Induction of robust B cell responses after influenza mRNA vaccination Is accompanied by circulating hemagglutinin-specific ICOS+ PD-1+ CXCR3+ T follicular helper cells
Open accessAbstract
Modified mRNA vaccines have developed into an effective and well-tolerated vaccine platform that offers scalable and precise antigen production. Nevertheless, the immunological events leading to strong antibody responses elicited by mRNA vaccines are largely unknown. In this study, we demonstrate that protective levels of antibodies to hemagglutinin were induced after two immunizations of modified non-replicating mRNA encoding influenza H10 encapsulated in lipid nanoparticles (LNP) in non-human primates. While both intradermal (ID) and intramuscular (IM) administration induced protective titers, ID delivery generated this response more rapidly. Circulating H10-specific memory B cells expanded after each immunization, along with a transient appearance of plasmablasts. The memory B cell pool waned over time but remained detectable throughout the 25-week study. Following prime immunization, H10-specific plasma cells were found in the bone marrow and persisted over time. Germinal centers were formed in vaccine-draining lymph nodes along with an increase in circulating H10-specific ICOS+ PD-1+ CXCR3+ T follicular helper cells, a population shown to correlate with high avidity antibody responses after seasonal influenza vaccination in humans. Collectively, this study demonstrates that mRNA/LNP vaccines potently induce an immunological repertoire associated with the generation of high magnitude and quality antibodies.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Intramuscular delivery of 1mΨ-modified mRNA vaccines results in rapid and potent induction of follicular T helper cells (Tfh).
“several studies have shown that i.m. delivery of 1mΨ-modified mRNA vaccines results in the rapid and potent induction of follicular T helper cells (Tfh) [71,72].”
From The dawn of mRNA vaccines: the COVID-19 case (2021) · cites this paper as [71]
Robust and sustained antigen expression of nucleoside-modified mRNA is associated with more optimal antibody responses compared to unmodified mRNA.
“Additionally, the robust and sustained antigen expression of nucleoside-modified mRNA was associated with more optimal antibody responses compared to unmodified mRNA [12,13].”
From Three decades of messenger RNA vaccine development (2019) · cites this paper as [13]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Follicular Helper CD4 T Cells (T <sub>FH</sub> )
Crotty, S. (2011) · Annual Review of Immunology · doi:10.1146/annurev-immunol-031210-101400 · Cited by 2,738 · see citing works
mRNA-based therapeutics--developing a new class of drugs
Sahin, U., Karikó, K., & Türeci, Ö. (2014) · Nature Reviews Drug Discovery · doi:10.1038/nrd4278 · Cited by 2,474 · see citing works
Interferon-γ and B Cell Stimulatory Factor-1 Reciprocally Regulate Ig Isotype Production
Snapper, C. M., & Paul, W. E. (1987) · Science · doi:10.1126/science.3107127 · Cited by 1,927 · see citing works
Victora, G. D., & Nussenzweig, M. C. (2012) · Annual Review of Immunology · doi:10.1146/annurev-immunol-020711-075032 · Cited by 1,878 · see citing works
Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis
Osterholm, M. T., Kelley, N. S., Sommer, A., & Belongia, E. A. (2012) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(11)70295-x · Cited by 1,789 · see citing works
Systemic RNA delivery to dendritic cells exploits antiviral defence for cancer immunotherapy
Kranz, L. M., Diken, M., Haas, H., Kreiter, S., Loquai, C., Reuter, K. C., Meng, M., Fritz, D., Vascotto, F., Hefesha, H., et al. (2016) · Nature · doi:10.1038/nature18300 · Cited by 1,771 · see citing works
Correlates of protection induced by vaccination
Plotkin, S. A. (2010) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00131-10 · Cited by 1,745 · see citing works
Morita, R., Schmitt, N., Bentebibel, S.-E., Ranganathan, R., Bourdery, L., Zurawski, G., Foucat, E., Dullaers, M., Oh, S., Sabzghabaei, N., et al. (2011) · Immunity · doi:10.1016/j.immuni.2010.12.012 · Cited by 1,563 · see citing works
The generation of antibody-secreting plasma cells
Nutt, S. L., Hodgkin, P. D., Tarlinton, D. M., & Corcoran, L. M. (2015) · Nature reviews. Immunology · doi:10.1038/nri3795 · Cited by 1,446 · see citing works
Safety and efficacy of RNAi therapy for transthyretin amyloidosis
Coelho, T., Adams, D., Silva, A., Lozeron, P., Hawkins, P. N., Mant, T., Perez, J., Chiesa, J., Warrington, S., Tranter, E., et al. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1208760 · Cited by 971 · see citing works
