The Third dose of CoronVac vaccination induces broad and potent adaptive immune responses that recognize SARS-CoV-2 Delta and Omicron variants

References

• Amit S, Gonen T, Regev-Yochay G. Covid-19 breakthrough infections in vaccinated health care workers. Reply. N Engl J Med. 2021 Oct 21;385(17):1630–1631.
   PubMed Web of Science ®Google Scholar
• Goldberg Y, Mandel M, Bar-On YM, et al. Waning immunity after the BNT162b2 vaccine in Israel. N Engl J Med. 2021 Dec 9;385(24):e85.
   PubMed Web of Science ®Google Scholar
• Espenhain L, Funk T, Overvad M, et al. Epidemiological characterisation of the first 785 SARS-CoV-2 Omicron variant cases in Denmark, December 2021. Euro Surveill. 2021 Dec;26(50):210146.
   Google Scholar
• Centers for Disease Control and Prevention. CDC COVID Data Tracker. (2022). Available online at: https://covid.cdc.gov/covid-data-tracker/#variant-proportions.
   Google Scholar
• Wang Y, Zhang L, Li Q, et al. The significant immune escape of pseudotyped SARS-CoV-2 variant omicron. Emerg Microbes Infect. 2022 Dec;11(1):1–5.
   PubMed Web of Science ®Google Scholar
• Krause PR, Fleming TR, Peto R, et al. Considerations in boosting COVID-19 vaccine immune responses. Lancet. 2021 Oct 9;398(10308):1377–1380.
   PubMed Web of Science ®Google Scholar
• Callaway E. COVID vaccine boosters: the most important questions. Nature. 2021 Aug;596(7871):178–180.
   PubMed Web of Science ®Google Scholar
• Kalafat E, Magee LA, von Dadelszen P, et al. COVID-19 booster doses in pregnancy and global vaccine equity. Lancet. 2022 Mar 5;399(10328):907–908.
   PubMed Web of Science ®Google Scholar
• SAGE. Highlights from the meeting of the Strategic Advisory Group of Experts (SAGE) on Immunization. Oct 11, 2021.
   Google Scholar
• Zeng G, Wu Q, Pan H, et al. Immunogenicity and safety of a third dose of CoronaVac, and immune persistence of a two-dose schedule, in healthy adults: interim results from two single-centre, double-blind, randomised, placebo-controlled phase 2 clinical trials. Lancet Infect Dis. 2022 Apr;22(4):483–495.
   PubMed Web of Science ®Google Scholar
• Souza WM, Amorim MR, Sesti-Costa R, et al. Neutralisation of SARS-CoV-2 lineage P.1 by antibodies elicited through natural SARS-CoV-2 infection or vaccination with an inactivated SARS-CoV-2 vaccine: an immunological study. Lancet Microbe. 2021 Oct;2(10):e527–e535.
   PubMedGoogle Scholar
• Ranzani OT, Hitchings MDT, Dorion M, et al. Effectiveness of the CoronaVac vaccine in older adults during a gamma variant associated epidemic of covid-19 in Brazil: test negative case-control study. Br Med J. 2021 Aug 20;374:n2015.
   PubMed Web of Science ®Google Scholar
• Bar-On YM, Goldberg Y, Mandel M, et al. Protection against Covid-19 by BNT162b2 booster across age groups. N Engl J Med. 2021 Dec 23;385(26):2421–2430.
   PubMed Web of Science ®Google Scholar
• Bar-On YM, Goldberg Y, Mandel M, et al. Protection of BNT162b2 vaccine booster against COVID-19 in Israel. N Engl J Med. 2021 Oct 7;385(15):1393–1400.
   PubMed Web of Science ®Google Scholar
• Ramasamy MN, Minassian AM, Ewer KJ, et al. Safety and immunogenicity of ChAdOx1 nCoV-19 vaccine administered in a prime-boost regimen in young and old adults (COV002): a single-blind, randomised, controlled, phase 2/3 trial. Lancet. 2021 Dec 19;396(10267):1979–1993.
   PubMed Web of Science ®Google Scholar
• Hotez PJ, Bottazzi ME. Whole inactivated virus and protein-based COVID-19 vaccines. Annu Rev Med. 2022 Jan 27;73:55–64.
