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A Promising Vaccination Strategy against COVID-19 on the Horizon: Heterologous Immunization

  • Mattoo, Sameer-ul-Salam (Korea Zoonosis Research Institute, Department of Bioactive Material Science and Genetic Engineering Research Institute, Jeonbuk National University) ;
  • Myoung, Jinjong (Korea Zoonosis Research Institute, Department of Bioactive Material Science and Genetic Engineering Research Institute, Jeonbuk National University)
  • Received : 2021.11.13
  • Accepted : 2021.12.17
  • Published : 2021.12.28

Abstract

To overcome the ongoing COVID-19 pandemic, vaccination campaigns are the highest priority of majority of countries. Limited supply and worldwide disproportionate availability issues for the approved vaccines, together with concerns about rare side-effects have recently initiated the switch to heterologous vaccination, commonly known as mixing of vaccines. The COVID-19 vaccines are highly effective in the general population. However, none of the vaccines is 100% efficacious or effective, with variants posing more challenges, resulting in breakthrough cases. This review summarizes the current knowledge of immune responses to variants of concern (VOC) and breakthrough infections. Furthermore, we discuss the scope of heterologous vaccination and future strategies to tackle the COVID-19 pandemic, including fractionation of vaccine doses and alternative route of vaccination.

Keywords

Acknowledgement

The research was supported by the Bio & Medical Techonology Development Program of the National Research Foundation (NRF) funded by the Ministry of Science & ICT (2021M3E5E3080533) and by "Research Base Construction Fund Support Program" funded by Jeonbuk National University in 2021.

References

  1. Ahn DG, Shin HJ, Kim MH, Lee S, Kim HS, Myoung J, et al. 2020. Current status of epidemiology, diagnosis, therapeutics, and vaccines for novel coronavirus disease 2019 (COVID-19). J. Microbiol. Biotechnol. 30: 313-324. https://doi.org/10.4014/jmb.2003.03011
  2. Dagan N, Barda N, Kepten E, Miron O, Perchik S, Katz MA, et al. 2021. BNT162b2 mRNA Covid-19 vaccine in a nationwide mass vaccination setting. New England J. Med. 384: 1412-1423. https://doi.org/10.1056/NEJMoa2101765
  3. Chemaitelly H, Yassine HM, Benslimane FM, Al Khatib HA, Tang P, Hasan MR, et al. 2021. mRNA-1273 COVID-19 vaccine effectiveness against the B.1.1.7 and B.1.351 variants and severe COVID-19 disease in Qatar. Nat. Med. 27: 1614-1621. https://doi.org/10.1038/s41591-021-01446-y
  4. Abu-Raddad LJ, Chemaitelly H, Butt AA. 2021. Effectiveness of the BNT162b2 Covid-19 vaccine against the B.1.1.7 and B.1.351 variants. New England J. Med. 385: 187-189. https://doi.org/10.1056/NEJMc2104974
  5. Novak N, Tordesillas L, Cabanillas B. 2021. Adverse rare events to vaccines for COVID-19: from hypersensitivity reactions to thrombosis and thrombocytopenia. Int. Rev. Immunol. 1-10.
  6. Our World in D. 2021. Coronavirus (COVID-19) Vaccinations - Statistics and Research. Available from https://ourworldindata.org/covid-vaccinations. Accessed Oct. 21, 2021.
  7. WHO. 2021. Tracking SARS-CoV-2 variants. Available from https://www.who.int/en/activities/tracking-SARS-CoV-2-variants/. Accessed Oct. 20, 2021.
  8. Graham MS, Sudre CH, May A, Antonelli M, Murray B, Varsavsky T, et al. 2021. Changes in symptomatology, reinfection, and transmissibility associated with the SARS-CoV-2 variant B.1.1.7: an ecological study. Lancet Public Health 6: e335-e345. https://doi.org/10.1016/S2468-2667(21)00055-4
  9. Davies NG, Abbott S, Barnard RC, Jarvis CI, Kucharski AJ, Munday JD, et al. 2021. Estimated transmissibility and impact of SARS-CoV-2 lineage B. 1.1. 7 in England. Science 372: eabg3055. https://doi.org/10.1126/science.abg3055
  10. Harvey WT, Carabelli AM, Jackson B, Gupta RK, Thomson EC, Harrison EM, et al. 2021. SARS-CoV-2 variants, spike mutations and immune escape. Nat. Rev. Microbiol. 19: 409-424. https://doi.org/10.1038/s41579-021-00573-0
  11. Campbell F, Archer B, Laurenson-Schafer H, Jinnai Y, Konings F, Batra N, et al. 2021. Increased transmissibility and global spread of SARS-CoV-2 variants of concern as at June 2021. Eurosurveillance 26: 2100509.
