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

Marciela M. DeGrace; Elodie Ghedin; Matthew B. Frieman; Florian Krammer; Alba Grifoni; Arghavan Alisoltani; Galit Alter; Rama R. Amara; Ralph S. Baric; Dan H. Barouch; Jesse D. Bloom; Louis Marie Bloyet; Gaston Bonenfant; Adrianus C.M. Boon; Eli A. Boritz; Debbie L. Bratt; Traci L. Bricker; Liliana Brown; William J. Buchser; Juan Manuel Carreño; Liel Cohen-Lavi; Tamarand L. Darling; Meredith E. Davis-Gardner; Bethany L. Dearlove; Han Di; Meike Dittmann; Nicole A. Doria-Rose; Daniel C. Douek; Christian Drosten; Venkata Viswanadh Edara; Ali Ellebedy; Thomas P. Fabrizio; Guido Ferrari; Will M. Fischer; William C. Florence; Ron A.M. Fouchier; John Franks; Adolfo García-Sastre; Adam Godzik; Ana Silvia Gonzalez-Reiche; Aubree Gordon; Bart L. Haagmans; Peter J. Halfmann; David D. Ho; Michael R. Holbrook; Yaoxing Huang; Sarah L. James; Lukasz Jaroszewski; Trushar Jeevan; Robert M. Johnson; Terry C. Jones; Astha Joshi; Yoshihiro Kawaoka; Lisa Kercher; Marion P.G. Koopmans; Bette Korber; Eilay Koren; Richard A. Koup; Eric B. LeGresley; Jacob E. Lemieux; Mariel J. Liebeskind; Zhuoming Liu; Brandi Livingston; James P. Logue; Yang Luo; Adrian B. McDermott; Margaret J. McElrath; Victoria A. Meliopoulos; Vineet D. Menachery; David C. Montefiori; Barbara Mühlemann; Vincent J. Munster; Jenny E. Munt; Manoj S. Nair; Antonia Netzl; Anna M. Niewiadomska; Sijy O’Dell; Andrew Pekosz; Stanley Perlman; Marjorie C. Pontelli; Barry Rockx; Morgane Rolland; Paul W. Rothlauf; Sinai Sacharen; Richard H. Scheuermann; Stephen D. Schmidt; Michael Schotsaert; Stacey Schultz-Cherry; Robert A. Seder; Mayya Sedova; Alessandro Sette; Reed S. Shabman; Xiaoying Shen; Pei Yong Shi; Maulik Shukla; Viviana Simon; Spencer Stumpf; Nancy J. Sullivan; Larissa B. Thackray; James Theiler; Paul G. Thomas; Sanja Trifkovic; Sina Türeli; Samuel A. Turner; Maria A. Vakaki; Harm van Bakel; Laura A. VanBlargan; Leah R. Vincent; Zachary S. Wallace; Li Wang; Maple Wang; Pengfei Wang; Wei Wang; Scott C. Weaver; Richard J. Webby; Carol D. Weiss; David E. Wentworth; Stuart M. Weston; Sean P.J. Whelan; Bradley M. Whitener; Samuel H. Wilks; Xuping Xie; Baoling Ying; Hyejin Yoon; Bin Zhou; Tomer Hertz; Derek J. Smith; Michael S. Diamond; Diane J. Post; Mehul S. Suthar

doi:10.1038/s41586-022-04690-5

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

Marciela M. DeGrace, Elodie Ghedin, Matthew B. Frieman, Florian Krammer, Alba Grifoni, Arghavan Alisoltani, Galit Alter, Rama R. Amara, Ralph S. Baric, Dan H. Barouch, Jesse D. Bloom, Louis Marie Bloyet, Gaston Bonenfant, Adrianus C.M. Boon, Eli A. Boritz, Debbie L. Bratt, Traci L. Bricker, Liliana Brown, William J. Buchser, Juan Manuel CarreñoLiel Cohen-Lavi, Tamarand L. Darling, Meredith E. Davis-Gardner, Bethany L. Dearlove, Han Di, Meike Dittmann, Nicole A. Doria-Rose, Daniel C. Douek, Christian Drosten, Venkata Viswanadh Edara, Ali Ellebedy, Thomas P. Fabrizio, Guido Ferrari, Will M. Fischer, William C. Florence, Ron A.M. Fouchier, John Franks, Adolfo García-Sastre, Adam Godzik, Ana Silvia Gonzalez-Reiche, Aubree Gordon, Bart L. Haagmans, Peter J. Halfmann, David D. Ho, Michael R. Holbrook, Yaoxing Huang, Sarah L. James, Lukasz Jaroszewski, Trushar Jeevan, Robert M. Johnson, Terry C. Jones, Astha Joshi, Yoshihiro Kawaoka, Lisa Kercher, Marion P.G. Koopmans, Bette Korber, Eilay Koren, Richard A. Koup, Eric B. LeGresley, Jacob E. Lemieux, Mariel J. Liebeskind, Zhuoming Liu, Brandi Livingston, James P. Logue, Yang Luo, Adrian B. McDermott, Margaret J. McElrath, Victoria A. Meliopoulos, Vineet D. Menachery, David C. Montefiori, Barbara Mühlemann, Vincent J. Munster, Jenny E. Munt, Manoj S. Nair, Antonia Netzl, Anna M. Niewiadomska, Sijy O’Dell, Andrew Pekosz, Stanley Perlman, Marjorie C. Pontelli, Barry Rockx, Morgane Rolland, Paul W. Rothlauf, Sinai Sacharen, Richard H. Scheuermann, Stephen D. Schmidt, Michael Schotsaert, Stacey Schultz-Cherry, Robert A. Seder, Mayya Sedova, Alessandro Sette, Reed S. Shabman, Xiaoying Shen, Pei Yong Shi, Maulik Shukla, Viviana Simon, Spencer Stumpf, Nancy J. Sullivan, Larissa B. Thackray, James Theiler, Paul G. Thomas, Sanja Trifkovic, Sina Türeli, Samuel A. Turner, Maria A. Vakaki, Harm van Bakel, Laura A. VanBlargan, Leah R. Vincent, Zachary S. Wallace, Li Wang, Maple Wang, Pengfei Wang, Wei Wang, Scott C. Weaver, Richard J. Webby, Carol D. Weiss, David E. Wentworth, Stuart M. Weston, Sean P.J. Whelan, Bradley M. Whitener, Samuel H. Wilks, Xuping Xie, Baoling Ying, Hyejin Yoon, Bin Zhou, Tomer Hertz, Derek J. Smith, Michael S. Diamond, Diane J. Post, Mehul S. Suthar

Research output: Contribution to journal › Review article › peer-review

108 Scopus citations

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.

