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SARS-CoV-2 variants, spike mutations and immune escape
Open accessAbstract
Although most mutations in the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) genome are expected to be either deleterious and swiftly purged or relatively neutral, a small proportion will affect functional properties and may alter infectivity, disease severity or interactions with host immunity. The emergence of SARS-CoV-2 in late 2019 was followed by a period of relative evolutionary stasis lasting about 11 months. Since late 2020, however, SARS-CoV-2 evolution has been characterized by the emergence of sets of mutations, in the context of 'variants of concern', that impact virus characteristics, including transmissibility and antigenicity, probably in response to the changing immune profile of the human population. There is emerging evidence of reduced neutralization of some SARS-CoV-2 variants by postvaccination serum; however, a greater understanding of correlates of protection is required to evaluate how this may impact vaccine effectiveness. Nonetheless, manufacturers are preparing platforms for a possible update of vaccine sequences, and it is crucial that surveillance of genetic and antigenic changes in the global virus population is done alongside experiments to elucidate the phenotypic impacts of mutations. In this Review, we summarize the literature on mutations of the SARS-CoV-2 spike protein, the primary antigen, focusing on their impacts on antigenicity and contextualizing them in the protein structure, and discuss them in the context of observed mutation frequencies in global sequence datasets.
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“D614G is again associated with the increase in transmissibility, infectivity, and viral load, making the Lambda variant even more lethal [55].”
From Waves and variants of SARS-CoV-2: understanding the causes and effect of the COVID-19 catastrophe (2022) · cites this paper as [55]
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“Each pathogen poses a unique set of challenges, including high lethality, rapid mutations, immune evasion, new strains and variants252–258.”
From mRNA vaccines for infectious diseases: principles, delivery and clinical translation (2021) · cites this paper as [252]
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“Mutations in the spike protein and RBD have been shown to affect antibody neutralisation and thus reduce vaccine-induced immunity [22].”
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In the citing paper
“The Lambda variant spike protein is found to be 3.3 times more resistant to neutralization by the convalescent sera than the parent D614G spike protein and 4.9 times to that of the Alpha variant ones.”
From Waves and variants of SARS-CoV-2: understanding the causes and effect of the COVID-19 catastrophe (2022) · cites this paper as [55]
Experimental — accuracy not yet measuredIn the citing paper
“However, reduced sensitivity of SARS-CoV-2 variants to antibody and serum neutralization has been widely observed (18–21).”
From Deep learning guided optimization of human antibody against SARS-CoV-2 variants with broad neutralization (2022) · cites this paper as [19]
In the citing paper
“both being immunodominant targets of neutralizing antibodies elicited by COVID-19 vaccines or by SARS-CoV-2 infection (5, 6).”
From Neutralization of SARS-CoV-2 Omicron by BNT162b2 mRNA vaccine–elicited human sera (2022) · cites this paper as [6]
In the citing paper
“However, sequencing data of SARS-CoV-2 from patients revealed persistent accumulation of new mutations over the last two years of the Covid19 pandemic, leading to the emergence of new viral strains that can be more transmissible or virulent5,6 or evade vaccines7–9.”
From The roles of APOBEC-mediated RNA editing in SARS-CoV-2 mutations, replication and fitness (2022) · cites this paper as [8]
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“A) is unknown but it is located in the receptor binding motif (16).”
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Receptor-binding domain of SARS-CoV-2 is a functional αv-integrin agonist
Norris, E. G., Pan, X. S., & Hocking, D. C. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.102922 · Cited by 31
“…regarding mechanisms underlying the differential susceptibility of vulnerable populations to severe manifestations of COVID-19 (3), as well as potential differences in infectivity, transmissibility, disease severity, and immune evasion associated with novel variants (https://covariants.org/) (90).”