  12. Faria NR, Mellan TA, Whittaker C, Claro IM, Candido DdS, Mishra S, et al. 2021. Genomics and epidemiology of the P.1 SARS-CoV-2 lineage in Manaus, Brazil. Science 372: 815-821. https://doi.org/10.1126/science.abh2644
  13. Cherian S, Potdar V, Jadhav S, Yadav P, Gupta N, Das M, et al. 2021. SARS-CoV-2 spike mutations, L452R, T478K, E484Q and P681R, in the second wave of COVID-19 in Maharashtra, India. Microorganisms 9: 1542. https://doi.org/10.3390/microorganisms9071542
  14. Chvatal-Medina M, Mendez-Cortina Y, Patino PJ, Velilla PA, Rugeles MT. 2021. Antibody responses in COVID-19: A Review. Front. Immunol. 12: 633184. https://doi.org/10.3389/fimmu.2021.633184
  15. Cromer D, Juno JA, Khoury D, Reynaldi A, Wheatley AK, Kent SJ, et al. 2021. Prospects for durable immune control of SARS-CoV-2 and prevention of reinfection. Nat. Rev. Immunol. 21: 395-404. https://doi.org/10.1038/s41577-021-00550-x
  16. Sette A, Crotty S. 2021. Adaptive immunity to SARS-CoV-2 and COVID-19. Cell 184: 861-880. https://doi.org/10.1016/j.cell.2021.01.007
  17. Weiskopf D, Schmitz KS, Raadsen MP, Grifoni A, Okba NMA, Endeman H, et al. 2020. Phenotype and kinetics of SARS-CoV-2-specific T cells in COVID-19 patients with acute respiratory distress syndrome. Sci. Immunol. 5: eabd2071-eabd2071. https://doi.org/10.1126/sciimmunol.abd2071
  18. Neidleman J, Luo X, Frouard J, Xie G, Gill G, Stein ES, et al. 2020. SARS-CoV-2-specific T cells exhibit phenotypic features of helper function, lack of terminal differentiation, and high proliferation potential. Cell Rep. Med. 1: 100081-100081. https://doi.org/10.1016/j.xcrm.2020.100081
  19. Sahin U, Muik A, Derhovanessian E, Vogler I, Kranz LM, Vormehr M, et al. 2020. COVID-19 vaccine BNT162b1 elicits human antibody and TH 1 T cell responses. Nature 586: 594-599. https://doi.org/10.1038/s41586-020-2814-7
  20. Swanson PA, Padilla M, Hoyland W, McGlinchey K, Fields PA, Bibi S, et al. 2021. T-cell mediated immunity after AZD1222 vaccination: A polyfunctional spike-specific Th1 response with a diverse TCR repertoire. medRxiv. doi: 10.1101/2021.06.17.21259027. Preprint
  21. Painter MM, Mathew D, Goel RR, Apostolidis SA, Pattekar A, Kuthuru O, et al. 2021. Rapid induction of antigen-specific CD4+ T cells is associated with coordinated humoral and cellular immunity to SARS-CoV-2 mRNA vaccination. Immunity 54: 2133-2142. e2133. https://doi.org/10.1016/j.immuni.2021.08.001
  22. Koutsakos M, Lee WS, Wheatley AK, Kent SJ, Juno JA. 2021. T follicular helper cells in the humoral immune response to SARS-CoV-2 infection and vaccination. J. Leukoc. Biol. 10.1002/JLB.5MR0821-464R.
  23. Sekine T, Perez-Potti A, Rivera-Ballesteros O, Stralin K, Gorin J-B, Olsson A, et al. 2020. Robust T cell immunity in convalescent individuals with asymptomatic or mild COVID-19. Cell 183: 158-168. e114. https://doi.org/10.1016/j.cell.2020.08.017
  24. Rydyznski Moderbacher C, Ramirez SI, Dan JM, Grifoni A, Hastie KM, Weiskopf D, et al. 2020. Antigen-specific adaptive immunity to SARS-CoV-2 in acute COVID-19 and associations with age and disease severity. Cell 183: 996-1012.e1019. https://doi.org/10.1016/j.cell.2020.09.038
  25. Schulien I, Kemming J, Oberhardt V, Wild K, Seidel LM, Killmer S, et al. 2021. Characterization of pre-existing and induced SARS-CoV-2-specific CD8(+) T cells. Nat. Med. 27: 78-85. https://doi.org/10.1038/s41591-020-01143-2
  26. Chen Y, Yin S, Tong X, Tao Y, Ni J, Pan J, et al. 2021. Dynamic SARS-CoV-2 specific B cell and T cell responses following immunization of an inactivated COVID-19 vaccine. Clin. Microbiol. Infect. S1198-743X(21)00605-4. doi: 10.1016/j.cmi.2021.10.006.
