Mutations in the SARS-CoV-2 spike receptor binding domain and their delicate balance between ACE2 affinity and antibody evasion

  • Song Xue ,
  • Yuru Han ,
  • Fan Wu ,
  • Qiao Wang
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  • Key Laboratory of Medical Molecular Virology (MOE/NHC/CAMS), Shanghai Institute of Infectious Disease and Biosecurity, Shanghai Frontiers Science Center of Pathogenic Microorganisms and Infection, School of Basic Medical Sciences, Shanghai Medical College, Fudan University, Shanghai 200032, China
wufan@shmu.edu.cn
wangqiao@fudan.edu.cn

Received date: 29 Nov 2023

Accepted date: 05 Feb 2024

Copyright

2024 The Author(s) 2024. Published by Oxford University Press on behalf of Higher Education Press.

Abstract

Intensive selection pressure constrains the evolutionary trajectory of SARS-CoV-2 genomes and results in various novel variants with distinct mutation profiles. Point mutations, particularly those within the receptor binding domain (RBD) of SARS-CoV-2 spike (S) protein, lead to the functional alteration in both receptor engagement and monoclonal antibody (mAb) recognition. Here, we review the data of the RBD point mutations possessed by major SARS-CoV-2 variants and discuss their individual effects on ACE2 affinity and immune evasion. Many single amino acid substitutions within RBD epitopes crucial for the antibody evasion capacity may conversely weaken ACE2 binding affinity. However, this weakened effect could be largely compensated by specific epistatic mutations, such as N501Y, thus maintaining the overall ACE2 affinity for the spike protein of all major variants. The predominant direction of SARS-CoV-2 evolution lies neither in promoting ACE2 affinity nor evading mAb neutralization but in maintaining a delicate balance between these two dimensions. Together, this review interprets how RBD mutations efficiently resist antibody neutralization and meanwhile how the affinity between ACE2 and spike protein is maintained, emphasizing the significance of comprehensive assessment of spike mutations.

Cite this article

Song Xue , Yuru Han , Fan Wu , Qiao Wang . Mutations in the SARS-CoV-2 spike receptor binding domain and their delicate balance between ACE2 affinity and antibody evasion[J]. Protein & Cell, 2024 , 15(6) : 403 -418 . DOI: 10.1093/procel/pwae007

1
Addetia A, Piccoli L, Case JB et al. Neutralization, effector function and immune imprinting of Omicron variants. Nature 2023;621:592–601.

DOI

2
Alcantara MC, Higuchi Y, Kirita Y et al. Deep mutational scanning to predict escape from bebtelovimab in SARS-CoV-2 Omicron subvariants. Vaccines (Basel) 2023;11:711.

DOI

3
Andreano E, Piccini G, Licastro D et al. SARS-CoV-2 escape from a highly neutralizing COVID-19 convalescent plasma. Proc Natl Acad Sci USA 2021;118:e2103154118.

DOI

4
Barton MI, MacGowan SA, Kutuzov MA et al. Effects of common mutations in the SARS-CoV-2 Spike RBD and its ligand, the human ACE2 receptor on binding affinity and kinetics. Elife 2021;10:e70658.

DOI

5
Bouhaddou M, Reuschl AK, Polacco BJ et al. SARS-CoV-2 variants evolve convergent strategies to remodel the host response. Cell 2023;186:4597–4614.e26.

DOI

6
Bruel T, Vrignaud LL, Porrot F et al. Antiviral activities of sotrovimab against BQ.1.1 and XBB.1.5 in sera of treated patients. medRxiv 2023.

DOI

7
Callaway E. COVID ‘variant soup’ is making winter surges hard to predict. Nature 2022;611:213–214.

DOI

8
Cao Y, Song W, Wang L et al. Characterization of the enhanced infectivity and antibody evasion of Omicron BA.2.75. Cell Host Microbe 2022a;30:1527–1539.e5.e1525.

DOI

9
Cao Y, Wang J, Jian F et al. Omicron escapes the majority of existing SARS-CoV-2 neutralizing antibodies. Nature 2022b;602:657–663.

DOI

10
Cao Y, Yisimayi A, Jian F et al. BA.2.12.1, BA.4 and BA.5 escape antibodies elicited by Omicron infection. Nature 2022c;608:593–602.

