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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Background
Nanomaterials to combat SARS-CoV-2: Strategies to prevent, diagnose and treat COVID-19
Valenzuela-Fernández, A., Cabrera-Rodríguez, R., Ciuffreda, L., Pérez-Yanes, S., Estévez‐Herrera, J., González‐Montelongo, R., Alcoba-Flórez, J., Trujillo‐González, R., de Artola, D. G.-M., Gil-Campesino, H., et al. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.1052436 · Cited by 8
Vaccine-elicited B- and T-cell immunity to SARS-CoV-2 is impaired in chronic lung disease patients
Liu, H., Aviszus, K., Zelarney, P. T., Liao, S., Gerber, A. N., Make, B. J., Wechsler, M. E., Marrack, P., & Reinhardt, R. L. (2023) · ERJ Open Research · doi:10.1183/23120541.00400-2023 · Cited by 7
COVID-19, des vaccins à la vitesse de l’éclair
Feraoun, Y., Maisonnasse, P., Grand, R. L., & Beignon, A. (2021) · médecine/sciences · doi:10.1051/medsci/2021094 · Cited by 9
Immunogenicity of SARS-CoV-2 Trimeric Spike Protein Associated to Poly(I:C) Plus Alum
dos-Santos, J. S., Firmino-Cruz, L., da Fonseca-Martins, A. M., Oliveira-Maciel, D., Pérez, G., Pereira, V. A. R., Dumard, C. H., Guedes-da-Silva, F. H., Santos, A. C. V., Leandro, M. D. S., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.884760 · Cited by 7
Trichinella spiralis Infection Inhibits the Efficacy of RBD Protein of SARS-CoV-2 Vaccination via Regulating Humoral and Cellular Immunity
Zhu, F., Zheng, W., Gong, Y., Zhang, J., Yu, Y., Zhang, J., Liu, M., Guan, F., & Lei, J. (2024) · Vaccines · doi:10.3390/vaccines12070729 · Cited by 6
“Given the widespread prevalence of helminth infections around the world, integrating our ﬁndings into the global antiviral vaccination strategy, deworming therapy needs to be considered when implementing COVID-19 vaccination strategies.”
Background
An oral vaccine based on the Ad5 vector with a double-stranded RNA adjuvant protects mice against respiratory syncytial virus
Chai, P., Shi, Y., Yu, J., Liu, X., Yang, M., Li, D., Li, K., Li, S., Kong, X., Zhang, Q., et al. (2024) · International Immunopharmacology · doi:10.1016/j.intimp.2024.113970 · Cited by 6
Immunological mechanisms of mRNA vaccines for infectious diseases
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“In mice, mRNA vaccines for SARS-CoV-2 elicit antigen-specific GC B cells, plasma cells and memory B cells more efficiently than an AddaVax-adjuvanted protein subunit vaccine 73,76 , resulting in a superior production of binding and neutralizing antibodies.”
Self-citation
A third SARS-CoV-2 mRNA vaccine dose in people receiving hemodialysis overcomes B cell defects but elicits a skewed CD4+ T cell profile
Sannier, G., Nicolas, A., Dubé, M., Marchitto, L., Nayrac, M., Tastet, O., Chatterjee, D., Tauzin, A., Lima-Barbosa, R., Laporte, M., et al. (2023) · Cell Reports Medicine · doi:10.1016/j.xcrm.2023.100955 · Cited by 6
pGM-CSF as an adjuvant in DNA vaccination against SARS-CoV-2
Liu, C., Xue, R., Li, G.-C., Zhang, Y., Wu, W.-Y., Liu, J.-Y., Feng, R., Jin, Z., Deng, Y., Jin, Z.-L., et al. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.130660 · Cited by 6
Plasma EV-miRNAs as Potential Biomarkers of COVID-19 Vaccine Immune Response in Cancer Patients
Almeida, B., Dias, T. R., Cruz, P., Sousa‐Pimenta, M., Teixeira, A. L., Pereira, C. E., Costa‐Silva, B., Oliveira, J., Medeiros, R., & Dias, F. (2024) · Vaccines · doi:10.3390/vaccines12080848 · Cited by 6
“…(NAbs) against SARS-CoV-2 spike proteins, proposed as the major correlate of protection, promoting robust germinal center responses in humans, and resulting in memory B cells that are specific for both the full-length SARS-CoV-2 spike protein and the spike-receptor-binding domain (RBD) [18–20].”
