mRNA vaccines induce durable immune memory to SARS-CoV-2 and variants of concern
Vaccination against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has proven highly effective at preventing severe COVID-19. However, the evolution of viral variants, and waning antibody levels over time, raise questions regarding the longevity of vaccine-induced immune protection. Go...
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| Published in | Science (American Association for the Advancement of Science) Vol. 374; no. 6572; p. abm0829 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
03.12.2021
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0036-8075 1095-9203 1095-9203 |
| DOI | 10.1126/science.abm0829 |
Cover
| Abstract | Vaccination against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has proven highly effective at preventing severe COVID-19. However, the evolution of viral variants, and waning antibody levels over time, raise questions regarding the longevity of vaccine-induced immune protection. Goel
et al
. examined B and T lymphocyte responses in individuals who received SARS-CoV-2 messenger RNA vaccines. They performed a 6-month longitudinal study of individuals who never had SARS-CoV-2 infection compared with people who had recovered from SARS-CoV-2. Humoral and cellular immune memory was observed in vaccinated individuals, as were functional immune responses against the Alpha (B.1.1.7), Beta (B.1.351), and Delta (B.1.617.2) viral variants. Analysis of T cell activity suggested that robust cellular immune memory may prevent hospitalization by limiting the development of severe disease. —PNK
Blood analysis of individuals vaccinated with the Moderna SARS-CoV-2 mRNA vaccine reveals distinct trajectories of immune memory responses.
The durability of immune memory after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) messenger RNA (mRNA) vaccination remains unclear. In this study, we longitudinally profiled vaccine responses in SARS-CoV-2–naïve and –recovered individuals for 6 months after vaccination. Antibodies declined from peak levels but remained detectable in most subjects at 6 months. By contrast, mRNA vaccines generated functional memory B cells that increased from 3 to 6 months postvaccination, with the majority of these cells cross-binding the Alpha, Beta, and Delta variants. mRNA vaccination further induced antigen-specific CD4
+
and CD8
+
T cells, and early CD4
+
T cell responses correlated with long-term humoral immunity. Recall responses to vaccination in individuals with preexisting immunity primarily increased antibody levels without substantially altering antibody decay rates. Together, these findings demonstrate robust cellular immune memory to SARS-CoV-2 and its variants for at least 6 months after mRNA vaccination. |
|---|---|
| AbstractList | The durability of immune memory after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) messenger RNA (mRNA) vaccination remains unclear. In this study, we longitudinally profiled vaccine responses in SARS-CoV-2–naïve and –recovered individuals for 6 months after vaccination. Antibodies declined from peak levels but remained detectable in most subjects at 6 months. By contrast, mRNA vaccines generated functional memory B cells that increased from 3 to 6 months postvaccination, with the majority of these cells cross-binding the Alpha, Beta, and Delta variants. mRNA vaccination further induced antigen-specific CD4
and CD8
T cells, and early CD4
T cell responses correlated with long-term humoral immunity. Recall responses to vaccination in individuals with preexisting immunity primarily increased antibody levels without substantially altering antibody decay rates. Together, these findings demonstrate robust cellular immune memory to SARS-CoV-2 and its variants for at least 6 months after mRNA vaccination. The durability of immune memory after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) messenger RNA (mRNA) vaccination remains unclear. In this study, we longitudinally profiled vaccine responses in SARS-CoV-2–naïve and –recovered individuals for 6 months after vaccination. Antibodies declined from peak levels but remained detectable in most subjects at 6 months. By contrast, mRNA vaccines generated functional memory B cells that increased from 3 to 6 months postvaccination, with the majority of these cells cross-binding the Alpha, Beta, and Delta variants. mRNA vaccination further induced antigen-specific CD4+ and CD8+ T cells, and early CD4+ T cell responses correlated with long-term humoral immunity. Recall responses to vaccination in individuals with preexisting immunity primarily increased antibody levels without substantially altering antibody decay rates. Together, these findings demonstrate robust cellular immune memory to SARS-CoV-2 and its variants for at least 6 months after mRNA vaccination.The durability of immune memory after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) messenger