DOI

11
Cao Y, Jian F, Wang J et al. Imprinted SARS-CoV-2 humoral immunity induces convergent Omicron RBD evolution. Nature 2023;614:521–529.

DOI

12
Carabelli AM, Peacock TP, Thorne LG et al. COVID-19 Genomics UK Consortium. SARS-CoV-2 variant biology: immune escape, transmission and fitness. Nat Rev Microbiol 2023;21:162–177.

DOI

13
Chakraborty S. E484K and N501Y SARS-CoV 2 spike mutants Increase ACE2 recognition but reduce affinity for neutralizing antibody. Int Immunopharmacol 2022;102:108424.

DOI

14
Chen RE, Zhang X, Case JB et al. Resistance of SARS-CoV-2 variants to neutralization by monoclonal and serum-derived polyclonal antibodies. Nat Med 2021;27:717–726.

DOI

15
Chen Y, Zhao X, Zhou H et al. Broadly neutralizing antibodies to SARS-CoV-2 and other human coronaviruses. Nat Rev Immunol 2023;23:189–199.

DOI

16
Chi X, Yan R, Zhang J et al. A neutralizing human antibody binds to the N-terminal domain of the Spike protein of SARS-CoV-2. Science 2020;369:650–655.

DOI

17
Cox M, Peacock TP, Harvey WT et al. COVID-19 Genomics UK (COG-UK) Consortium. SARS-CoV-2 variant evasion of monoclonal antibodies based on in vitro studies. Nat Rev Microbiol 2023;21:112–124.

DOI

18
Cui Z, Liu P, Wang N et al. Structural and functional characterizations of infectivity and immune evasion of SARS-CoV-2 Omicron. Cell 2022;185:860–871.e13.

DOI

19
Dadonaite B, Crawford KHD, Radford CE et al. A pseudovirus system enables deep mutational scanning of the full SARS-CoV-2 spike. Cell 2023;186:1263–1278.e20.

DOI

20
Dejnirattisai W, Zhou D, Supasa P et al. Antibody evasion by the P.1 strain of SARS-CoV-2. Cell 2021;184:2939–2954.e9.

DOI

21
Dejnirattisai W, Huo J, Zhou D et al. OPTIC Consortium. SARS-CoV-2 Omicron-B.1.1.529 leads to widespread escape from neutralizing antibody responses. Cell 2022;185:467–484.e15.

22
Driouich JS, Bernadin O, Touret F et al. Activity of Sotrovimab against BQ.1.1 and XBB.1 Omicron sublineages in a hamster model. Antiviral Res 2023;215:105638.

DOI

23
Duffy S, Shackelton LA, Holmes EC. Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 2008;9:267–276.

DOI

24
Dyer O. Covid-19: Infections climb globally as EG.5 variant gains ground. Bmj 2023;382:1900.

DOI

25
Fan Y, Li X, Zhang L et al. SARS-CoV-2 Omicron variant: recent progress and future perspectives. Signal Transduct Target Ther 2022;7:141.

DOI

26
Faraone JN, Qu P, Goodarzi N et al. Immune evasion and membrane fusion of SARS-CoV-2 XBB Subvariants EG.5.1 and XBB.2.3. Emerg Microbes Infect 2023;12:2–13.

DOI

27
Focosi D, McConnell S, Casadevall A et al. Monoclonal antibody therapies against SARS-CoV-2. Lancet Infect Dis 2022;22:e311–e326.

DOI

28
Focosi D, Quiroga R, McConnell S et al. Convergent evolution in SARS-CoV-2 spike creates a variant soup from which new COVID-19 waves emerge. Int J Mol Sci 2023;24:2264.

DOI

29
Frank F, Keen MM, Rao A et al. Deep mutational scanning identifies SARS-CoV-2 Nucleocapsid escape mutations of currently available rapid antigen tests. Cell 2022;185:3603–3616.e13.

DOI

30
Gobeil SM, Janowska K, McDowell S et al. D614G mutation Alters SARS-CoV-2 spike conformation and enhances protease cleavage at the S1/S2 junction. Cell Rep 2021;34:108630.

DOI

31
Greaney AJ, Loes AN, Crawford KHD et al. Comprehensive mapping of mutations in the SARS-CoV-2 receptor-binding domain that affect recognition by polyclonal human plasma antibodies. Cell Host Microbe 2021a;29:463–476.e6.

