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Immune Correlates of Protection by mRNA-1273 Immunization against SARS-CoV-2 Infection in Nonhuman Primates

Kizzmekia S. Corbett, Martha C. Nason, Britta Flach, Matthew Gagne, Sarah O’ Connell, Timothy S. Johnston, Shruti N. Shah, Venkata Viswanadh Edara, Katharine Floyd, Lilin Lai, Charlene McDanal, Joseph R. Francica, Barbara Flynn, Kai Wu, Angela Choi, Matthew Koch, Olubukola M. Abiona, Anne P. Werner, Gabriela S. Alvarado, Shayne F. Andrew, Mitzi M. Donaldson, Jonathan Fintzi, Dillon R. Flebbe, Evan Lamb, Amy T. Noe, Saule T. Nurmukhambetova, Samantha J. Provost, Anthony Cook, Alan Dodson, Andrew Faudree, Jack Greenhouse, Swagata Kar, Laurent Pessaint, Maciel Porto, Katelyn Steingrebe, Daniel Valentin, Serge Zouantcha, Kevin W. Bock, Mahnaz Minai, Bianca M. Nagata, Juan I. Moliva, Renee van de Wetering, Seyhan Boyoglu-Barnum, Kwanyee Leung, Wei Shi, Eun Sung Yang, Yi Zhang, John-Paul M. Todd, Lingshu Wang, Hanne Andersen, Kathryn E. Foulds, Darin K. Edwards, John R. Mascola, Ian N. Moore, Mark G. Lewis, Andrea Carfi, David Montefiori, View ORCID ProfileMehul S. Suthar, Adrian McDermott, Nancy J. Sullivan, Mario Roederer, Daniel C. Douek, Barney S. Graham, Robert A. Seder
doi: https://doi.org/10.1101/2021.04.20.440647
Kizzmekia S. Corbett
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Martha C. Nason
2Biostatistics Research Branch, Division of Clinical Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Britta Flach
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Matthew Gagne
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Sarah O’ Connell
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Timothy S. Johnston
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Shruti N. Shah
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Venkata Viswanadh Edara
3Center for Childhood Infections and Vaccines of Children’s Healthcare of Atlanta, Department of Pediatrics, Department of Microbiology and Immunology, Emory Vaccine Center, Emory University, Atlanta, Georgia, 30322, United States of America
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Katharine Floyd
3Center for Childhood Infections and Vaccines of Children’s Healthcare of Atlanta, Department of Pediatrics, Department of Microbiology and Immunology, Emory Vaccine Center, Emory University, Atlanta, Georgia, 30322, United States of America
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Lilin Lai
3Center for Childhood Infections and Vaccines of Children’s Healthcare of Atlanta, Department of Pediatrics, Department of Microbiology and Immunology, Emory Vaccine Center, Emory University, Atlanta, Georgia, 30322, United States of America
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Charlene McDanal
4Department of Surgery, Duke University Medical Center, Durham, North Carolina, 27708; United States of America
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Joseph R. Francica
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Barbara Flynn
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Kai Wu
5Moderna Inc., Cambridge, MA, 02139; United States of America
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Angela Choi
5Moderna Inc., Cambridge, MA, 02139; United States of America
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Matthew Koch
5Moderna Inc., Cambridge, MA, 02139; United States of America
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Olubukola M. Abiona
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Anne P. Werner
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Gabriela S. Alvarado
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Shayne F. Andrew
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Mitzi M. Donaldson
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Jonathan Fintzi
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Dillon R. Flebbe
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Evan Lamb
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Amy T. Noe
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Saule T. Nurmukhambetova
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Samantha J. Provost
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Anthony Cook
6Bioqual, Inc.; Rockville, Maryland, 20850; United States of America
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Alan Dodson
6Bioqual, Inc.; Rockville, Maryland, 20850; United States of America
