SARS-CoV-2 Omicron variant escapes neutralizing antibodies and T cell responses more efficiently than other variants in mild COVID-19 convalescents

Cell Reports Medicine - Tập 3 - Trang 100651 - 2022
Pablo Garcia-Valtanen1, Christopher M. Hope2,3, Makutiro G. Masavuli1, Arthur Eng Lip Yeow1, Harikrishnan Balachandran4, Zelalem A. Mekonnen1, Zahraa Al-Delfi1, Arunasingam Abayasingam4, David Agapiou4, Alberto Ospina Stella5, Anupriya Aggarwal5, George Bouras6,7, Jason Gummow8, Catherine Ferguson9, Stephanie O’Connor10, Erin M. McCartney9, David J. Lynn11,12, Guy Maddern13, Eric J. Gowans1, Benjamin A.J. Reddi10
1Viral Immunology Group, Adelaide Medical School, University of Adelaide and Basil Hetzel Institute for Translational Health Research, Adelaide, SA, Australia
2Molecular Immunology, Robinson Research Institute, University of Adelaide, Adelaide, SA, Australia
3Women’s and Children’s Health Network, North Adelaide, SA, Australia
4School of Medical Sciences, Faculty of Medicine, UNSW, Australia, Sydney, NSW, Australia
5The Kirby Institute, The University of New South Wales, Sydney, NSW, Australia
6Adelaide Medical School, Faculty of Health and Medical Sciences, The University of Adelaide, Adelaide, SA, Australia
7The Department of Surgery - Otolaryngology, Head and Neck Surgery, University of Adelaide and the Basil Hetzel Institute for Translational Health Research, Central Adelaide Local Health Network, Woodville South, SA, Australia
8Gene Silencing and Expression Core Facility, Adelaide Health and Medical Sciences, Robinson Research Institute, University of Adelaide, Adelaide, SA, Australia
9Infectious Diseases Department, Royal Adelaide Hospital, Central Adelaide Local Health Network, Adelaide, SA, Australia
10Intensive Care Unit, Royal Adelaide Hospital, Central Adelaide Local Health Network and Adelaide Medical School, University of Adelaide, Adelaide, SA, Australia
11Precision Medicine Theme, South Australian Health and Medical Research Institute, Adelaide, SA 5001, Australia
12Flinders Health and Medical Research Institute, Flinders University, Bedford Park, SA 5042, Australia
13Discipline of Surgery, The University of Adelaide, Adelaide, SA 5000, Australia

Tài liệu tham khảo

Zhou, 2020, A pneumonia outbreak associated with a new coronavirus of probable bat origin, Nature, 579, 270, 10.1038/s41586-020-2012-7 Huang, 2021, The impact of lockdown timing on COVID-19 transmission across US counties, EClinicalMedicine, 38, 101035, 10.1016/j.eclinm.2021.101035 Rossman, 2021, COVID-19 dynamics after a national immunization program in Israel, Nat. Med., 27, 1055, 10.1038/s41591-021-01337-2 Barandalla, 2021, Impact of scaling up SARS-CoV-2 vaccination on COVID-19 hospitalizations in Spain, Int. J. Infect. Dis., 112, 81, 10.1016/j.ijid.2021.09.022 Pritchard, 2021, Impact of vaccination on new SARS-CoV-2 infections in the United Kingdom, Nat. Med., 27, 1370, 10.1038/s41591-021-01410-w Bahl, 2021, Vaccination reduces need for emergency care in breakthrough COVID-19 infections: a multicenter cohort study, Lancet Reg. Health. Am., 4, 100065 Doroshenko, 2021, The combined effect of vaccination and nonpharmaceutical public health interventions—ending the COVID-19 pandemic, JAMA Netw. Open, 4, e2111675, 10.1001/jamanetworkopen.2021.11675 Lau, 2021, Neutralizing antibody titres in SARS-CoV-2 infections, Nat. Commun., 12, 63, 10.1038/s41467-020-20247-4 Li, 2021, Twelve-month specific IgG response