Modified mRNA vaccines protect against zika virus infection
Richner, J. M., Himansu, S., Dowd, K. A., Butler, S. L., Salazar, V., Fox, J. M., Julander, J. G., Tang, W. W., Shresta, S., Pierson, T. C., et al. (2017) · Cell · doi:10.1016/j.cell.2017.02.017 · Cited by 909 · see citing works
Zika virus protection by a single low-dose nucleoside-modified mRNA vaccination
Pardi, N., Hogan, M. J., Pelc, R. S., Muramatsu, H., Andersen, H., DeMaso, C. R., Dowd, K. A., Sutherland, L. L., Scearce, R. M., Parks, R., et al. (2017) · Nature · doi:10.1038/nature21428 · Cited by 884 · see citing works
CellProfiler™: Free, Versatile Software for Automated Biological Image Analysis
Lamprecht, M. R., Sabatini, D. M., & Carpenter, A. E. (2007) · BioTechniques · doi:10.2144/000112257 · Cited by 880 · see citing works
Locci, M., Havenar‐Daughton, C., Landais, E., Wu, J. E., Kroenke, M. A., Arlehamn, C. S. L., Su, L. F., Cubas, R. A., Davis, M. M., Sette, A., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.08.031 · Cited by 859 · see citing works
DiLillo, D. J., Tan, G. S., Palese, P., & Ravetch, J. V. (2014) · Nature Medicine · doi:10.1038/nm.3443 · Cited by 749 · see citing works
Bahl, K., Senn, J. J., Yuzhakov, O., Bulychev, A., Brito, L. A., Hassett, K. J., Laska, M. E., Smith, M., Almarsson, Ö., Thompson, J., et al. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2017.03.035 · Cited by 642 · see citing works
He, J., Tsai, L. M., Leong, Y. A., Hu, X., Ma, C. S., Chevalier, N., Sun, X., Vandenberg, K. L., Rockman, S., Ding, Y. P., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.09.007 · Cited by 637 · see citing works
Bentebibel, S.-E., Lopez, S. M. C., Obermoser, G., Schmitt, N., Mueller, C., Harrod, C., Flaño, E., Mejías, A., Albrecht, R. A., Blankenship, D., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005191 · Cited by 590 · see citing works
A Temporal Switch in the Germinal Center Determines Differential Output of Memory B and Plasma Cells
Weisel, F. J., Zuccarino-Catania, G. V., Chikina, M., & Shlomchik, M. J. (2016) · Immunity · doi:10.1016/j.immuni.2015.12.004 · Cited by 524 · see citing works
Petsch, B., Schnee, M., Vogel, A. B., Lange, E., Hoffmann, B., Voss, D., Schlake, T., Thess, A., Kallen, K.-J., Stitz, L., et al. (2012) · Nature Biotechnology · doi:10.1038/nbt.2436 · Cited by 461 · see citing works
Phenotype and functions of memory Tfh cells in human blood
Schmitt, N., Bentebibel, S.-E., & Ueno, H. (2014) · Trends in Immunology · doi:10.1016/j.it.2014.06.002 · Cited by 408 · see citing works
Liang, F., Lindgren, G., Lin, A., Thompson, E. A., Ols, S., Röhss, J., John, S., Hassett, K., Yuzhakov, O., Bahl, K., et al. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2017.08.006 · Cited by 395 · see citing works
Self-citationCXCL13 is a plasma biomarker of germinal center activity
Havenar‐Daughton, C., Lindqvist, M., Heit, A., Wu, J. E., Reiss, S. M., Kendric, K. J., Bélanger, S., Kasturi, S. P., Landais, E., Akondy, R. S., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1520112113 · Cited by 343 · see citing works
Plasticity of Human CD4 T Cell Subsets
Geginat, J., Paroni, M., Maglie, S., Alfen, J. S., Kastirr, I., Gruarin, P., Simone, M. C. D., Pagani, M., & Abrignani, S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00630 · Cited by 289 · see citing works
Circulating T follicular regulatory and helper cells have memory-like properties
Sage, P. T., Álvarez, D., Godec, J., von Andrian, U. H., & Sharpe, A. H. (2014) · Journal of Clinical Investigation · doi:10.1172/jci76861 · Cited by 277 · see citing works
Rapidly produced SAM <sup>®</sup> vaccine against H7N9 influenza is immunogenic in mice
Hekele, A., Bertholet, S., Archer, J., Gibson, D. G., Palladino, G., Brito, L. A., Otten, G. R., Brazzoli, M., Buccato, S., Bonci, A., et al. (2013) · Emerging Microbes & Infections · doi:10.1038/emi.2013.54 · Cited by 226 · see citing works
Modified mRNA Vaccines Protect against Zika Virus Infection
Richner, J. M., Himansu, S., Dowd, K. A., Butler, S. L., Salazar, V., Fox, J. M., Julander, J. G., Tang, W. W., Shresta, S., Pierson, T. C., et al. (2017) · Cell · doi:10.1016/j.cell.2017.03.016 · Cited by 221 · see citing works
Liang, F., Lindgren, G., Sandgren, K. J., Thompson, E. A., Francica, J. R., Seubert, A., Gregorio, E. D., Barnett, S. W., O’Hagan, D. T., Sullivan, N. J., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aal2094 · Cited by 206 · see citing works
Plasma cell and memory B cell differentiation from the germinal center
Suan, D., Sundling, C., & Brink, R. A. (2017) · Current Opinion in Immunology · doi:10.1016/j.coi.2017.03.006 · Cited by 184 · see citing works
