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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]
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“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]
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“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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BackgroundMethodCirculation and Evolution of SARS-CoV-2 in India: Let the Data Speak
Limaye, S., Kasibhatla, S. M., Ramtirthkar, M. R., Kinikar, M., Kale, M. M., & Kulkarni‐Kale, U. (2021) · Viruses · doi:10.3390/v13112238 · Cited by 18
“The variable sites N439K/I/T, V445F/I/Y/G/C, and G446V/A are flanking a segment under selection consisting of N440H/I/K/S/Y, L441I/M/R/V/Y, D442E/F/N/V/Y, S443A/C/F/L/Y, and K444F/I/L/M/N/Y, and therefore, the mutations in the region 439–446 need to be monitored, as it is a major antigenic site that is part of the bin…”
BackgroundMicroRNA-Mediated Regulation of the Virus Cycle and Pathogenesis in the SARS-CoV-2 Disease
Battaglia, R., Alonzo, R., Pennisi, C., Caponnetto, A., Ferrara, C., Stella, M., Barbagallo, C., Barbagallo, D., Ragusa, M., Purrello, M., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222413192 · Cited by 17
“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 [16].”
BackgroundNunhofer, V., Weidner, L., Hoeggerl, A. D., Zimmermann, G., Badstuber, N., Grabmer, C., Jungbauer, C., Lindlbauer, N., Held, N., Pascariuc, M., et al. (2022) · Viruses · doi:10.3390/v14030637 · Cited by 17
“Despite the availability of vaccination since the beginning of 2021, several variants of SARS-CoV-2 have recently led to further pandemic waves [2,3]: In spring 2021, the SARS-CoV-2 variant B1.”
BackgroundDesign of SARS-CoV-2 Variant-Specific PCR Assays Considering Regional and Temporal Characteristics
Oh, C., Sashittal, P., Zhou, A., Wang, L., El-Kebir, M., & Nguyen, T. H. (2022) · Applied and Environmental Microbiology · doi:10.1128/aem.02289-21 · Cited by 19
Shah, M., Moon, S. U., Kim, J. H., Thao, T. T., & Woo, H. G. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.04.030 · Cited by 15
“525), Theta (P.3), Lota (B.1.526), Kappa (B.1.617.1), and Lambda (C.37) [8–9] raised concerns over the efficacy of neutralizing antibodies response that is either induced by the vaccines [9–10], collected from the convalescent plasma or developed in the lab against the wild-type Spike antigen.”
InfluentialDumache, R., Enache, A., Macasoi, I. G., Dehelean, C. A., Dumitrascu, V. C., Mihailescu, A., Popescu, R., Vlad, M., Vlad, C. S., & Mureşan, C. O. (2022) · Pathogens · doi:10.3390/pathogens11050516 · Cited by 17
“Throughout the pandemic, scientists have made great efforts to fully understand the viral genome, as well as to identify any variants that may occur [14].”
BackgroundAdhikari, P., Jawad, B., Rao, P. R., Podgornik, R., & Ching, W. Y. (2022) · Viruses · doi:10.3390/v14030465 · Cited by 14
“SARS-CoV-2 itself is most likely the result of a recombination between different SARS-related coronaviruses [61], with different subsequent mutations affecting their many biological and biomedical properties, such as pathogenicity, infectivity, transmissibility, and/or antigenicity, even though they tend to be either…”
BackgroundPotent neutralization by monoclonal human IgM against SARS‐CoV‐2 is impaired by class switch
Callegari, I., Schneider, M., Berloffa, G., Mühlethaler, T., Holdermann, S., Galli, E., Roloff, T. C., Boss, R., Infanti, L., Khanna, N., et al. (2022) · EMBO Reports · doi:10.15252/embr.202153956 · Cited by 17
“Mutations of E484 are well known to mediate escape from neutralizing antibodies and are present in the beta and gamma variants of the virus (Harvey et al , 2021).”