Original language	English
Pages (from-to)	640-652
Number of pages	13
Journal	Nature
Volume	605
Issue number	7911
DOIs	https://doi.org/10.1038/s41586-022-04690-5
State	Published - 26 May 2022

ASJC Scopus subject areas

General

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1038/s41586-022-04690-5

Cite this

DeGrace, M. M., Ghedin, E., Frieman, M. B., Krammer, F., Grifoni, A., Alisoltani, A., Alter, G., Amara, R. R., Baric, R. S., Barouch, D. H., Bloom, J. D., Bloyet, L. M., Bonenfant, G., Boon, A. C. M., Boritz, E. A., Bratt, D. L., Bricker, T. L., Brown, L., Buchser, W. J., ... Suthar, M. S. (2022). Defining the risk of SARS-CoV-2 variants on immune protection. Nature, 605(7911), 640-652. https://doi.org/10.1038/s41586-022-04690-5

@article{c2570ca830a1408e9ab80716e4d86c3e,

title = "Defining the risk of SARS-CoV-2 variants on immune protection",

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.",

author = "DeGrace, {Marciela M.} and Elodie Ghedin and Frieman, {Matthew B.} and Florian Krammer and Alba Grifoni and Arghavan Alisoltani and Galit Alter and Amara, {Rama R.} and Baric, {Ralph S.} and Barouch, {Dan H.} and Bloom, {Jesse D.} and Bloyet, {Louis Marie} and Gaston Bonenfant and Boon, {Adrianus C.M.} and Boritz, {Eli A.} and Bratt, {Debbie L.} and Bricker, {Traci L.} and Liliana Brown and Buchser, {William J.} and Carre{\~n}o, {Juan Manuel} and Liel Cohen-Lavi and Darling, {Tamarand L.} and Davis-Gardner, {Meredith E.} and Dearlove, {Bethany L.} and Han Di and Meike Dittmann and Doria-Rose, {Nicole A.} and Douek, {Daniel C.} and Christian Drosten and Edara, {Venkata Viswanadh} and Ali Ellebedy and Fabrizio, {Thomas P.} and Guido Ferrari and Fischer, {Will M.} and Florence, {William C.} and Fouchier, {Ron A.M.} and John Franks and Adolfo Garc{\'i}a-Sastre and Adam Godzik and Gonzalez-Reiche, {Ana Silvia} and Aubree Gordon and Haagmans, {Bart L.} and Halfmann, {Peter J.} and Ho, {David D.} and Holbrook, {Michael R.} and Yaoxing Huang and James, {Sarah L.} and Lukasz Jaroszewski and Trushar Jeevan and Johnson, {Robert M.} and Jones, {Terry C.} and Astha Joshi and Yoshihiro Kawaoka and Lisa Kercher and Koopmans, {Marion P.G.} and Bette Korber and Eilay Koren and Koup, {Richard A.} and LeGresley, {Eric B.} and Lemieux, {Jacob E.} and Liebeskind, {Mariel J.} and Zhuoming Liu and Brandi Livingston and Logue, {James P.} and Yang Luo and McDermott, {Adrian B.} and McElrath, {Margaret J.} and Meliopoulos, {Victoria A.} and Menachery, {Vineet D.} and Montefiori, {David C.} and Barbara M{\"u}hlemann and Munster, {Vincent J.} and Munt, {Jenny E.} and Nair, {Manoj S.} and Antonia Netzl and Niewiadomska, {Anna M.} and Sijy O{\textquoteright}Dell and Andrew Pekosz and Stanley Perlman and Pontelli, {Marjorie C.} and Barry Rockx and Morgane Rolland and Rothlauf, {Paul W.} and Sinai Sacharen and Scheuermann, {Richard H.} and Schmidt, {Stephen D.} and Michael Schotsaert and Stacey Schultz-Cherry and Seder, {Robert A.} and Mayya Sedova and Alessandro Sette and Shabman, {Reed S.} and Xiaoying Shen and Shi, {Pei Yong} and Maulik Shukla and Viviana Simon and Spencer Stumpf and Sullivan, {Nancy J.} and Thackray, {Larissa B.} and James Theiler and Thomas, {Paul G.} and Sanja Trifkovic and Sina T{\"u}reli and Turner, {Samuel A.} and Vakaki, {Maria A.} and {van Bakel}, Harm and VanBlargan, {Laura A.} and Vincent, {Leah R.} and Wallace, {Zachary S.} and Li Wang and Maple Wang and Pengfei Wang and Wei Wang and Weaver, {Scott C.} and Webby, {Richard J.} and Weiss, {Carol D.} and Wentworth, {David E.} and Weston, {Stuart M.} and Whelan, {Sean P.J.} and Whitener, {Bradley M.} and Wilks, {Samuel H.} and Xuping Xie and Baoling Ying and Hyejin Yoon and Bin Zhou and Tomer Hertz and Smith, {Derek J.} and Diamond, {Michael S.} and Post, {Diane J.} and Suthar, {Mehul S.}",