Havenar‐Daughton, C., Carnathan, D. G., de la Peña, A. T., Pauthner, M. G., Briney, B. S., Reiss, S. M., Wood, J., Kaushik, K., van Gils, M. J., Rosales, S. L., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.10.085 · Cited by 175 · see citing works
Bentebibel, S.-E., Khurana, S., Schmitt, N., Kurup, P., Mueller, C., Obermoser, G., Palucka, A. K., Albrecht, R. A., García‐Sastre, A., Golding, H., et al. (2016) · Scientific Reports · doi:10.1038/srep26494 · Cited by 171 · see citing works
Herati, R. S., Muselman, A., Vella, L., Bengsch, B., Parkhouse, K., Del Alcazar, D., Kotzin, J., Doyle, S. A., Tebas, P., Hensley, S. E., et al. (2017) · Science Immunology · doi:10.1126/sciimmunol.aag2152 · Cited by 167 · see citing works
Michiels, B., Govaerts, F., Remmen, R., Vermeire, E., & Coenen, S. (2011) · Vaccine · doi:10.1016/j.vaccine.2011.08.008 · Cited by 143 · see citing works
Overview of Serological Techniques for Influenza Vaccine Evaluation: Past, Present and Future
Trombetta, C. M., Perini, D., Mather, S. T., Temperton, N. J., & Montomoli, E. (2014) · Vaccines · doi:10.3390/vaccines2040707 · Cited by 116 · see citing works
Vaccination establishes clonal relatives of germinal center T cells in the blood of humans
Heit, A., Schmitz, F., Gerdts, S. E., Flach, B., Moore, M. S., Perkins, J. A., Robins, H. S., Aderem, A. A., Spearman, P. W., Tomaras, G. D., et al. (2017) · The Journal of Experimental Medicine · doi:10.1084/jem.20161794 · Cited by 115 · see citing works
Can follicular helper T cells be targeted to improve vaccine efficacy?
Linterman, M. A., & Hill, D. L. (2016) · F1000Research · doi:10.12688/f1000research.7388.1 · Cited by 95 · see citing works
Recent innovations in mRNA vaccines
Ulmer, J. B., & Geall, A. J. (2016) · Current Opinion in Immunology · doi:10.1016/j.coi.2016.05.008 · Cited by 91 · see citing works
Martinez-Murillo, P., Tran, K., Guenaga, J., Lindgren, G., Ádori, M., Feng, Y., Phad, G. E., Bernat, N. V., Bale, S., Ingale, J., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.04.021 · Cited by 91 · see citing works
Pilkinton, M. A., Nicholas, K. J., Warren, C. M., Smith, R. M., Yoder, S. M., Talbot, H. K., & Kalams, S. A. (2016) · Vaccine · doi:10.1016/j.vaccine.2016.11.059 · Cited by 64 · see citing works
Iyer, S. S., Gangadhara, S., Victor, B., Gomez, R., Basu, R., Hong, J. J., LaBranche, C. C., Montefiori, D. C., Villinger, F. J., Moss, B., et al. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1500083 · Cited by 55 · see citing works
Ma, Y., & Ross, A. C. (2009) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00282-09 · Cited by 34 · see citing works
Sundling, C., Martinez-Murillo, P., Soldemo, M., Spångberg, M., Bengtsson, K. L., Stertman, L., Forsell, M. N. E., & Hedestam, G. B. K. (2012) · The Journal of Infectious Diseases · doi:10.1093/infdis/jis696 · Cited by 30 · see citing works
Zhang, X., Casartelli, N., Lemoine, S., Mozeleski, B., Azria, É., Ray, C. L., Schwartz, O., Launay, O., Leclerc, C., & Lo‐Man, R. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu103 · Cited by 29 · see citing works
Spångberg, M., Martinez-Murillo, P., Fredlund, H., Hedestam, G. B. K., & Sundling, C. (2014) · Journal of Immunological Methods · doi:10.1016/j.jim.2014.05.004 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Alameh, M.-G., Tombácz, I., Bettini, E., Lederer, K., Ndeupen, S., Sittplangkoon, C., Wilmore, J. R., Gaudette, B. T., Soliman, O. Y., Pine, M., et al. (2021) · Immunity · doi:10.1016/j.immuni.2021.11.001 · Cited by 775 · see citing works
Advances in mRNA Vaccines for Infectious Diseases
Zhang, C., Maruggi, G., Shan, H., & Li, J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00594 · Cited by 680 · see citing works
Lipid nanoparticles for nucleic acid delivery: Current perspectives
Samaridou, E., Heyes, J. A., & Lutwyche, P. (2020) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2020.06.002 · Cited by 593 · see citing works
New Vaccine Technologies to Combat Outbreak Situations
Rauch, S., Jasny, E., Schmidt, K. E., & Petsch, B. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01963 · Cited by 579 · see citing works
Pardi, N., Hogan, M. J., Naradikian, M. S., Parkhouse, K., Cain, D. W., Jones, L., Moody, M. A., Verkerke, H. P., Myles, A., Willis, E., et al. (2018) · Journal of Experimental Medicine · doi:10.1084/jem.20171450 · Cited by 530 · see citing works
mRNA as a Transformative Technology for Vaccine Development to Control Infectious Diseases
Maruggi, G., Zhang, C., Li, J., Ulmer, J. B., & Yu, D. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2019.01.020 · Cited by 507 · see citing works