RNA (mRNA) vaccination remains unclear. In this study, we longitudinally profiled vaccine responses in SARS-CoV-2–naïve and –recovered individuals for 6 months after vaccination. Antibodies declined from peak levels but remained detectable in most subjects at 6 months. By contrast, mRNA vaccines generated functional memory B cells that increased from 3 to 6 months postvaccination, with the majority of these cells cross-binding the Alpha, Beta, and Delta variants. mRNA vaccination further induced antigen-specific CD4+ and CD8+ T cells, and early CD4+ T cell responses correlated with long-term humoral immunity. Recall responses to vaccination in individuals with preexisting immunity primarily increased antibody levels without substantially altering antibody decay rates. Together, these findings demonstrate robust cellular immune memory to SARS-CoV-2 and its variants for at least 6 months after mRNA vaccination. Vaccination against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has proven highly effective at preventing severe COVID-19. However, the evolution of viral variants, and waning antibody levels over time, raise questions regarding the longevity of vaccine-induced immune protection. Goel et al . examined B and T lymphocyte responses in individuals who received SARS-CoV-2 messenger RNA vaccines. They performed a 6-month longitudinal study of individuals who never had SARS-CoV-2 infection compared with people who had recovered from SARS-CoV-2. Humoral and cellular immune memory was observed in vaccinated individuals, as were functional immune responses against the Alpha (B.1.1.7), Beta (B.1.351), and Delta (B.1.617.2) viral variants. Analysis of T cell activity suggested that robust cellular immune memory may prevent hospitalization by limiting the development of severe disease. —PNK Blood analysis of individuals vaccinated with the Moderna SARS-CoV-2 mRNA vaccine reveals distinct trajectories of immune memory responses. The durability of immune memory after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) messenger RNA (mRNA) vaccination remains unclear. In this study, we longitudinally profiled vaccine responses in SARS-CoV-2–naïve and –recovered individuals for 6 months after vaccination. Antibodies declined from peak levels but remained detectable in most subjects at 6 months. By contrast, mRNA vaccines generated functional memory B cells that increased from 3 to 6 months postvaccination, with the majority of these cells cross-binding the Alpha, Beta, and Delta variants. mRNA vaccination further induced antigen-specific CD4 + and CD8 + T cells, and early CD4 + T cell responses correlated with long-term humoral immunity. Recall responses to vaccination in individuals with preexisting immunity primarily increased antibody levels without substantially altering antibody decay rates. Together, these findings demonstrate robust cellular immune memory to SARS-CoV-2 and its variants for at least 6 months after mRNA vaccination. The durability of immune memory after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) messenger RNA (mRNA) vaccination remains unclear. In this study, we longitudinally profiled vaccine responses in SARS-CoV-2–naïve and –recovered individuals for 6 months after vaccination. Antibodies declined from peak levels but remained detectable in most subjects at 6 months. By contrast, mRNA vaccines generated functional memory B cells that increased from 3 to 6 months postvaccination, with the majority of these cells cross-binding the Alpha, Beta, and Delta variants. mRNA vaccination further induced antigen-specific CD4+ and CD8+ T cells, and early CD4+ T cell responses correlated with long-term humoral immunity. Recall responses to vaccination in individuals with preexisting immunity primarily increased antibody levels without substantially altering antibody decay rates. Together, these findings demonstrate robust cellular immune memory to SARS-CoV-2 and its variants for at least 6 months after mRNA vaccination. Immune memory after vaccinationVaccination against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has proven highly effective at preventing severe COVID-19. However, the evolution of viral variants, and waning antibody levels over time, raise questions regarding the longevity of vaccine-induced immune protection. Goel et al. examined B and T lymphocyte responses in individuals who received SARS-CoV-2 messenger RNA vaccines. They performed a 6-month longitudinal study of individuals who never had SARS-CoV-2 infection compared with people who had recovered from SARS-CoV-2. Humoral and cellular immune memory was observed in vaccinated individuals, as were functional immune responses against the Alpha (B.1.1.7), Beta (B.1.351), and Delta (B.1.617.2) viral variants. Analysis of T cell activity suggested that robust cellular immune memory may prevent hospitalization by limiting the development of severe