Background
Ipsilateral or contralateral boosting of mice with mRNA vaccines confers equivalent immunity and protection against a SARS-CoV-2 Omicron strain
Ying, B., Liang, C.-Y., Desai, P., Scheaffer, S. M., Elbashir, S. M., Edwards, D. K., Thackray, L. B., & Diamond, M. (2024) · Journal of Virology · doi:10.1128/jvi.00574-24 · Cited by 8
Fc-empowered exosomes with superior epithelial layer transmission and lung distribution ability for pulmonary vaccination
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“Fc endowed the exosomes with good lung epithelial layer transmission ability via FcRn-mediated transcytosis [40], Lamp2b served as an exosome membrane anchor to increase the fusion protein density [41], and RBD played a vital role in activating the anti-viral immune response [42].”
Background
Impact of Metabolic States on SARS-CoV-2 Vaccine Responses in Mouse Models of Obesity and Diabetes
Smith, O. A., Fujimoto, B., Wong, T. A. S., To, A., Odo, T., Ball, A. H., Haun, B. K., Muramatsu, H., Tam, Y. K., Pardi, N., et al. (2024) · COVID · doi:10.3390/covid5010002 · Cited by 7
Self-citation
Looking beyond the origin of SARS-CoV-2: Significant strategic aspects during the five-year journey of COVID-19 vaccine development
Chakraborty, C., Lo, Y.-H., Bhattacharya, M., Das, A., & Wen, Z. (2025) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2025.102527 · Cited by 8
“89,194,195 However, this is a great recognition to the COVID-19 vaccine researcher for their contribution to the vaccine development field.”
Immunologically relevant aspects of the new COVID-19 vaccines—an ÖGAI (Austrian Society for Allergology and Immunology) and AeDA (German Society for Applied Allergology) position paper
Untersmayr, E., Förster‐Waldl, E., Bonelli, M. M., Boztuǧ, K., Brunner, P. M., Eiwegger, T., Eller, K., Göschl, L., Grabmeier‐Pfistershammer, K., Hötzenecker, W., et al. (2021) · Allergo Journal International · doi:10.1007/s40629-021-00178-2 · Cited by 7
Delivering an mRNA vaccine using a lymphatic drug delivery device improves humoral and cellular immunity against SARS-CoV-2
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“…of plasma B cells do diﬀerentiate into memory B cells following infection and/or vaccination, leading to persistent germinal center formation within LNs where somatic hypermutation takes place ( Lederer et al., 2020 ; Gaebler et al., 2021 ; Turner et al., 2021 ; Laidlaw and Ellebedy, 2022 ) .”
Intradermal administration of DNA vaccine targeting Omicron SARS-CoV-2 via pyro-drive jet injector provides the prolonged neutralizing antibody production via germinal center reaction
Hayashi, H., Sun, J., Yanagida, Y., Otera, T., Tai, J. A., Nishikawa, T., Yamashita, K., Sakaguchi, N., Yoshida, S., Baba, S., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-40172-y · Cited by 6
Pre-clinical models to define correlates of protection for SARS-CoV-2
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Protection from SARS-CoV-2 Delta one year after mRNA-1273 vaccination in nonhuman primates is coincident with an anamnestic antibody response in the lower airwayPreprint
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A SARS-CoV-2 vaccine on an NIR-II/SWIR emitting nanoparticle platform
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“Mouse experiments demonstrated that SARS- CoV-2 mRNA vaccines elicit potent GC B cells responses and T FH cells, closely intertwined with an efficient induction of SARS- CoV-2–specific neutralizing antibodies and MBC ( 76 ).”
An mRNA vaccine encoding the Ebola virus glycoprotein induces high neutralizing antibody titers and provides strong protection against lethal infections in mouse models
Stromberg, Z. R., Silva, E. E., Johnston, S. C., Johnson, D. M., Hall, D. E., Adjei, E., Altin, J. A., Abisoye-Ogunniyan, A., Gollott, T. R., He, W., et al. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1682418 · Cited by 5
mRNA-based influenza vaccine expands the B cell response breadth in humans
Matz, H. C., Yu, T.-G., Dixit, K., Kikawa, C., Zhou, J. Q., Alzua, G. P., Peyton, L., Madsen, A., Han, F., Farrell, A. G., et al. (2026) · Nature Immunology · doi:10.1038/s41590-026-02569-5 · Cited by 12
“In the context of SARS-CoV-2, mRNA vaccines have been found to induce strong GC responses in mice and humans 16,20 .”