note = "Funding Information: D.H.B. is listed as a co-inventor on provisional vaccine patents (63/121,482; 63/133,969; 63/135,182). J.D.B. consults for Moderna and Flagship Labs 77 on topics related to viral evolution, and is an inventor on Fred Hutch licensed patents related to viral deep mutational scanning (62/692,398; PCT/US2019/039952; 17/281,540; 19824586.2; 62/935,954; 17/097,853; 62/812,804; PCT/US2020/020429). The Boon laboratory has received unrelated funding support in sponsored research agreements from AI Therapeutics, GreenLight Biosciences, and Nano targeting & Therapy Biopharma. The Boon laboratory has received funding support from AbbVie, for the commercial development of SARS-CoV-2 monoclonal antibodies. A.C.M.B. was a recipient of a licensing agreement with Abbvie for the commercial development of SARS-CoV-2 monoclonal antibodies. M.S.D. is a consultant for Inbios, Vir Biotechnology, Senda Biosciences and Carnival Corporation, and on the scientific advisory boards of Moderna and Immunome. The Diamond laboratory has received unrelated funding support in sponsored research agreements from Vir Biotechnology, Moderna and Emergent BioSolutions. The Ellebedy laboratory received funding under sponsored research agreements that are unrelated to the data presented in the current study from Emergent BioSolutions and from AbbVie. A.E. has received consulting fees from InBios International, Fimbrion Therapeutics, Mubadala Investment Company and Goldman Sachs and is the founder of ImmuneBio Consulting. M.B.F. has funding from Novavax, which is outside the scope of this research. They had no role in the funded research from the SAVES consortium. The Garcia-Sastre laboratory has received research support from Pfizer, Senhwa Biosciences, Kenall Manufacturing, Avimex, Johnson & Johnson, Dynavax, 7Hills Pharma, Pharmamar, ImmunityBio, Accurius, Nanocomposix, Hexamer, N-fold, Model Medicines and Merck, outside of the reported work. A.G.-S. has consulting agreements for the following companies involving cash and/or stock: Vivaldi Biosciences, Contrafect, 7Hills Pharma, Avimex, Vaxalto, Pagoda, Accurius, Esperovax, Farmak, Applied Biological Laboratories, Pharmamar and Pfizer, outside of the reported work. A.G.-S. is listed as an inventor on patents and patent applications on the use of antivirals and vaccines for the treatment and prevention of virus infections and cancer, owned by the Icahn School of Medicine at Mount Sinai, New York, outside of the reported work (5,820,871; 5,854,037; 6,001,634; 6,146,642; 6,451,323; 6,468,544; 6,544,785; 6,573,079; 6,635,416; 6,649,372; 6,669,943; 6,740,519; 6,852,522; 6,866,853; 6,884,414; 6,887,699; 7,060,430; 7,384,774; 7,442,379; 7,494, 808; 7,588,768; 7,833,774; 8,012,490; 8,057,803; 8,124,101; 8,137,676; 8,591,881; 8,629,283; 8,673,314; 8,709,442; 8,709,730; 8,765,139; 8,828,406; 8,999,352; 9,051,359; 9,096,585; 9,175,069; 9,217,136; 9,217,157; 9,238,851; 9,352,033; 9,371,366; 9,387,240; 9,387,242; . 9,549,975; 9,701,723; 9,708,373; 9,849,172; 9,908,930; 9,968,670; 10,035,984; .10,098,945; 10,131,695; 10,137,189; 10,179,806; 10,251,922; 10,308,913; 10,543,268; 10,544,207; 10,583,188; 10,736,956; 11,254,733; 11,266,734). A. Gordon serves on a scientific advisory board for Janssen, Erasmus MC has a proprietary IP on MERS. B.K. is part of provisional patent applications for strategies for next-generation SARS-CoV-2 vaccines that address diversity (63/256,848, 17/234,590; S133955). The Icahn School of Medicine at Mount Sinai has filed patent applications relating to SARS-CoV-2 serological assays that list V.S. as a co-inventor (62/994,252; 63/018,457; 63/020,503; 63/024,436) and NDV-based SARS-CoV-2 vaccines that list F.K. as a co-inventor (63/251,020). Mount Sinai has spun out a company, Kantaro, to market serological tests for SARS-CoV-2. F.K. has consulted for Merck and Pfizer (before 2020), and is currently consulting for Pfizer, Seqirus, 3rd Rock Ventures and Avimex. The Krammer laboratory is also collaborating with Pfizer on animal models of SARS-CoV-2. V.D.M. has filed a patent on the reverse genetic system and reporter SARS-CoV-2 (63/000,713; 63/041,667). D.C.M. receives funding from Moderna to perform blinded assessments of vaccine-elicited neutralizing antibody responses in clinical studies of their COVID-19 vaccines. A.S. is a consultant for Gritstone Bio, Flow Pharma, Arcturus Therapeutics, ImmunoScape, CellCarta, Avalia, Moderna, Fortress and Repertoire. P.-Y.S. laboratory has received funding support in sponsored research agreements from GSK, Pfizer, Gilead, Novartis, Merck, IGM Biosciences and Atea Pharmaceuticals. P.-Y.S. is a member of the scientific advisory boards of AbImmune and is Founder of FlaviTech. M.S.S. serves on the advisory board for Moderna and Ocugen. P.G.T. serves on the scientific advisory board for Immunoscape and Cytoagents and has consulted for Johnson and Johnson. P.G.T. has received travel support and honoraria from Illumina and 10x Genomics. P.G.T. has patents related to viral infection treatment and T cell receptor biology (11,083,725; 2021/0299118; US-2019-0040381; 17/616,279; WO2021/214637). S.P.J.W. has filed a patent with Washington University for VSV- SARS-CoV-2 mutants to characterize antibody panels (PCT/US2021/027275). S.P.J.W. has received unrelated funding support in sponsored research agreements with Vir Biotechnology, AbbVie, and sAB therapeutics. Funding Information: A.A. is funded by HHSN272201700060C; G.A. 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; D.C.M. and X.S. 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; A.E., A. Gordon, J.M.C., F.K. and V.S. are funded in part by NIH/NIAID CIVIC under contract 75N93019C00051, Icahn School of Medicine at Mount Sinai; G.A., B.L., V.A.M., S.S.-C. and P.G.T. 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; M.S.D., V.S., L.B.T., H.v.B., L.A.V., R.A.M.F., A.G.-S., M.B.F., R.M.J., J.P.L., S.M.W., B.L.H., D.D.H., Y.H., Y.L., M.S.N., P.W., M.W., D.J.S., A.N., E.B.L., S.L.J., S. T{\"u}reli, S.M.W., S.A.T., J.M.C., F.K., B.M.W., B.R. and B.Y. are supported by the NIH/NIAID Centers of Excellence for Influenza Research and Response (CEIRR) under contract 75N93021C00014, Icahn School of Medicine at Mount Sinai; T.P.F., G.F., J.F., T.J., L.K., B.L., V.A.M., S.S.-C., A.S., S.T., P.G.T., E.K., L.C.-L., T.H., S. Sacharen and R.J.W. are funded in part by the NIH\NIAID CEIRR under contract 75N9302100016, St Jude Children{\textquoteright}s Research Hospital; R.R.A., V.-V.E., M.E.D.-G. and M.S.S. are funded in part by the NIH/NIAID CEIRR under contract 75N93021C00017, Emory University; A.E., T.P.F., J.F., T.J., L.K., B.L., V.A.M., S.S.-C., S.T. S.P.J.W., Z.L., L.-M.B., P.W.R., M.C.P., S. Stumpf, A.G., A.S. and R.J.W. are funded in part by the NIH/NIAID Centers of Excellence for Influenza Research and Surveillance (CEIRS) under contract HHSN272201400006C, St Jude Children{\textquoteright}s Research Hospital; A.P. is supported in part by the NIH/NIAID CEIRS under contract HHS N2772201400007C, Johns Hopkins University; A.E., M.B.F., R.M.J., A.G.