disease. —PNKINTRODUCTIONSevere acute respiratory syndrome coronavirus 2 (SARS-CoV-2) mRNA vaccines are highly effective at preventing infection and especially severe disease. However, the emergence of variants of concern (VOCs) and increasing infections in vaccinated individuals have raised questions about the durability of immunity after vaccination.RATIONALETo study immune memory, we longitudinally profiled antigen-specific antibody, memory B cell, and memory T cell responses in 61 individuals receiving mRNA vaccines from baseline to 6 months postvaccination. A subgroup of 16 individuals had recovered from prior SARS-CoV-2 infection, providing insight into boosting preexisting immunity with mRNA vaccines.RESULTSmRNA vaccination induced robust anti-spike, anti–receptor binding domain (RBD), and neutralizing antibodies that remained above prevaccine baseline levels in most individuals at 6 months postvaccination, although antibodies did decline over time. mRNA vaccination also generated spike- and RBD-specific memory B cells, including memory B cells that cross-bound Alpha, Beta, and Delta RBDs, that were capable of rapidly producing functional antibodies after stimulation. Notably, the frequency of SARS-CoV-2–specific memory B cells continued to increase from 3 to 6 months postvaccination. mRNA vaccines also generated a higher frequency of variant cross-binding memory B cells than mild SARS-CoV-2 infection alone, with >50% of RBD-specific memory B cells cross-binding all three VOCs at 6 months. These variant-binding memory B cells were more hypermutated than wild-type–only binding cells. SARS-CoV-2–specific memory CD4+ and CD8+ T cell responses contracted from peak levels after the second vaccine dose, with relative stabilization of SARS-CoV-2–specific memory CD4+ T cells from 3 to 6 months. T follicular helper cell responses after the first vaccine dose correlated with antibodies at 6 months, highlighting a key role for early CD4+ T cell responses. Finally, recall responses to mRNA vaccination in individuals with preexisting immunity led to an increase in circulating antibody titers that correlated with preexisting memory B cell frequency. However, there was no substantial increase in the long-term frequency of memory B and T cells. There was also no significant difference in the decay rates of antibodies in SARS-CoV-2–naïve versus –recovered subjects after vaccination, which suggests that the main benefit of recall responses to mRNA vaccination may be a robust but transient increase in circulating antibodies.CONCLUSIONThese findings demonstrate multicomponent immune memory after SARS-CoV-2 mRNA vaccination, with memory B and T cell responses remaining durable even as antibodies decline. Immune memory was resilient to VOCs and generated an efficient recall response upon antigen reexposure. These durable memory cells may be responsible for continued protection against severe disease in vaccinated individuals, despite a gradual reduction in antibodies. Our data may also inform expectations for the immunological outcomes of booster vaccination.The durability of immune memory after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) messenger RNA (mRNA) vaccination remains unclear. In this study, we longitudinally profiled vaccine responses in SARS-CoV-2–naïve and –recovered individuals for 6 months after vaccination. Antibodies declined from peak levels but remained detectable in most subjects at 6 months. By contrast, mRNA vaccines generated functional memory B cells that increased from 3 to 6 months postvaccination, with the majority of these cells cross-binding the Alpha, Beta, and Delta variants. mRNA vaccination further induced antigen-specific CD4+ and CD8+ T cells, and early CD4+ T cell responses correlated with long-term humoral immunity. Recall responses to vaccination in individuals with preexisting immunity primarily increased antibody levels without substantially altering antibody decay rates. Together, these findings demonstrate robust cellular immune memory to SARS-CoV-2 and its variants for at least 6 months after mRNA vaccination. |
| Author | Meng, Wenzhao Apostolidis, Sokratis A. Painter, Mark M. Giles, Josephine R. Weiskopf, Daniela Goel, Rishi R. Rosenfeld, Aaron M. Kuri-Cervantes, Leticia Tanenbaum, Nicole Long, Sherea Sette, Alessandro Wherry, E. John McAllister, Christopher M. Reynaldi, Arnold Drapeau, Elizabeth M. Khoury, David S. D’Andrea, Kurt Baxter, Amy E. Awofolaju, Moses Davenport, Miles P. Grifoni, Alba Hensley, Scott E. Gouma, Sigrid Adamski, Sharon Dougherty, Jeanette Hicks, Amanda Hamilton, Jacob T. Herring, Sarah Hicks, Philip Korte, Scott Pattekar, Ajinkya Williams, Justine C. Sharma, Harsh Lundgreen, Kendall A. McLaughlin, Maura Weirick, Madison E. Frank, Ian Betts, Michael R. Bates, Paul Vella, Laura A. Kuthuru, Oliva Luning Prak, Eline T. Greenplate, Allison R. Oldridge, Derek A. Mathew, Divij Dysinger, Sarah |