  27. Planas D, Veyer D, Baidaliuk A, Staropoli I, Guivel-Benhassine F, Rajah MM, et al. 2021. Reduced sensitivity of SARS-CoV-2 variant Delta to antibody neutralization. Nature 596: 276-280. https://doi.org/10.1038/s41586-021-03777-9
  28. Supasa P, Zhou D, Dejnirattisai W, Liu C, Mentzer AJ, Ginn HM, et al. 2021. Reduced neutralization of SARS-CoV-2 B.1.1.7 variant by convalescent and vaccine sera. Cell 184: 2201-2211.e2207. https://doi.org/10.1016/j.cell.2021.02.033
  29. Zhou D, Dejnirattisai W, Supasa P, Liu C, Mentzer AJ, Ginn HM, et al. 2021. Evidence of escape of SARS-CoV-2 variant B. 1.351 from natural and vaccine-induced sera. Cell 184: 2348-2361. e2346. https://doi.org/10.1016/j.cell.2021.02.037
  30. Dejnirattisai W, Zhou D, Supasa P, Liu C, Mentzer AJ, Ginn HM, et al. 2021. Antibody evasion by the P.1 strain of SARS-CoV-2. Cell 184: 2939-2954.e2939. https://doi.org/10.1016/j.cell.2021.03.055
  31. Liu C, Ginn HM, Dejnirattisai W, Supasa P, Wang B, Tuekprakhon A, et al. 2021. Reduced neutralization of SARS-CoV-2 B.1.617 by vaccine and convalescent serum. Cell 184: 4220-4236.e4213. https://doi.org/10.1016/j.cell.2021.06.020
  32. Hoffmann M, Arora P, Gross R, Seidel A, Hornich BF, Hahn AS, et al. 2021. SARS-CoV-2 variants B.1.351 and P.1 escape from neutralizing antibodies. Cell 184: 2384-2393.e2312. https://doi.org/10.1016/j.cell.2021.03.036
  33. Wu K, Werner AP, Koch M, Choi A, Narayanan E, Stewart-Jones GBE, et al. 2021. Serum neutralizing activity elicited by mRNA-1273 vaccine. New Engl. J. Med. 384: 1468-1470. https://doi.org/10.1056/NEJMc2102179
  34. Wall EC, Wu M, Harvey R, Kelly G, Warchal S, Sawyer C, et al. 2021. Neutralising antibody activity against SARS-CoV-2 VOCs B.1.617.2 and B.1.351 by BNT162b2 vaccination. Lancet 397: 2331-2333. https://doi.org/10.1016/S0140-6736(21)01290-3
  35. Choi A, Koch M, Wu K, Dixon G, Oestreicher J, Legault H, et al. 2021. Serum neutralizing activity of mRNA-1273 against SARS-CoV-2 variants. J. Virol. 95: e0131321. https://doi.org/10.1128/JVI.01313-21
  36. Chen RE, Zhang X, Case JB, Winkler ES, Liu Y, VanBlargan LA, et al. 2021. Resistance of SARS-CoV-2 variants to neutralization by monoclonal and serum-derived polyclonal antibodies. Nat. Med. 27: 717-726. https://doi.org/10.1038/s41591-021-01294-w
  37. Emary KRW, Golubchik T, Aley PK, Ariani CV, Angus B, Bibi S, et al. 2021. Efficacy of ChAdOx1 nCoV-19 (AZD1222) vaccine against SARS-CoV-2 variant of concern 202012/01 (B.1.1.7): an exploratory analysis of a randomised controlled trial. Lancet. 397: 1351-1362. https://doi.org/10.1016/S0140-6736(21)00628-0
  38. Vacharathit V, Aiewsakun P, Manopwisedjaroen S, Srisaowakarn C, Laopanupong T, Ludowyke N, et al. 2021. CoronaVac induces lower neutralising activity against variants of concern than natural infection. Lancet Infect. Dis. 21: 1352-1354. https://doi.org/10.1016/S1473-3099(21)00568-5
  39. Jalkanen P, Kolehmainen P, Hakkinen HK, Huttunen M, Tahtinen PA, Lundberg R, et al. 2021. COVID-19 mRNA vaccine induced antibody responses against three SARS-CoV-2 variants. Nat. Commun. 12: 3991-3991. https://doi.org/10.1038/s41467-021-24285-4