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Andrew Faudree
6Bioqual, Inc.; Rockville, Maryland, 20850; United States of America
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Jack Greenhouse
6Bioqual, Inc.; Rockville, Maryland, 20850; United States of America
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Swagata Kar
6Bioqual, Inc.; Rockville, Maryland, 20850; United States of America
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Laurent Pessaint
6Bioqual, Inc.; Rockville, Maryland, 20850; United States of America
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Maciel Porto
6Bioqual, Inc.; Rockville, Maryland, 20850; United States of America
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Katelyn Steingrebe
6Bioqual, Inc.; Rockville, Maryland, 20850; United States of America
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Daniel Valentin
6Bioqual, Inc.; Rockville, Maryland, 20850; United States of America
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Serge Zouantcha
6Bioqual, Inc.; Rockville, Maryland, 20850; United States of America
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Kevin W. Bock
7Infectious Disease Pathogenesis Section; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Mahnaz Minai
7Infectious Disease Pathogenesis Section; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Bianca M. Nagata
7Infectious Disease Pathogenesis Section; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Juan I. Moliva
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Renee van de Wetering
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Seyhan Boyoglu-Barnum
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Kwanyee Leung
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Wei Shi
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Eun Sung Yang
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Yi Zhang
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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John-Paul M. Todd
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Lingshu Wang
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Hanne Andersen
6Bioqual, Inc.; Rockville, Maryland, 20850; United States of America
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Kathryn E. Foulds
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Darin K. Edwards
5Moderna Inc., Cambridge, MA, 02139; United States of America
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John R. Mascola
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Ian N. Moore
7Infectious Disease Pathogenesis Section; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Mark G. Lewis
6Bioqual, Inc.; Rockville, Maryland, 20850; United States of America
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Andrea Carfi
5Moderna Inc., Cambridge, MA, 02139; United States of America
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David Montefiori
4Department of Surgery, Duke University Medical Center, Durham, North Carolina, 27708; United States of America
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Mehul S. Suthar
3Center for Childhood Infections and Vaccines of Children’s Healthcare of Atlanta, Department of Pediatrics, Department of Microbiology and Immunology, Emory Vaccine Center, Emory University, Atlanta, Georgia, 30322, United States of America
8Department of Microbiology and Immunology; Emory University; Atlanta, Georgia, 30329, United States of America
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  • ORCID record for Mehul S. Suthar
Adrian McDermott
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Nancy J. Sullivan
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Mario Roederer
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Daniel C. Douek
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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Barney S. Graham
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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  • For correspondence: rseder@mail.nih.gov bgraham@nih.gov
Robert A. Seder
1Vaccine Research Center; National Institute of Allergy and Infectious Diseases; National Institutes of Health; Bethesda, Maryland, 20892; United States of America
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  • For correspondence: rseder@mail.nih.gov bgraham@nih.gov
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Abstract

