Nucleoside-modified mRNA vaccines induce potent T follicular helper and germinal center B cell responses
Abstract
T follicular helper (Tfh) cells are required to develop germinal center (GC) responses and drive immunoglobulin class switch, affinity maturation, and long-term B cell memory. In this study, we characterize a recently developed vaccine platform, nucleoside-modified, purified mRNA encapsulated in lipid nanoparticles (mRNA-LNPs), that induces high levels of Tfh and GC B cells. Intradermal vaccination with nucleoside-modified mRNA-LNPs encoding various viral surface antigens elicited polyfunctional, antigen-specific, CD4+T cell responses and potent neutralizing antibody responses in mice and nonhuman primates. Importantly, the strong antigen-specific Tfh cell response and high numbers of GC B cells and plasma cells were associated with long-lived and high-affinity neutralizing antibodies and durable protection. Comparative studies demonstrated that nucleoside-modified mRNA-LNP vaccines outperformed adjuvanted protein and inactivated virus vaccines and pathogen infection. The incorporation of noninflammatory, modified nucleosides in the mRNA is required for the production of large amounts of antigen and for robust immune responses.
- Authors:
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[2];
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- Univ. of Pennsylvania, Philadelphia, PA (United States)
- Duke University School of Medicine, Durham, NC (United States)
- Univ. of Washington, Seattle, WA (United States)
- Duke University Medical Center, Durham, NC (United States)
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
- Acuitas Therapeutics, Vancouver, BC (Canada)
- Icahn School of Medicine at Mount Sinai, New York, NY (United States)
- BioNTech RNA Pharmaceuticals, Mainz (Germany)
- The Children’s Hospital of Philadelphia, Philadelphia, PA (United States)
- Bioqual Inc., Rockville, MD (United States)
- Publication Date:
- Research Org.:
- Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
- Sponsoring Org.:
- USDOE; National Institutes of Health (NIH)
- OSTI Identifier:
- 1505995
- Report Number(s):
- LA-UR-17-26175
Journal ID: ISSN 0022-1007
- Grant/Contract Number:
- 89233218CNA000001
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Experimental Medicine
- Additional Journal Information:
- Journal Volume: 215; Journal Issue: 6; Journal ID: ISSN 0022-1007
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Pardi, Norbert, Hogan, Michael J., Naradikian, Martin S., Parkhouse, Kaela, Cain, Derek W., Jones, Letitia, Moody, M. Anthony, Verkerke, Hans P., Myles, Arpita, Willis, Elinor, LaBranche, Celia C., Montefiori, David C., Lobby, Jenna L., Saunders, Kevin O., Liao, Hua-Xin, Korber, Bette T., Sutherland, Laura L., Scearce, Richard M., Hraber, Peter T., Tombácz, István, Muramatsu, Hiromi, Ni, Houping, Balikov, Daniel A., Li, Charles, Mui, Barbara L., Tam, Ying K., Krammer, Florian, Karikó, Katalin, Polacino, Patricia, Eisenlohr, Laurence C., Madden, Thomas D., Hope, Michael J., Lewis, Mark G., Lee, Kelly K., Hu, Shiu-Lok, Hensley, Scott E., Cancro, Michael P., Haynes, Barton F., and Weissman, Drew. Nucleoside-modified mRNA vaccines induce potent T follicular helper and germinal center B cell responses. United States: N. p., 2018.
Web. doi:10.1084/jem.20171450.
Pardi, Norbert, Hogan, Michael J., Naradikian, Martin S., Parkhouse, Kaela, Cain, Derek W., Jones, Letitia, Moody, M. Anthony, Verkerke, Hans P., Myles, Arpita, Willis, Elinor, LaBranche, Celia C., Montefiori, David C., Lobby, Jenna L., Saunders, Kevin O., Liao, Hua-Xin, Korber, Bette T., Sutherland, Laura L., Scearce, Richard M., Hraber, Peter T., Tombácz, István, Muramatsu, Hiromi, Ni, Houping, Balikov, Daniel A., Li, Charles, Mui, Barbara L., Tam, Ying K., Krammer, Florian, Karikó, Katalin, Polacino, Patricia, Eisenlohr, Laurence C., Madden, Thomas D., Hope, Michael J., Lewis, Mark G., Lee, Kelly K., Hu, Shiu-Lok, Hensley, Scott E., Cancro, Michael P., Haynes, Barton F., & Weissman, Drew. Nucleoside-modified mRNA vaccines induce potent T follicular helper and germinal center B cell responses. United States. https://doi.org/10.1084/jem.20171450
Pardi, Norbert, Hogan, Michael J., Naradikian, Martin S., Parkhouse, Kaela, Cain, Derek W., Jones, Letitia, Moody, M. Anthony, Verkerke, Hans P., Myles, Arpita, Willis, Elinor, LaBranche, Celia C., Montefiori, David C., Lobby, Jenna L., Saunders, Kevin O., Liao, Hua-Xin, Korber, Bette T., Sutherland, Laura L., Scearce, Richard M., Hraber, Peter T., Tombácz, István, Muramatsu, Hiromi, Ni, Houping, Balikov, Daniel A., Li, Charles, Mui, Barbara L., Tam, Ying K., Krammer, Florian, Karikó, Katalin, Polacino, Patricia, Eisenlohr, Laurence C., Madden, Thomas D., Hope, Michael J., Lewis, Mark G., Lee, Kelly K., Hu, Shiu-Lok, Hensley, Scott E., Cancro, Michael P., Haynes, Barton F., and Weissman, Drew. Tue .