Azzouzi, M., Ouafi, Z. E., Azougagh, O., Daoudi, W., Ghazal, H., Barkany, S. E., Rfaki, A., Mazières, S., Aatiaoui, A. E., & Oussaid, A. (2023) · Journal of Molecular Structure · doi:10.1016/j.molstruc.2023.135525 · Cited by 31
Cheng, Z., Elmes, M. J., Kirkup, S. E., Abayasekara, D. R. E., & Wathes, D. C. (2004) · Journal of Endocrinology · doi:10.1677/joe.0.1820249 · Cited by 31
Modelling the adjustment of COVID-19 response and exit from dynamic zero-COVID in ChinaPreprint
Leung, K. S. M., Leung, G. M., & Wu, J. T. K. (2022) · medRxiv · doi:10.1101/2022.12.14.22283460 · Cited by 32
Pratama, N. R., Wafa, I. A., Budi, D. S., Sutanto, H., Asmarawati, T. P., Barlian Effendi, G., & Wungu, C. D. K. (2022) · Vaccines · doi:10.3390/vaccines10122180 · Cited by 30
“, 2022(38) Casecontrol United States 283 12-18 years Viral genome sequencing MIS-C: 63 (48-89) N/A BNT162b2 Severe infection 1-OR”
BackgroundLee, J., Jeong, S. Y., Li, Z., Kim, H., Kim, H., Yoo, M. J., Jang, H. J., Kim, D., Cho, N., Yoo, H. M., et al. (2023) · Biomaterials Research · doi:10.1186/s40824-023-00357-y · Cited by 30
“Introduction Coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has spread globally, and new variants of the virus have been identified over the course of the pandemic [1].”
BackgroundBeck, C., Ramanujam, D. P., Vaccarello, P., Widenmeyer, F., Feuerherd, M., Cheng, C., Bomhard, A., Abikeeva, T., Schädler, J., Sperhake, J., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-40185-1 · Cited by 30
INMI1 Zika Virus NS4B Antagonizes the Interferon Signaling by Suppressing STAT1 Phosphorylation
Fanunza, E., Grandi, N., Quartu, M., Carletti, F., Ermellino, L., Milia, J., Corona, A., Capobianchi, M. R., Ippolito, G., & Tramontano, E. (2021) · Viruses · doi:10.3390/v13122448 · Cited by 30
Mapping cross-variant neutralizing sites on the SARS-CoV-2 spike protein
Xu, S., Wang, Y., Wang, Y., Zhang, C., Qin, H., Gu, C., Xu, R., Wang, T., Yang, Y. P., Zang, J., et al. (2021) · Emerging Microbes & Infections · doi:10.1080/22221751.2021.2024455 · Cited by 28
“These variants carry multiple mutations in the RBD and NTD regions of the S protein, leading to their increased resistance to neutralization by MAbs raised against the original strain in the early phase of the pandemic [20,27].”
BackgroundHoffmann, M., Sidarovich, A., Arora, P., Krüger, N., Nehlmeier, I., Kempf, A. M., Graichen, L., Winkler, M. S., Niemeyer, D., Goffinet, C., et al. (2022) · mBio · doi:10.1128/mbio.00364-22 · Cited by 30
Cahyani, I., Putro, E. W., Ridwanuloh, A. M., Wibowo, S. H. B., Hariyatun, H., Syahputra, G., Akbariani, G., Utomo, A. R. H., Ilyas, M., Loose, M., et al. (2022) · Viruses · doi:10.3390/v14040778 · Cited by 30
“Studies on viruses with these two mutations also showed correlation to an increased infectivity, by way of ACE2 receptor binding, and viral transmissibility [43]–[46].”