| AuthorAffiliation | 2 Immune Health™, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USAs 3 Division of Rheumatology, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USA 12 Department of Medicine, Division of Infectious Diseases and Global Public Health, University of California, San Diego (UCSD), La Jolla, CA, USA 8 Parker Institute for Cancer Immunotherapy, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USA 7 Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USA 9 Division of Infectious Disease, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USA 10 Division of Infectious Disease, Department of Pediatrics, Children’s Hospital of Philadelphia; Philadelphia, PA, USA 1 Institute for Immunology, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USA 5 Department of Microbiology, University of Pennsy |
| AuthorAffiliation_xml | – name: 2 Immune Health™, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USAs – name: 3 Division of Rheumatology, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USA – name: 5 Department of Microbiology, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USA – name: 11 Center for Infectious Disease and Vaccine Research, La Jolla Institute for Immunology (LJI); La Jolla, CA, USA – name: 4 Department of Pathology and Laboratory Medicine, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USA – name: 12 Department of Medicine, Division of Infectious Diseases and Global Public Health, University of California, San Diego (UCSD), La Jolla, CA, USA – name: 6 Kirby Institute, University of New South Wales; Sydney, Australia – name: 9 Division of Infectious Disease, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USA – name: 10 Division of Infectious Disease, Department of Pediatrics, Children’s Hospital of Philadelphia; Philadelphia, PA, USA – name: 1 Institute for Immunology, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USA – name: 7 Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USA – name: 8 Parker Institute for Cancer Immunotherapy, University of Pennsylvania Perelman School of Medicine; Philadelphia, PA, USA |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34648302$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY). |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author Contributions: RRG, MMP, and EJW designed the study. RRG, MMP, SAA, DM, WM, KL, SG, LKC, PH, SD, MEW, CMM, MA, NT, and EMD carried out experiments. RRG, SAA, JD, SL, and OK were involved in clinical recruitment and sample collection. WM, AMR, AR, DSK, DAO, JRG, MPD, and ELP provided expertise on statistical analyses. RRG, MMP, DM, and AEB contributed to the methodology. RRG, MMP, AP, AH, HS, SH, SK, JTH, JCW, and SA processed peripheral blood samples and managed the sample database. IF, AG, DW, and AS provided key samples and/or reagents. ELP, ARG and EJW supervised the study. All authors participated in data analysis and interpretation. RRG, MMP, ELP, and EJW wrote the manuscript. Equal contribution The UPenn COVID Processing Unit included individuals from diverse laboratories at the University of Pennsylvania who volunteered their time and effort to enable study of COVID-19 patients during the pandemic: S. Adamski, Z. Alam, M. M. Addison, K.T. Byrne, A. Chandra, H. C. Descamps, N. Han, Y. Kaminskiy, S. C. Kammerman, J. Kim, A. R. Greenplate, J. T. Hamilton, N. Markosyan, J. Han Noll, D. K. Omran, A.Pattekar, E. Perkey, E. M. Prager, D. Pueschl, A. Rennels, J. B. Shah, J. S. Shilan, N. Wilhausen, A. N. Vanderbeck. All are affiliated with the University of Pennsylvania Perelman School of Medicine. Members of the UPenn COVID Processing Unit are listed in the acknowledgments |
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| Snippet | Vaccination against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has proven highly effective at preventing severe COVID-19. However, the... The durability of immune memory after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) messenger RNA (mRNA) vaccination remains unclear. In this... Immune memory after vaccinationVaccination against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has proven highly effective at preventing... |
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| SubjectTerms | Antibodies Antigens Binding CD4 antigen CD8 antigen Coronaviruses Correlation COVID-19 COVID-19 Vaccines - immunology Decay Decay rate Durability Humans Humoral immunity Immunity Immunologic Memory Immunological memory Immunology Infections Longitudinal studies Lymphocytes Lymphocytes B Lymphocytes T Memory Memory cells mRNA mRNA vaccines mRNA Vaccines - immunology Questions Recall Respiratory diseases Robustness SARS-CoV-2 - genetics SARS-CoV-2 - immunology Severe acute respiratory syndrome coronavirus 2 Subgroups Vaccines Viral diseases |
| Title | mRNA vaccines induce durable immune memory to SARS-CoV-2 and variants of concern |
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