Defining the risk of SARS-CoV-2 variants on immune protection

• Type of Material: Article
• Authors: Marciela M DeGrace, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Elodie Ghedin, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Matthew B Frieman, The University of Maryland; Florian Krammer, Icahn School of Medicine at Mount Sinai; Alba Grifoni, La Jolla Institute for Immunology; Arghavan Alisoltani, University of California Riverside; Galit Alter, Massachusetts Institute of Technology; Rama Amara, Emory University; Ralph S Baric, University of North Carolina Chapel Hill; Dan H Barouch, Beth Israel Deaconess Medical Center; Jesse D Bloom, Howard Hughes Medical Institute; Louis-Marie Bloyet, Washington University; Gaston Bonenfant, CDC COVID 19 Emergency Response; Adrianus CM Boon, Washington University in St. Louis; Eli A Boritz, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Debbie L Bratt, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Traci L Bricker, Washington University in St. Louis; Liliana Brown, National Institute of Allergy and Infectious Diseases, NIH, Rockville; William J Buchser, Washington University in St. Louis; Juan Manuel Carreño, Icahn School of Medicine at Mount Sinai; Liel Cohen-Lavi, Ben-Gurion University of the Negev; Tamarand L Darling, Washington University in St. Louis; Meredith E Davis-Gardner, Emory University; Bethany L Dearlove, Jackson Foundation for the Advancement of Military Medicine, Inc.; Han Di, Centers for Disease Control and Prevention, Atlanta; Meike Dittmann, New York University; Nicole A Doria-Rose, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Daniel C Douek, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Christian Drosten, Charité – Universitätsmedizin and German Center for Infection Research (DZIF); Venkata-Viswanadh Edara, Emory University; Ali Ellebedy, Washington University in St. Louis; Thomas P Fabrizio, St Jude Childrens Research Hospital; Guido Ferrari, Duke University Medical Center; William C Florence, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Ron AM Fouchier, Erasmus MC; John Franks, St Jude Childrens Research Hospital; Adolfo García-Sastre, Icahn School of Medicine at Mount Sinai; Adam Godzik, University of California Riverside; Ana Silvia Gonzalez-Reiche, Icahn School of Medicine at Mount Sinai; Aubree Gordon, University of Michigan; Bart L Haagmans, Erasmus MC; Peter J Halfmann, University of Wisconsin, Madison; David D Ho, Columbia University; Michael R Holbrook, National Institute of Allergy and Infectious Diseases Integrated Research Facility, Frederick; Yaxoing Huang, Columbia University; Sarah L James, University of Cambridge; Lukasz Jaroszewski, University of California Riverside; Trushar Jeevan, St Jude Childrens Research Hospital; Robert M Johnson, Univ Maryland; Terry C Jones, Charité – Universitätsmedizin and German Center for Infection Research (DZIF); Astha Joshi, Washington University in St. Louis; Yoshihiro Kawaoka, University of Wisconsin-Madison; Lisa Kercher, St Jude Childrens Res Hosp; Marion PG Koopmans, Erasmus MC; Bette Korber, Los Alamos National Laboratory; Eilay Koren, Ben-Gurion University of the Negev; Richard A Koup, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Eric B LeGresley, University of Cambridge; Jacob E Lemieux, Broad Inst MIT & Harvard; Mariel J Liebeskind, Washington University in St. Louis; Zhuoming Liu, Washington University in St. Louis; Brandi Livingston, St Jude Childrens Res Hosp; James P Logue, University of Maryland; Yang Luo, Columbia University; Adrian B McDermott, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Margaret J McElrath, Fred Hutchinson Cancer Research Center, Seattle; Victoria A Meliopoulos, St Jude Childrens Research Hospital; Vineet D Menachery, University of Texas Medical Branch, Galveston; David C Montefiori, Duke University; Barbara Mühlemann, Charité – Universitätsmedizin and German Center for Infection Research (DZIF); Vincent J Munster, Natl Inst Allergy & Infect Dis; Jenny E Munt, University of North Carolina Chapel Hill; Manoj S Nair, Columbia University; Antonia Netzl, University of Cambridge; Anna M Niewiadomska, J. Craig Venter Institute; Sijy O'Dell, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Andrew Pekosz, Johns Hopkins Bloomberg Sch Publ Hlth; Stanley Perlman, University of Iowa; Marjorue C Pontelli, Washington University in St. Louis; Barry Rockx, Erasmus MC; Morgane Rolland, Walter Reed Army Institute of Research; Paul W Rothlauf, Washington University in St. Louis; Sinai Sacharen, Ben-Gurion University of the Negev; Richard H Scheuermann, J. Craig Venter Institute; Stephen D Schmidt, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Michael Schotsaert, Icahn