  40. Wang P, Nair MS, Liu L, Iketani S, Luo Y, Guo Y, et al. 2021. Antibody resistance of SARS-CoV-2 variants B.1.351 and B.1.1.7. Nature 593: 130-135. https://doi.org/10.1038/s41586-021-03398-2
  41. Liu Y, Liu J, Xia H, Zhang X, Fontes-Garfias CR, Swanson KA, et al. 2021. Neutralizing activity of BNT162b2-elicited serum. New Engl. J. Med. 384: 1466-1468. https://doi.org/10.1056/NEJMc2102017
  42. Alter G, Yu J, Liu J, Chandrashekar A, Borducchi EN, Tostanoski LH, et al. 2021. Immunogenicity of Ad26.COV2.S vaccine against SARS-CoV-2 variants in humans. Nature 596: 268-272. https://doi.org/10.1038/s41586-021-03681-2
  43. Planas D, Bruel T, Grzelak L, Guivel-Benhassine F, Staropoli I, Porrot F, et al. 2021. Sensitivity of infectious SARS-CoV-2 B.1.1.7 and B.1.351 variants to neutralizing antibodies. Nat. Med. 27: 917-924. https://doi.org/10.1038/s41591-021-01318-5
  44. Hoffmann M, Hofmann-Winkler H, Kruger N, Kempf A, Nehlmeier I, Graichen L, et al. 2021. SARS-CoV-2 variant B.1.617 is resistant to bamlanivimab and evades antibodies induced by infection and vaccination. Cell Rep. 36: 109415. https://doi.org/10.1016/j.celrep.2021.109415
  45. Liu J, Liu Y, Xia H, Zou J, Weaver SC, Swanson KA, et al. 2021. BNT162b2-elicited neutralization of B.1.617 and other SARS-CoV-2 variants. Nature 596: 273-275. https://doi.org/10.1038/s41586-021-03693-y
  46. Edara V-V, Pinsky BA, Suthar MS, Lai L, Davis-Gardner ME, Floyd K, et al. 2021. Infection and vaccine-induced neutralizing-antibody responses to the SARS-CoV-2 B.1.617 variants. New Engl. J. Med. 385: 664-666. https://doi.org/10.1056/NEJMc2107799
  47. Barouch DH, Stephenson KE, Sadoff J, Yu J, Chang A, Gebre M, et al. 2021. Durable humoral and cellular immune responses 8 months after Ad26.COV2.S vaccination. New Engl. J. Med. 385: 951-953. https://doi.org/10.1056/NEJMc2108829
  48. Liu G, Carter B, Gifford DK. 2021. Predicted cellular immunity population coverage gaps for SARS-CoV-2 subunit vaccines and their augmentation by compact peptide sets. Cell Systems 12: 102-107.e104. https://doi.org/10.1016/j.cels.2020.11.010
  49. Corbett KS, Edwards DK, Leist SR, Abiona OM, Boyoglu-Barnum S, Gillespie RA, et al. 2020. SARS-CoV-2 mRNA vaccine design enabled by prototype pathogen preparedness. Nature 586: 567-571. https://doi.org/10.1038/s41586-020-2622-0
  50. Tarke A, Sidney J, Methot N, Yu ED, Zhang Y, Dan JM, et al. 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: 100355-100355. https://doi.org/10.1016/j.xcrm.2021.100355
  51. Geers D, Shamier MC, Bogers S, den Hartog G, Gommers L, Nieuwkoop NN, et al. 2021. SARS-CoV-2 variants of concern partially escape humoral but not T-cell responses in COVID-19 convalescent donors and vaccinees. Sci. Immunol. 6: eabj1750-eabj1750. https://doi.org/10.1126/sciimmunol.abj1750
  52. Agerer B, Koblischke M, Gudipati V, Montano-Gutierrez LF, Smyth M, Popa A, et al. 2021. SARS-CoV-2 mutations in MHC-I-restricted epitopes evade CD8(+) T cell responses. Sci. Immunol. 6: eabag6461.
