Cited by 383SARS-CoV-2 and COVID-19 ResearchT-cell and B-cell ImmunologyImmune responses and vaccinations

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SARS-CoV-2 mRNA Vaccines Foster Potent Antigen-Specific Germinal Center Responses Associated with Neutralizing Antibody Generation

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Lederer, Katlyn, Castaño, Diana, Gómez Atria, Daniela, Oguin, Thomas H., Wang, Sidney, Manzoni, Tomaz B., Muramatsu, Hiromi, Hogan, Michael J., Amanat, Fatima, Cherubin, Patrick, Lundgreen, Kendall A., Tam, Ying K., Fan, Steven H.Y., Eisenlohr, Laurence C., Maillard, Ivan, Weissman, Drew, Bates, Paul, Krammer, Florian, Sempowski, Gregory D., Pardi, Norbert, Locci, Michela·2020·Immunity

DOI 10.1016/j.immuni.2020.11.009PMC PMC7680029

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Abstract

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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Influential
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Influential

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Background
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Background
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Background
Germinal Centre Shutdown
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Background
Recent Advancements in mRNA Vaccines: From Target Selection to Delivery Systems
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Background
Antibody-mediated immunity to SARS-CoV-2 spike
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“11,18 Consistent with the idea of long-lived plasma cell trafﬁcking to the bone marrow, convalescent patients have reduced plasmablasts in circulation relative to those with acute illness, and the SHM footprint in the repertoire of the remaining cells was signiﬁcantly diminished from what we had…”
Background
Specific antibody response of patients with common variable immunodeficiency to BNT162b2 coronavirus disease 2019 vaccination
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Rapid induction of antigen-specific CD4 + T cells guides coordinated humoral and cellular immune responses to SARS-CoV-2 mRNA vaccinationPreprint
Painter, M. M., Mathew, D., Goel, R. R., Apostolidis, S. A., Pattekar, A., Kuthuru, O., Baxter, A. E., Herati, R. S., Oldridge, D. A., Gouma, S., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.21.440862 · Cited by 23
“…CD4+ T cells, are primed by the vaccine (Anderson et al., 2020; Angyal, 2021; Camara et al., 2021; Jackson et al., 2020; Kalimuddin et al., 2021; Lederer et al., 2020; Mazzoni et al., 2021; Prendecki et al., 2021; Sahin et al., 2020; Stamatatos et al., 2021; Tarke et al., 2021b; Woldemeskel et…”
BackgroundSelf-citation
A nucleoside-modified mRNA vaccine forming rabies virus-like particle elicits strong cellular and humoral immune responses against rabies virus infection in mice
Liu, J., Sun, J., Ding, X., Liu, W., Wang, Y., Wang, Z., Peng, H., Zhang, Y., Su, W., & Jiang, C. (2024) · Emerging Microbes & Infections · doi:10.1080/22221751.2024.2389115 · Cited by 24
“…are sufficient to elicit high Nab titres and cellular immune responses. mRNA vaccines can be rapidly manufactured and can activate GC reactions, which are required for the generation of prolonged humoral responses by eliciting long-lived plasma cells (LLPC) and memory B cells (MBC) [8,29,30].”
Background
Modulation of lipid nanoparticle-formulated plasmid DNA drives innate immune activation promoting adaptive immunity
Tursi, N. J., Tiwari, S., Bedanova, N. M., Kannan, T., Parzych, E. M., Okba, N. M. A., Liaw, K., Sárközy, A., Livingston, C., Trullen, M. I., et al. (2025) · Cell Reports Medicine · doi:10.1016/j.xcrm.2025.102035 · Cited by 27
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Thinking Quantitatively of RNA-Based Information Transfer via Extracellular Vesicles: Lessons to Learn for the Design of RNA-Loaded EVs
Piffoux, M., Volatron, J., Silva, A., & Gazeau, F. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13111931 · Cited by 24
“following assumptions: 10:1 lipid to siRNA ratio [113,114], mean nanoparticle size 80 nm.”
Method
mRNA vaccines offer hope for HIV
Morris, L. (2021) · Nature Medicine · doi:10.1038/s41591-021-01602-4 · Cited by 21
Immunogenicity of COVID ‐19 vaccines in chronic liver disease patients and liver transplant recipients: A systematic review and meta‐analysis