School of Medicine at Mount Sinai; Stacey Schultz-Cherry, St Jude Childrens Research Hospital; Robert A Seder, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Mayya Sedova, University of California Riverside; Alessandro Sette, La Jolla Institute for Allergy and Immunology; Reed S Shabman, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Xiaoying Shen, Duke University; Pei-Yong Shi, The University of Texas Medical Branch, Galveston; Maulik Shukla, University of Chicago; Viviana Simon, Icahn School of Medicine at Mount Sinai; Spencer Stumpf, Washington University in St. Louis; Nancy J Sullivan, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Larissa B Thackray, Washington University in St. Louis; James Theiler, Los Alamos National Laboratory; Paul G Thomas, St Jude Childrens Research Hospital; Sanja Trifkovic, St Jude Childrens Research Hospital; Sina Tureli, University of Cambridge; Samuel A Turner, University of Cambridge; Maria A Vakaki, Washington University in St. Louis; Harm van Bakel, Icahn School of Medicine at Mount Sinai; Laura A VanBlargan, Washington University in St. Louis; Leah R Vincent, NIAID; Zachary S Wallace, J. Craig Venter Institute; Li Wang, CDC COVID 19 Emergency Response; Maple Wang, Columbia University; Pengfei Wang, Columbia University; Wei Wang, US Food and Drug Administration, Center for Biologics Evaluation and Research; Scott C Weaver, University of Texas Medical Branch, Galveston; Richard J Webby, St Jude Childrens Research Hospital; Carol D Weiss, US Food and Drug Administration, Center for Biologics Evaluation and Research; David E Wentworth, CDC COVID 19 Emergency Response; Stuart M Weston, University of Maryland; Sean PJ Whelan, Washington University in St. Louis; Bradley M Whitener, Washington University in St. Louis; Samuel H Wilks, University of Cambridge; Xuping Xie, The University of Texas Medical Branch; Baoling Ying, Washington University in St. Louis; Hyejin Yoon, Los Alamos National Laboratory; Bin Zhou, CDC COVID 19 Emergency Response; Tomer Hertz, Ben-Gurion University of the Negev; Derek J Smith, University of Cambridge; Michael S Diamond, Washington University in St. Louis; Diane DJ Post, National Institute of Allergy and Infectious Diseases, NIH, Rockville; Mehul Suthar, Emory University
• Language: English
• Date: 2022-03-31
• Publisher: NATURE PORTFOLIO
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2022, Springer Nature Limited
• Final Published Version (URL): http://dx.doi.org/10.1038/s41586-022-04690-5
• Title of Journal or Parent Work: NATURE
• Volume: 605
• Issue: 7911
• Start Page: 640
• End Page: 652
• Grant/Funding Information: AA is funded by HHSN272201700060C, GA is funded by the Ragon Institute of MGH, MIT, and Harvard, the Massachusetts Consortium on Pathogen Readiness (MassCPR), the National Institutes of Health (NIH) (3R37AI080289-11S1, R01AI146785, U19AI42790-01, U19AI135995-02, U19AI42790-01, 1U01CA260476-01), the Gates Foundation Global Health Vaccine Accelerator Platform funding (OPP1146996 and INV-001650), and the Musk Foundation, DCM and XS are supported in part by the National Institute of Allergy and Infectious Diseases (NIAID)/NIH Collaborative Influenza Vaccine Innovation Centers (CIVIC) under contract 75N93019C00050- Duke University, AE, AGor, JMC, FK, and VS are funded in part by NIH/NIAID CIVIC under contract 75N93019C00051-Icahn School of Medicine at Mt. Sinai, GA, BL, VAM, SSC, and PGT are funded in part by the NIH/NIAID Center for Influenza Vaccine Research for High-Risk Populations (CIVR-HRP) CIVIC under contract 75N93019C0052- University of Georgia, MSD, VS, LBT, HVB, LAV, RAMF, AGS, MBF, RMJ, JPL, SMW, BLH, DDH, YH, YL, MSN, PW, MW, DJS, AN, EBL, SLJ, STüre, SW, STurn, JMC, FK, BMW, BR and BY are supported by the NIH/NIAID Centers of Excellence for Influenza Research and Response (CEIRR) under contract 75N93021C00014-Icahn School of Medicine at Mt. Sinai, TPF, GF, JF, TJ, LK, BL, VAM, SSC, AS, ST, PGT, EK, LC-L, TH, SSac and RJW are funded in part by the NIH\NIAID CEIRR under contract 75N9302100016-St Jude Children’s Research Hospital, RRA, VVE, MDG and MSS is funded in part by the NIH/NIAID CEIRR under contract 75N93021C00017-Emory University, AE, TPF, JF, TJ, LK, BL, VAM, SSC, and ST SPJW, ZL, L-MB, PWR, MCP, Sstu, AG, AS and RJW are funded in part by the NIH/NIAID Centers of Excellence for Influenza Research and Surveillance (CEIRS) under contract HHSN272201400006C-St Jude Children’s Research Hospital, AP is supported in part by the NIH/NIAID CEIRS under contract HHS N2772201400007C- Johns Hopkins University, AE, MBF, RMJ, AGS, JPL, SMW, PJH, YK, JMC, FK, MSc, and VS are funded in part by the NIH/NIAID CEIRS under contract HHSN272201400008C- Icahn