Kim, J., Eygeris, Y., Gupta, M., & Sahay, G. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2020.12.014 · Cited by 514 · see citing works
Innate immune mechanisms of mRNA vaccines
Verbeke, R., Hogan, M. J., Loré, K., & Pardi, N. (2022) · Immunity · doi:10.1016/j.immuni.2022.10.014 · Cited by 518 · see citing works
Recent advances in mRNA vaccine technology
Pardi, N., Hogan, M. J., & Weissman, D. (2020) · Current Opinion in Immunology · doi:10.1016/j.coi.2020.01.008 · Cited by 512 · see citing works
The dawn of mRNA vaccines: the COVID-19 case
Verbeke, R., Lentacker, I., De Smedt, S. C., & Dewitte, H. (2021) · Journal of Controlled Release · doi:10.1016/j.jconrel.2021.03.043 · Cited by 504 · see citing works
Röltgen, K., Nielsen, S. C. A., Silva, O., Younes, S. F., Zaslavsky, M., Costales, C., Yang, F., Wirz, O. F., Solis, D., Hoh, R. A., et al. (2022) · Cell · doi:10.1016/j.cell.2022.01.018 · Cited by 459 · see citing works
Feldman, R. A., Fuhr, R., Smolenov, I., (Mick) Ribeiro, A., Panther, L., Watson, M., Senn, J. J., Smith, M., Almarsson, Ӧ., Pujar, H. S., et al. (2019) · Vaccine · doi:10.1016/j.vaccine.2019.04.074 · Cited by 454 · see citing works
mRNA vaccine: a potential therapeutic strategy
Wang, Y., Zhang, Z., Luo, J., Han, X., Wei, Y., & Wei, X. (2021) · Molecular Cancer · doi:10.1186/s12943-021-01311-z · Cited by 422 · see citing works
Lederer, K., Castaño, D., Gómez Atria, D., Oguin, T. H., Wang, S., Manzoni, T. B., Muramatsu, H., Hogan, M. J., Amanat, F., Cherubin, P., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.11.009 · Cited by 383 · see citing works
“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.”
Laczko, D. I., Hogan, M. J., Toulmin, S. A., Hicks, P. D., Lederer, K., Gaudette, B. T., Castaño, D., Amanat, F., Muramatsu, H., Oguin, T. H., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.07.019 · Cited by 366 · see citing works
Novel approaches for vaccine development
Gebre, M. S., Brito, L. A., Tostanoski, L. H., Edwards, D. K., Carfi, A., & Barouch, D. H. (2021) · Cell · doi:10.1016/j.cell.2021.02.030 · Cited by 347 · see citing works
Self-citationThree decades of messenger RNA vaccine development
Verbeke, R., Lentacker, I., De Smedt, S. C., & Dewitte, H. (2019) · Nano Today · doi:10.1016/j.nantod.2019.100766 · Cited by 342 · see citing works
Freyn, A. W., Ramos da Silva, J., Rosado, V. C., Bliss, C. M., Pine, M., Mui, B. L., Tam, Y. K., Madden, T. D., de Souza Ferreira, L. C., Weissman, D., et al. (2020) · Molecular Therapy · doi:10.1016/j.ymthe.2020.04.018 · Cited by 299 · see citing works
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
SARS-CoV-2 mRNA Vaccines: Immunological Mechanism and Beyond
Bettini, E., & Locci, M. (2021) · Vaccines · doi:10.3390/vaccines9020147 · Cited by 283 · see citing works
From influenza to COVID-19: Lipid nanoparticle mRNA vaccines at the frontiers of infectious diseases
Pilkington, E. H., Suys, E. J. A., Trevaskis, N. L., Wheatley, A. K., Zukancic, D., Algarni, A., Al-Wassiti, H. A., Davis, T. P., Pouton, C. W., Kent, S. J., et al. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.06.023 · Cited by 265 · 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
Ghattas, M., Dwivedi, G., Lavertu, M., & Alameh, M. (2021) · Vaccines · doi:10.3390/vaccines9121490 · Cited by 266 · see citing works
Lipid Nanoparticles as Delivery Systems for RNA-Based Vaccines
Aldosari, B. N., Alfagih, I. M., & Almurshedi, A. S. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13020206 · Cited by 242 · see citing works
Kose, N., Fox, J. M., Sapparapu, G., Bombardi, R., Tennekoon, R. N., de Silva, A. D., Elbashir, S. M., Theisen, M. A., Humphris-Narayanan, E., Ciaramella, G., et al. (2019) · Science Immunology · doi:10.1126/sciimmunol.aaw6647 · Cited by 202 · see citing works
Espeseth, A. S., Cejas, P. J., Citron, M. P., Wang, D., DiStefano, D. J., Callahan, C., Donnell, G. O., Galli, J. D., Swoyer, R., Touch, S., et al. (2020) · npj Vaccines · doi:10.1038/s41541-020-0163-z · Cited by 190 · see citing works
Prediction of lipid nanoparticles for mRNA vaccines by the machine learning algorithm
Wang, W., Feng, S., Ye, Z., Gao, H., Lin, J., & Ouyang, D. (2021) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2021.11.021 · Cited by 170 · see citing works
Immune Responses Induced by mRNA Vaccination in Mice, Monkeys and Humans
Cagigi, A., & Loré, K. (2021) · Vaccines · doi:10.3390/vaccines9010061 · Cited by 153 · see citing works
Route of Vaccine Administration Alters Antigen Trafficking but Not Innate or Adaptive Immunity