Wieczorek, L., Zemil, M., Merbah, M., Dussupt, V., Kavusak, E., Molnar, S., Heller, J., Beckman, B., Wollen-Roberts, S. E., Peachman, K. K., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.901217 · Cited by 16
Li, J., Wu, J., Long, Q., Wu, Y., Hu, X., He, Y., Jiang, M., Li, J., Zhao, L., Yang, S., et al. (2022) · Research · doi:10.34133/2022/9873831 · Cited by 15
Munigela, A., Sowpati, D. T., Sasikala, M., Banu, S., Siva, A. B., Kumar, J., Nutalapati, C., Vishnubhotla, R., Kulkarni, A. V., Mukherjee, P., et al. (2022) · IJID Regions · doi:10.1016/j.ijregi.2022.08.016 · Cited by 17
Co-Infection Associated with SARS-CoV-2 and Their Management
Chavda, V. P., Patel, A., Pandya, A., Vora, L. K., Patravale, V. B., Tambuwala, Z. M., Aljabali, A. A. A., Serrano‐Aroca, Á., Mishra, V. K., & Tambuwala, M. M. (2022) · Future Science OA · doi:10.2144/fsoa-2022-0011 · Cited by 18
“Similarly, A Beta variant was identified in South Africa, while a Gamma variant was reported in Japan and Brazil in late 2020 [19].”
BackgroundCiuffreda, L., Lorenzo-Salazar, J. M., Alcoba-Flórez, J., Rodríguez‐Pérez, H., Gil-Campesino, H., Íñigo-Campos, A., de Artola, D. G.-M., Valenzuela-Fernández, A., Peraza, M. H., Rojo‐Alba, S., et al. (2021) · Journal of Infection · doi:10.1016/j.jinf.2021.07.028 · Cited by 17
“06 mutations/day [3]) (Onesample Wilcoxon test, p=0.”
von Wintersdorff, C. J. H., Dingemans, J., van Alphen, L. B., Wolffs, P. F. G., van der Veer, B. M. J. W., Hoebe, C. J. P. A., & Savelkoul, P. H. M. (2021) · Research Square · doi:10.21203/rs.3.rs-777577/v1 · Cited by 17
Yurkovetskiy, L., Egri, S. B., Kurhade, C., Díaz-Salinas, M. A., Jaimes, J. A., Nyalile, T., Xie, X., Choudhary, M. C., Dauphin, A., Li, J. Z., et al. (2023) · SSRN Electronic Journal · doi:10.1101/2023.03.30.535005 · Cited by 18
Fast SARS-CoV-2 Variant Detection Using Snapback Primer High-Resolution Melting
Lownik, J. C., Farrar, J. S., Way, G. W., McKay, A., Roychoudhury, P., Greninger, A. L., & Martin, R. (2021) · Diagnostics · doi:10.3390/diagnostics11101788 · Cited by 16
“Since it was first sequenced in January 2020, the SARS-CoV-2 virus has diverged into several clades and variants [1].”
BackgroundLhomme, S., Latour, J., Jeanne, N., Trémeaux, P., Ranger, N., Migueres, M., Salin, G., Donnadieu, C., & Izopet, J. (2021) · Viruses · doi:10.3390/v13122544 · Cited by 16
“Analysis of the S1 domain, including the RBD, is well suited to monitor the appearance of immune-escaping mutations [31].”