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The mRNA vaccine, a swift warhead against a moving infectious disease target
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“The elicitation of germinal center reaction and induction of T FH cell response was observed in the preclinical studies of mRNA vaccines against SARS-CoV-2, HIV-1 and Zika virus [75].”
Advances in the study of LNPs for mRNA delivery and clinical applications
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“Many studies [64, 68, 69] have shown that LNPs used for many preclinical studies are highly inflammatory.”
The mRNA component of LNP-mRNA vaccines triggers IFNAR-dependent immune activation which attenuates the adaptive immune response
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T Cell/B Cell Interactions in the Establishment of Protective Immunity
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Rapid progression of marginal zone B-cell lymphoma after COVID-19 vaccination (BNT162b2): A case report
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A Review of Extracellular Vesicles in COVID‐19 Diagnosis, Treatment, and Prevention
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Immune responses related to the immunogenicity and reactogenicity of COVID-19 mRNA vaccines
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Vaccination boosts protective responses and counters SARS-CoV-2-induced pathogenic memory B cellsPreprint
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“Our works confirms studies showing potent immune responses induced by anti-SARS-CoV-2 vaccines (for example, (15, 40)).”
Background
Lipid nanoparticles as adjuvant of norovirus VLP vaccine augment cellular and humoral immune responses in a TLR9- and type I IFN-dependent pathway
Dai, W., Xing, M., Sun, L., Lv, L., Wang, X., Wang, Y., Pang, X., Guo, Y., Ren, J., & Zhou, D. (2024) · Journal of Virology · doi:10.1128/jvi.01699-24 · Cited by 22
Microfluidic and Turbulent Mixing for mRNA LNP Vaccines
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“This critical pre-pandemic mRNA LNP influenza research was then rapidly applied to successfully preparing COVID-19 mRNA LNP vaccines [87–89].”
Axillary Lymphadenopathy After COVID-19 Vaccination in a Woman With Breast Cancer
Lam, D. L., & Flanagan, M. R. (2021) · JAMA · doi:10.1001/jama.2021.20010 · Cited by 19
A Novel Bacterial Protease Inhibitor Adjuvant in RBD-Based COVID-19 Vaccine Formulations Containing Alum Increases Neutralizing Antibodies, Specific Germinal Center B Cells and Confers Protection Against SARS-CoV-2 Infection in Mice
Coria, L. M., Saposnik, L. M., Castro, C. P., Castro, E. F., Bruno, L. A., Stone, W. B., Pérez, P. S., Darriba, M. L., Chemes, L. B., Alcaín, J., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.844837 · Cited by 20
“It has also been suggested that prolonged antigen availability along with continuous presentation of antigens via major histocompatibility complex class II can improve GC reactions (61).”
Background
SARS-CoV-2 spike-ferritin-nanoparticle adjuvanted with ALFQ induces long-lived plasma cells and cross-neutralizing antibodies
Shrivastava, S., Carmen, J. M., Lu, Z., Basu, S., Sankhala, R. S., Chen, W., Nguyen, P., Chang, W. C., King, J., Corbitt, C., et al. (2023) · npj Vaccines · doi:10.1038/s41541-023-00638-6 · Cited by 19
Anti-CD20 antibodies and bendamustine attenuate humoral immunity to COVID-19 vaccination in patients with B-cell non-Hodgkin lymphoma
Ishio, T., Tsukamoto, S., Yokoyama, E., Izumiyama, K., Saito, M., Muraki, H., Kobayashi, M., Mori, A., Morioka, M., & Kondo, T. (2023) · Annals of Hematology · doi:10.1007/s00277-023-05204-7 · Cited by 19
Harnessing mucosal immunity for protective vaccines
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“The mRNA–LNP injectable vaccine has been shown to elicit robust and durable GC responses in draining lymph nodes 145,146 .”
Antisense oligonucleotide: A promising therapeutic option to beat COVID ‐19
Quéméner, A. M., & Galibert, M. (2021) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1703 · Cited by 18
“They are highly potent (Lederer et al., 2020) and are able to be developed in record time, as seen with the COVID-19 outbreak, at a lower cost than conventional vaccines.”
Background
Immunity to Seasonal Coronavirus Spike Proteins Does Not Protect from SARS-CoV-2 Challenge in a Mouse Model but Has No Detrimental Effect on Protection Mediated by COVID-19 mRNA Vaccination