Ols, S., Yang, L., Thompson, E. A., Pushparaj, P., Tran, K., Liang, F., Lin, A., Eriksson, B. M., Hedestam, G. B. K., Wyatt, R. T., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.111 · Cited by 146 · see citing works
Immunological basis for enhanced immunity of nanoparticle vaccines
Kelly, H. G., Kent, S. J., & Wheatley, A. K. (2019) · Expert Review of Vaccines · doi:10.1080/14760584.2019.1578216 · Cited by 146 · see citing works
mRNA vaccination induces tick resistance and prevents transmission of the Lyme disease agent
Sajid, A., Matias, J., Arora, G., Kurokawa, C., DePonte, K., Tang, X., Lynn, G. E., Wu, M.-J., Pal, U., Strank, N. O., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abj9827 · Cited by 141 · see citing works
Knife’s edge: Balancing immunogenicity and reactogenicity in mRNA vaccines
Lee, J., Woodruff, M. C., Kim, E. H., & Nam, J. (2023) · Experimental & Molecular Medicine · doi:10.1038/s12276-023-00999-x · Cited by 137 · see citing works
Antigen Presentation of mRNA-Based and Virus-Vectored SARS-CoV-2 Vaccines
Rijkers, G. T., Weterings, N., Obregón‐Henao, A., Dutt, T., Dutt, T. S., van Overveld, F. J., & Henao-Tamayo, M. I. (2021) · Vaccines · doi:10.3390/vaccines9080848 · Cited by 134 · see citing works
Development of multivalent mRNA vaccine candidates for seasonal or pandemic influenza
Chivukula, S., Plitnik, T., Tibbitts, T., Karve, S., Dias, A., Zhang, D., Goldman, R., Gopani, H., Khanmohammed, A., Sarode, A., et al. (2021) · npj Vaccines · doi:10.1038/s41541-021-00420-6 · Cited by 117 · see citing works
Samanovic, M. I., Cornelius, A. R., Gray-Gaillard, S. L., Allen, J. R., Karmacharya, T., Wilson, J. P., Hyman, S., Tuen, M., Koralov, S. B., Mulligan, M. J., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abi8961 · Cited by 112 · see citing works
Wu, L., Li, X., Qian, X., Wang, S., Liu, J., & Yan, J. (2024) · Vaccines · doi:10.3390/vaccines12020186 · Cited by 125 · see citing works
Zhu, Y., Ma, J., Shen, R., Lin, J., Li, S., Lu, X., Stelzel, J. L., Kong, J., Cheng, L., Vuong, I., et al. (2023) · Nature Biomedical Engineering · doi:10.1038/s41551-023-01131-0 · Cited by 109 · see citing works
Characterization of HIV-1 Nucleoside-Modified mRNA Vaccines in Rabbits and Rhesus Macaques
Pardi, N., LaBranche, C. C., Ferrari, G., Cain, D. W., Tombácz, I., Parks, R. J., Muramatsu, H., Mui, B. L., Tam, Y. K., Karikó, K., et al. (2019) · Molecular Therapy - Nucleic Acids · doi:10.1016/j.omtn.2019.03.003 · Cited by 103 · see citing works
Advances in gene-based vaccine platforms to address the COVID-19 pandemic
Pushparajah, D., Jimenez, S., Wong, S. L., Alattas, H., Nafissi, N., & Slavcev, R. A. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.01.003 · Cited by 98 · see citing works
RNA-based pharmacotherapy for tumors: From bench to clinic and back
Liang, X., Li, D., Leng, S., & Zhu, X. M. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.109997 · Cited by 96 · see citing works
Messenger RNA-Based Vaccines Against Infectious Diseases
Alameh, M.-G., Weissman, D., & Pardi, N. (2020) · Current Topics in Microbiology and Immunology · doi:10.1007/82_2020_202 · Cited by 96 · see citing works
Zhang, C., Ma, Y., Zhang, J., Kuo, J. C., Zhang, Z., Xie, H., Zhu, J., & Liu, T. (2022) · Molecules · doi:10.3390/molecules27061943 · Cited by 93 · see citing works
Enlisting the mRNA Vaccine Platform to Combat Parasitic Infections
Versteeg, L., Almutairi, M. M., Hotez, P. J., & Pollet, J. B. K. (2019) · Vaccines · doi:10.3390/vaccines7040122 · Cited by 93 · see citing works
New Kids on the Block: RNA-Based Influenza Virus Vaccines
Scorza, F. B., & Pardi, N. (2018) · Vaccines · doi:10.3390/vaccines6020020 · Cited by 89 · see citing works
mRNA nanodelivery systems: targeting strategies and administration routes
Yuan, M., Han, Z., Liang, Y., Sun, Y., He, B., Chen, W., & Fan, L. (2023) · Biomaterials Research · doi:10.1186/s40824-023-00425-3 · Cited by 90 · see citing works
Microfluidic production of mRNA-loaded lipid nanoparticles for vaccine applications
Lopes, C., Cristóvão, J. S., Silvério, V., Lino, P. R., & Fonte, P. (2022) · Expert Opinion on Drug Delivery · doi:10.1080/17425247.2022.2135502 · Cited by 85 · see citing works
Lipid Nanoparticle Delivery Systems to Enable mRNA-Based Therapeutics
Semple, S. C., Leone, R. D., Barbosa, C., Tam, Y. K., & Lin, P. J. C. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14020398 · Cited by 80 · see citing works
Thompson, E. A., Ols, S., Miura, K., Rausch, K. M., Narum, D. L., Spångberg, M., Juraska, M., Wille-Reece, U., Weiner, A. J., Howard, R. F., et al. (2018) · JCI Insight · doi:10.1172/jci.insight.120692 · Cited by 73 · see citing works