-S., J.P.L., S.M.W., P.J.H., Y.K., J.M.C., F.K., M. Schotsaert and V.S. are funded in part by the NIH/NIAID CEIRS under contract HHSN272201400008C, Icahn School of Medicine at Mount Sinai; R.R.A. is funded by 3R01AI148378-01S1; J.D.B. is supported in part by R01AI141707 and is an Investigator of the Howard Hughes Medical Institute; A.C.M.B. is funded by U01AI151810; E.A.B. is supported by an Intramural NIH Research Program project ZIA AI005156-02; D.L.B. is supported by NIH/NIAID under contract 75N93019D0025 to CAMRIS International; E.G. and V.J.M. are supported by the Intramural Research Program of the NIAID, NIH; B.L.D. and M.R. are supported by a cooperative agreement between The Henry M. Jackson Foundation for the Advancement of Military Medicine and the US Department of the Army (W81XWH-18-2-0040); M.S.D. is supported in part by R01AI157155; M.D. is supported by 1R01AI143639; N.A.D.-R., D.C.D., A.B.M., N.J.S., R.A.K., S.O., S.D.S. and R.A.S. are supported by the Intramural Research Program of the Vaccine Research Center, NIAID and NIH; C.D., B.A.M. and T.C.J. are funded in part by the German Ministry of research under project codes DZIF, MolTrax and PREPARED; A.E. is supported by NIAID grants U01AI141990 and 1U01AI150747; V.-V.E., M.E.D.-G. and M.S.S. 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; L.J. and M. Sedova are supported by HHSN272201700060C; A. Gordon is supported by R01AI20997; M.R.H. is supported by NIAID contract HHSN272201800013C; M.P.G.K. 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{\textquoteright}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{\textquoteright} funded by ZonMw (project 10150062010005, APW 202645827); to support the structured evaluation of SARS-CoV-2 evolution funded by the 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 the WHO. B.K., J.T. and H.Y. are funded by the Los Alamos National Laboratory and the Gates Foundation OPP1169339; R.A.K. is funded by Intramural NIH funding; M.J.M. is supported by UM1AI068618; V.D.M. is supported by R01AI153602; S.P. is supported by P01AI060699 and R01AI129269; P.-Y.S. 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; V.S. is supported by the NIH/NCI: Serological Sciences Network (SeroNet) 75N91019D00024; P.G.T. is supported by U01AI144616, U01AI150747, R01AI136514, R01AI154470; Z.S.W., R.H.S., A.M.N. and M. Shukla are supported by NIH, NIAID Contract 75N93019C00076; W.W. and C.D.W. are supported by US Food and Drug Administration institutional research funds; and S.C.W. is supported by NIH grant R24 AI120942 and by the Sealy and Smith Foundation. The findings and conclusions in this Review are those of the authors and do not necessarily represent the official position of the US Centers for Disease Control and Prevention. Use of trade names is for identification only and does not imply endorsement by the US Centers for Disease Control and Prevention or the US Department of Health and Human Services. Funding Information: A.A. is funded by HHSN272201700060C; G.A. 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; D.C.M. and X.S. 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; A.E., A. Gordon, J.M.C., F.K. and V.S. are funded in part by NIH/NIAID CIVIC under contract 75N93019C00051, Icahn School of Medicine at Mount Sinai; G.A., B.L., V.A.M., S.S.-C. and P.G.T. 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; M.S.D., V.S., L.B.T., H.v.B., L.A.V., R.A.M.F., A.G.-S., M.B.F., R.M.J., J.P.L., S.M.W., B.L.H., D.D.H., Y.H., Y.L., M.S.N., P.W., M.W., D.J.S., A.N., E.B.L., S.L.J., S. T{\"u}reli, S.M.W., S.A.T., J.M.C., F.K., B.M.W., B.R. and B.Y. are supported by the NIH/NIAID Centers of Excellence for Influenza Research and Response (CEIRR) under contract 75N93021C00014, Icahn School of Medicine at Mount Sinai; T.P.F., G.F., J.F., T.J., L.K., B.L., V.A.M., S.S.-C., A.S., S.T., P.G.T., E.K., L.C.-L., T.H., S. Sacharen and R.J.W. are funded in part by the NIH\NIAID CEIRR under contract 75N9302100016, St Jude Children{\textquoteright}s Research Hospital; R.R.A., V.-V.E., M.E.D.-G. and M.S.S. are funded in part by the NIH/NIAID CEIRR under contract 75N93021C00017, Emory University; A.E., T.P.F., J.F., T.J., L.K., B.L., V.A.M., S.S.-C., S.T. S.P.J.W., Z.L., L.-M.B., P.W.R., M.C.P., S. Stumpf, A.G., A.S. and R.J.W. are funded in part by the NIH/NIAID Centers of Excellence for Influenza Research and Surveillance (CEIRS) under contract HHSN272201400006C, St Jude Children{\textquoteright}s Research Hospital; A.P. is supported in part by the NIH/NIAID CEIRS under contract HHS N2772201400007C, Johns Hopkins University; A.E., M.B.F., R.M.J., A.G.-S., J.P.L., S.M.W., P.J.H., Y.K., J.M.C., F.K., M. Schotsaert and V.S. are funded in part by the NIH/NIAID CEIRS under contract HHSN272201400008C, Icahn School of Medicine at Mount Sinai; R.R.A. is funded by 3R01AI148378-01S1; J.D.B. is supported in part by R01AI141707 and is an Investigator of the Howard Hughes Medical Institute; A.C.M.B. is funded by U01AI151810; E.A.B. is supported by an Intramural NIH Research Program project ZIA AI005156-02; D.L.B. is supported by NIH/NIAID under contract 75N93019D0025 to CAMRIS International; E.G. and V.J.M. are supported by the Intramural Research Program of the NIAID, NIH; B.L.D. and M.R. are supported by a cooperative agreement between The Henry M. Jackson Foundation for the Advancement of Military Medicine and the US Department of the Army (W81XWH-18-2-0040); M.S.D. is supported in part by R01AI157155; M.D. is supported by 1R01AI143639; N.A.D.-R., D.C.D., A.B.M., N.J.S., R.A.K., S.O., S.D.S. and R.A.S. are supported by the Intramural Research Program of the Vaccine Research Center, NIAID and NIH; C.D., B.A.M. and T.C.J. are funded in part by the German Ministry of research under project codes DZIF, MolTrax and PREPARED; A.E. is supported by NIAID grants U01AI141990 and 1U01AI150747; V.-V.E., M.E.D.-G. and M.S.S. 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; L.J. and M. Sedova are supported by HHSN272201700060C; A. Gordon is supported by R01AI20997; M.R.H. is supported by NIAID contract HHSN272201800013C; M.P.G.K. 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{\textquoteright}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{\textquoteright} funded by ZonMw (project 10150062010005, APW 202645827); to support the structured evaluation of SARS-CoV-2 evolution funded by the 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 the WHO. B.K., J.T. and H.Y. are funded by the Los Alamos National Laboratory and the Gates Foundation OPP1169339; R.A.K. is funded by Intramural NIH funding; M.J.M. is supported by UM1AI068618; V.D.M. is supported by R01AI153602; S.P. is supported by P01AI060699 and R01AI129269; P.-Y.S. 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; V.S. is supported by the NIH/NCI: Serological Sciences Network (SeroNet) 75N91019D00024; P.G.T. is supported by U01AI144616, U01AI150747, R01AI136514, R01AI154470; Z.S.W., R.H.S., A.M.N. and M. Shukla are supported by NIH, NIAID Contract 75N93019C00076; W.W. and C.D.W. are supported by US Food and Drug Administration institutional research funds; and S.C.W. is supported by NIH grant R24 AI120942 and by the Sealy and Smith Foundation. The findings and conclusions in this Review are those of the authors and do not necessarily represent the official position of the US Centers for Disease Control and Prevention. Use of trade names is for identification only and does not imply endorsement by the US Centers for Disease Control and Prevention or the US Department of Health and Human Services. Publisher Copyright: {\textcopyright} 2022, Springer Nature Limited.",