  53. Lustig Y, Sapir E, Regev-Yochay G, Cohen C, Fluss R, Olmer L, et al. 2021. BNT162b2 COVID-19 vaccine and correlates of humoral immune responses and dynamics: a prospective, single-centre, longitudinal cohort study in health-care workers. Lancet Respir. Med. 9: 999-1009. https://doi.org/10.1016/S2213-2600(21)00220-4
  54. Bergwerk M, Gonen T, Lustig Y, Amit S, Lipsitch M, Cohen C, et al. 2021. Covid-19 breakthrough infections in vaccinated health care workers. New Engl. J. Med. 385: 1145-1146. https://doi.org/10.1056/NEJMc2108076
  55. Mallapaty S. 2021. A blood marker predicts who gets 'breakthrough' COVID. Nature doi: 10.1038/d41586-021-02096-3. Online ahead of print.
  56. Ulhaq ZS, Soraya GV, Indriana K. 2021. Breakthrough COVID-19 case after full-dose administration of CoronaVac vaccine. Indian J. Med. Microbiol. 39: 562-563. https://doi.org/10.1016/j.ijmmb.2021.05.017
  57. Selingerova I, Valik D, Gescheidtova L, Sramek V, Cermakova Z, Zdrazilova-Dubska L. 2021. Interpretive discrepancies caused by target values inter-batch variations in chemiluminescence immunoassay for SARS-CoV-2 IgM/IgG by MAGLUMI. J. Med. Virol. 93: 1805-1809. https://doi.org/10.1002/jmv.26612
  58. Hacisuleyman E, Hale C, Saito Y, Blachere NE, Bergh M, Conlon EG, et al. 2021. Vaccine breakthrough infections with SARS-CoV-2 variants. New Engl. J. Med. 384: 2212-2218. https://doi.org/10.1056/NEJMoa2105000
  59. Wise J. 2021. Covid-19: European countries suspend use of Oxford-AstraZeneca vaccine after reports of blood clots. BMJ 372: n699-n699. https://doi.org/10.1136/bmj.n699
  60. Greinacher A, Thiele T, Warkentin TE, Weisser K, Kyrle PA, Eichinger S. 2021. Thrombotic thrombocytopenia after ChAdOx1 nCov-19 vaccination. New Engl. J. Med. 384: 2092-2101. https://doi.org/10.1056/NEJMoa2104840
  61. Borobia AM, Carcas AJ, Perez-Olmeda M, Castano L, Bertran MJ, Garcia-Perez J, et al. 2021. Immunogenicity and reactogenicity of BNT162b2 booster in ChAdOx1-S-primed participants (CombiVacS): a multicentre, open-label, randomised, controlled, phase 2 trial. Lancet 398: 121-130. https://doi.org/10.1016/S0140-6736(21)01420-3
  62. Richardson CD. 2021. Heterologous ChAdOx1-nCoV19?NT162b2 vaccination provides superior immunogenicity against COVID-19. Lancet Respir. Med. 314: 1936-1938.
  63. Benning L, Tollner M, Hidmark A, Schaier M, Nusshag C, Kalble F, et al. 2021. Heterologous ChAdOx1 nCoV-19/BNT162b2 prime-boost vaccination induces strong humoral responses among health care workers. Vaccines 9: 857-857. https://doi.org/10.3390/vaccines9080857
  64. Heath PT, Galiza EP, Baxter DN, Boffito M, Browne D, Burns F, et al. 2021. Safety and Efficacy of NVX-CoV2373 Covid-19 vaccine. New Engl. J. Med. 385: 1172-1183. https://doi.org/10.1056/NEJMoa2107659
  65. Shaw RH, Stuart A, Greenland M, Liu X, Nguyen Van-Tam JS, Snape MD. 2021. Heterologous prime-boost COVID-19 vaccination: initial reactogenicity data. Lancet 397: 2043-2046.
  66. Hillus D, Schwarz T, Tober-Lau P, Vanshylla K, Hastor H, Thibeault C, et al. 2021. Safety, reactogenicity, and immunogenicity of homologous and heterologous prime-boost immunisation with ChAdOx1 nCoV-19 and BNT162b2: a prospective cohort study. Lancet Respir. Med. 9: 918-918.