"Nucleoside-modified mRNA vaccines induce potent T follicular helper and germinal center B cell responses". United States. https://doi.org/10.1084/jem.20171450. https://www.osti.gov/servlets/purl/1505995.
@article{osti_1505995,
title = {Nucleoside-modified mRNA vaccines induce potent T follicular helper and germinal center B cell responses},
author = {Pardi, Norbert and Hogan, Michael J. and Naradikian, Martin S. and Parkhouse, Kaela and Cain, Derek W. and Jones, Letitia and Moody, M. Anthony and Verkerke, Hans P. and Myles, Arpita and Willis, Elinor and LaBranche, Celia C. and Montefiori, David C. and Lobby, Jenna L. and Saunders, Kevin O. and Liao, Hua-Xin and Korber, Bette T. and Sutherland, Laura L. and Scearce, Richard M. and Hraber, Peter T. and Tombácz, István and Muramatsu, Hiromi and Ni, Houping and Balikov, Daniel A. and Li, Charles and Mui, Barbara L. and Tam, Ying K. and Krammer, Florian and Karikó, Katalin and Polacino, Patricia and Eisenlohr, Laurence C. and Madden, Thomas D. and Hope, Michael J. and Lewis, Mark G. and Lee, Kelly K. and Hu, Shiu-Lok and Hensley, Scott E. and Cancro, Michael P. and Haynes, Barton F. and Weissman, Drew},
abstractNote = {T follicular helper (Tfh) cells are required to develop germinal center (GC) responses and drive immunoglobulin class switch, affinity maturation, and long-term B cell memory. In this study, we characterize a recently developed vaccine platform, nucleoside-modified, purified mRNA encapsulated in lipid nanoparticles (mRNA-LNPs), that induces high levels of Tfh and GC B cells. Intradermal vaccination with nucleoside-modified mRNA-LNPs encoding various viral surface antigens elicited polyfunctional, antigen-specific, CD4+T cell responses and potent neutralizing antibody responses in mice and nonhuman primates. Importantly, the strong antigen-specific Tfh cell response and high numbers of GC B cells and plasma cells were associated with long-lived and high-affinity neutralizing antibodies and durable protection. Comparative studies demonstrated that nucleoside-modified mRNA-LNP vaccines outperformed adjuvanted protein and inactivated virus vaccines and pathogen infection. The incorporation of noninflammatory, modified nucleosides in the mRNA is required for the production of large amounts of antigen and for robust immune responses.},
doi = {10.1084/jem.20171450},
journal = {Journal of Experimental Medicine},
number = 6,
volume = 215,
place = {United States},
year = {Tue May 08 00:00:00 EDT 2018},
month = {Tue May 08 00:00:00 EDT 2018}
}
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- Cancer Immunology, Immunotherapy, Vol. 66, Issue 2
The use of self-adjuvanting nanofiber vaccines to elicit high-affinity B cell responses to peptide antigens without inflammation
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- Biomaterials, Vol. 34, Issue 34
Germinal Center Selection and the Antibody Response to Influenza
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- Victora, Gabriel D.; Wilson, Patrick C.
- Cell, Vol. 163, Issue 3
Modified mRNA Vaccines Protect against Zika Virus Infection
journal, March 2017
- Richner, Justin M.; Himansu, Sunny; Dowd, Kimberly A.
- Cell, Vol. 168, Issue 6
Novel universal influenza virus vaccine approaches
journal, April 2016
- Krammer, Florian
- Current Opinion in Virology, Vol. 17
Type I Interferon Signaling in Dendritic Cells Stimulates the Development of Lymph-Node-Resident T Follicular Helper Cells
journal, September 2009
- Cucak, Helena; Yrlid, Ulf; Reizis, Boris
- Immunity, Vol. 31, Issue 3
Human Antibodies that Neutralize HIV-1: Identification, Structures, and B Cell Ontogenies
journal, September 2012
- Kwong, Peter D.; Mascola, John R.
- Immunity, Vol. 37, Issue 3
T Follicular Helper Cell Differentiation, Function, and Roles in Disease
journal, October 2014
- Crotty, Shane
- Immunity, Vol. 41, Issue 4
Skin dendritic cells induce follicular helper T cells and protective humoral immune responses
journal, November 2015
- Yao, Chen; Zurawski, Sandra M.; Jarrett, Elizabeth S.