Self-citation
Site-Specific O-glycosylation of SARS-CoV-2 Spike Protein and Its Impact on Immune and Autoimmune Responses
Hanisch, F. (2024) · Cells · doi:10.3390/cells13020107 · Cited by 5
COVID‐19 vaccination: are more jabs needed or are we now immune?
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Staggered immunization with mRNA vaccines encoding SARS-CoV-2 polymerase or spike antigens broadens the T cell epitope repertoire
Abt, E. R., Lam, A. K., Noguchi, M., Rashid, K., McLaughlin, J., Teng, P.-L., Tran, W., Cheng, D., Nesterenko, P. A., Mao, Z., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2406332121 · Cited by 6
Self-citation
Dynamics of T follicular helper cells in patients with rheumatic diseases and subsequent antibody responses in a three‐dose immunization regimen of CoronaVac
Zhou, X., Wang, Y., Huang, B., Feng, R., Zhou, X., Li, C., Zhang, X., Shao, M., Gan, Y., Jin, Y., et al. (2022) · Immunology · doi:10.1111/imm.13572 · Cited by 6
Self-citation
The Effects of CoronaVac (Sinovac) and BNT162b2 (BioNTech/ Pfizer) Vaccination on Oncologic 18F-FDG PET/CT Studies
Şan, H., & Alagöz, E. (2022) · Molecular Imaging and Radionuclide Therapy · doi:10.4274/mirt.galenos.2022.86570 · Cited by 5
Adapting to the world: The determination and plasticity of T follicular helper cells
Han, F., Zhao, Z., & Dong, C. (2022) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2022.09.018 · Cited by 6
Trimeric protein vaccine based on Beta variant elicits robust immune response against BA.4/5-included SARS-CoV-2 Omicron variants
He, C., Chen, L., Yang, J., Chen, Z., Hong, L., Hong, W., Song, X., Yang, L., Li, J., Wang, W., et al. (2023) · Molecular Biomedicine · doi:10.1186/s43556-023-00121-7 · Cited by 5
An mRNA vaccine with broad-spectrum neutralizing protection against Omicron variant sublineages BA.4/5 -included SARS-CoV-2
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Self-citation
Adaptive immunity to SARS-CoV-2 in cancer patients: The CAPTURE studyPreprint
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Humoral and Memory B Cell Responses Following SARS-CoV-2 Infection and mRNA Vaccination
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Advances in the structure-based design of protein vaccines for respiratory infectious diseases
Tie, X., Li, J., Wu, H., Weng, R., Zhang, Y., Li, J., & Chen, K. (2025) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2025.10.008 · Cited by 5
“For example, MF59 [81] a water-in-oil emulsion, has been widely used in influenza vaccines; its mechanism involves enhancing the effective presentation of antigens, thereby promoting B cell activation and antibody production [82,83], which significantly boosts the overall immune response.”