  67. Barros-Martins J, Hammerschmidt SI, Cossmann A, Odak I, Stankov MV, Morillas Ramos G, et al. 2021. Immune responses against SARS-CoV-2 variants after heterologous and homologous ChAdOx1 nCoV-19/BNT162b2 vaccination. Nat. Med. 27: 1525-1529. https://doi.org/10.1038/s41591-021-01449-9
  68. Schmidt T, Klemis V, Schub D, Mihm J, Hielscher F, Marx S, et al. 2021. Immunogenicity and reactogenicity of heterologous ChAdOx1 nCoV-19/mRNA vaccination. Nat. Med. 27: 1530-1535. https://doi.org/10.1038/s41591-021-01464-w
  69. Ostadgavahi AT, Booth R, Sisson G, McMullen N, Warhuus M, Robertson P, et al. 2021. Heterologous immunization with Covishield and Pfizer vaccines against SARS-CoV-2 elicits a robust humoral immune response. J. Infect. Dev. Ctries. 15: 653-656. https://doi.org/10.3855/jidc.15368
  70. Mulligan MJ, Lyke KE, Kitchin N, Absalon J, Gurtman A, Lockhart S, et al. 2020. Phase I/II study of COVID-19 RNA vaccine BNT162b1 in adults. Nature 586: 589-593. https://doi.org/10.1038/s41586-020-2639-4
  71. Liu X, Shaw RH, Stuart ASV, Greenland M, Aley PK, Andrews NJ, et al. 2021. Safety and immunogenicity of heterologous versus homologous prime-boost schedules with an adenoviral vectored and mRNA COVID-19 vaccine (Com-COV): a single-blind, randomised, non-inferiority trial. Lancet (London, England) 398: 856-869. https://doi.org/10.1016/S0140-6736(21)01694-9
  72. Jara A, Undurraga EA, Gonzalez C, Paredes F, Fontecilla T, Jara G, et al. 2021. Effectiveness of an Inactivated SARS-CoV-2 Vaccine in Chile. New Engl. J. Med. 385: 875-884. https://doi.org/10.1056/NEJMoa2107715
  73. Crotty S. 2021. Hybrid immunity. Science 372: 1392-1393. https://doi.org/10.1126/science.abj2258
  74. Tan C-W, Chia W-N, Young BE, Zhu F, Lim B-L, Sia W-R, et al. 2021. Pan-sarbecovirus neutralizing antibodies in BNT162b2-immunized SARS-CoV-1 survivors. N. Engl. J. Med. 385: 1401-1406. https://doi.org/10.1056/NEJMoa2108453
  75. Stamatatos L, Czartoski J, Wan YH, Homad LJ, Rubin V, Glantz H, et al. 2021. mRNA vaccination boosts cross-variant neutralizing antibodies elicited by SARS-CoV-2 infection. Science 25: eabg9175.
  76. Goel RR, Apostolidis SA, Painter MM, Mathew D, Pattekar A, Kuthuru O, et al. 2021. Distinct antibody and memory B cell responses in SARS-CoV-2 naive and recovered individuals after mRNA vaccination. Sci. Immunol. 6: eabi6950. https://doi.org/10.1126/sciimmunol.abi6950
  77. Bae S, Lee JY, Myoung J. 2020. Chikungunya virus nsP2 impairs MDA5/RIG-I-mediated induction of NF-kappaB promoter activation: A potential target for virus-specific therapeutics. J. Microbiol. Biotechnol. 30: 1801-1809. https://doi.org/10.4014/jmb.2012.12005
  78. Ngueyen TTN, Kim SJ, Lee JY, Myoung J. 2019. Zika virus proteins NS2A and NS4A are major antagonists that reduce IFN-beta promoter activity induced by the MDA5/RIG-I signaling pathway. J. Microbiol. Biotechnol. 29: 1665-1674. https://doi.org/10.4014/jmb.1909.09017
  79. Myoung J, Min K. 2019. Dose-dependent inhibition of melanoma differentiation-associated gene 5-mediated activation of type I interferon responses by methyltransferase of hepatitis E virus. J. Microbiol. Biotechnol. 29: 1137-1143. https://doi.org/10.4014/jmb.1905.05040
  80. Myoung J, Lee SA, Lee HR. 2019. Beyond viral interferon regulatory factors: Immune evasion strategies. J. Microbiol. Biotechnol. 29: 1873-1881. https://doi.org/10.4014/jmb.1910.10004
  81. Myoung J, Lee JY, Min KS. 2019. Methyltransferase of a cell culture-adapted hepatitis E inhibits the MDA5 receptor signaling pathway. J. Microbiol. 57: 1126-1131. https://doi.org/10.1007/s12275-019-9478-8
  82. Lee JY, Kim SJ, Myoung J. 2019. Middle east respiratory syndrome coronavirus-encoded ORF8b inhibits RIG-I-like receptors in a differential mechanism. J. Microbiol. Biotechnol. 29: 2014-2021. https://doi.org/10.4014/jmb.1911.11024
