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Cited by 785SARS-CoV-2 and COVID-19 ResearchCOVID-19 Clinical Research StudiesAnimal Virus Infections Studies

SARS-CoV-2 Omicron is an immune escape variant with an altered cell entry pathway

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Willett, Brian J., Grove, Joe, MacLean, Oscar A., Wilkie, Craig, De Lorenzo, Giuditta, Furnon, Wilhelm, Cantoni, Diego, Scott, Sam +686 more·2022·Nature Microbiology
DOI 10.1038/s41564-022-01143-7PMC PMC9352574

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Abstract

Vaccines based on the spike protein of SARS-CoV-2 are a cornerstone of the public health response to COVID-19. The emergence of hypermutated, increasingly transmissible variants of concern (VOCs) threaten this strategy. Omicron (B.1.1.529), the fifth VOC to be described, harbours multiple amino acid mutations in spike, half of which lie within the receptor-binding domain. Here we demonstrate substantial evasion of neutralization by Omicron BA.1 and BA.2 variants in vitro using sera from individuals vaccinated with ChAdOx1, BNT162b2 and mRNA-1273. These data were mirrored by a substantial reduction in real-world vaccine effectiveness that was partially restored by booster vaccination. The Omicron variants BA.1 and BA.2 did not induce cell syncytia in vitro and favoured a TMPRSS2-independent endosomal entry pathway, these phenotypes mapping to distinct regions of the spike protein. Impaired cell fusion was determined by the receptor-binding domain, while endosomal entry mapped to the S2 domain. Such marked changes in antigenicity and replicative biology may underlie the rapid global spread and altered pathogenicity of the Omicron variant.

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  1. [11]Basile, K. et al. Improved neutralization of the SARS-CoV-2 Omicron variant after Pfizer-BioNTech BNT162b2 COVID-19 vaccine boosting. Preprint at bioRxiv10.1101/2021.12.12.472252 (2021).
  2. [14]Cele S Omicron extensively but incompletely escapes Pfizer BNT162b2 neutralization Nature 2022 602 654 656 35016196 PMC8866126
  3. [59]Meng B Altered TMPRSS2 usage by SARS-CoV-2 Omicron impacts tropism and fusogenicity Nature 2022 603 706 714 35104837 PMC8942856
  4. [78]Davis C Reduced neutralisation of the Delta (B. 1.617. 2) SARS-CoV-2 variant of concern following vaccination PLoS Pathog. 2021 17 e1010022 34855916 PMC8639073