   PubMed Web of Science ®Google Scholar
• Stamatatos L, Czartoski J, Wan YH, et al. mRNA vaccination boosts cross-variant neutralizing antibodies elicited by SARS-CoV-2 infection. Science. 2021 Mar 25;372(6549):1413–1418.
   PubMed Web of Science ®Google Scholar
• Garcia-Beltran WF, St Denis KJ, Hoelzemer A, et al. mRNA-based COVID-19 vaccine boosters induce neutralizing immunity against SARS-CoV-2 Omicron variant. Cell. 2022 Feb 3;185(3):457–466 e4.
   PubMed Web of Science ®Google Scholar
• Pajon R, Doria-Rose NA, Shen X, et al. SARS-CoV-2 Omicron variant neutralization after mRNA-1273 booster vaccination. N Engl J Med. 2022 Mar 17;386(11):1088–1091.
   PubMed Web of Science ®Google Scholar
• Chen Y, Shen H, Huang R, et al. Serum neutralising activity against SARS-CoV-2 variants elicited by CoronaVac. Lancet Infect Dis. 2021 Aug;21(8):1071–1072.
   PubMed Web of Science ®Google Scholar
• Chen Y, Yin S, Tong X, et al. Dynamic SARS-CoV-2-specific B-cell and T-cell responses following immunization with an inactivated COVID-19 vaccine. Clin Microbiol Infect. 2022 Mar;28(3):410–418.
   PubMed Web of Science ®Google Scholar
• Li T, Han X, Gu C, et al. Potent SARS-CoV-2 neutralizing antibodies with protective efficacy against newly emerged mutational variants. Nat Commun. 2021 Nov 2;12(1):6304.
   PubMed Web of Science ®Google Scholar
• Wrapp D, Wang N, Corbett KS, et al. Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Science. 2020 Mar 13;367(6483):1260–1263.
   PubMed Web of Science ®Google Scholar
• Tan CW, Chia WN, Qin X, et al. A SARS-CoV-2 surrogate virus neutralization test based on antibody-mediated blockage of ACE2-spike protein-protein interaction. Nat Biotechnol. 2020 Sep;38(9):1073–1078.
   PubMed Web of Science ®Google Scholar
• Dan JM, Lindestam Arlehamn CS, et al. A cytokine-independent approach To identify antigen-specific human germinal center T follicular helper cells and rare antigen-specific CD4+ T cells in blood. J Immunol. 2016 Aug 1;197:983–993.
   PubMed Web of Science ®Google Scholar
• Dan JM, Mateus J, Kato Y, et al. Immunological memory to SARS-CoV-2 assessed for up to 8 months after infection. Science. 2021 Jan 6;371(6529):eabf4063.
   PubMed Web of Science ®Google Scholar
• Painter MM, Mathew D, Goel RR, et al. Rapid induction of antigen-specific CD4(+) T cells is associated with coordinated humoral and cellular immunity to SARS-CoV-2 mRNA vaccination. Immunity. 2021 Sep14;54:2133–2142 e3.
   PubMed Web of Science ®Google Scholar
• Bates TA, Leier HC, Lyski ZL, et al. Age-Dependent neutralization of SARS-CoV-2 and P.1 variant by vaccine immune serum samples. JAMA. 2021 Jul 21;326(9):868–869. doi: 10.1001/jama.2021.11656.
   PubMed Web of Science ®Google Scholar
• Qi H. T follicular helper cells in space-time. Nat Rev Immunol. 2016 Oct;16(10):612–625.
   PubMed Web of Science ®Google Scholar
• Crotty S. Follicular helper CD4 T cells (TFH). Annu Rev Immunol. 2011;29:621–663.
   PubMed Web of Science ®Google Scholar
• Morita R, Schmitt N, Bentebibel SE, et al. Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity. 2011 Jan 28;34(1):108–121.
   PubMed Web of Science ®Google Scholar
• Schmitt N, Bentebibel SE, Ueno H. Phenotype and functions of memory Tfh cells in human blood. Trends Immunol. 2014 Sep;35(9):436–442.