  83. Lee JY, Bae S, Myoung J. 2019. Middle East respiratory syndrome coronavirus-encoded ORF8b strongly antagonizes IFN-beta promoter activation: its implication for vaccine design. J. Microbiol. 57: 803-811. https://doi.org/10.1007/s12275-019-9272-7
  84. Lee JY, Bae S, Myoung J. 2019. Middle East respiratory syndrome coronavirus-encoded accessory proteins impair MDA5-and TBK1-mediated activation of NF-kappaB. J. Microbiol. Biotechnol. 29: 1316-1323. https://doi.org/10.4014/jmb.1908.08004
  85. Lee J, Bae S, Myoung J. 2019. Generation of full-length infectious cDNA clones of middle East respiratory syndrome coronavirus. J. Microbiol. Biotechnol. 29: 999-1007. https://doi.org/10.4014/jmb.1905.05061
  86. Cowling BJ, Lim WW, Cobey S. 2021. Fractionation of COVID-19 vaccine doses could extend limited supplies and reduce mortality. Nat. Med. 27: 1321-1323. https://doi.org/10.1038/s41591-021-01440-4
  87. WHO. 2021. Interim statement on dose-sparing strategies for COVID-19 vaccines (fractionated vaccine doses). Available from https://www.who.int/news/item/10-08-2021-interim-statement-on-dose-sparing-strategies-for-covid-19-vaccines-(fractionated-vaccine-doses). Accessed Oct. 21, 2021.
  88. Wu JT, Peak CM, Leung GM, Lipsitch M. 2016. Fractional dosing of yellow fever vaccine to extend supply: a modelling study. Lancet (London, England) 388: 2904-2911. https://doi.org/10.1016/S0140-6736(16)31838-4
  89. WHO. 2017. WHO position on the use of fractional doses - June 2017, addendum to vaccines and vaccination against yellow fever WHO: Position paper - June 2013. Vaccine 35: 5751-5752. https://doi.org/10.1016/j.vaccine.2017.06.087
  90. Chu L, McPhee R, Huang W, Bennett H, Pajon R, Nestorova B, et al. 2021. A preliminary report of a randomized controlled phase 2 trial of the safety and immunogenicity of mRNA-1273 SARS-CoV-2 vaccine. Vaccine 39: 2791-2799. https://doi.org/10.1016/j.vaccine.2021.02.007
  91. Voysey M, Clemens SAC, Madhi SA, Weckx LY, Folegatti PM, Aley PK, et al. 2021. Safety and efficacy of the ChAdOx1 nCoV-19 vaccine (AZD1222) against SARS-CoV-2: an interim analysis of four randomised controlled trials in Brazil, South Africa, and the UK. Lancet 397: 99-111. https://doi.org/10.1016/S0140-6736(20)32661-1
  92. Callaway E. 2021. COVID vaccine boosters: the most important questions. Nature 596: 178-180. https://doi.org/10.1038/d41586-021-02158-6
  93. Turner JS, O'Halloran JA, Kalaidina E, Kim W, Schmitz AJ, Zhou JQ, et al. 2021. SARS-CoV-2 mRNA vaccines induce persistent human germinal centre responses. Nature 596: 109-113. https://doi.org/10.1038/s41586-021-03738-2
  94. Krause PR, Fleming TR, Peto R, Longini IM, Figueroa JP, Sterne JAC, et al. 2021. Considerations in boosting COVID-19 vaccine immune responses. Lancet (London, England) 6736: 21-24.
  95. Tregoning JS, Flight KE, Higham SL, Wang Z, Pierce BF. 2021. Progress of the COVID-19 vaccine effort: viruses, vaccines and variants versus efficacy, effectiveness and escape. Nat. Rev. Immunol. 21: 626-636. https://doi.org/10.1038/s41577-021-00592-1
  96. Sekine T, Perez-Potti A, Rivera-Ballesteros O, Stralin K, Gorin J-B, Olsson A, et al. 2020. Robust T cell immunity in convalescent individuals with asymptomatic or mild COVID-19. Cell 183: 158-168.e114. https://doi.org/10.1016/j.cell.2020.08.017
  97. Gallais F, Velay A, Nazon C, Wendling M-J, Partisani M, Sibilia J, et al. 2021. Intrafamilial exposure to SARS-CoV-2 associated with cellular immune response without seroconversion, France. Emerg. Infect. Dis. 27: 113-121. https://doi.org/10.3201/eid2701.203611
  98. Yang J, Zhong M, Hong K, Yang Q, Zhang E, Zhou D, et al. 2021. Characteristics of T-cell responses in COVID-19 patients with prolonged SARS-CoV-2 positivity - a cohort study. Clin. Transl. Immunol. 10: e1259-e1259.