DOI

32
Greaney AJ, Starr TN, Barnes CO et al. Mapping mutations to the SARS-CoV-2 RBD that escape binding by different classes of antibodies. Nat Commun 2021b;12:4196.

DOI

33
Greaney AJ, Starr TN, Gilchuk P et al. Complete mapping of mutations to the SARS-CoV-2 spike receptor-binding domain that escape antibody recognition. Cell Host Microbe 2021c;29:44–57.e9.

DOI

34
Greaney AJ, Starr TN, Bloom JD. An antibody-escape estimator for mutations to the SARS-CoV-2 receptor-binding domain. Virus Evol 2022;8:veac021.

DOI

35
Gupta D, Sharma P, Singh M et al. Structural and functional insights into the spike protein mutations of emerging SARS-CoV-2 variants. Cell Mol Life Sci 2021;78:7967–7989.

DOI

36
Han P, Li L, Liu S et al. Receptor binding and complex structures of human ACE2 to spike RBD from omicron and delta SARS-CoV-2. Cell 2022;185:630–640.e10.

DOI

37
Hastie KM, Li H, Bedinger D et al. CoVIC-DB team1. Defining variant-resistant epitopes targeted by SARS-CoV-2 antibodies: a global consortium study. Science 2021;374:472–478.

DOI

38
He Q, Wu L, Xu Z et al. An updated atlas of antibody evasion by SARS-CoV-2 Omicron sub-variants including BQ.1.1 and XBB. Cell Rep Med 2023;4:100991.

DOI

39
Hoffmann M, Arora P, Groß R et al. SARS-CoV-2 variants B.1.351 and P.1 escape from neutralizing antibodies. Cell 2021;184:2384–2393.e12.e2312.

DOI

40
Huo J, Dijokaite-Guraliuc A, Liu C et al. OPTIC consortium. A delicate balance between antibody evasion and ACE2 affinity for Omicron BA.2.75. Cell Rep 2023;42:111903.

DOI

41
Iketani S, Mohri H, Culbertson B et al. Multiple pathways for SARS-CoV-2 resistance to nirmatrelvir. Nature 2023;613:558–564.

DOI

42
Jackson CB, Farzan M, Chen B et al. Mechanisms of SARS-CoV-2 entry into cells. Nat Rev Mol Cell Biol 2022;23:3–20.

DOI

43
Javanmardi K, Chou CW, Terrace CI et al. Rapid characterization of spike variants via mammalian cell surface display. Mol Cell 2021;81:5099–5111.e8.

DOI

44
Javanmardi K, Segall-Shapiro TH, Chou CW et al. Antibody escape and cryptic cross-domain stabilization in the SARS-CoV-2 Omicron spike protein. Cell Host Microbe 2022;30:12421254.e6.e1246.

DOI

45
Jian F, Yu Y, Song W et al. Further humoral immunity evasion of emerging SARS-CoV-2 BA.4 and BA.5 subvariants. Lancet Infect Dis 2022;22:1535–1537.

DOI

46
Kabinger F, Stiller C, Schmitzová J et al. Mechanism of molnupiravir- induced SARS-CoV-2 mutagenesis. Nat Struct Mol Biol 2021;28:740–746.

DOI

47
Kaku Y, Kosugi Y, Uriu K et al. Antiviral efficacy of the SARS-CoV-2 XBB breakthrough infection sera against omicron subvariants including EG.5. Lancet Infect Dis 2023;23:e395–e396.

DOI

48
Ke Z, Oton J, Qu K et al. Structures and distributions of SARS-CoV-2 spike proteins on intact virions. Nature 2020;588:498–502.

DOI

49
Kemp SA, Collier DA, Datir RP et al. SARS-CoV-2 evolution during treatment of chronic infection. Nature 2021;592:277–282.

DOI

50
Knezevic I, Mattiuzzo G, Page M et al. WHO International Standard for evaluation of the antibody response to COVID-19 vaccines: call for urgent action by the scientific community. Lancet Microbe 2022;3:e235–e240.

DOI

51
Korber B, Fischer WM, Gnanakaran S et al. Sheffield COVID-19 Genomics Group. Tracking changes in SARS-CoV-2 spike: evidence that D614G increases infectivity of the COVID-19 virus. Cell 2020;182:812–827.e19.e819.