BackgroundWinklmeier, S., Eisenhut, K., Taskin, D., Rübsamen, H., Gerhards, R., Schneider, C., Wratil, P. R., Stern, M., Eichhorn, P., Keppler, O. T., et al. (2021) · iScience · doi:10.1016/j.isci.2021.103659 · Cited by 31
Roberts, D. S., Mann, M. W., Li, B. H., Kim, D., Braiser, A. R., Jin, S., & Ge, Y. (2022) · Chemical Science · doi:10.1039/d2sc02132c · Cited by 29
Lan, Q., Wang, L., Jiao, F., Lu, L., Xia, S., & Jiang, S. (2022) · Journal of Medical Virology · doi:10.1002/jmv.28143 · Cited by 30
The Mutational Landscape of SARS-CoV-2
Saldivar‐Espinoza, B., Garcia‐Segura, P., Novau-Ferré, N., Macip, G., Martínez, R., Puigbò, P., Cereto‐Massagué, A., Pujadas, G., & Garcı́a-Vallvé, S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24109072 · Cited by 30
Structural understanding of SARS-CoV-2 virus entry to host cells
Le, K. P. U., Kannappan, S., Kim, T., Lee, J. H., Lee, H.-R., & Kim, K. K. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2023.1288686 · Cited by 34
Raisinghani, N., Alshahrani, M., Gupta, G., & Verkhivker, G. M. (2024) · Viruses · doi:10.3390/v16091458 · Cited by 33
“…results are broadly consistent with previous computational analysis and experimental data that quantified the effect of RBD mutations on the interactions with the ACE2 receptor, particularly showing that N501Y can result in one of the highest gains in ACE2 affinity conferred by RBD mutation [121].”
ResultCheng, C., Aruchunan, E., & Aziz, N. (2025) · Scientific Reports · doi:10.1038/s41598-025-85440-1 · Cited by 31
Karim, M. A., Shilts, J., Schwartzentruber, J., Hayhurst, J. D., Buniello, A., Mohammed, E. S. E., Zheng, J., Holmes, M. V., Ochoa, D., Carmona, M., et al. (2021) · eLife · doi:10.7554/elife.69719 · Cited by 28
SCoV2-MD: a database for the dynamics of the SARS-CoV-2 proteome and variant impact predictions
Torrens‐Fontanals, M., Peralta-García, A., Talarico, C., Guixà-González, R., Toni Giorgino, A., & Selent, J. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab977 · Cited by 30
“The diffusion of the COVID-19 pandemic has produced emerging variants (1), which have been tracked through massive sequencing efforts at an unprecedented rate soon surpassing that of any other pathogen and phylogenetic analysis (2–4).”
A perspective on the applications of furin inhibitors for the treatment of SARS-CoV-2
Devi, K. P., Pourkarim, M. R., Thijssen, M., Sureda, A., Khayatkashani, M., Cismaru, C. A., Neagoe, I. B., Habtemariam, S., Razmjouei, S., & Kashani, H. R. K. (2022) · Pharmacological Reports · doi:10.1007/s43440-021-00344-x · Cited by 30
“However, an important aspect to consider is the possible existence of mutations in protein S, which may affect the S1/S2 cleavage site, and confer resistance to higher susceptibility to furininduced cleavage and, thus altering viral entry and cell–cell fusion [19].”
BackgroundCasasnovas, J. M., Margolles, Y., Noriega, M. A., Guzmán, M. Á., Arranz, R., Melero, R., Casanova, M., Sánchez, J. A. C., de Oya, N. J., Gastaminza, P., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.863831 · Cited by 30
“The RBD mutations found in these variants pose a threat to the efficacy of current vaccines and human therapeutic Abs (22, 24, 25), which may also generate an additional pressure for viral evolution and selection of new variants that escape human immune neutralization.”
BackgroundTherapeutics to Tackle Omicron Outbreak
Chavda, V. P., Ghali, E. N. H. K., Yallapu, M. M., & Apostolopoulos, V. (2022) · Immunotherapy · doi:10.2217/imt-2022-0064 · Cited by 31
“Conventional escape mutation research contains mutations that originate in virus populations that are exposed to either mAbs or convalescent plasma comprising polyclonal antibodies, targeted characteristics of specific mutations, and broader research of either huge numbers of propagating variants or all feasible amino…”
BackgroundInfluentialThe Spike Protein of SARS-CoV-2 Is Adapting Because of Selective Pressures
López-Cortés, G. I., Palacios-Pérez, M., Veledíaz, H. F., Hernández-Aguilar, M. M., López-Hernández, G. R., Zamudio, G. S., & José, M. V. (2022) · Vaccines · doi:10.3390/vaccines10060864 · Cited by 26
Popovic, M. E. (2022) · BioTech · doi:10.3390/biotech11040045 · Cited by 29
“SARS-CoV-2 appeared in 2019 as the Hu-1 variant (wild type), causing the COVID-19 pandemic [79,80].”