  99. Jeyanathan M, Afkhami S, Smaill F, Miller MS, Lichty BD, Xing Z. 2020. Immunological considerations for COVID-19 vaccine strategies. Nat. Rev. Immunol. 20: 615-632. https://doi.org/10.1038/s41577-020-00434-6
  100. Szabo PA, Miron M, Farber DL. 2019. Location, location, location: Tissue resident memory T cells in mice and humans. Sci. Immunol. 4: eaas9673-eaas9673. https://doi.org/10.1126/sciimmunol.aas9673
  101. Jeyanathan M, Yao Y, Afkhami S, Smaill F, Xing Z. 2018. New Tuberculosis vaccine strategies: taking aim at un-natural immunity. Trends Immunol. 39: 419-433. https://doi.org/10.1016/j.it.2018.01.006
  102. Hassan AO, Kafai NM, Dmitriev IP, Fox JM, Smith BK, Harvey IB, et al. 2020. A single-dose intranasal ChAd vaccine protects upper and lower respiratory tracts against SARS-CoV-2. Cell 183: 169-184.e113. https://doi.org/10.1016/j.cell.2020.08.026
  103. Pizzolla A, Wakim LM. 2019. Memory T cell dynamics in the lung during influenza virus infection. J. Immunol. 202: 374-381. https://doi.org/10.4049/jimmunol.1800979
  104. Brinkley-Rubinstein L, Peterson M, Martin R, Chan P, Berk J. 2021. Breakthrough SARS-CoV-2 infections in prison after vaccination. N. Engl. J. Med. 385: 1051-1052. https://doi.org/10.1056/NEJMc2108479
  105. Kustin T, Harel N, Finkel U, Perchik S, Harari S, Tahor M, et al. 2021. Evidence for increased breakthrough rates of SARS-CoV-2 variants of concern in BNT162b2-mRNA-vaccinated individuals. Nat. Med. 27: 1379-1384. https://doi.org/10.1038/s41591-021-01413-7
  106. Niyas VKM, Arjun R. 2021. Breakthrough COVID-19 infections among health care workers after two doses of ChAdOx1 nCoV-19 vaccine. QJM: Int. J. Med. 114: 757-758. https://doi.org/10.1093/qjmed/hcab167
  107. Butt AA, Nafady-Hego H, Chemaitelly H, Abou-Samra A-B, Khal AA, Coyle PV, et al. 2021. Outcomes among patients with breakthrough SARS-CoV-2 infection after vaccination. Int. J. Infect. Dis. 110: 353-358. https://doi.org/10.1016/j.ijid.2021.08.008
  108. Lange B, Gerigk M, Tenenbaum T. 2021. Breakthrough infections in BNT162b2-vaccinated health care workers. N. Engl. J. Med. 385: 1145-1146. https://doi.org/10.1056/NEJMc2108076
  109. Duerr R, Dimartino D, Marier C, Zappile P, Wang G, Lighter J, et al. 2021. Dominance of Alpha and Iota variants in SARS-CoV-2 vaccine breakthrough infections in New York City. J. Clin. Invest. 131: e152702. https://doi.org/10.1172/JCI152702
  110. Estofolete CF, Banho CA, Campos GRF, Marques BdC, Sacchetto L, Ullmann LS, et al. 2021. Case study of two post vaccination SARS-CoV-2 infections with P1 variants in coronaVac vaccinees in Brazil. Viruses 13: 1237-1237. https://doi.org/10.3390/v13071237
  111. Ioannou P, Karakonstantis S, Astrinaki E, Saplamidou S, Vitsaxaki E, Hamilos G, et al. 2021. Transmission of SARS-CoV-2 variant B.1.1.7 among vaccinated health care workers. Infect. Dis. 53: 876-879. https://doi.org/10.1080/23744235.2021.1945139
  112. Martinot M, Carnein S, Kempf C, Gantner P, Gallais F, Fafi-Kremer S. 2021. Outbreak of SARS-CoV-2 infection in a long-term care facility after COVID-19 BNT162b2 mRNA vaccination. Clin. Microbiol. Infect. 27: 1537-1539. https://doi.org/10.1016/j.cmi.2021.06.038