DOI

52
Kumar V, Singh J, Hasnain SE et al. Possible link between higher transmissibility of alpha, kappa and delta variants of SARS-CoV-2 and increased structural stability of its spike protein and hACE2 affinity. Int J Mol Sci 2021;22:9131.

DOI

53
Kumar S, Thambiraja TS, Karuppanan K et al. Omicron and Delta variant of SARS-CoV-2: a comparative computational study of spike protein. J Med Virol 2022;94:1641–1649.

DOI

54
Kumaraswamy S, Tobias R. Label-free kinetic analysis of an antibody-antigen interaction using biolayer interferometry. Methods Mol Biol 2015;1278:165–182.

DOI

55
Li L, Liao H, Meng Y et al. Structural basis of human ACE2 higher binding affinity to currently circulating Omicron SARS-CoV-2 sub-variants BA.2 and BA.1.1. Cell 2022;185:2952–2960.e10.e2910.

DOI

56
Liu C, Ginn HM, Dejnirattisai W et al. Reduced neutralization of SARS-CoV-2 B.1.617 by vaccine and convalescent serum. Cell 2021;184:4220–4236.e4213.

57
Liu Y, Liu J, Plante KS et al. The N501Y spike substitution enhances SARS-CoV-2 infection and transmission. Nature 2022;602:294–299.

DOI

58
Ma W, Fu H, Jian F et al. Immune evasion and ACE2 binding affinity contribute to SARS-CoV-2 evolution. Nat Ecol Evol 2023;7:1457–1466.

DOI

59
Mannar D, Saville JW, Zhu X et al. Structural analysis of receptor binding domain mutations in SARS-CoV-2 variants of concern that modulate ACE2 and antibody binding. Cell Rep 2021;37:110156.

DOI

60
Mannar D, Saville JW, Zhu X et al. SARS-CoV-2 Omicron variant: Antibody evasion and cryo-EM structure of spike protein-ACE2 complex. Science 2022;375:760–764.

DOI

61
Martin DP, Weaver S, Tegally H et al. NGS-SA. The emergence and ongoing convergent evolution of the SARS-CoV-2 N501Y lineages. Cell 2021;184:5189e5187–515200.e7.

DOI

62
McCallum M, Czudnochowski N, Rosen LE et al. Structural basis of SARS-CoV-2 Omicron immune evasion and receptor engagement. Science 2022;375:864–868.

DOI

63
McGrath ME, Xue Y, Dillen C et al. SARS-CoV-2 variant spike and accessory gene mutations alter pathogenesis. Proc Natl Acad Sci USA 2022;119:e2204717119.

DOI

64
Meng B, Abdullahi A, Ferreira I et al. Altered TMPRSS2 usage by SARS-CoV-2 Omicron impacts infectivity and fusogenicity. Nature 2022;603:706–714.

DOI

65
Moeller NH, Shi K, Demir O et al. Structure and dynamics of SARS-CoV-2 proofreading exoribonuclease ExoN. Proc Natl Acad Sci USA 2022;119:e2106379119.

DOI

66
Motozono C, Toyoda M, Zahradnik J et al. Genotype to Phenotype Japan (G2P-Japan) Consortium. SARS-CoV-2 spike L452R variant evades cellular immunity and increases infectivity. Cell Host Microbe 2021;29:1124–1136.e11.e1111.

DOI

67
Moulana A, Dupic T, Phillips AM et al. Compensatory epistasis maintains ACE2 affinity in SARS-CoV-2 Omicron BA.1. Nat Commun 2022;13:7011.

DOI

68
Muruato AE, Fontes-Garfias CR, Ren P et al. A high-throughput neutralizing antibody assay for COVID-19 diagnosis and vaccine evaluation. Nat Commun 2020;11:4059.

DOI

69
Nie J, Li Q, Wu J et al. Quantification of SARS-CoV-2 neutralizing antibody by a pseudotyped virus-based assay. Nat Protoc 2020;15:3699–3715.

DOI

70
Ozono S, Zhang Y, Ode H et al. SARS-CoV-2 D614G spike mutation increases entry efficiency with enhanced ACE2-binding affinity. Nat Commun 2021;12:848.