BackgroundWidyasari, K., & Kim, J. N. (2023) · Antibodies · doi:10.3390/antib12010005 · Cited by 29
“The changes in the genetic codes of SARS-CoV-2 may affect the virus’ characteristics, including transmissibility, antigenicity, infectivity, and severity [42].”
BackgroundFantini, J., Azzaz, F., Chahinian, H., & Yahi, N. (2023) · Viruses · doi:10.3390/v15020284 · Cited by 30
Kwon, P. S., Xu, S., Oh, H., Kwon, S., Rodrigues, A. L., Feroz, M. M., Fraser, K., He, P., Zhang, F., Hong, J. J., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-04789-z · Cited by 30
Li, X., Singh, N. K., Collins, D. R., Ng, R., Zhang, A. Y., Lamothe, P. A., Shahinian, P., Xu, S., Tan, K., Trocha, A. K., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-38573-8 · Cited by 29
Structural and functional characteristics of the SARS-CoV-2 Omicron subvariant BA.2 spike protein
Zhang, J., Tang, W., Gao, H., Lavine, C. L., Shi, W. K., Peng, H., Zhu, H., Anand, K., Kosikova, M., Kwon, H. J., et al. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-01023-6 · Cited by 29
Structure-activity relationships of B.1.617 and other SARS-CoV-2 spike variantsPreprint
Yang, T., Yu, P., Chang, Y., Chang, N.-E., Tsai, Y.-X., Liang, K.-H., Drączkowski, P., Lin, B., Wang, Y., Chien, Y.-C., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.12.459978 · Cited by 30
Herbert, J. A., & Panagiotou, S. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-818731-9.00235-4 · Cited by 33
(2022) · doi:10.1371/journal.pone.0266844 · Cited by 28
“However, SARS-CoV-2 can, like other viruses, develop immune evasion strategies through antigenic variations in order to escape these immune responses [15, 72].”
BackgroundFirst cases of infection with the 21L/BA.2 Omicron variant in Marseille, France
Colson, P., Delerce, J., Beye, M., Levasseur, A., Boschi, C., Houhamdi, L., Tissot‐Dupont, H., Yahi, N., Million, M., Scola, B. L., et al. (2022) · Journal of Medical Virology · doi:10.1002/jmv.27695 · Cited by 28
Humoral Response to BNT162b2 Vaccine Against SARS-CoV-2 Variants Decays After Six Months
Lopera, T. J., Chvatal‐Medina, M., Flórez‐Álvarez, L., Zapata-Cardona, M. I., Taborda, N. A., Rugeles, M. T., & Hernández, J. C. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.879036 · Cited by 29
Defining neutralization and allostery by antibodies against COVID-19 variants
Tulsian, N. K., Raghuvamsi, P. V., Qian, X., Gu, Y., Shunmuganathan, B. D. O., Samsudin, F., Wong, Y. H., Lin, J., Purushotorman, K., Kozma, M., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42408-x · Cited by 27
Self-citationSARS-CoV-2: pathogenesis, therapeutics, variants, and vaccines
Li, X., Mi, Z., Liu, Z., & Rong, P. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1334152 · Cited by 34
“…Beta (B.1.351) and Gamma (P.1), which were first identified in the United Kingdom, South Africa and Brazil, respectively, carry a common N501Y mutation (Andreano et al., 2021; Faria et al., 2021; Harvey et al., 2021; The COVID-19 Genomics UK (COG-UK) consortium et al., 2021; Tian et al., 2022).”
BackgroundInfluentialSampson, A., Heeney, J. L., Cantoni, D. M., Ferrari, M., Sans, M. S., George, C. L., Genova, C. D., Neto, M. M., Einhauser, S., Asbach, B., et al. (2021) · Viruses · doi:10.3390/v13081579 · Cited by 27
Mertens, J. C., Coppens, J., Loens, K., Mercier, M. L., Xavier, B. B., Lammens, C., Vandamme, S., Jansens, H., Goossens, H., & Matheeussen, V. (2021) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2021.09.007 · Cited by 28
“Even though SARS-CoV-2 displays only one or two nucleotide changes/month/lineage, high incidence rates and selection pressure due to increasing population immunity result in rapid occurrence of new variants [9,15].”