to SARS-CoV-2 receptor-binding domain among COVID-19 convalescent plasma donors in Wuhan, Nat. Commun., 12, 4144, 10.1038/s41467-021-24230-5 Naaber, 2021, Dynamics of antibody response to BNT162b2 vaccine after six months: a longitudinal prospective study, Lancet Reg. Health Eur., 10, 100208, 10.1016/j.lanepe.2021.100208 Israel, 2021, Large-scale study of antibody titer decay following BNT162b2 mRNA vaccine or SARS-CoV-2 infection, medRxiv. Liu, 2021, Neutralizing activity of BNT162b2-elicited serum, N. Engl. J. Med., 384, 1466, 10.1056/NEJMc2102017 Hammerschmidt, 2021, Neutralization of the SARS-CoV-2 Delta variant after heterologous and homologous BNT162b2 or ChAdOx1 nCoV-19 vaccination, Cell. Mol. Immunol., 18, 2455, 10.1038/s41423-021-00755-z Planas, 2021, Reduced sensitivity of SARS-CoV-2 variant Delta to antibody neutralization, Nature, 596, 276, 10.1038/s41586-021-03777-9 Davis, 2021, Reduced neutralisation of the Delta (B.1.617.2) SARS-CoV-2 variant of concern following vaccination, medRxiv Shen, 2021, Neutralization of SARS-CoV-2 variants B.1.429 and B.1.351, N. Engl. J. Med., 384, 2352, 10.1056/NEJMc2103740 Yadav, 2021, Neutralization of Beta and Delta variant with sera of COVID-19 recovered cases and vaccinees of inactivated COVID-19 vaccine BBV152/Covaxin, J. Trav. Med., 28, taab104, 10.1093/jtm/taab104 Bates, 2021, Neutralization of SARS-CoV-2 variants by convalescent and BNT162b2 vaccinated serum, Nat. Commun., 12, 5135, 10.1038/s41467-021-25479-6 Shinde, 2021, Efficacy of NVX-CoV2373 Covid-19 vaccine against the B.1.351 variant, N. Engl. J. Med., 384, 1899, 10.1056/NEJMoa2103055 Tarke, 2021, Comprehensive analysis of T cell immunodominance and immunoprevalence of SARS-CoV-2 epitopes in COVID-19 cases, Cell Rep. Med., 2, 100204, 10.1016/j.xcrm.2021.100204 Grifoni, 2020, A sequence homology and bioinformatic approach can predict candidate targets for immune responses to SARS-CoV-2, Cell Host Microbe, 27, 671, 10.1016/j.chom.2020.03.002 Dan, 2021, Immunological memory to SARS-CoV-2 assessed for up to 8 months after infection, Science, 371, eabf4063, 10.1126/science.abf4063 Grifoni, 2020, Targets of T Cell responses to SARS-CoV-2 coronavirus in humans with COVID-19 disease and unexposed individuals, Cell, 181, 1489, 10.1016/j.cell.2020.05.015 Grifoni, 2021, SARS-CoV-2 human T cell epitopes: adaptive immune response against COVID-19, Cell Host Microbe, 29, 1076, 10.1016/j.chom.2021.05.010 Tarke, 2021, Impact of SARS-CoV-2 variants on the total CD4+ and CD8+ T cell reactivity in infected or vaccinated individuals, Cell Rep. Med., 2, 100355, 10.1016/j.xcrm.2021.100355 Geers, 2021, SARS-CoV-2 variants of concern partially escape humoral but not T cell responses in COVID-19 convalescent donors and vaccine recipients, Sci. Immunol., 6, eabj1750, 10.1126/sciimmunol.abj1750 Le Bert, 2020, SARS-CoV-2-specific T cell immunity in cases of COVID-19 and SARS, and uninfected controls, Nature, 584, 457, 10.1038/s41586-020-2550-z Bar-On, 2021, Protection of BNT162b2 vaccine booster against Covid-19 in Israel, N. Engl. J. Med., 385, 1393, 10.1056/NEJMoa2114255 van Riel, 2020, Next-generation vaccine platforms for COVID-19, Nat. Mater., 19, 810, 10.1038/s41563-020-0746-0 Heinz, 2021, Distinguishing features of current COVID-19 vaccines: knowns and unknowns of antigen presentation and modes of action, NPJ Vaccines, 6, 104, 10.1038/s41541-021-00369-6 Australia Abayasingam, 2021, Long-term persistence