DOI

71
Park YJ, Pinto D, Walls AC et al. Imprinted antibody responses against SARS-CoV-2 Omicron sublineages. Science 2022;378:619–627.

DOI

72
Piliarik M, Vaisocherová H, Homola J. Surface plasmon resonance biosensing. Methods Mol Biol 2009;503:65–88.

DOI

73
Planas D, Bruel T, Staropoli I et al. Resistance of Omicron subvariants BA.2.75.2, BA.4.6, and BQ.1.1 to neutralizing antibodies. Nat Commun 2023;14:824.

DOI

74
Plante JA, Liu Y, Liu J et al. Spike mutation D614G alters SARS-CoV-2 fitness. Nature 2021;592:116–121.

DOI

75
Qu P, Evans JP, Faraone JN et al. Enhanced neutralization resistance of SARS-CoV-2 Omicron subvariants BQ.1, BQ.1.1, BA.4.6, BF.7, and BA.2.75.2. Cell Host Microbe 2023a;31:9–17.e3.e13.

DOI

76
Qu P, Faraone JN, Evans JP et al. Enhanced evasion of neutralizing antibody response by Omicron XBB.1.5, CH.1.1, and CA.3.1 variants. Cell Rep 2023b;42:112443.

DOI

77
Qu P, Xu K, Faraone JN et al. Immune evasion, infectivity, and fusogenicity of SARS-CoV-2 omicron BA.2.86 and FLip variants. bioRxiv 2023c.

DOI

78
Ramanathan M, Ferguson ID, Miao W et al. SARS-CoV-2 B.1.1.7 and B.1.351 spike variants bind human ACE2 with increased affinity. Lancet Infect Dis 2021;21:1070.

DOI

79
Ray D, Le L, Andricioaei I. Distant residues modulate conformational opening in SARS-CoV-2 spike protein. Proc Natl Acad Sci USA 2021;118:e2100943118.

DOI

80
Riddell AC, Cutino-Moguel T. The origins of new SARS-COV-2 variants in immunocompromised individuals. Curr Opin HIV AIDS 2023;18:148–156.

DOI

81
Riepler L, Rössler A, Falch A et al. Comparison of four SARS-CoV-2 neutralization assays. Vaccines (Basel) 2020;9:13.

DOI

82
Robson F, Khan KS, Le TK et al. Coronavirus RNA Proofreading: Molecular Basis and Therapeutic Targeting. Mol Cell 2020;79:710–727.

DOI

83
Rochman ND, Koonin EV. Learn from the past to predict viral pandemics. Nature 2023;622:700–702.

DOI

84
Saito A, Irie T, Suzuki R et al. Genotype to Phenotype Japan (G2P-Japan) Consortium. Enhanced fusogenicity and pathogenicity of SARS-CoV-2 Delta P681R mutation. Nature 2022;602:300–306.

DOI

85
Scarpa F, Pascarella S, Ciccozzi A et al. Genetic and structural analyses reveal the low potential of the SARS-CoV-2 EG.5 variant. J Med Virol 2023;95:e29075.

DOI

86
Schmidt F, Weisblum Y, Muecksch F et al. Measuring SARS-CoV-2 neutralizing antibody activity using pseudotyped and chimeric viruses. J Exp Med 2020;217:e20201181.

DOI

87
Scialo F, Daniele A, Amato F et al. ACE2: the major cell entry receptor for SARS-CoV-2. Lung 2020;198:867–877.

DOI

88
Shang J, Ye G, Shi K et al. Structural basis of receptor recognition by SARS-CoV-2. Nature 2020;581:221–224.

DOI

89
Sheward DJ, Kim C, Fischbach J et al. Evasion of neutralising antibodies by omicron sublineage BA.2.75. Lancet Infect Dis 2022;22:1421–1422.

DOI

90
Shrestha LB, Foster C, Rawlinson W et al. Evolution of the SARS-CoV-2 omicron variants BA.1 to BA.5: implications for immune escape and transmission. Rev Med Virol 2022;32:e2381.

DOI

91
Shu Y, McCauley J. GISAID: global initiative on sharing all influenza data—from vision to reality. Euro Surveill 2017;22:30494.

DOI

92
Shuai H, Chan JF, Hu B et al. Attenuated replication and pathogenicity of SARS-CoV-2 B.1.1.529 Omicron. Nature 2022;603:693–699.