   PubMed Web of Science ®Google Scholar
• Tarke A, Sidney J, Methot N, et al. Impact of SARS-CoV-2 variants on the total CD4(+) and CD8(+) T cell reactivity in infected or vaccinated individuals. Cell Rep Med. 2021 Jul 20;2(7):100355.
   PubMedGoogle Scholar
• Geers D, Shamier MC, Bogers S, et al. SARS-CoV-2 variants of concern partially escape humoral but not T-cell responses in COVID-19 convalescent donors and vaccinees. Sci Immunol. 2021 May 25;6(59):eabj1750, doi: 10.1126/sciimmunol.abj1750.
   PubMed Web of Science ®Google Scholar
• Liu L, Iketani S, Guo Y, et al. Striking antibody evasion manifested by the Omicron variant of SARS-CoV-2. Nature. 2022 Feb;602(7898):676–681.
   PubMed Web of Science ®Google Scholar
• Sterlin D, Mathian A, Miyara M, et al. IgA dominates the early neutralizing antibody response to SARS-CoV-2. Sci Transl Med. 2021 Jan 20;13(577):eabd2223.
   PubMed Web of Science ®Google Scholar
• Bates TA, McBride SK, Winders B, et al. Antibody response and variant cross-neutralization after SARS-CoV-2 breakthrough infection. JAMA. 2022 Jan 11;327(2):179–181.
   PubMed Web of Science ®Google Scholar
• Goel RR, Painter MM, Apostolidis SA, et al. mRNA vaccines induce durable immune memory to SARS-CoV-2 and variants of concern. Science. 2021 Dec 3;374(6572):abm0829.
   PubMed Web of Science ®Google Scholar
• Brenna E, Davydov AN, Ladell K, et al. CD4(+) t follicular helper cells in human tonsils and blood Are clonally convergent but divergent from non-Tfh CD4(+) cells. Cell Rep. 2020 Jan 7;30(1):137–152. e5.
   PubMed Web of Science ®Google Scholar
• Juno JA, Tan HX, Lee WS, et al. Humoral and circulating follicular helper T cell responses in recovered patients with COVID-19. Nat Med. 2020 Sep;26(9):1428–1434.
   PubMed Web of Science ®Google Scholar
• Mudd PA, Minervina AA, Pogorelyy MV, et al. SARS-CoV-2 mRNA vaccination elicits a robust and persistent T follicular helper cell response in humans. Cell. 2022 Feb 17;185(4):603–613 e15.
   PubMed Web of Science ®Google Scholar
• Farooq F, Beck K, Paolino KM, et al. Circulating follicular T helper cells and cytokine profile in humans following vaccination with the rVSV-ZEBOV ebola vaccine. Sci Rep. 2016 Jun 21;6:27944.
   PubMed Web of Science ®Google Scholar
• Tarke A, Sidney J, Methot N, et al. Impact of SARS-CoV-2 variants on the total CD4(+) and CD8(+) T cell reactivity in infected or vaccinated individuals. Cell Rep Med. 2021 Jul 20;2(7):100355.
   PubMedGoogle Scholar
• Liu J, Chandrashekar A, Sellers D, et al. Vaccines elicit highly conserved cellular immunity to SARS-CoV-2 omicron. Nature. 2022 Mar;603(7901):493–496.
   PubMed Web of Science ®Google Scholar
• Keeton R, Tincho MB, Ngomti A, et al. T cell responses to SARS-CoV-2 spike cross-recognize omicron. Nature. 2022 Mar;603(7901):488–492.
   PubMed Web of Science ®Google Scholar
• Tarke A, Coelho CH, Zhang Z, et al. SARS-CoV-2 vaccination induces immunological T cell memory able to cross-recognize variants from Alpha to omicron. Cell. 2022 Mar 3;185(5):847–859 e11.
   PubMed Web of Science ®Google Scholar
• Wolter N, Jassat W, Walaza S, et al. Early assessment of the clinical severity of the SARS-CoV-2 omicron variant in South Africa: a data linkage study. Lancet. 2022 Jan 29;399(10323):437–446.
   PubMed Web of Science ®Google Scholar