Immune correlates of protection can be used as surrogate endpoints for vaccine efficacy. The nonhuman primate (NHP) model of SARS-CoV-2 infection replicates key features of human infection and may be used to define immune correlates of protection following vaccination. Here, NHP received either no vaccine or doses ranging from 0.3 – 100 μg of mRNA-1273, a mRNA vaccine encoding the prefusion-stabilized SARS-CoV-2 spike (S-2P) protein encapsulated in a lipid nanoparticle. mRNA-1273 vaccination elicited robust circulating and mucosal antibody responses in a dose-dependent manner. Viral replication was significantly reduced in bronchoalveolar lavages and nasal swabs following SARS-CoV-2 challenge in vaccinated animals and was most strongly correlated with levels of anti-S antibody binding and neutralizing activity. Consistent with antibodies being a correlate of protection, passive transfer of vaccine-induced IgG to naïve hamsters was sufficient to mediate protection. Taken together, these data show that mRNA-1273 vaccine-induced humoral immune responses are a mechanistic correlate of protection against SARS-CoV-2 infection in NHP.

One-Sentence Summary mRNA-1273 vaccine-induced antibody responses are a mechanistic correlate of protection against SARS-CoV-2 infection in NHP.

Competing Interest Statement

K.S.C. and B.S.G. are inventors on U.S. Patent No. 10,960,070 B2 and International Patent Application No. WO/2018/081318 entitled Prefusion Coronavirus Spike Proteins and Their Use. K.S.C., O.M.A., and B.S.G. are inventors on US Patent Application No. 62/972,886 entitled 2019-nCoV Vaccine.

Footnotes

  • Editorial changes such as author names and units have been changed where necessary.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Immune Correlates of Protection by mRNA-1273 Immunization against SARS-CoV-2 Infection in Nonhuman Primates
Kizzmekia S. Corbett, Martha C. Nason, Britta Flach, Matthew Gagne, Sarah O’ Connell, Timothy S. Johnston, Shruti N. Shah, Venkata Viswanadh Edara, Katharine Floyd, Lilin Lai, Charlene McDanal, Joseph R. Francica, Barbara Flynn, Kai Wu, Angela Choi, Matthew Koch, Olubukola M. Abiona, Anne P. Werner, Gabriela S. Alvarado, Shayne F. Andrew, Mitzi M. Donaldson, Jonathan Fintzi, Dillon R. Flebbe, Evan Lamb, Amy T. Noe, Saule T. Nurmukhambetova, Samantha J. Provost, Anthony Cook, Alan Dodson, Andrew Faudree, Jack Greenhouse, Swagata Kar, Laurent Pessaint, Maciel Porto, Katelyn Steingrebe, Daniel Valentin, Serge Zouantcha, Kevin W. Bock, Mahnaz Minai, Bianca M. Nagata, Juan I. Moliva, Renee van de Wetering, Seyhan Boyoglu-Barnum, Kwanyee Leung, Wei Shi, Eun Sung Yang, Yi Zhang, John-Paul M. Todd, Lingshu Wang, Hanne Andersen, Kathryn E. Foulds, Darin K. Edwards, John R. Mascola, Ian N. Moore, Mark G. Lewis, Andrea Carfi, David Montefiori, Mehul S. Suthar, Adrian McDermott, Nancy J. Sullivan, Mario Roederer, Daniel C. Douek, Barney S. Graham, Robert A. Seder
bioRxiv 2021.04.20.440647; doi: https://doi.org/10.1101/2021.04.20.440647
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Immune Correlates of Protection by mRNA-1273 Immunization against SARS-CoV-2 Infection in Nonhuman Primates
Kizzmekia S. Corbett, Martha C. Nason, Britta Flach, Matthew Gagne, Sarah O’ Connell, Timothy S. Johnston, Shruti N. Shah, Venkata Viswanadh Edara, Katharine Floyd, Lilin Lai, Charlene McDanal, Joseph R. Francica, Barbara Flynn, Kai Wu, Angela Choi, Matthew Koch, Olubukola M. Abiona, Anne P. Werner, Gabriela S. Alvarado, Shayne F. Andrew, Mitzi M. Donaldson, Jonathan Fintzi, Dillon R. Flebbe, Evan Lamb, Amy T. Noe, Saule T. Nurmukhambetova, Samantha J. Provost, Anthony Cook, Alan Dodson, Andrew Faudree, Jack Greenhouse, Swagata Kar, Laurent Pessaint, Maciel Porto, Katelyn Steingrebe, Daniel Valentin, Serge Zouantcha, Kevin W. Bock, Mahnaz Minai, Bianca M. Nagata, Juan I. Moliva, Renee van de Wetering, Seyhan Boyoglu-Barnum, Kwanyee Leung, Wei Shi, Eun Sung Yang, Yi Zhang, John-Paul M. Todd, Lingshu Wang, Hanne Andersen, Kathryn E. Foulds, Darin K. Edwards, John R. Mascola, Ian N. Moore, Mark G. Lewis, Andrea Carfi, David Montefiori, Mehul S. Suthar, Adrian McDermott, Nancy J. Sullivan, Mario Roederer, Daniel C. Douek, Barney S. Graham, Robert A. Seder
bioRxiv 2021.04.20.440647; doi: https://doi.org/10.1101/2021.04.20.440647

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