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Willett, B. J., Grove, J., MacLean, O. A., Wilkie, C., De Lorenzo, G., Furnon, W., Cantoni, D., Scott, S., Logan, N., Ashraf, S., Manali, M., Szemiel, A., Cowton, V., Vink, E., Harvey, W. T., Davis, C., Asamaphan, P., Smollett, K., Tong, L., Orton, R., Hughes, J., Holland, P., Silva, V., Pascall, D. J., Puxty, K., da Silva Filipe, A., Yebra, G., Shaaban, S., Holden, M. T. G., Pinto, R. M., Gunson, R., Templeton, K., Murcia, P. R., Patel, A. H., Klenerman, P., Dunachie, S., PITCH Consortium, Dunachie, S., Klenerman, P., Barnes, E., Brown, A., Adele, S., Kronsteiner, B., Murray, S. M., Abraham, P., Deeks, A., Ansari, M. A., de Silva, T., Turtle, L., Moore, S., Austin, J., Richter, A., Duncan, C., Payne, R., The COVID-19 Genomics UK (COG-UK) Consortium, Ash, A., Koshy, C., Kele, B., Cutino-Moguel, T., Fairley, D. J., McKenna, J. P., Curran, T., Adams, H., Fraser, C., Bonsall, D., Fryer, H., Lythgoe, K., Thomson, L., Golubchik, T., Murray, A., Singleton, D., Beckwith, S. M., Mantzouratou, A., Barrow, M., Buchan, S. L., Reynolds, N., Warne, B., Maksimovic, J., Spellman, K., McCluggage, K., John, M., Beer, R., Afifi, S., Morgan, S., Mack, A., Marchbank, A., Price, A., Morriss, A., Bresner, C., Kitchen, C., Merrick, I., Southgate, J., Guest, M., Jones, O., Munn, R., Connor, T. R., Whalley, T., Workman, T., Fuller, W., Patel, A., Patel, B., Nebbia, G., Edgeworth, J., Snell, L. B., Batra, R., Charalampous, T., Beckett, A. H., Shelest, E., Robson, S. C., Underwood, A. P., Taylor, B. E. W., Yeats, C. A., Aanensen, D. M., Abudahab, K., Menegazzo, M., Joseph, A., Clark, G., Howson-Wells, H. C., Berry, L., Khakh, M., Lister, M. M., Boswell, T., Fleming, V. M., Holmes, C. W., McMurray, C. L., Shaw, J., Tang, J. W., Fallon, K., Odedra, M., Willford, N. J., Bird, P. W., Helmer, T., Williams, L.-A., Sheriff, N., Campbell, S., Raviprakash, V., Blakey, V., Moore, C., Sang, F., Debebe, J., Carlile, M., Loose, M. W., Holmes, N., Wright, V., Torok, M. E., Hamilton, W. L., Carabelli, A. M., Jermy, A., Blane, B., Churcher, C. M., Ludden, C., Aggarwal, D., Westwick, E., Brooks, E., McManus, G. M., Galai, K., Smith, K., Smith, K. S., Cox, M., Fragakis, M., Maxwell, P., Judges, S., Peacock, S. J., Feltwell, T., Kenyon, A., Eldirdiri, S., Davis, T., Taylor, J. F., Tan, N. K., Zarebski, A. E., Gutierrez, B., Raghwani, J., du Plessis, L., Kraemer, M. U. G., Pybus, O. G., Francois, S., Attwood, S. W., Vasylyeva, T. I., Jahun, A. S., Goodfellow, I. G., Georgana, I., Pinckert, M. L., Hosmillo, M., Izuagbe, R., Chaudhry, Y., Ryan, F., Lowe, H., Moses, S., Bedford, L., Cargill, J. S., Hughes, W., Moore, J., Stonehouse, S., Shah, D., Lee, J. C. D., Brown, J. R., Harris, K. A., Atkinson, L., Storey, N., Spyer, M. J., Flaviani, F., Alcolea-Medina, A., Sehmi, J., Ramble, J., Ohemeng-Kumi, N., Smith, P., Bertolusso, B., Thomas, C., Vernet, G., Lynch, J., Moore, N., Cortes, N., Williams, R., Kidd, S. P., Levett, L. J., Pusok, M., Grant, P. R., Kirk, S., Chatterton, W., Xu-McCrae, L., Smith, D. L., Young, G. R., Bashton, M., Kitchman, K., Gajee, K., Eastick, K., Lillie, P. J., Burns, P. J., Everson, W., Cox, A., Holmes, A. H., Bolt, F., Price, J. R., Pond, M., Randell, P. A., Madona, P., Mookerjee, S., Volz, E. M., Geidelberg, L., Ragonnet-Cronin, M., Boyd, O., Johnson, R., Pope, C. F., Witney, A. A., Monahan, I. M., Laing, K. G., Smollett, K. L., McNally, A., McMurray, C., Stockton, J., Quick, J., Loman, N. J., Poplawski, R., Nicholls, S., Rowe, W., Castigador, A., Macnaughton, E., Bouzidi, K. E., Sudhanva, M., Lampejo, T., Martinez Nunez, R. T., Breen, C., Sluga, G., Withell, K. T., Machin, N. W., George, R. P., Ahmad, S. S. Y., Pritchard, D. T., Binns, D., Wong, N., James, V., Williams, C., Illingworth, C. J., Jackson, C., de Angelis, D., Pascall, D., Mukaddas, A., Broos, A., da Silva