year = "2022",

month = may,

day = "26",

doi = "10.1038/s41586-022-04690-5",

language = "English",

volume = "605",

pages = "640--652",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Research",

number = "7911",

}

DeGrace, MM, Ghedin, E, Frieman, MB, Krammer, F, Grifoni, A, Alisoltani, A, Alter, G, Amara, RR, Baric, RS, Barouch, DH, Bloom, JD, Bloyet, LM, Bonenfant, G, Boon, ACM, Boritz, EA, Bratt, DL, Bricker, TL, Brown, L, Buchser, WJ, Carreño, JM, Cohen-Lavi, L, Darling, TL, Davis-Gardner, ME, Dearlove, BL, Di, H, Dittmann, M, Doria-Rose, NA, Douek, DC, Drosten, C, Edara, VV, Ellebedy, A, Fabrizio, TP, Ferrari, G, Fischer, WM, Florence, WC, Fouchier, RAM, Franks, J, García-Sastre, A, Godzik, A, Gonzalez-Reiche, AS, Gordon, A, Haagmans, BL, Halfmann, PJ, Ho, DD, Holbrook, MR, Huang, Y, James, SL, Jaroszewski, L, Jeevan, T, Johnson, RM, Jones, TC, Joshi, A, Kawaoka, Y, Kercher, L, Koopmans, MPG, Korber, B, Koren, E, Koup, RA, LeGresley, EB, Lemieux, JE, Liebeskind, MJ, Liu, Z, Livingston, B, Logue, JP, Luo, Y, McDermott, AB, McElrath, MJ, Meliopoulos, VA, Menachery, VD, Montefiori, DC, Mühlemann, B, Munster, VJ, Munt, JE, Nair, MS, Netzl, A, Niewiadomska, AM, O’Dell, S, Pekosz, A, Perlman, S, Pontelli, MC, Rockx, B, Rolland, M, Rothlauf, PW, Sacharen, S, Scheuermann, RH, Schmidt, SD, Schotsaert, M, Schultz-Cherry, S, Seder, RA, Sedova, M, Sette, A, Shabman, RS, Shen, X, Shi, PY, Shukla, M, Simon, V, Stumpf, S, Sullivan, NJ, Thackray, LB, Theiler, J, Thomas, PG, Trifkovic, S, Türeli, S, Turner, SA, Vakaki, MA, van Bakel, H, VanBlargan, LA, Vincent, LR, Wallace, ZS, Wang, L, Wang, M, Wang, P, Wang, W, Weaver, SC, Webby, RJ, Weiss, CD, Wentworth, DE, Weston, SM, Whelan, SPJ, Whitener, BM, Wilks, SH, Xie, X, Ying, B, Yoon, H, Zhou, B, Hertz, T, Smith, DJ, Diamond, MS, Post, DJ & Suthar, MS 2022, 'Defining the risk of SARS-CoV-2 variants on immune protection', Nature, vol. 605, no. 7911, pp. 640-652. https://doi.org/10.1038/s41586-022-04690-5

TY - JOUR

T1 - Defining the risk of SARS-CoV-2 variants on immune protection

AU - DeGrace, Marciela M.

AU - Ghedin, Elodie

AU - Frieman, Matthew B.

AU - Krammer, Florian

AU - Grifoni, Alba

AU - Alisoltani, Arghavan

AU - Alter, Galit

AU - Amara, Rama R.

AU - Baric, Ralph S.

AU - Barouch, Dan H.

AU - Bloom, Jesse D.

AU - Bloyet, Louis Marie

AU - Bonenfant, Gaston

AU - Boon, Adrianus C.M.

AU - Boritz, Eli A.

AU - Bratt, Debbie L.

AU - Bricker, Traci L.

AU - Brown, Liliana

AU - Buchser, William J.

AU - Carreño, Juan Manuel

AU - Cohen-Lavi, Liel

AU - Darling, Tamarand L.

AU - Davis-Gardner, Meredith E.

AU - Dearlove, Bethany L.

AU - Di, Han

AU - Dittmann, Meike

AU - Doria-Rose, Nicole A.

AU - Douek, Daniel C.

AU - Drosten, Christian

AU - Edara, Venkata Viswanadh

AU - Ellebedy, Ali

AU - Fabrizio, Thomas P.