DOI

93
Starr TN, Thornton JW. Epistasis in protein evolution. Protein Sci 2016;25:1204–1218.

DOI

94
Starr TN, Greaney AJ, Hilton SK et al. Deep mutational scanning of SARS-CoV-2 receptor binding domain reveals constraints on folding and ACE2 binding. Cell 2020;182:1295–1310.e20e1220.

DOI

95
Starr TN, Greaney AJ, Hannon WW et al. Shifting mutational constraints in the SARS-CoV-2 receptor-binding domain during viral evolution. Science 2022a;377:420–424.

DOI

96
Starr TN, Greaney AJ, Stewart CM et al. Deep mutational scans for ACE2 binding, RBD expression, and antibody escape in the SARS-CoV-2 Omicron BA.1 and BA.2 receptor-binding domains. PLoS Pathog 2022b;18:e1010951.

DOI

97
Starr TN, Zepeda SK, Walls AC et al. ACE2 binding is an ancestral and evolvable trait of sarbecoviruses. Nature 2022c;603:913–918.

DOI

98
Supasa P, Zhou D, Dejnirattisai W et al. Reduced neutralization of SARS-CoV-2 B.1.1.7 variant by convalescent and vaccine sera. Cell 2021;184:2201–2211.e2207.

99
Tamura T, Ito J, Uriu K et al. Genotype to Phenotype Japan (G2P-Japan) Consortium. Virological characteristics of the SARS-CoV-2 XBB variant derived from recombination of two Omicron subvariants. Nat Commun 2023a;14:2800.

DOI

100
Tamura T, Ito J, Uriu K et al. Genotype to Phenotype Japan (G2P-Japan) Consortium. Virological characteristics of the SARS-CoV-2 XBB variant derived from recombination of two Omicron subvariants. Nat Commun 2023b;14:2800.

DOI

101
Tan TJC, Mou Z, Lei R et al. High-throughput identification of prefusion-stabilizing mutations in SARS-CoV-2 spike. Nat Commun 2023;14:2003.

DOI

102
Taylor AL, Starr TN. Deep mutational scans of XBB.1.5 and BQ.1.1 reveal ongoing epistatic drift during SARS-CoV-2 evolution. bioRxiv 2023;19:e1011901.

DOI

103
Telenti A, Arvin A, Corey L et al. After the pandemic: perspectives on the future trajectory of COVID-19. Nature 2021;596:495–504.

DOI

104
Thadani NN, Gurev S, Notin P et al. Learning from prepandemic data to forecast viral escape. Nature 2023;622:818–825.

DOI

105
Thorne LG, Bouhaddou M, Reuschl AK et al. Evolution of enhanced innate immune evasion by SARS-CoV-2. Nature 2022;602:487–495.

DOI

106
Tian D, Sun Y, Zhou J et al. The global epidemic of SARS-CoV-2 variants and their mutational immune escape. J Med Virol 2022;94:847–857.

DOI

107
Tregoning JS, Flight KE, Higham SL et al. Progress of the COVID-19 vaccine effort: viruses, vaccines and variants versus efficacy, effectiveness and escape. Nat Rev Immunol 2021;21:626–636.

DOI

108
Tuekprakhon A, Nutalai R, Dijokaite-Guraliuc A et al. OPTIC Consortium. Antibody escape of SARS-CoV-2 Omicron BA.4 and BA.5 from vaccine and BA.1 serum. Cell 2022;185:2422–2433.e13.e2413.

DOI

109
Uriu K, Ito J, Zahradnik J et al. Genotype to Phenotype Japan (G2P-Japan) Consortium. Enhanced transmissibility, infectivity, and immune resistance of the SARS-CoV-2 omicron XBB.1.5 variant. Lancet Infect Dis 2023;23:280–281.

DOI

110
Walls AC, Park YJ, Tortorici MA et al. Structure, function, and antigenicity of the SARS-CoV-2 spike glycoprotein. Cell 2020;181:281–292.e6.e286.

DOI

111
Wang P, Nair MS, Liu L et al. Antibody resistance of SARS-CoV-2 variants B.1.351 and B.1.1.7. Nature 2021;593:130–135.