BackgroundConstruction and characterization of two SARS‐CoV‐2 minigenome replicon systems
Zhang, H., Fischer, D. K., Shuda, M., Moore, P. S., Gao, S., Ambrose, Z., & Guo, H. (2022) · Journal of Medical Virology · doi:10.1002/jmv.27650 · Cited by 16
“Despite the development and application of SARS‐CoV‐2 vaccines, the rapid evolution of viral spike (S) protein and emergence of many variants of concern have often resulted in vaccine breakthrough cases and caused new waves of infections.(4,5) SARS‐CoV‐2 is an enveloped, positive‐sense RNA virus, belonging to the Coro…”
BackgroundThere is nothing exempt from the peril of mutation – The Omicron spike
Behl, T., Kaur, I., Sehgal, A., Singh, S., Sharma, N., Anwer, M. K., Makeen, H. A., Albratty, M., Alhazmi, H. A., Bhatia, S., et al. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.112756 · Cited by 16
Evasion of Vaccine-Induced Humoral Immunity by Emerging Sub-Variants of SARS-CoV-2
Koyama, T., Miyakawa, K., Tokumasu, R., Jeremiah, S. S., Kudo, M., & Ryo, A. (2022) · Future Microbiology · doi:10.2217/fmb-2022-0025 · Cited by 15
Evolutionary Dynamics of Indels in SARS-CoV-2 Spike Glycoprotein
Rao, R. S. P., Ahsan, N., Xu, C., Su, L., Verburgt, J. C., Fornelli, L., Kihara, D., & Xu, D. H. (2021) · Evolutionary Bioinformatics · doi:10.1177/11769343211064616 · Cited by 14
“For example, recurrent deletions (Δ141-144 and Δ146, and Δ243-244) in spike N-terminal domain (NTD) abolished its binding with neutralizing antibody 4A8, and Δ140 caused four-fold reduction in neutralization titre (Harvey et al., 2021).”
BackgroundTorrente-Rodríguez, R. M., Montero‐Calle, A., Bartolomé, C. S., Cano, O., Vázquez, M., Iglesias‐Caballero, M., Corral‐Lugo, A., McConnell, M. J., Pascal, M., Más, V., et al. (2022) · Angewandte Chemie International Edition · doi:10.1002/anie.202203662 · Cited by 17
Liwsrisakun, C., Pata, S., Laopajon, W., Takheaw, N., Chaiwong, W., Inchai, J., Pothirat, C., Bumroongkit, C., Deesomchok, A., Theerakittikul, T., et al. (2022) · Immunity & Ageing · doi:10.1186/s12979-022-00279-8 · Cited by 16
“Importantly, these mutation sites are the immunodominant targets of NAbs elicited by SARS-CoV-2 infection or COVID-19 vaccines [36, 37].”
BackgroundBajpai, P., Singh, V., Chandele, A., & Kumar, S. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.928279 · Cited by 16
“Limited exposure of these regions to the host immune response or critical requirement of their conserved sequences may be responsible for low antibody-mediated immune pressure, hence limiting the occurrence of mutations in these epitopes (Harvey et al., 2021; Pinto et al., 2021; Upadhyay et al., 2021).”
BackgroundInfluentialSuppression of SARS‐CoV‐2 Replication with Stabilized and Click‐Chemistry Modified siRNAs
Traube, F. R., Stern, M., Tölke, A. J., Rudelius, M., Mejías‐Pérez, E., Raddaoui, N., Kümmerer, B. M., Douat, C., Streshnev, F., Albanese, M., et al. (2022) · Angewandte Chemie International Edition · doi:10.1002/anie.202204556 · Cited by 15
Marco, C. D., Veneziano, C., Massacci, A., Pallocca, M., Marascio, N., Quirino, A., Barreca, G. S., Giancotti, A., Gallo, L., Lamberti, A. G., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.934993 · Cited by 16
“On the contrary, K417N decreased ACE2 binding affinity though, in parallel, reduced also the neutralization potential of RBD-specific antibodies (Harvey et al., 2021; Laffeber et al., 2021).”
BackgroundFc engineered ACE2-Fc is a potent multifunctional agent targeting SARS-CoV2
Wines, B. D., Kurtovic, L., Trist, H. M., Esparon, S. E., López, E., Chappin, K., Chan, L., Mordant, F. L., Lee, W. S., Gherardin, N. A., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.889372 · Cited by 15
“This includes profound escape from neutralization by some mAbs (11–15) and significant loss of neutralization activity of convalescent sera (13, 16, 17) and of humoral responses to first generation vaccines (12, 18, 19) reviewed in (10).”