Filipe, A., Mair, D., Robertson, D. L., Wright, D. W., Thomson, E. C., Starinskij, I., Tsatsani, I., Shepherd, J. G., Nichols, J., Hughes, J., Nomikou, K., Tong, L., Orton, R. J., Vattipally, S., Harvey, W. T., Sanderson, R., O’Brien, S., Rushton, S., Perkins, J., Blacow, R., Gunson, R. N., Gallagher, A., Wastnedge, E., Templeton, K. E., McHugh, M. P., Dewar, R., Cotton, S., Coupland, L., Stanley, R., Dervisevic, S., Spurgin, L. G., Smith, L., Graham, C., Padgett, D., Barton, E., Scott, G., Cross, A., Mirfenderesky, M., Swindells, E., Greenaway, J., Denton-Smith, R., Turnbull, R., Idle, G., Cole, K., Hollis, A., Nelson, A., McCann, C. M., Henderson, J. H., Crown, M. R., Yew, W. C., Stanley, W., Duckworth, N., Clarke, P., Walsh, S., Sloan, T. J., Bicknell, K., Impey, R., Wyllie, S., Elliott, S., Glaysher, S., Bradley, D. T., Killough, N. F., Wyatt, T., Bosworth, A., Vipond, B. B., Pearson, C., Allara, E., Robinson, E., Pymont, H. M., Osman, H., Muir, P., Hopes, R., Hutchings, S., Curran, M. 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J., Rudder, S., Le-Viet, T., Casey, A., Ratcliffe, L., Singh, A., Mariappan, A., Baxter, C., Radulescu, C., Simpson, D. A., Lavin, D., Rogan, F., Miskelly, J., Fuchs, M., Tang, M., Carvalho, S. F., Bridgett, S., Skvortsov, T., Molnar, Z., Ramadan, N. A., Knight, B. A., Jones, C. R., Auckland, C., Morcrette, H., Poyner, J., Irish-Tavares, D., Witele, E., Hart, J., Mahungu, T. W., Haque, T., Bourgeois, Y., Fearn, C., Cook, K. F., Loveson, K. F., Goudarzi, S., Evans, C., Partridge, D. G., Johnson, K., Yavus, M., Raza, M., Mower, C., Baker, P., Essex, S., Bonner, S., Murray, L. J., Watson, L. K., Liggett, S., Lawton, A. I., Lyons, R. A., Payne, B. A. I., Eltringham, G., Collins, J., Waugh, S., Burton-Fanning, S., Taha, Y., Jeanes, C., Gomes, A. N., Murray, D. R., Kimuli, M., Dobie, D., Ashfield, P., Best, A., Percival, B., Moles-Garcia, E., Ashford, F., Mirza, J., Crawford, L., Mayhew, M., Cumley, N., Megram, O., Frampton, D., Heaney, J., Byott, M., Houlihan, C., Williams, C. A., Nastouli, E., Lowe, H. L., Hartley, J. A., Breuer, J., Maftei, L., Ensell, L., Cotic, M., Mondani, M., Driscoll, M., Bayzid, N., Williams, R. J., Roy, S., Mahanama, A. I. K., Samaraweera, B., Wilson-Davies, E., Pelosi, E., Umpleby, H., Wheeler, H., Prieto, J. A., Saeed, K., Harvey, M., Jeremiah, S., Silviera, S., Aplin, S., Sass, T., Macklin, B., Crudgington, D., Sheridan, L. A., Cogger, B. J., Malone, C. S., Munemo, F., Huckson, H., Lewis, J., Easton, L. J., Mutingwende, M., Erkiert, M. J., Hassan-Ibrahim, M. O., Chaloner, N. J., Podplomyk, O., Randell, P., Nicodemi, R., Lowdon, S., Somassa, T., Richter, A., Beggs, A., Hesketh, A. R., Smith, C. P., Bucca, G., Ruis, C., Cormie, C., Higginson, E. E., Young, J., Dias, J., Kermack, L. M., Maes, M., Gupta, R. K., Forrest, S., Girgis, S. T., Davidson, R. K., O’Toole, Á., Rambaut, A., Jackson, B., Balcazar, C. E., Maloney, D., Scher, E., McCrone, J. T., Williamson, K. A., Gallagher, M. D., Medd, N., Colquhoun, R., Stanton, T. D., Williams, T., Hill, V., Jeffries, A. R., Temperton, B., Sambles, C. M., Studholme, D. J., Warwick-Dugdale, J., Jackson, L. M., Michelsen, M. L., Manley, R., Michell, S. L., Darby, A. C., Lucaci, A. O., Nelson, C., Wierzbicki, C., Vamos, E. E., Webster, H. J., Jackson, K. A., Rainbow, L., Hughes, M., Whitehead, M., Gemmell, M., Iturriza-Gomara, M., Eccles, R., Gregory, R., Haldenby, S. T., Paterson, S., Angyal, A., Keeley, A. J., Foulkes, B. H., Lindsey, B. B., Wang, D., Hornsby, H. R., Green, L. R., Pohare, M., Gallis, M., Parker, M. D., Whiteley, M., Smith, N., Wolverson, P., Zhang, P., Hansford, S. E., Hsu, S. N., Louka, S. F., de Silva, T. I., Freeman, T. M., Mori, M., Park, E. J., Hill, J. D., Dey, J., Ball, J., Chappell, J. G., McClure, P. C., Byaruhanga, T., Fanaie, A., Yaze, G., Hilson, R. A., Trebes, A., Green, A., Buck, D., MacIntyre-Cockett, G., Todd, J. A., Bassett, A. R., Whitwham, A., Langford, C. F., Rajan, D., Kwiatkowski, D., Harrison, E. M., Bronner, I. F., Tovar-Corona, J. M., Liddle, J., Durham, J., Bellis, K. L., Lewis, K., Aigrain, L., Redshaw, N. M., Davies, R. M., Moll, R. J., McCarthy, S. A., Lensing, S. V., Leonard, S., Farr, B. W., Scott, C., Beaver, C., Ariani, C. V., Weldon, D., Jackson, D. K., Betteridge, E., Tonkin-Hill, G., Johnston, I., Martincorena, I., Bonfield, J., Barrett, J. C., Sillitoe, J., Keatley, J.-P., Oliver, K., James, K., Shirley, L., Prestwood, L., Foulser, L., Gourtovaia, M., Dorman, M. J., Quail, M. A., Spencer Chapman, M. H., Park, N. R., Livett, R., Amato, R., Kay, S., Goodwin, S., Thurston, S. A. J., Rajatileka, S., Gonçalves, S., Lo, S., Sanderson, T., Maclean, A., Goldstein, E. J., Ferguson, L., Tomb, R., Catalan, J., Jones, N., Haughney, J., Robertson, D. L., Palmarini, M., Ray, S., & Thomson, E. C.