of RBD+ memory B cells encoding neutralizing antibodies in SARS-CoV-2 infection, Medicine, 2, 100228 Sette, 2021, Adaptive immunity to SARS-CoV-2 and COVID-19, Cell, 184, 861, 10.1016/j.cell.2021.01.007 Saini, 2021, SARS-CoV-2 genome-wide T cell epitope mapping reveals immunodominance and substantial CD8(+) T cell activation in COVID-19 patients, Sci. Immunol., 6, eabf7550, 10.1126/sciimmunol.abf7550 Carrasco Pro, 2015, Automatic generation of validated specific epitope sets, J. Immunol. Res., 2015, 763461 Jung, 2021, SARS-CoV-2-specific T cell memory is sustained in COVID-19 convalescent patients for 10 months with successful development of stem cell-like memory T cells, Nat. Commun., 12, 4043, 10.1038/s41467-021-24377-1 Kumar, 2018, Human T cell development, localization, and function throughout life, Immunity, 48, 202, 10.1016/j.immuni.2018.01.007 Juno, 2020, Humoral and circulating follicular helper T cell responses in recovered patients with COVID-19, Nat. Med., 26, 1428, 10.1038/s41591-020-0995-0 Le Bert, 2022, Mutations of SARS-CoV-2 variants of concern escaping Spike-specific T cells, bioRxiv Vitale, 2021, Assessment of SARS-CoV-2 reinfection 1 Year after primary infection in a population in Lombardy, Italy, JAMA Intern. Med., 181, 1407, 10.1001/jamainternmed.2021.2959 Lumley, 2021, Antibody status and incidence of SARS-CoV-2 infection in health care workers, N. Engl. J. Med., 384, 533, 10.1056/NEJMoa2034545 Hall, 2021, SARS-CoV-2 infection rates of antibody-positive compared with antibody-negative health-care workers in England: a large, multicentre, prospective cohort study (SIREN), Lancet, 397, 1459, 10.1016/S0140-6736(21)00675-9 Wheatley, 2021, Evolution of immune responses to SARS-CoV-2 in mild-moderate COVID-19, Nat. Commun., 12, 1162, 10.1038/s41467-021-21444-5 Khoury, 2021, Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection, Nat. Med., 27, 1205, 10.1038/s41591-021-01377-8 Deng, 2020, Primary exposure to SARS-CoV-2 protects against reinfection in rhesus macaques, Science, 369, 818, 10.1126/science.abc5343 Tea, 2021, SARS-CoV-2 neutralizing antibodies: longevity, breadth, and evasion by emerging viral variants, PLoS Med., 18, e1003656, 10.1371/journal.pmed.1003656 Townsend, 2021, The durability of immunity against reinfection by SARS-CoV-2: a comparative evolutionary study, Lancet. Microbe, 2, e666, 10.1016/S2666-5247(21)00219-6 Altarawneh, 2022, Protection against the Omicron variant from previous SARS-CoV-2 infection, N. Engl. J. Med., 386, 1288, 10.1056/NEJMc2200133 Gasser, 2021, Major role of IgM in the neutralizing activity of convalescent plasma against SARS-CoV-2, Cell Rep., 34, 108790, 10.1016/j.celrep.2021.108790 Andreano, 2020, SARS-CoV-2 escape <em>in vitro</em> from a highly neutralizing COVID-19 convalescent plasma, bioRxiv. Liu, 2021, Reduced neutralization of SARS-CoV-2 B.1.617 by vaccine and convalescent serum, Cell, 184, 4220, 10.1016/j.cell.2021.06.020 Planas, 2022, Considerable escape of SARS-CoV-2 Omicron to antibody neutralization, Nature, 602, 671, 10.1038/s41586-021-04389-z Cele, 2022, Omicron extensively but incompletely escapes Pfizer BNT162b2 neutralization, Nature, 602, 654, 10.1038/s41586-021-04387-1 Gordon, 2017, Tissue reservoirs of antiviral T cell immunity in persistent human CMV infection, J. Exp. Med., 214, 651, 10.1084/jem.20160758 Goel, 2021, mRNA vaccines induce durable immune memory to SARS-CoV-2 and variants of concern, Science, 