mRNA vaccines: Past, present, future
Karam, M., & Daoud, G. (2022) · Asian Journal of Pharmaceutical Sciences · doi:10.1016/j.ajps.2022.05.003 · Cited by 74 · see citing works
Mettelman, R. C., Souquette, A. H., de Velde, L.-A. V., Vegesana, K., Allen, E. K., Kackos, C. M., Trifkovic, S., DeBeauchamp, J., Wilson, T. L., James, D. G. S., et al. (2023) · Nature Immunology · doi:10.1038/s41590-023-01590-2 · Cited by 62 · see citing works
Current progress in the development of prophylactic and therapeutic vaccines
Li, T., Qian, C., Gu, Y., Zhang, J., Li, S., & Xia, N. (2022) · Science China Life Sciences · doi:10.1007/s11427-022-2230-4 · Cited by 57 · see citing works
Live attenuated pertussis vaccine BPZE1 induces a broad antibody response in humans
Lin, A., Apostolović, D., Jahnmatz, M., Liang, F., Ols, S., Tecleab, T., Wu, C., van Hage, M., Solovay, K., Rubin, K., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci135020 · Cited by 58 · see citing works
New Technologies for Influenza Vaccines
Rockman, S. P., Laurie, K., Parkes, S., Wheatley, A. K., & Barr, I. (2020) · Microorganisms · doi:10.3390/microorganisms8111745 · Cited by 55 · see citing works
Willis, E., Pardi, N., Parkhouse, K., Mui, B. L., Tam, Y. K., Weissman, D., & Hensley, S. E. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.aav5701 · Cited by 54 · see citing works
Design Strategies for and Stability of mRNA–Lipid Nanoparticle COVID-19 Vaccines
Liu, T., Tian, Y., Zheng, A., & Cui, C. (2022) · Polymers · doi:10.3390/polym14194195 · Cited by 52 · see citing works
Nel, A. E., & Miller, J. F. (2021) · ACS Nano · doi:10.1021/acsnano.1c01845 · Cited by 50 · see citing works
An Update on mRNA-Based Viral Vaccines
Jeeva, S., Kim, K., Shin, C. H., Wang, B., & Kang, S. (2021) · Vaccines · doi:10.3390/vaccines9090965 · Cited by 49 · see citing works
Hellgren, F., Cagigi, A., Cerveira, R. A., Ols, S., Kern, T., Lin, A., Eriksson, B., Dodds, M., Jasny, E., Schwendt, K., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39421-5 · Cited by 49 · see citing works
Röltgen, K., Nielsen, S. C. A., Arunachalam, P. S., Yang, F., Hoh, R. A., Wirz, O. F., Lee, A. S., Gao, F., Mallajosyula, V., Li, C., et al. (2021) · doi:10.1101/2021.04.05.21254952 · Cited by 45 · see citing works
The Development of mRNA Vaccines for Infectious Diseases: Recent Updates
Nitika, Wei, J., & Hui, A. (2021) · Infection and Drug Resistance · doi:10.2147/idr.s341694 · Cited by 42 · see citing works
Lenart, K., Hellgren, F., Ols, S., Yan, X., Cagigi, A., Cerveira, R. A., Winge, I. P., Hanczak, J., Mueller, S. O., Jasny, E., et al. (2022) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2022.10.001 · Cited by 39 · see citing works
Influenza Viruses: Innate Immunity and mRNA Vaccines
Lee, S., & Ryu, J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.710647 · Cited by 35 · see citing works
A Pvs25 mRNA vaccine induces complete and durable transmission-blocking immunity to Plasmodium vivax
Kunkeaw, N., Nguitragool, W., Takashima, E., Kangwanrangsan, N., Muramatsu, H., Tachibana, M., Ishino, T., Lin, P. J. C., Tam, Y. K., Pichyangkul, S., et al. (2023) · npj Vaccines · doi:10.1038/s41541-023-00786-9 · Cited by 34 · see citing works
Targeting the hallmarks of aging to improve influenza vaccine responses in older adults
Cadar, A. N., Martin, D. E., & Bartley, J. M. (2023) · Immunity & Ageing · doi:10.1186/s12979-023-00348-6 · Cited by 32 · see citing works
mRNA-Based Vaccines and Mode of Action
Gergen, J., & Petsch, B. (2020) · Current topics in microbiology and immunology · doi:10.1007/82_2020_230 · Cited by 32 · see citing works
COVID‐19: Clinical status of vaccine development till date
Kumar, S., Basu, M., Ghosh, P., Ansari, A., & Ghosh, M. (2022) · British Journal of Clinical Pharmacology · doi:10.1111/bcp.15552 · Cited by 18 · see citing works
Germinal center responses to SARS-CoV-2 mRNA vaccines in healthy and immunocompromised individuals
Lederer, K., Parvathaneni, K., Painter, M. M., Bettini, E., Agarwal, D., Lundgreen, K. A., Weirick, M., Goel, R. R., Xu, X., Drapeau, E. M., et al. (2021) · doi:10.1101/2021.09.16.21263686 · Cited by 179 · see citing works
An old problem with new solutions: Strategies to improve vaccine efficacy in the elderly
Bell, M. R., & Kutzler, M. A. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2022.114175 · Cited by 29 · see citing works
Nucleic acid delivery and nanoparticle design for COVID vaccines
Andresen, J. L., & Fenton, O. S. (2021) · MRS Bulletin · doi:10.1557/s43577-021-00169-2 · Cited by 29 · see citing works
Have mRNA vaccines sentenced DNA vaccines to death?
