).”
Lofano, G., Mancini, F., Salvatore, G., Cantisani, R., Monaci, E., Carrisi, C., Tavarini, S., Sammicheli, C., Paccani, S. R., Soldaini, E., et al. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402604 · Cited by 81 · cited 9× · see citing works
“A previously published study also described small GC formation by microscopy after one immunization with a protein antigen inMF59 (Liang et al., 2017).”
Influentialマウスおよびヒトはい中心におけるCCR6は記憶B細胞前駆体,光帯を明らかにする位置と主要な低抗原親和性【Powered by NICT】
Dan, S., Nike, J. K., Jesper, L. V. M., Danyal, B., Bourne, K., Jana, R., Tullman‐Ercek, D., Young, C., Aaron, S., Michael, E., et al. (2017) · Immunity · Cited by 57 · see citing works
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Self-citationAge-related immune response heterogeneity to SARS-CoV-2 vaccine BNT162b2
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Self-citationMechanisms of innate and adaptive immunity to the Pfizer-BioNTech BNT162b2 vaccine
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A Comprehensive Review of mRNA Vaccines
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The first 12 months of COVID-19: a timeline of immunological insights
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Self-citationCOVID-19 vaccine development: milestones, lessons and prospects
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“3).(21,22,32) Upon the interaction of T cells and B cells, some activated Th cells move to the lymphatic follicles and then differentiate into Tfh cells.”
BackgroundRapid and stable mobilization of CD8+ T cells by SARS-CoV-2 mRNA vaccine
Oberhardt, V., Luxenburger, H., Kemming, J., Schulien, I., Ciminski, K., Giese, S., Csernalabics, B., Lang-Meli, J., Janowska, I., Staniek, J., et al. (2021) · Nature · doi:10.1038/s41586-021-03841-4 · Cited by 391 · see citing works
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COVID-19 mRNA vaccines: Platforms and current developments
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SARS-CoV-2 Variants, Vaccines, and Host Immunity
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mRNA-based therapeutics: looking beyond COVID-19 vaccines
Parhiz, H., Atochina‐Vasserman, E. N., & Weissman, D. (2024) · The Lancet · doi:10.1016/s0140-6736(23)02444-3 · Cited by 296 · see citing works
Self-citationSARS-CoV-2 mRNA Vaccines: Immunological Mechanism and Beyond
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“LLPCs secrete Abs, some of which are neutralizing Abs (nAbs) and can poten- tially mediate sterilizing immunity [39].”
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The germinal centre B cell response to SARS-CoV-2
Laidlaw, B. J., & Ellebedy, A. H. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-021-00657-1 · Cited by 250 · see citing works
mRNA Vaccines in the COVID-19 Pandemic and Beyond
Hogan, M. J., & Pardi, N. (2021) · Annual Review of Medicine · doi:10.1146/annurev-med-042420-112725 · Cited by 252 · see citing works
Self-citationBNT162b2 vaccination induces durable SARS-CoV-2–specific T cells with a stem cell memory phenotype
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Immunosenescence, aging and successful aging
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“35,36 However, this was achieved at RNA doses at least 10-fold greater than the lowest effective LUNAR-COV19 RNA dose (2 m g), and no virus challenge study was conducted to demonstrate protective immunity.”
Chimeric spike mRNA vaccines protect against Sarbecovirus challenge in mice
Martinez, D. R., Schäfer, A., Leist, S. R., la Cruz, G. D., West, A., Atochina‐Vasserman, E. N., Lindesmith, L. C., Pardi, N., Parks, R., Barr, M., et al. (2021) · Science · doi:10.1126/science.abi4506 · Cited by 189 · see citing works
“This mRNA LNP stimulate robust T 96 follicular helper cell activity, germinal center B cell responses, and durable long-lived plasma 97 cells and memory B cell responses (20, 28).”
BackgroundSelf-citationPowell, A. E., Zhang, K., Sanyal, M., Tang, S., Weidenbacher, P. A. B., Li, S., Pham, T. D., Pak, J. E., Chiu, W., & Kim, P. S. (2021) · ACS Central Science · doi:10.1021/acscentsci.0c01405 · Cited by 174 · see citing works
Germinal center responses to SARS-CoV-2 mRNA vaccines in healthy and immunocompromised individuals
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Self-citationPolymer nanoparticles deliver mRNA to the lung for mucosal vaccination
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“Consistent with our observations on robust cTfh induction by BNT162b2mRNA, it was shown that SARS-CoV-2mRNA vaccine had a superior capacity, in comparison to rRBD-AddaVax, to elicit potent SARS-CoV-2-specific GC B cell responses after the administration of a single vaccine dose, suggesting that GC B cells and Tfh cell…”
Prediction of lipid nanoparticles for mRNA vaccines by the machine learning algorithm
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“demonstrated that intramuscular immunization with a SARS-CoV-2 (m1Ψ) mRNA-LNP vaccine in mice induced robust spike-specific GC B cells and follicular CD4+ T cell responses [217].”
BackgroundExtended interval BNT162b2 vaccination enhances peak antibody generation
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Nanotechnology-based strategies against SARS-CoV-2 variants
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Knife’s edge: Balancing immunogenicity and reactogenicity in mRNA vaccines
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“In the application of the SARS-CoV-2 vaccine, mRNA vaccines have been well demonstrated to induce cellular immunity.(20,32) It is consistent with our findings that the MPXV quadrivalent mRNA vaccine was able to elicit excellent cellular immunity (Fig.”