Equal Maintenance of Anti-SARS-CoV-2 Antibody Levels Induced by Heterologous and Homologous Regimens of the BNT162b2, ChAdOx1, CoronaVac and Ad26.COV2.S Vaccines: A Longitudinal Study Up to the 4th Dose of Booster
do Nascimento, T. A., Nogami, P. Y., de Oliveira, C. F., Neto, W. F. F., da Silva, C. P., Ribeiro, A. C. D. S., de Sousa, A. W., Freitas, M. N. O., Chiang, J. O., Silva, F. A., et al. (2024) · Vaccines · doi:10.3390/vaccines12070792 · Cited by 5
ChAdOx1 nCoV-19, BNT162b2 and CoronaVac Vaccines Do Not Induce as Strong Neutralising Antibodies with Broad Variant Protection as Infection and Suggest Vaccines that Induce Broader Sterilising Immunity are Essential to Stop the Pandemic
Chua, J. X., Durrant, L. G., Chok, Y. L., & Lai, O. M. (2022) · iScience · doi:10.1016/j.isci.2022.105379 · Cited by 4
Ultrasound during the COVID-19 Pandemic: A Global Approach
Lombardi, A., Luca, M. D., Fabiani, D., Sabatella, F., Giudice, C. D., Caputo, A., Cante, L. C., Gambardella, M., Palermi, S., Tavarozzi, R., et al. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12031057 · Cited by 4
Comparative single‐cell RNA sequencing analysis of immune response to inactivated vaccine and natural SARS‐CoV‐2 infection
He, S., Liu, S., Teng, X., He, J., Yang, L., Gao, J., Wu, Y., Hu, W., Dong, Z., Bei, J., et al. (2024) · Journal of Medical Virology · doi:10.1002/jmv.29577 · Cited by 4
The physiological landscape and specificity of antibody repertoires are consolidated by multiple immunizations
Csepregi, L., Hoehn, K. B., Neumeier, D., Taft, J. M., Friedensohn, S., Weber, C. R., Kummer, A., Sesterhenn, F., Correia, B. E., & Reddy, S. T. (2024) · eLife · doi:10.7554/elife.92718 · Cited by 7
Effects of nonsteroidal anti‐inflammatory drugs on ultrasound findings of mRNA COVID‐19 vaccine‐related lymphadenopathy
Akman, B., & Ahmet Turan, K. A. Y. A. (2022) · Journal of Clinical Ultrasound · doi:10.1002/jcu.23390 · Cited by 4
MicroRNAs Derived from Extracellular Vesicles: Keys to Understanding SARS-CoV-2 Vaccination Response in Cancer Patients?
Almeida, B., Dias, T. R., Teixeira, A. L., Dias, F., & Medeiros, R. (2023) · Cancers · doi:10.3390/cancers15164017 · Cited by 4
The Regulation of Nucleic Acid Vaccine Responses by the Microbiome
Johnson, A. M. F., Hager, K., Alameh, M., Van, P., Potchen, N. B., Mayer-Blackwell, K., Fiore-Gartland, A. J., Minot, S. S., Lin, P. J. C., Tam, Y. K., et al. (2023) · The Journal of Immunology · doi:10.4049/jimmunol.2300196 · Cited by 6
Self-citation
Vaccination Against SARS-CoV-2 in Immunosuppressed Patients with Rheumatic Diseases: Position Statement of the Greek Rheumatology Society
(2020) · Mediterranean Journal of Rheumatology · doi:10.31138/mjr.31.4.430 · Cited by 4
A single dose, BCG-adjuvanted COVID-19 vaccine provides sterilizing immunity against SARS-CoV-2 infection in micePreprint
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Chimeric hemagglutinin-based universal influenza mRNA vaccine induces protective immunity and bone marrow plasma cells in rhesus macaques
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Self-citation
An innovative and stable mRNA-LNP microneedle vaccine elicits humoral and multifunctional cellular immune responses
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“Alternative approaches more effectively elicit antigen-specific GC B and Tfh cell responses, which correlate with enhanced neutralizing antibody production (Lederer et al. 2020).”
Plug-and-display nanoparticle immunization of the core epitope domain induces potent neutralizing antibody and cellular immune responses against PEDV
Li, M., Chen, Y., Wang, S., Sun, X., Du, Y., Liu, S., Li, R., Chang, Z., Ding, P., & Zhang, G. (2024) · Journal of Integrative Agriculture · doi:10.1016/j.jia.2024.05.002 · Cited by 3
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A T7 autogene-mediated DNA vaccine platform for SARS-CoV-2: Overcoming DNA vaccine limitations with enhanced spike mRNA production
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Low switched memory B cells are associated with no humoral response after SARS-CoV-2 vaccine boosters in kidney transplant recipients
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Virus-Mimetic Extracellular-Vesicle Vaccine Boosts Systemic and Mucosal Immunity via Immune Recruitment
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Effectiveness of and Immune Responses to SARS-CoV-2 mRNA Vaccines and Their Mechanisms
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“Generation of germinal center (GC) B cells after SARS CoV-2 vaccination is associated with potent SARS CoV-2 neutralizing antibody responses (4).”
Background

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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