AU - Ferrari, Guido

AU - Fischer, Will M.

AU - Florence, William C.

AU - Fouchier, Ron A.M.

AU - Franks, John

AU - García-Sastre, Adolfo

AU - Godzik, Adam

AU - Gonzalez-Reiche, Ana Silvia

AU - Gordon, Aubree

AU - Haagmans, Bart L.

AU - Halfmann, Peter J.

AU - Ho, David D.

AU - Holbrook, Michael R.

AU - Huang, Yaoxing

AU - James, Sarah L.

AU - Jaroszewski, Lukasz

AU - Jeevan, Trushar

AU - Johnson, Robert M.

AU - Jones, Terry C.

AU - Joshi, Astha

AU - Kawaoka, Yoshihiro

AU - Kercher, Lisa

AU - Koopmans, Marion P.G.

AU - Korber, Bette

AU - Koren, Eilay

AU - Koup, Richard A.

AU - LeGresley, Eric B.

AU - Lemieux, Jacob E.

AU - Liebeskind, Mariel J.

AU - Liu, Zhuoming

AU - Livingston, Brandi

AU - Logue, James P.

AU - Luo, Yang

AU - McDermott, Adrian B.

AU - McElrath, Margaret J.

AU - Meliopoulos, Victoria A.

AU - Menachery, Vineet D.

AU - Montefiori, David C.

AU - Mühlemann, Barbara

AU - Munster, Vincent J.

AU - Munt, Jenny E.

AU - Nair, Manoj S.

AU - Netzl, Antonia

AU - Niewiadomska, Anna M.

AU - O’Dell, Sijy

AU - Pekosz, Andrew

AU - Perlman, Stanley

AU - Pontelli, Marjorie C.

AU - Rockx, Barry

AU - Rolland, Morgane

AU - Rothlauf, Paul W.

AU - Sacharen, Sinai

AU - Scheuermann, Richard H.

AU - Schmidt, Stephen D.

AU - Schotsaert, Michael

AU - Schultz-Cherry, Stacey

AU - Seder, Robert A.

AU - Sedova, Mayya

AU - Sette, Alessandro

AU - Shabman, Reed S.

AU - Shen, Xiaoying

AU - Shi, Pei Yong

AU - Shukla, Maulik

AU - Simon, Viviana

AU - Stumpf, Spencer

AU - Sullivan, Nancy J.

AU - Thackray, Larissa B.

AU - Theiler, James

AU - Thomas, Paul G.

AU - Trifkovic, Sanja

AU - Türeli, Sina

AU - Turner, Samuel A.

AU - Vakaki, Maria A.

AU - van Bakel, Harm

AU - VanBlargan, Laura A.

AU - Vincent, Leah R.

AU - Wallace, Zachary S.

AU - Wang, Li

AU - Wang, Maple

AU - Wang, Pengfei

AU - Wang, Wei

AU - Weaver, Scott C.

AU - Webby, Richard J.

AU - Weiss, Carol D.

AU - Wentworth, David E.

AU - Weston, Stuart M.

AU - Whelan, Sean P.J.

AU - Whitener, Bradley M.

AU - Wilks, Samuel H.

AU - Xie, Xuping

AU - Ying, Baoling

AU - Yoon, Hyejin

AU - Zhou, Bin

AU - Hertz, Tomer

AU - Smith, Derek J.

AU - Diamond, Michael S.

AU - Post, Diane J.

AU - Suthar, Mehul S.