Cagigi, A., & Douradinha, B. G. (2023) · Expert Review of Vaccines · doi:10.1080/14760584.2023.2282065 · Cited by 29 · see citing works
Ige, M. A., Ren, X., Yang, Y., Zhang, H., Shen, C., Jiang, Y., Li, J., & Wan, X. (2025) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2025.102721 · Cited by 29 · see citing works
Yu, M., Charles, A., Cagigi, A., Christ, W., Österberg, B., Falck‐Jones, S., Azizmohammadi, L., Åhlberg, E., Falck‐Jones, R., Svensson, J., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37835-9 · Cited by 27 · see citing works
The race toward a universal influenza vaccine: Front runners and the future directions
Hu, L., Lao, G., Liu, R., Feng, J., Long, F., & Peng, T. (2022) · Antiviral Research · doi:10.1016/j.antiviral.2022.105505 · Cited by 24 · see citing works
Nanoparticle-based delivery platforms for mRNA vaccine development
Okay, S., Özcan, Ö. Ö., & Karahan, M. (2020) · AIMS Biophysics · doi:10.3934/biophy.2020023 · Cited by 23 · see citing works
Advancing mRNA Therapeutics: The Role and Future of Nanoparticle Delivery Systems
Li, J., Zhang, Y., Yang, Y., & Sun, T. (2024) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.4c00276 · Cited by 23 · see citing works
Better, Faster, Stronger: mRNA Vaccines Show Promise for Influenza Vaccination in Older Adults
Bartley, J. M., Cadar, A. N., & Martin, D. E. (2021) · Immunological Investigations · doi:10.1080/08820139.2021.1909617 · Cited by 21 · see citing works
Lipid‐based nucleic acid therapeutics with in vivo efficacy
Sufian, M. A., & Ilies, M. A. (2022) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1856 · Cited by 22 · see citing works
Ackun‐Farmmer, M. A., & Jewell, C. M. (2023) · Advanced NanoBiomed Research · doi:10.1002/anbr.202200135 · Cited by 21 · see citing works
Chaudhari, R. H., Tandel, N., Sahu, K., Negi, S., Bashir, H., Rupareliya, A., Mishra, R. P. N., Dalai, S. K., & Tyagi, R. K. (2021) · Nanomaterials · doi:10.3390/nano11020406 · Cited by 21 · see citing works
Scaglione, A., Opp, S., Hurtado, A., Pampeno, C., Lin, Z., Noval, M. G., Thannickal, S. A., Stapleford, K. A., & Meruelo, D. (2021) · bioRxiv · doi:10.3389/fimmu.2021.719077 · Cited by 15 · see citing works
Wolf, M. A., O’Hara, J. M., Bitzer, G. J., Narayanan, E., Boehm, D. T., Bevere, J. R., DeJong, M. A., Hall, J. M., Wong, T. Y., Falcone, S., et al. (2024) · npj Vaccines · doi:10.1038/s41541-024-00890-4 · Cited by 18 · see citing works
Sandberg, J. T., Ols, S., Löfling, M., Varnaitė, R., Lindgren, G., Nilsson, O., Rombo, L., Kalén, M., Loré, K., Blom, K. G., et al. (2021) · The Journal of Immunology · doi:10.4049/jimmunol.2001381 · Cited by 19 · see citing works
Role of T Follicular Helper Cells in Viral Infections and Vaccine Design
Ahmadivand, S., Fux, R., & Palić, D. (2025) · Cells · doi:10.3390/cells14070508 · Cited by 18 · see citing works
Roozen, G. V. T., Prins, M. L. M., van Binnendijk, R. S., den Hartog, G., Kuiper, V. P., Prins, C., Janse, J. J., Kruithof, A. C., Feltkamp, M. C. W., Kuijer, M., et al. (2021) · medRxiv · doi:10.1101/2021.07.27.21261116 · Cited by 18 · see citing works
CircRNA: Unlocking new frontiers in therapeutic and vaccine development
Bahrulolum, H., Rouzbahani, F. N., Hoseini, Z. S., Chaharmahali, M., & Hosseini, S. M. (2025) · Molecular Therapy · doi:10.1016/j.ymthe.2025.10.038 · Cited by 18 · see citing works
Boretti, A. (2024) · Clinical and Experimental Medicine (Testo stampato) · doi:10.1007/s10238-023-01264-1 · Cited by 19 · see citing works
Flynn, J. A., Weber, T., Cejas, P. J., Cox, K. S., Touch, S., Austin, L. A., Ou, Y., Citron, M. P., Luo, B., Gindy, M. E., et al. (2022) · Vaccine · doi:10.1016/j.vaccine.2022.03.063 · Cited by 16 · see citing works
Tjiam, M. C., Fernández, S., & French, M. A. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.738123 · Cited by 15 · see citing works