Amanat, F., Clark, J. J., Carreño, J. M., Strohmeier, S., Yellin, T., Meade, P. S., Bhavsar, D., Muramatsu, H., Sun, W., Coughlan, L., et al. (2023) · Journal of Virology · doi:10.1128/jvi.01664-22 · Cited by 21
Self-citation
Current innovations in mRNA vaccines for targeting multidrug-resistant ESKAPE pathogens
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Temporal Associations of B and T Cell Immunity with Robust Vaccine Responsiveness in a 16-Week Interval BNT162B2 Regimen
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“…may contribute to recovery from COVID-19 (Bange et al., 2021; Wurm et al., 2020). mRNA vaccines elicit CD4+ T cell responses (Anderson et al., 2020; Lederer et al., 2020; Painter et al., 2021; Prendecki et al., 2021; Rodda et al., 2022; Sahin et al., 2020) that are likely important determinants of…”
Background
Inhalable polymer nanoparticles for versatile mRNA delivery and mucosal vaccinationPreprint
Suberi, A., Grun, M. K., Mao, T., Israelow, B., Reschke, M., Grundler, J., Akhtar, L., Lee, T., Shin, K., Piotrowski-Daspit, A. S., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.03.22.485401 · Cited by 18
“Systemically administered mRNA vaccines elicit TFH and germinal center B cells, which strongly correlates with neutralizing antibody production (33, 34).”
Background
Nucleoside modifications of in vitro transcribed mRNA to reduce immunogenicity and improve translation of prophylactic and therapeutic antigens
Alameh, M., & Weissman, D. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-821595-1.00014-2 · Cited by 17
Self-citation
GM-CSF-activated human dendritic cells promote type 1 T follicular helper cell polarization in a CD40-dependent manner
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Mechanisms and implications of IgG4 responses to SARS-CoV-2 and other repeatedly administered vaccines
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In Vitro Investigations on Optimizing and Nebulization of IVT-mRNA Formulations for Potential Pulmonary-Based Alpha-1-Antitrypsin Deficiency Treatment
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T follicular helper cells and their impact on humoral responses during pathogen and vaccine challenge
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Altering the mRNA-1273 dosing interval impacts the kinetics, quality, and magnitude of immune responses in mice
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Comparison of antigen-specific B cell responses reveals disparity in immunogenicity and memory B cell formation across COVID-19 vaccine platforms
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“It is noteworthy that a single dose of the mRNA vaccine elicits a relatively short-lived GC response in mice, as shown in this and the previous studies [90].”
Intranasal inoculation of IFN-λ resolves SARS-CoV-2 lung infection via the rapid reduction of viral burden and improvement of tissue damage
Shin, H., Kim, S.-J., Jo, A., Won, J., Gil, C. H., Yoon, S. Y., Cha, H., & Kim, H. J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1009424 · Cited by 15
“However, interest in effective SARS-CoV-2 therapeutics is increasing rapidly, and the emergence of SARS-CoV-2 variants has highlighted a need for new viral therapeutics (3, 4).”
Background
Optimization of an LNP-mRNA vaccine candidate targeting SARS-CoV-2 receptor-binding domainPreprint
Kobiyama, K., Imai, M., Jounai, N., Nakayama, M., Hioki, K., Iwatsuki‐Horimoto, K., Yamayoshi, S., Tsuchida, J., Niwa, T., Suzuki, T., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.04.433852 · Cited by 15
Molecular engineering tools for the development of vaccines against infectious diseases: current status and future directions
Xue, W., Li, T., Gu, Y., Li, S., & Xia, N. (2023) · Expert Review of Vaccines · doi:10.1080/14760584.2023.2227699 · Cited by 19
“Several preclinical studies have shown high inflammatory reactions associated with lipid nanoparticles (LNPs) [172,173].”
Background
Ipsilateral immunization after a prior SARS-CoV-2 mRNA vaccination elicits superior B cell responses compared to contralateral immunization
Jiang, W., Maldeney, A. R., Yuan, X., Richer, M. J., Renshaw, S. E., & Luo, W. (2024) · Cell Reports · doi:10.1016/j.celrep.2023.113665 · Cited by 16