DOI

112
Wang K, Jia Z, Bao L et al. Memory B cell repertoire from triple vaccinees against diverse SARS-CoV-2 variants. Nature 2022;603:919–925.

DOI

113
Wang Q, Guo Y, Zhang RM et al. Antibody neutralisation of emerging SARS-CoV-2 subvariants: EG.5.1 and XBC.1.6. Lancet Infect Dis 2023a;23:e397–e398.

DOI

114
Wang Q, Iketani S, Li Z et al. Alarming antibody evasion properties of rising SARS-CoV-2 BQ and XBB subvariants. Cell 2023b;186:279–286.e8.e278.

DOI

115
Westendorf K, Žentelis S, Wang L et al. LY-CoV1404 (bebtelovimab) potently neutralizes SARS-CoV-2 variants. Cell Rep 2022;39:110812.

DOI

116
Wilkinson E, Giovanetti M, Tegally H et al. A year of genomic surveillance reveals how the SARS-CoV-2 pandemic unfolded in Africa. Science 2021;374:423–431.

DOI

117
Wrapp D, Wang N, Corbett KS et al. Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Science 2020;367:1260–1263.

DOI

118
Xu K, Gao P, Liu S et al. Protective prototype-Beta and Delta-Omicron chimeric RBD-dimer vaccines against SARS-CoV-2. Cell 2022;185:2265–2278.e2214.

DOI

119
Xu Y, Liu T, Li Y et al. Transmission of SARS-CoV-2 Omicron variant under a dynamic clearance strategy in Shandong, China. Microbiol Spectr 2023;11:e0463222.

DOI

120
Yan R, Zhang Y, Li Y et al. Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2. Science 2020;367:1444–1448.

DOI

121
Yang K, Wang C, White KI et al. Structural conservation among variants of the SARS-CoV-2 spike postfusion bundle. Proc Natl Acad Sci USA 2022;119:e2119467119.

DOI

122
Yin W, Xu Y, Xu P et al. Structures of the Omicron spike trimer with ACE2 and an anti-Omicron antibody. Science 2022;375:1048–1053.

DOI

123
Yu TC, Thornton ZT, Hannon WW et al. A biophysical model of viral escape from polyclonal antibodies. Virus Evol 2022;8:veac110.

DOI

124
Yuan M, Huang D, Lee CD et al. Structural and functional ramifications of antigenic drift in recent SARS-CoV-2 variants. Science 2021;373:818–823.

DOI

125
Yue C, Song W, Wang L et al. ACE2 binding and antibody evasion in enhanced transmissibility of XBB.1.5. Lancet Infect Dis 2023;23:278–280.

DOI

126
Zhang L, Jackson CB, Mou H et al. SARS-CoV-2 spike-protein D614G mutation increases virion spike density and infectivity. Nat Commun 2020;11:6013.

DOI

127
Zhang J, Xiao T, Cai Y et al. Membrane fusion and immune evasion by the spike protein of SARS-CoV-2 Delta variant. Science 2021a;374:1353–1360.

DOI

128
Zhang Q, Xiang R, Huo S et al. Molecular mechanism of interaction between SARS-CoV-2 and host cells and interventional therapy. Signal Transduct Target Ther 2021b;6:233.

DOI

129
Zhang W, Shi K, Geng Q et al. Structural basis for mouse receptor recognition by SARS-CoV-2 omicron variant. Proc Natl Acad Sci USA 2022;119:e2206509119.

DOI

130
Zhang L, Kempf A, Nehlmeier I et al. Neutralisation sensitivity of SARS-CoV-2 lineages EG.5.1 and XBB.2.3. Lancet Infect Dis 2023;23:e391–e392.

DOI

131
Zhao Z, Xie Y, Bai B et al. Structural basis for receptor binding and broader interspecies receptor recognition of currently circulating Omicron sub-variants. Nat Commun 2023;14:4405.

DOI

132
Zhou D, Dejnirattisai W, Supasa P et al. Evidence of escape of SARS-CoV-2 variant B.1.351 from natural and vaccine-induced sera. Cell 2021;184:2348–2361.e2346.

DOI

133
Zhou T, Wang L, Misasi J et al. Structural basis for potent antibody neutralization of SARS-CoV-2 variants including B.1.1.529. Science 2022;376:eabn8897.

DOI

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