N1 - Funding Information: D.H.B. is listed as a co-inventor on provisional vaccine patents (63/121,482; 63/133,969; 63/135,182). J.D.B. consults for Moderna and Flagship Labs 77 on topics related to viral evolution, and is an inventor on Fred Hutch licensed patents related to viral deep mutational scanning (62/692,398; PCT/US2019/039952; 17/281,540; 19824586.2; 62/935,954; 17/097,853; 62/812,804; PCT/US2020/020429). The Boon laboratory has received unrelated funding support in sponsored research agreements from AI Therapeutics, GreenLight Biosciences, and Nano targeting & Therapy Biopharma. The Boon laboratory has received funding support from AbbVie, for the commercial development of SARS-CoV-2 monoclonal antibodies. A.C.M.B. was a recipient of a licensing agreement with Abbvie for the commercial development of SARS-CoV-2 monoclonal antibodies. M.S.D. is a consultant for Inbios, Vir Biotechnology, Senda Biosciences and Carnival Corporation, and on the scientific advisory boards of Moderna and Immunome. The Diamond laboratory has received unrelated funding support in sponsored research agreements from Vir Biotechnology, Moderna and Emergent BioSolutions. The Ellebedy laboratory received funding under sponsored research agreements that are unrelated to the data presented in the current study from Emergent BioSolutions and from AbbVie. A.E. has received consulting fees from InBios International, Fimbrion Therapeutics, Mubadala Investment Company and Goldman Sachs and is the founder of ImmuneBio Consulting. M.B.F. has funding from Novavax, which is outside the scope of this research. They had no role in the funded research from the SAVES consortium. The Garcia-Sastre laboratory has received research support from Pfizer, Senhwa Biosciences, Kenall Manufacturing, Avimex, Johnson & Johnson, Dynavax, 7Hills Pharma, Pharmamar, ImmunityBio, Accurius, Nanocomposix, Hexamer, N-fold, Model Medicines and Merck, outside of the reported work. A.G.-S. has consulting agreements for the following companies involving cash and/or stock: Vivaldi Biosciences, Contrafect, 7Hills Pharma, Avimex, Vaxalto, Pagoda, Accurius, Esperovax, Farmak, Applied Biological Laboratories, Pharmamar and Pfizer, outside of the reported work. A.G.-S. is listed as an inventor on patents and patent applications on the use of antivirals and vaccines for the treatment and prevention of virus infections and cancer, owned by the Icahn School of Medicine at Mount Sinai, New York, outside of the reported work (5,820,871; 5,854,037; 6,001,634; 6,146,642; 6,451,323; 6,468,544; 6,544,785; 6,573,079; 6,635,416; 6,649,372; 6,669,943; 6,740,519; 6,852,522; 6,866,853; 6,884,414; 6,887,699; 7,060,430; 7,384,774; 7,442,379; 7,494, 808; 7,588,768; 7,833,774; 8,012,490; 8,057,803; 8,124,101; 8,137,676; 8,591,881; 8,629,283; 8,673,314; 8,709,442; 8,709,730; 8,765,139; 8,828,406; 8,999,352; 9,051,359; 9,096,585; 9,175,069; 9,217,136; 9,217,157; 9,238,851; 9,352,033; 9,371,366; 9,387,240; 9,387,242; . 9,549,975; 9,701,723; 9,708,373; 9,849,172; 9,908,930; 9,968,670; 10,035,984; .10,098,945; 10,131,695; 10,137,189; 10,179,806; 10,251,922; 10,308,913; 10,543,268; 10,544,207; 10,583,188; 10,736,956; 11,254,733; 11,266,734). A. Gordon serves on a scientific advisory board for Janssen, Erasmus MC has a proprietary IP on MERS. B.K. is part of provisional patent applications for strategies for next-generation SARS-CoV-2 vaccines that address diversity (63/256,848, 17/234,590; S133955). The Icahn School of Medicine at Mount Sinai has filed patent applications relating to SARS-CoV-2 serological assays that list V.S. as a co-inventor (62/994,252; 63/018,457; 63/020,503; 63/024,436) and NDV-based SARS-CoV-2 vaccines that list F.K. as a co-inventor (63/251,020). Mount Sinai has spun out a company, Kantaro, to market serological tests for SARS-CoV-2. F.K. has consulted for Merck and Pfizer (before 2020), and is currently consulting for Pfizer, Seqirus, 3rd Rock Ventures and Avimex. The Krammer laboratory is also collaborating with Pfizer on animal models of SARS-CoV-2. V.D.M. has filed a patent on the reverse genetic system and reporter SARS-CoV-2 (63/000,713; 63/041,667). D.C.M. receives funding from Moderna to perform blinded assessments of vaccine-elicited neutralizing antibody responses in clinical studies of their COVID-19 vaccines. A.S. is a consultant for Gritstone Bio, Flow Pharma, Arcturus Therapeutics, ImmunoScape, CellCarta, Avalia, Moderna, Fortress and Repertoire. P.-Y.S. laboratory has received funding support in sponsored research agreements from GSK, Pfizer, Gilead, Novartis, Merck, IGM Biosciences and Atea Pharmaceuticals. P.-Y.S. is a member of the scientific advisory boards of AbImmune and is Founder of FlaviTech. M.S.S. serves on the advisory board for Moderna and Ocugen. P.G.T. serves on the scientific advisory board for Immunoscape and Cytoagents and has consulted for Johnson and Johnson. P.G.T. has received travel support and honoraria from Illumina and 10x Genomics. P.G.T. has patents related to viral infection treatment and T cell receptor biology (11,083,725; 2021/0299118; US-2019-0040381; 17/616,279; WO2021/214637). S.P.J.W. has filed a patent with Washington University for VSV- SARS-CoV-2 mutants to characterize antibody panels (PCT/US2021/027275). S.P.J.W. has received unrelated funding support in sponsored research agreements with Vir Biotechnology, AbbVie, and sAB therapeutics. Funding Information: A.A. is funded by HHSN272201700060C; G.A. 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; D.C.M. and X.S. 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; A.E., A. Gordon, J.M.C., F.K. and V.S. are funded in part by NIH/NIAID CIVIC under contract 75N93019C00051, Icahn School of Medicine at Mount Sinai; G.A., B.L., V.A.M., S.S.-C. and P.G.T. 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; M.S.D., V.S., L.B.T., H.v.B., L.A.V., R.A.M.F., A.G.-S., M.B.F., R.M.J., J.P.L., S.M.W., B.L.H., D.D.H., Y.H., Y.L., M.S.N., P.W., M.W., D.J.S., A.N., E.B.L., S.L.J., S. Türeli, S.M.W., S.A.T., J.M.C., F.K., B.M.W., B.R. and B.Y. are supported by the NIH/NIAID Centers of Excellence for Influenza Research and Response (CEIRR) under contract 75N93021C00014, Icahn School of Medicine at Mount Sinai; T.P.F., G.F., J.F., T.J., L.K., B.L., V.A.M., S.S.-C., A.S., S.T., P.G.T., E.K., L.C.-L., T.H., S. Sacharen and R.J.W. are funded in part by the NIH\NIAID CEIRR under contract 75N9302100016, St Jude Children’s Research Hospital; R.R.A., V.-V.E., M.E.D.-G. and M.S.S. are funded in part by the NIH/NIAID CEIRR under contract 75N93021C00017, Emory University; A.E., T.P.F., J.F., T.J., L.K., B.L., V.A.M., S.S.-C., S.T. S.P.J.W., Z.L., L.-M.B., P.W.R., M.C.P., S. Stumpf, A.G., A.S. and R.J.W. 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; A.P. is supported in part by the NIH/NIAID CEIRS under contract HHS N2772201400007C, Johns Hopkins University; A.E., M.B.F., R.M.J., A.G.