374, eabm0829, 10.1126/science.abm0829 Collins, 2020, CD8+ T cells in HIV control, cure and prevention, Nat. Rev. Immunol., 20, 471, 10.1038/s41577-020-0274-9 Ciurea, 2001, CD4+ T-cell–epitope escape mutant virus selected in vivo, Nat. Med., 7, 795, 10.1038/89915 Price, 2000, Viral escape by selection of cytotoxic T cell-resistant variants in influenza A virus pneumonia, J. Exp. Med., 191, 1853, 10.1084/jem.191.11.1853 Uebelhoer, 2008, Stable cytotoxic T cell escape mutation in hepatitis C virus is linked to maintenance of viral fitness, PLoS Pathog., 4, e1000143, 10.1371/journal.ppat.1000143 Bozio, 2021, Laboratory-confirmed COVID-19 among adults hospitalized with COVID-19–like illness with infection-induced or mRNA vaccine-induced SARS-CoV-2 immunity — Nine States, January–September 2021, MMWR Morb. Mortal. Wkly. Rep., 70, 1539, 10.15585/mmwr.mm7044e1 Abu-Raddad, 2021, Association of prior SARS-CoV-2 infection with risk of breakthrough infection following mRNA vaccination in Qatar, JAMA, 326, 1930, 10.1001/jama.2021.19623 2020 Uriu, 2021, Neutralization of the SARS-CoV-2 Mu variant by convalescent and vaccine serum, N. Engl. J. Med., 385, 2397, 10.1056/NEJMc2114706 Bugembe, 2021, Emergence and spread of a SARS-CoV-2 lineage A variant (A.23.1) with altered spike protein in Uganda, Nat. Microbiol., 6, 1094, 10.1038/s41564-021-00933-9 Ryan, 2021, Long-term perturbation of the peripheral immune system months after SARS-CoV-2 infection, medRxiv. Hope, 2019, Peptidase inhibitor 16 identifies a human regulatory T-cell subset with reduced FOXP3 expression over the first year of recent onset type 1 diabetes, Eur. J. Immunol., 49, 10.1002/eji.201948094 Hsieh, 2020, Structure-based design of prefusion-stabilized SARS-CoV-2 spikes, Science, 369, 1501, 10.1126/science.abd0826 Amanat, 2020, A serological assay to detect SARS-CoV-2 seroconversion in humans, Nat. Med., 26, 1033, 10.1038/s41591-020-0913-5 Hoffmann, 2020, A multibasic cleavage site in the spike protein of SARS-CoV-2 is essential for infection of human lung cells, Mol. Cell, 78, 779, 10.1016/j.molcel.2020.04.022 Keck, 2009, Mutations in hepatitis C virus E2 located outside the CD81 binding sites lead to escape from broadly neutralizing antibodies but compromise virus infectivity, J. Virol., 83, 6149, 10.1128/JVI.00248-09 Bartosch, 2003, In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes, Proc. Natl. Acad. Sci. U. S. A, 100, 14199, 10.1073/pnas.2335981100 Kalemera, 2020, Optimised cell systems for the investigation of hepatitis C virus E1E2 glycoproteins, bioRxiv. Crawford, 2020, Protocol and Reagents for Pseudotyping Lentiviral Particles with SARS-CoV-2 Spike Protein for Neutralization Assays, Viruses, 12, 513, 10.3390/v12050513 Hoaglin, 1993, Revising a display of multidimensional laboratory measurements to improve accuracy of perception, Methods Inf. Med., 32, 418, 10.1055/s-0038-1634957 Le, 2021, Comparative anti-inflammatory effects of Salix cortex extracts and acetylsalicylic acid in SARS-CoV-2 peptide and LPS-activated human in vitro systems, Int. J. Mol. Sci., 22, 6766, 10.3390/ijms22136766 Mateus, 2021, Low-dose mRNA-1273 COVID-19 vaccine generates durable memory enhanced by cross-reactive T cells, Science, 374, eabj9853, 10.1126/science.abj9853 Abayasingam, 2021, Long-term persistence of RBD-positive memory B cells encoding neutralising antibodies in SARS-CoV-2 infection, Cell Rep. Med., 2, 100228, 10.1016/j.xcrm.2021.100228