BackgroundDelshad, M., Sanaei, M., Pourbagheri‐Sigaroodi, A., & Bashash, D. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.109128 · Cited by 18
MVsim is a toolset for quantifying and designing multivalent interactions
Bruncsics, B., Errington, W. J., & Sarkar, C. A. (2022) · Nature Communications · doi:10.1038/s41467-022-32496-6 · Cited by 16
Biosynthetic proteins targeting the SARS-CoV-2 spike as anti-virals
Thébault, S., Lejal, N., Dogliani, A., Donchet, A., Urvoas, A., Valerio‐Lepiniec, M., Lavie, M., Baronti, C., Touret, F., da Costa, B. R., et al. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010799 · Cited by 19
“92 Most SARS-CoV-2 infected people presents serum neutralizing antibody activity against the 93 RBD indicating its immunodominance [13].”
BackgroundColson, P., Delerce, J., Marion‐Paris, E., Lagier, J., Levasseur, A., Fournier, P., Scola, B. L., & Raoult, D. (2022) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2022.105360 · Cited by 15
SARS-CoV-2 Variants, Current Vaccines and Therapeutic Implications for COVID-19
Liang, H., Wu, Y., Yau, V., Yin, H.-X., Lowe, S., Bentley, R., Ahmed, M. A., Zhao, W., & Sun, C. (2022) · Vaccines · doi:10.3390/vaccines10091538 · Cited by 16
Ling, Z., Yi, C., Sun, X., Yang, Z., & Sun, B. (2022) · Science China Life Sciences · doi:10.1007/s11427-022-2215-6 · Cited by 16
“Several distinct mechanisms by which mutations affect the antigenic properties of SARS-CoV-2 have been identified, including substitutions of epitope residues, glycan shielding, allosteric structural effects, deletions and insertions, and transformation of entry pathways (Harvey et al., 2021).”
BackgroundPerera, G., Rahman, M. A., Blazevski, A., Wood, A., Walia, S., Bhaskaran, M., & Sriram, S. (2022) · Advanced Materials & Technologies · doi:10.1002/admt.202200965 · Cited by 13
Therapeutic potential of compounds targeting SARS-CoV-2 helicase
Halma, M. T. J., Wever, M. J. A., Abeln, S., Roche, D., & Wuite, G. J. L. (2022) · Frontiers in Chemistry · doi:10.3389/fchem.2022.1062352 · Cited by 16
“The potential of immune escape of future SARS-CoV2 strains from the immunity imparted by the current vaccination program motivates the development of backup treatment options (Harvey et al., 2021; Lazarevic et al., 2021).”
BackgroundVijayanand, S., Patil, S., Menon, I., Gomes, K. B., Kale, A., Bagwe, P., Uddin, M. N., Zughaier, S. M., & D’Souza, M. J. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15030895 · Cited by 16
Jia, Z.-J., Lan, X.-W., Lu, K., Meng, X., Jing, W.-J., Jia, S., Zhao, K., & Dai, Y.-N. (2023) · Journal of Molecular Structure · doi:10.1016/j.molstruc.2023.135409 · Cited by 18
Designing and fabrication of electrochemical nano-biosensor for the fast detection of SARS-CoV-2-RNA
Hussein, H. A., Hanora, A., Solyman, S. M., & Hassan, R. Y. A. (2023) · Scientific Reports · doi:10.1038/s41598-023-32168-5 · Cited by 16
Farrag, M., Dwivedi, R., Sharma, P., Kumar, D., Tandon, R., & Pomin, V. H. (2023) · PLoS ONE · doi:10.1371/journal.pone.0285539 · Cited by 16
“Since the onset of the outbreak with the wild-type (Wuhan-HU-1) SARS-CoV-2 strain in late 2019 in Wuhan, China, SARS-CoV-2 variants of concern (VOC) have been emerging [2].”
BackgroundWu, H.-B., Wang, C., Chung, Y., Shan, Y.-S., Lin, Y.-J., Tsai, H., & Lee, G. (2023) · Analytica Chimica Acta · doi:10.1016/j.aca.2023.341531 · Cited by 16
Kugathasan, R., Sukhova, K., Moshe, M., Kellam, P., & Barclay, W. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011545 · Cited by 16
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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