-S., J.P.L., S.M.W., P.J.H., Y.K., J.M.C., F.K., M. Schotsaert and V.S. are funded in part by the NIH/NIAID CEIRS under contract HHSN272201400008C, Icahn School of Medicine at Mount Sinai; R.R.A. is funded by 3R01AI148378-01S1; J.D.B. is supported in part by R01AI141707 and is an Investigator of the Howard Hughes Medical Institute; A.C.M.B. is funded by U01AI151810; E.A.B. is supported by an Intramural NIH Research Program project ZIA AI005156-02; D.L.B. is supported by NIH/NIAID under contract 75N93019D0025 to CAMRIS International; E.G. and V.J.M. are supported by the Intramural Research Program of the NIAID, NIH; B.L.D. and M.R. are supported by a cooperative agreement between The Henry M. Jackson Foundation for the Advancement of Military Medicine and the US Department of the Army (W81XWH-18-2-0040); M.S.D. is supported in part by R01AI157155; M.D. is supported by 1R01AI143639; N.A.D.-R., D.C.D., A.B.M., N.J.S., R.A.K., S.O., S.D.S. and R.A.S. are supported by the Intramural Research Program of the Vaccine Research Center, NIAID and NIH; C.D., B.A.M. and T.C.J. are funded in part by the German Ministry of research under project codes DZIF, MolTrax and PREPARED; A.E. is supported by NIAID grants U01AI141990 and 1U01AI150747; V.-V.E., M.E.D.-G. and M.S.S. 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; L.J. and M. Sedova are supported by HHSN272201700060C; A. Gordon is supported by R01AI20997; M.R.H. is supported by NIAID contract HHSN272201800013C; M.P.G.K. 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 the 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 the WHO. B.K., J.T. and H.Y. are funded by the Los Alamos National Laboratory and the Gates Foundation OPP1169339; R.A.K. is funded by Intramural NIH funding; M.J.M. is supported by UM1AI068618; V.D.M. is supported by R01AI153602; S.P. is supported by P01AI060699 and R01AI129269; P.-Y.S. 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; V.S. is supported by the NIH/NCI: Serological Sciences Network (SeroNet) 75N91019D00024; P.G.T. is supported by U01AI144616, U01AI150747, R01AI136514, R01AI154470; Z.S.W., R.H.S., A.M.N. and M. Shukla are supported by NIH, NIAID Contract 75N93019C00076; W.W. and C.D.W. are supported by US Food and Drug Administration institutional research funds; and S.C.W. is supported by NIH grant R24 AI120942 and by the Sealy and Smith Foundation. The findings and conclusions in this Review are those of the authors and do not necessarily represent the official position of the US Centers for Disease Control and Prevention. Use of trade names is for identification only and does not imply endorsement by the US Centers for Disease Control and Prevention or the US Department of Health and Human Services. Funding Information: A.A. is funded by HHSN272201700060C; G.A. 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; D.C.M. and X.S. 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; A.E., A. Gordon, J.M.C., F.K. and V.S. are funded in part by NIH/NIAID CIVIC under contract 75N93019C00051, Icahn School of Medicine at Mount Sinai; G.A., B.L., V.A.M., S.S.-C. and P.G.T. 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; M.S.D., V.S., L.B.T., H.v.B., L.A.V., R.A.M.F., A.G.-S., M.B.F., R.M.J., J.P.L., S.M.W., B.L.H., D.D.H., Y.H., Y.L., M.S.N., P.W., M.W., D.J.S., A.N., E.B.L., S.L.J., S. Türeli, S.M.W., S.A.T., J.M.C., F.K., B.M.W., B.R. and B.Y. are supported by the NIH/NIAID Centers of Excellence for Influenza Research and Response (CEIRR) under contract 75N93021C00014, Icahn School of Medicine at Mount Sinai; T.P.F., G.F., J.F., T.J., L.K., B.L., V.A.M., S.S.-C., A.S., S.T., P.G.T., E.K., L.C.-L., T.H., S. Sacharen and R.J.W. are funded in part by the NIH\NIAID CEIRR under contract 75N9302100016, St Jude Children’s Research Hospital; R.R.A., V.-V.E., M.E.D.-G. and M.S.S. are funded in part by the NIH/NIAID CEIRR under contract 75N93021C00017, Emory University; A.E., T.P.F., J.F., T.J., L.K., B.L., V.A.M., S.S.-C., S.T. S.P.J.W., Z.L., L.-M.B., P.W.R., M.C.P., S. Stumpf, A.G., A.S. and R.J.W. 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; A.P. is supported in part by the NIH/NIAID CEIRS under contract HHS N2772201400007C, Johns Hopkins University; A.E., M.B.F., R.M.J., A.G.-S., J.P.L., S.M.W., P.J.H., Y.K., J.M.C., F.K., M. Schotsaert and V.S. are funded in part by the NIH/NIAID CEIRS under contract HHSN272201400008C, Icahn School of Medicine at Mount Sinai; R.R.A. is funded by 3R01AI148378-01S1; J.D.B. is supported in part by R01AI141707 and is an Investigator of the Howard Hughes Medical Institute; A.C.M.B. is funded by U01AI151810; E.A.B. is supported by an Intramural NIH Research Program project ZIA AI005156-02; D.L.B. is supported by NIH/NIAID under contract 75N93019D0025 to CAMRIS International; E.G. and V.J.M. are supported by the Intramural Research Program of the NIAID, NIH; B.L.D. and M.R. are supported by a cooperative agreement between The Henry M. Jackson Foundation for the Advancement of Military Medicine and the US Department of the Army (W81XWH-18-2-0040); M.S.D. is supported in part by R01AI157155; M.D. is supported by 1R01AI143639; N.A.D.-R., D.C.D., A.B.M., N.J.S., R.A.K., S.O., S.D.S. and R.A.S. are supported by the Intramural Research Program of the Vaccine Research Center, NIAID and NIH; C.D., B.A.M. and T.C.J. are funded in part by the German Ministry of research under project codes DZIF, MolTrax and PREPARED; A.E. is supported by NIAID grants U01AI141990 and 1U01AI150747; V.-V.E., M.E.D.-G. and M.S.S. 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; L.J. and M. Sedova are supported by HHSN272201700060C; A. Gordon is supported by R01AI20997; M.R.H. is supported by NIAID contract HHSN272201800013C; M.P.G.K. 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 the 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 the WHO. B.K., J.T. and H.Y. are funded by the Los Alamos National Laboratory and the Gates Foundation OPP1169339; R.A.K. is funded by Intramural NIH funding; M.J.M. is supported by UM1AI068618; V.D.M. is supported by R01AI153602; S.P. is supported by P01AI060699 and R01AI129269; P.-Y.S. 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; V.S. is supported by the NIH/NCI: Serological Sciences Network (SeroNet) 75N91019D00024; P.G.T. is supported by U01AI144616, U01AI150747, R01AI136514, R01AI154470; Z.S.W., R.H.S., A.M.N. and M. Shukla are supported by NIH, NIAID Contract 75N93019C00076; W.W. and C.D.W. are supported by US Food and Drug Administration institutional research funds; and S.C.W. is supported by NIH grant R24 AI120942 and by the Sealy and Smith Foundation. The findings and conclusions in this Review are those of the authors and do not necessarily represent the official position of the US Centers for Disease Control and Prevention. Use of trade names is for identification only and does not imply endorsement by the US Centers for Disease Control and Prevention or the US Department of Health and Human Services. Publisher Copyright: © 2022, Springer Nature Limited.

PY - 2022/5/26

Y1 - 2022/5/26

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85129706085&partnerID=8YFLogxK

U2 - 10.1038/s41586-022-04690-5

DO - 10.1038/s41586-022-04690-5

M3 - Review article

C2 - 35361968

AN - SCOPUS:85129706085

SN - 0028-0836

VL - 605

SP - 640

EP - 652

JO - Nature

JF - Nature

IS - 7911

ER -

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

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