The inflammaging microenvironment induces dysfunctional rewiring of Tfh cell differentiation
Nelson, C. S., Podestà, M. A., Gempler, M., Lee, J.-M., Batty, C. J., Mathenge, P. G., Sainju, A., Chang, M., Ke, H., Chandrakar, P., et al. (2025) · JCI Insight · doi:10.1172/jci.insight.187271 · Cited by 14 · see citing works
Immunology of RNA-based vaccines: The critical interplay between inflammation and expression
Tregoning, J. S., Wang, Z., Sridhar, S., Shattock, R. J., & DeRosa, F. (2025) · Molecular Therapy · doi:10.1016/j.ymthe.2025.09.011 · Cited by 19 · see citing works
Recent Advances in Messenger Ribonucleic Acid (mRNA) Vaccines and Their Delivery Systems: A Review
Belay, W. Y., Nibret, G., & Aschale, Y. (2023) · Clinical Pharmacology Advances and Applications · doi:10.2147/cpaa.s418314 · Cited by 16 · see citing works
Roznik, K., Xue, J., Stavrakis, G., Johnston, T. S., Kalluri, D., Ohsie, R., Qin, C. X., McAteer, J., Segev, D. L., Mogul, D. B., et al. (2024) · npj Vaccines · doi:10.1038/s41541-024-00866-4 · Cited by 13 · see citing works
mRNA vaccines against HIV : Hopes and challenges
Zubair, A., Ahmad, H., Arif, M. M., & Ali, M. (2025) · HIV Medicine · doi:10.1111/hiv.70024 · Cited by 14 · see citing works
Agallou, M., Koutsoni, O. S., Michail, M., Zisimopoulou, P., Tsitsilonis, O., & Karagouni, E. (2022) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiac421 · Cited by 11 · see citing works
Determination of significant immunological timescales from mRNA-LNP-based vaccines in humans
Moyles, I. R., Korosec, C. S., & Heffernan, J. M. (2023) · Journal of Mathematical Biology · doi:10.1007/s00285-023-01919-3 · Cited by 10 · see citing works
Lee, H., Punt, J. A., Miller, D. C., Nagpal, A., Smith, C., Sayeed, Y. A., Patel, J., Stojanovic, M. P., Popescu, A., & McCormick, Z. L. (2021) · Pain Medicine · doi:10.1093/pm/pnab063 · Cited by 12 · see citing works
Thompson, E. A., Ngecu, W., Stoddart, L., Johnston, T. S., Chang, A. Y., Cascino, K., Alejo, J. L., Abedon, A. T., Samaha, H., Rouphael, N., et al. (2023) · JCI Insight · doi:10.1172/jci.insight.168470 · Cited by 11 · see citing works
Potent and Targeted Sindbis Virus Platform for Immunotherapy of Ovarian Cancer
Opp, S., Hurtado, A. M., Pampeno, C. L., Lin, Z., & Meruelo, D. (2022) · Cells · doi:10.3390/cells12010077 · Cited by 11 · see citing works
La nueva generación de vacunas de ARN mensajero (ARNm) frente a la gripe
Reina, J. (2021) · Enfermedades Infecciosas y Microbiología Clínica · doi:10.1016/j.eimc.2021.07.009 · Cited by 11 · see citing works
- Authors
- Lindgren, G., Ols, S., Liang, F., Thompson, E. A., Lin, A., Hellgren, F., Bahl, K., John, S., Yuzhakov, O., Hassett, K. J., Brito, L. A., Salter, H., Ciaramella, G., & Loré, K.
- Affiliations
- Karolinska Institutet (SE)
- Moderna Therapeutics (United States) (US)
- Corresponding author
- Loré, Karin
- ORCID
- Venue
- Frontiers in Immunology
- Publisher
- Frontiers Media SA
- Published
- 2017-11-13
- Volume
- 8
- Pages
- 1539-1539
- ISSN
- 1664-3224 (ISSN-L)
- PMC
- PMC5693886
- OpenAlex
- W2767992446
- Cited by
- 132
- References
- 44
- Citations by year
- 2026: 3 · 2025: 13 · 2024: 9 · 2023: 16 · 2022: 25 · 2021: 37 · 2020: 15 · 2019: 10 · 2018: 4
- FWCI
- 6.21
- Type
- journal article
- Language
- en
- Update notices
- corrigendum (2019-04-02)
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Immunology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Karolinska Institutet
- Vetenskapsrådet
- China Scholarship Council
- Topics
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Keywords
- T follicular helper cells, ICOS, PD-1, CXCR3, memory B cells, plasma cells, germinal center, intradermal vaccination, intramuscular vaccination, non-human primates, vaccine immunogenicity
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review