“Previous studies have shown that a single dose of mRNA vaccination can result in persistent GC response, 4,6–8 suggesting the presence of different microenvironments in ipsilateral LNs compared to contralateral LNs at the time of the booster immunization.”
Bivalent norovirus mRNA vaccine elicits cellular and humoral responses protecting human enteroids from GII.4 infection
Atochina‐Vasserman, E. N., Lindesmith, L. C., Mirabelli, C., Ona, N. A., Reagan, E. K., Brewer-Jensen, P. D., Mercado-López, X., Shahnawaz, H., Meshanni, J. A., Baboo, I., et al. (2024) · npj Vaccines · doi:10.1038/s41541-024-00976-z · Cited by 14
Self-citation
Comparative immunogenicity analysis of intradermal versus intramuscular administration of SARS-CoV-2 RBD epitope peptide-based immunogen In vivo
Yadav, N., Vishwakarma, P., Khatri, R., Siddqui, G., Awasthi, A., Ahmed, S., & Samal, S. (2021) · Microbes and Infection · doi:10.1016/j.micinf.2021.104843 · Cited by 14
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Prime-Pull Immunization of Mice with a BcfA-Adjuvanted Vaccine Elicits Sustained Mucosal Immunity That Prevents SARS-CoV-2 Infection and Pathology
Shamseldin, M. M., Zani, A., Kenney, A., Evans, J. P., Zeng, C., Read, K. A., Caution, K., Hall, J. M., Brown, J. M., Gunsch, G., et al. (2023) · The Journal of Immunology · doi:10.4049/jimmunol.2200297 · Cited by 16
Advances in understanding the formation and fate of B-cell memory in response to immunization or infection
Kealy, L. C., & Good‐Jacobson, K. L. (2021) · Oxford Open Immunology · doi:10.1093/oxfimm/iqab018 · Cited by 14
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Zhang, J. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e34577 · Cited by 13
“Studies had indicated that COVID-19 mRNA vaccines can initiate germinal center reactions and TFH cell responses specific to the SARS-CoV-2 S protein, critical to neutralizing antibody production [99,100].”
Background
Regulating Immune Responses Induced by PEGylated Messenger RNA–Lipid Nanoparticle Vaccine
Jo, H., Jeoung, J., Kim, W., & Jeoung, D. (2024) · Vaccines · doi:10.3390/vaccines13010014 · Cited by 17
The nasal symbiont Staphylococcus species restricts the transcription of SARS-CoV-2 entry factors in human nasal epithelium
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Antigen transfer from non-APCs to APCs impacts the efficacy and safety of protein- and mRNA- based vaccines
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Physical Characteristics of Injection Site Pain After COVID-19 mRNA BNT162b2 Vaccination
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A minimalist supramolecular nanovaccine forcefully propels the Tfh cell and GC B cell responses
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Antibody and T-Cell Subsets Analysis Unveils an Immune Profile Heterogeneity Mediating Long-term Responses in Individuals Vaccinated Against SARS-CoV-2
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Sustained delivery of CpG oligodeoxynucleotide by acetalated dextran microparticles augments effector response to Computationally Optimized Broadly Reactive Antigen (COBRA) influenza hemagglutinin
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A rabies mRNA vaccine provides a rapid and long-term immune response in mice
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Self-citation
M cells targeted H. pylori antigen SAM-FAdE displayed on bacterium-like particles induce protective immunity
Zhang, F., Chen, J., Zhang, Z., Wu, J., Qu, Y., Ni, L., Zhang, G., Liu, K., & Guo, L. (2025) · Journal of Nanobiotechnology · doi:10.1186/s12951-025-03111-9 · Cited by 12

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: Lederer, Katlyn
Castaño, Diana
Oguin, Thomas H.
Wang, Sidney
Manzoni, Tomaz B.
Muramatsu, Hiromi
Amanat, Fatima
Lundgreen, Kendall A.
Tam, Ying K.
Eisenlohr, Laurence C.
Maillard, Ivan
Weissman, Drew
Bates, Paul
Krammer, Florian
Sempowski, Gregory D.
Pardi, Norbert
Locci, Michela
Venue: Immunity
Publisher: Elsevier BV
Published: 2020-12
Volume: 53
Issue: 6
Pages: 1281-1295.e5
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/j.immuni.2020.11.009
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 379 d)
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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SARS-CoV-2 mRNA Vaccines Foster Potent Antigen-Specific Germinal Center Responses Associated with Neutralizing Antibody Generation

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