- Journal of Allergy and Clinical Immunology, Vol. 136, Issue 5
N1-methylpseudouridine-incorporated mRNA outperforms pseudouridine-incorporated mRNA by providing enhanced protein expression and reduced immunogenicity in mammalian cell lines and mice
journal, November 2015
- Andries, Oliwia; Mc Cafferty, Séan; De Smedt, Stefaan C.
- Journal of Controlled Release, Vol. 217
Purification of recombinant vaccinia virus-expressed monomeric HIV-1 gp120 to apparent homogeneity
journal, July 2013
- Guo, Wenjin; Cleveland, Brad; Davenport, Thaddeus M.
- Protein Expression and Purification, Vol. 90, Issue 1
Lymphatic-targeted cationic liposomes: A robust vaccine adjuvant for promoting long-term immunological memory
journal, September 2014
- Wang, Ce; Liu, Peng; Zhuang, Yan
- Vaccine, Vol. 32, Issue 42
Characterization of a thymus-tropic HIV-1 isolate from a rapid progressor: role of the envelope
journal, October 2004
- Meissner, Eric G.; Duus, Karen M.; Gao, Feng
- Virology, Vol. 328, Issue 1
Cross-reactive monoclonal antibodies to multiple HIV-1 subtype and SIVcpz envelope glycoproteins
journal, November 2009
- Gao, Feng; Scearce, Richard M.; Alam, S. Munir
- Virology, Vol. 394, Issue 1
Immunogenicity and protective efficacy of influenza vaccination
journal, July 2004
- Hannoun, Claude; Megas, Francoise; Piercy, James
- Virus Research, Vol. 103, Issue 1-2
Preclinical and Clinical Demonstration of Immunogenicity by mRNA Vaccines against H10N8 and H7N9 Influenza Viruses
journal, June 2017
- Bahl, Kapil; Senn, Joe J.; Yuzhakov, Olga
- Molecular Therapy, Vol. 25, Issue 6
Efficient Targeting and Activation of Antigen-Presenting Cells In Vivo after Modified mRNA Vaccine Administration in Rhesus Macaques
journal, December 2017
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Is there a future for mRNAs as viral vaccines?
journal, September 2017
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- The Lancet, Vol. 390, Issue 10101
Incorporation of Pseudouridine Into mRNA Yields Superior Nonimmunogenic Vector With Increased Translational Capacity and Biological Stability
journal, November 2008
- Karikó, Katalin; Muramatsu, Hiromi; Welsh, Frank A.
- Molecular Therapy, Vol. 16, Issue 11
Biodegradable Lipids Enabling Rapidly Eliminated Lipid Nanoparticles for Systemic Delivery of RNAi Therapeutics
journal, August 2013
- Maier, Martin A.; Jayaraman, Muthusamy; Matsuda, Shigeo
- Molecular Therapy, Vol. 21, Issue 8
Zika virus protection by a single low-dose nucleoside-modified mRNA vaccination
journal, February 2017
- Pardi, Norbert; Hogan, Michael J.; Pelc, Rebecca S.
- Nature, Vol. 543, Issue 7644
Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs
journal, July 2005
- Morrissey, David V.; Lockridge, Jennifer A.; Shaw, Lucinda
- Nature Biotechnology, Vol. 23, Issue 8
Activin A programs the differentiation of human TFH cells
journal, July 2016
- Locci, Michela; Wu, Jennifer E.; Arumemi, Fortuna
- Nature Immunology, Vol. 17, Issue 8
mRNA vaccines — a new era in vaccinology
journal, January 2018
- Pardi, Norbert; Hogan, Michael J.; Porter, Frederick W.
- Nature Reviews Drug Discovery, Vol. 17, Issue 4
Broadly neutralizing antibodies and the search for an HIV-1 vaccine: the end of the beginning
journal, August 2013
- Kwong, Peter D.; Mascola, John R.; Nabel, Gary J.
- Nature Reviews Immunology, Vol. 13, Issue 9
Unmodified mRNA in LNPs constitutes a competitive technology for prophylactic vaccines
journal, October 2017
- Lutz, Johannes; Lazzaro, Sandra; Habbeddine, Mohamed
- npj Vaccines, Vol. 2, Issue 1
Affinity maturation in an HIV broadly neutralizing B-cell lineage through reorientation of variable domains
journal, June 2014
- Fera, D.; Schmidt, A. G.; Haynes, B. F.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 28
Sustained antigen availability during germinal center initiation enhances antibody responses to vaccination
journal, October 2016
- Tam, Hok Hei; Melo, Mariane B.; Kang, Myungsun
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 43
Progress in developing virus-like particle influenza vaccines
journal, May 2016
- Quan, Fu-Shi; Lee, Young-Tae; Kim, Ki-Hye
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