Lee, C., Fang, Y.-P., Wang, L.-C., Chou, T., & Liu, H. (2021) · Viruses · doi:10.3390/v14010032 · Cited by 28
“Similar to SARS-CoV2, the RNA virus has a propensity to mutate over time, leading to the emergence of highly transmissible viral variants [31].”
ResultKnown Cellular and Receptor Interactions of Animal and Human Coronaviruses: A Review
Everest, H., Stevenson-Leggett, P., Bailey, D., Bickerton, E., & Keep, S. (2022) · Viruses · doi:10.3390/v14020351 · Cited by 28
Li, Q., Zhang, M., Liang, Z., Zhang, L., Wu, X., Yang, C., An, Y., Tong, J., Liu, S., Li, T., et al. (2022) · MedComm · doi:10.1002/mco2.130 · Cited by 26
Liang, Y., Zou, L., Lin, H., Li, B., Zhao, J., Wang, H., Sun, J., Chen, J., Mo, Y., Yang, X., et al. (2022) · ACS Synthetic Biology · doi:10.1021/acssynbio.1c00643 · Cited by 28
de Souza, A. S., Amorim, V. M. D. F., Guardia, G. D. A., dos Santos, F. F., Ulrich, H., Galante, P. A. F., de Souza, R. F., & Guzzo, C. R. (2022) · Viruses · doi:10.3390/v14040827 · Cited by 28
Metadata
- Authors
- Harvey, W. T., Carabelli, A. M., Jackson, B., Gupta, R. K., Thomson, E. C., Harrison, E. M., Ludden, C., Reeve, R., Rambaut, A., COVID-19 Genomics UK (COG-UK) Consortium, Peacock, S. J., & Robertson, D. L.
- Affiliations
- MRC University of Glasgow Centre for Virus Research (GB)
- University of Cambridge (GB)
- University of Edinburgh (GB)
- Wellcome Sanger Institute (GB)
- University of Glasgow (GB)
- Corresponding author
- Robertson, David L.
- ORCID
- Venue
- Nature Reviews Microbiology
- Published
- 2021-06-01
- Volume
- 19
- Issue
- 7
- Pages
- 409-424
- ISSN
- 1740-1526 (ISSN-L)
- 1740-1534
- PMC
- PMC8167834
- OpenAlex
- W3165479483
- Cited by
- 3,528
- References
- 103
- Citations by year
- 2026: 220 · 2025: 310 · 2024: 475 · 2023: 801 · 2022: 1283 · 2021: 420
- FWCI
- 87.86
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Nature Reviews Microbiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion, cc-by-sa)
- Northumbria Research Link (Northumbria University) (acceptedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Apollo (University of Cambridge) (submittedVersion)
- Apollo
- Funders
- Wellcome Trust (Z/17/Z, 206298/Z/17/Z, 220977/Z/20/Z, 220977/Z/20/Z, 206298/Z/17/Z, 206298)
- UK Research and Innovation (MR/W005611/1/, MC_PC_19027)
- National Institute for Health and Care Research
- Academy of Medical Sciences (AMS-CSF4-Torok)
- University of Glasgow
- Directorate for Biological Sciences
- Medical Research Council (MC_UU_12014, MC UU 12014/12, MC_PC_19026, MR/W005611/1, MR/S00291X/1, COVID-19, MR/R024758/1)
- Biotechnology and Biological Sciences Research Council (BB/R012679/1)
- H2020 European Research Council (725422)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › vaccines and immunoinformatics approaches
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Keywords
- SARS-CoV-2, spike protein mutations, variants of concern, immune evasion, antigenicity, neutralizing antibodies, vaccine effectiveness, vaccine update, viral evolution, mutation frequency, COVID-19 pandemic
- MeSH terms
- COVID-19, SARS-CoV-2, COVID-19 Vaccines, Amino Acids, Epitopes, Antigenic Variation, Humans, Mutation, Protein Conformation, Immune Evasion, Spike Glycoprotein, Coronavirus
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