Affiliations
  • MRC University of Glasgow Centre for Virus Research (GB)
  • University of Glasgow (GB)
  • NHS Greater Glasgow and Clyde (GB)
  • John Radcliffe Hospital (GB)
  • University of Oxford (GB)
  • University of Liverpool (GB)
  • Newcastle upon Tyne Hospitals NHS Foundation Trust (GB)
  • Newcastle University (GB)
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Corresponding author
  • Willett, Brian J.
  • Grove, Joe
ORCID
Venue
Nature Microbiology
Publisher
Springer Science and Business Media LLC
Published
2022-07-07
Volume
7
Issue
8
Pages
1161-1179
ISSN
2058-5276 (ISSN-L)
DOI
10.1038/s41564-022-01143-7
PMC
PMC9352574
OpenAlex
W4284886202
Cited by
785
References
105
Citations by year
2026: 68 · 2025: 112 · 2024: 181 · 2023: 255 · 2022: 166 · 2021: 2 · 2020: 1
FWCI
87.49
Type
journal article
Language
en
Update notices
correction (2022-09-16)
Open access
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  • Nature Microbiology (publishedVersion, cc-by)
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  • Apollo
Funders
  • Bournemouth University
  • University of Portsmouth
  • Northumbria University
  • Wellcome Trust (204721/Z/16/Z, WT 109965MA, MR/W005611/1, 107653, 211153/Z/18/Z, 220977/Z/20/Z, MC_UU_12014/12, 220977, 107653/Z/15/Z, 107653/Z/15/A)
  • King's College Hospital NHS Foundation Trust
  • Nottingham University Hospitals NHS Trust
  • University Hospitals of Leicester NHS Trust
  • Alan Turing Institute
  • Betsi Cadwaladr University Health Board
  • University Hospitals Birmingham NHS Foundation Trust
  • UK Research and Innovation (MR/W005611/1/, MR/V038613/1, MC_UU_12014, MC_PC_20058, MC_UU_1201412, MR/W02067X/1, BB/R019843/1, MR/R024758/1, MC_PC_19027)
  • National Institute for Health Research Health Protection Research Unit (MC_PC_19027)
  • National Institute for Health and Care Research (BB/R019843/1, MR/V038613/1, COVID-19, MC_PC_19027, MC_PC_20058, NIHR300791, ACF-2018-04-014, NF-SI-0617-10139)
  • Department of Health and Social Care (COVID-19, BB/R019843/1)
  • Academy of Medical Sciences (AMS-CSF4-Torok)
  • University of Cambridge
  • University of St Andrews
  • Imperial College London
  • Imperial College Healthcare NHS Trust
  • King's College London
  • University College London
  • University of Oxford
  • Newcastle University
  • University of Nottingham
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  • Cambridge University Hospitals
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  • St George's University Hospitals NHS Foundation Trust
  • Sheffield Teaching Hospitals NHS Foundation Trust
  • Barts Health NHS Trust
  • Liverpool University Hospitals NHS Foundation Trust
  • Directorate for Biological Sciences
  • Medical Research Council (MC_PC_19027, MC_UU_12014, MC UU 12014/12, MC_PC_19026, MR/W005611/1, MC_PC_20058, MC_UU_00002/11, MR/R024758/1, MR/V038613/1, COVID-19)
  • Engineering and Physical Sciences Research Council (MR/W005611/1, MR/V038613/1)
  • Biotechnology and Biological Sciences Research Council (BB/R019843/1, BB/R004250/1, MR/W005611/1)
  • Great Ormond Street Institute of Child Health
  • NIHR Oxford Biomedical Research Centre
  • Institute of Infection and Immunity
  • Health Data Research UK (MC_PC_20058)
Topics
  • Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
  • Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
Keywords
Omicron variant, immune evasion, spike protein mutations, receptor binding domain, vaccine effectiveness, booster vaccination, endosomal entry, S2 domain, cell fusion, COVID-19 variants of concern
MeSH terms
COVID-19, SARS-CoV-2, BNT162 Vaccine, Antibodies, Viral, Humans, Membrane Glycoproteins, Viral Envelope Proteins, Virus Internalization, Spike Glycoprotein, Coronavirus

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