School of Medicine at Mt. Sinai, RRA is funded by 3R01AI148378-01S1, JDB is supported in part by R01AI141707 and is an Investigator of the Howard Hughes Medical Institute, ACMB is funded by U01AI151810, EB is supported by an Intramural NIH Research Program project #ZIA AI005156-02, DLB is supported by NIH/NIAID under contract 75N93019D0025 to CAMRIS International, EG and VJM are supported by the Intramural Research Program of the NIAID, NIH, BLD and MR are supported by a cooperative agreement between The Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc. and the U.S. Department of the Army (W81XWH-18-2-0040), MSD is supported in part by R01AI157155, MD is supported by 1R01AI143639, NADR, DCD, ABM, NJS, RAK, SO,SDS, and RAS are supported by the Intramural Research Program of the Vaccine Research Center, NIAID and NIH, CD, BAM, and TCJ are funded in part by the German Ministry of research under project codes DZIF, MolTrax and PREPARED, AE is supported by NIAID grants U01AI141990 and 1U01AI150747, VVE, MDG and MSS are supported in part by the NIH\NIAID (P51OD011132 and 3U19AI057266-17S1), Emory Executive Vice President for Health Affairs Synergy Fund award, and Woodruff Health Sciences Center 2020 COVID-19 CURE Award, Agod, LJ, MSe are supported by HHSN272201700060C, AGor is supported by R01AI20997, MRH is supported by NIAID contract HHSN272201800013C, MPGK is supported by VEO - Versatile emerging infectious disease observatory: Forecasting, nowcasting and tracking in a changing world. VEO has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement No. 874735, COVID-19 vaccination in kidney patients (RECOVAC) - ZonMw # 10430072010002 Monitoring the evolution, spread and transmission of SARS-CoV-2 through whole genome sequencing to enable fast genotype to phenotype prediction’ funded by ZonMw - project# 10150062010005, APW 202645827; To support the structured evaluation of SARS-CoV-2 evolution funded by WHO APW 202605269; To gain in-depth understanding of the evolution, spread and transmission of SARS-CoV-2 during the coming phase of the pandemic funded by WHO, BK, JT and HY are funded by the Los Alamos National Laboratory and the Gates Foundation OPP1169339, RAK is funded by Intramural NIH funding, MJM is supported by UM1AI068618, VDM is supported by R01AI153602, SMP is supported by P01AI060699 and R01AI129269, PYS is supported by NIH grants AI134907 and awards from the Sealy Smith Foundation, the Kleberg Foundation, the John S. Dunn Foundation, the Amon G. Carter Foundation, the Gillson Longenbaugh Foundation, and the Summerfield Robert Foundation, VS is supported by the NIH/NCI: Serological Sciences Network (SeroNet) 75N91019D00024, PGT is supported by U01AI144616, U01AI150747, R01AI136514, R01AI154470, ZSW, RHS, AMN, MSh are supported by NIH, NIAID Contract 75N93019C00076, WW and CDW are supported by US Food and Drug Administration institutional research funds. SCW is supported by NIH grant R24 AI120942 and by the Sealy and Smith Foundation.
• Keywords: Science & Technology - Other Topics; MUTATIONS; HIV-1; VACCINE; EFFECTOR FUNCTIONS; RECEPTOR-BINDING DOMAIN; INFLUENZA-VIRUS INFECTION; Science & Technology; NEUTRALIZING ANTIBODIES; Multidisciplinary Sciences; EVOLUTION; MONOCLONAL-ANTIBODIES; EFFICACY

Abstract

The global emergence of many severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants jeopardizes the protective antiviral immunity induced after infection or vaccination. To address the public health threat caused by the increasing SARS-CoV-2 genomic diversity, the National Institute of Allergy and Infectious Diseases within the National Institutes of Health established the SARS-CoV-2 Assessment of Viral Evolution (SAVE) programme. This effort was designed to provide a real-time risk assessment of SARS-CoV-2 variants that could potentially affect the transmission, virulence, and resistance to infection- and vaccine-induced immunity. The SAVE programme is a critical data-generating component of the US Government SARS-CoV-2 Interagency Group to assess implications of SARS-CoV-2 variants on diagnostics, vaccines and therapeutics, and for communicating public health risk. Here we describe the coordinated approach used to identify and curate data about emerging variants, their impact on immunity and effects on vaccine protection using animal models. We report the development of reagents, methodologies, models and notable findings facilitated by this collaborative approach and identify future challenges. This programme is a template for the response to rapidly evolving pathogens with pandemic potential by monitoring viral evolution in the human population to identify variants that could reduce the effectiveness of countermeasures.