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Self-citationDevelopment of an mRNA-lipid nanoparticle vaccine against Lyme disease
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“39,41,42 As anticipated, the dLNs of animals immunized with OspA mRNA-LNP exhibited signi fi cantly higher frequency and total number of OspA-speci fi c FAS + GL7 + GC B cells than in those administered either with Luc mRNA-LNP or rOspA + alum (Figures 2C and 2D).”
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“Long-lived plasma cells (LLPCs) persistently secrete Abs without the need for antigen re-exposure and are responsible for maintaining levels of circulating Abs that can prevent or hinder reinfection by pathogens (35, 36).”
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HIV mRNA Vaccines—Progress and Future Paths
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“TFH cells are important for inducing and sustaining antibody responses (Corbett et al., 2021b; Lederer et al., 2020; Painter et al., 2021; Pardi et al., 2018).”
BackgroundCellular and humoral immunogenicity of a SARS-CoV-2 mRNA vaccine in patients on haemodialysis
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“Additionally, the amount of trimer produced after mRNA immunization may be larger than the protein dose, and antigen availability may be increased as a consequence of protein expression kinetics (Pardi et al., 2015, 2018; Lederer et al., 2020).”
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Brief review of the mRNA vaccines COVID-19
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Lipid nanoparticles for mRNA delivery
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“Immunization with mRNA vaccine encoding the SARSCoV-2 RBD was demonstrated to elicit robust NAbs and memory T, B cell responses in rodents without the detection of antibodydependent enhancement (ADE) of infection.(6,7) More than 130 vaccine candidates against SARS-CoV-2 are in clinical development, and at least 55 of…”
BackgroundBreaking the mold with RNA—a “RNAissance” of life science
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“APCs which have taken up mRNA/LNP directly or antigen indirectly, traf fi c to lymph nodes where they prime CD4 and CD8 T lymphocytes and initiate germinal center reaction through T follicular helper cells, resulting in the generation of memory B cells and antibody-producing plasma cells 25,28,30 .”
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“Since host cells are responsible for antigen production, correct folding of the protein and natural glycosylation are guaranteed [7].”
BackgroundImpact of age and comorbidities on SARS-CoV-2 vaccine-induced T cell immunity
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“Hence, most SARS-CoV-2 mRNA vaccine studies have focused on characterizing the post-immunization humoral response 8 – 12 .”
B Cell Response to Vaccination
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“High single-dose immunization of mice with mRNA (15 μg) encoding the spike receptor-binding domain (RBD) [104] or mRNA of the full-length spike with cleavage mutation (30 μg) could induce sustained neutralizing antibody responses, germinal center formation [100], long-lived plasma and memory B cells, and type 1 CD4 T…”
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Follicular Helper T Cells in the Immunopathogenesis of SARS-CoV-2 Infection
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“In immunocompetent subjects, it has been suggested that the infection generates more robust GC responses than the mRNA vaccine [44] and spike-specific B cell responses differ in immunized and convalescents with striking differences in the cell composition and transcriptional profiles of circulating immune cells, possi…”
BackgroundT follicular helper 17 (Tfh17) cells are superior for immunological memory maintenance
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“As antigen-specific B cells are detected in the spleen at day 60 post-mRNA–LNP vaccination i.m. 17,18,37 , the spleen could also serve as a potential source of B M cells that could migrate into the lung when the interval between priming and intranasal boosting is prolonged.”
Fractionating a COVID-19 Ad5-vectored vaccine improves virus-specific immunity
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Distinct components of mRNA vaccines cooperate to instruct efficient germinal center responses
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- Authors
- Lederer, K., Castaño, D., Gómez Atria, D., Oguin, T. H., Wang, S., Manzoni, T. B., Muramatsu, H., Hogan, M. J., Amanat, F., Cherubin, P., Lundgreen, K. A., Tam, Y. K., Fan, S. H. Y., Eisenlohr, L. C., Maillard, I., Weissman, D., Bates, P., Krammer, F., Sempowski, G. D., Pardi, N., & Locci, M.
- Affiliations
- University of Pennsylvania (US)
- Universidad de Antioquia (CO)
- Duke University (US)
- Children's Hospital of Philadelphia (US)
- Icahn School of Medicine at Mount Sinai (US)
- Acuitas Therapeutics (Canada) (CA)
- Corresponding author
- Locci, Michela
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2020-12
- Volume
- 53
- Issue
- 6
- Pages
- 1281-1295.e5
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC7680029
- OpenAlex
- W3109969518
- Cited by
- 383
- References
- 65
- Citations by year
- 2026: 27 · 2025: 39 · 2024: 50 · 2023: 61 · 2022: 97 · 2021: 105 · 2020: 4
- FWCI
- 8.75
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Institutional Repository University of Antioquia (University of Antioquia) (publishedVersion, cc-by-nc-nd)
- Funders
- National Institutes of Health
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Keywords
- SARS-CoV-2, COVID-19 vaccines, mRNA vaccines, recombinant protein vaccine, MF59 adjuvant, germinal center reaction, T follicular helper cells, long-lived plasma cells, memory B cells, neutralizing antibodies, B cell response, vaccine platform comparison
- MeSH terms
- COVID-19, SARS-CoV-2, COVID-19 Vaccines, mRNA Vaccines, Epitopes, Antigens, Viral, B-Lymphocytes, Cells, Cultured, T-Lymphocytes, Helper-Inducer, Humans, Lymphocyte Activation, Polysorbates, Recombinant Proteins, RNA, Viral, Squalene, Vaccination, Vaccines, Synthetic, Germinal Center, Antibodies, Neutralizing
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