IMMUNE NETWORK

The Korean Association of Immunobiologists (대한면역학회)
권호 표지
DOI QR코드

DOI QR Code

Pre-existing Immunity to Endemic Human Coronaviruses Does Not Affect the Immune Response to SARS-CoV-2 Spike in a Murine Vaccination Model

  • Ahn Young Jeong (Infectious Disease Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Pureum Lee (Infectious Disease Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Moo-Seung Lee (Department of Bioscience, University of Science and Technology (UST)) ;
  • Doo-Jin Kim (Infectious Disease Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB))
  • Received : 2022.09.30
  • Accepted : 2023.03.07
  • Published : 2023.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

Endemic human coronaviruses (HCoVs) have been evidenced to be cross-reactive to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Although a correlation exists between the immunological memory to HCoVs and coronavirus disease 2019 (COVID-19) severity, there is little experimental evidence for the effects of HCoV memory on the efficacy of COVID-19 vaccines. Here, we investigated the Ag-specific immune response to COVID-19 vaccines in the presence or absence of immunological memory against HCoV spike Ags in a mouse model. Pre-existing immunity against HCoV did not affect the COVID-19 vaccine-mediated humoral response with regard to Ag-specific total IgG and neutralizing Ab levels. The specific T cell response to the COVID-19 vaccine Ag was also unaltered, regardless of pre-exposure to HCoV spike Ags. Taken together, our data suggest that COVID-19 vaccines elicit comparable immunity regardless of immunological memory to spike of endemic HCoVs in a mouse model.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grants funded by the Government of Korea (MSIT: 2018M3A9H4077992) and the Korea Research Institute of Bioscience and Biotechnology (KRIBB) Research Initiative Programs (KGM9942213 and KGM1062211).

References

  1. Centers for Disease Control and Prevention. Long COVID or post-COVID conditions [Internet]. Available at https://www.cdc.gov/coronavirus/2019-ncov/long-term-effects/index.html [accessed on 3 September 2022].
  2. Anderson EM, Goodwin EC, Verma A, Arevalo CP, Bolton MJ, Weirick ME, Gouma S, McAllister CM, Christensen SR, Weaver J, et al. Seasonal human coronavirus antibodies are boosted upon SARS-CoV-2 infection but not associated with protection. Cell 2021;184:1858-1864.e10. https://doi.org/10.1016/j.cell.2021.02.010
  3. Manning J, Zaidi I, Lon C, Rosas LA, Park JK, Ponce A, Bohl J, Chea S, Karkanitsa M, Sreng S, et al. SARS-CoV-2 cross-reactivity in prepandemic serum from rural malaria-infected persons, Cambodia. Emerg Infect Dis 2022;28:440-444. https://doi.org/10.3201/eid2802.211725
  4. Sim KY, Ko GH, Bae SE, Choi KY, Lee JS, Kim BC, Lee KH, Song MR, Park SG. Two opposing roles of SARS-CoV-2 RBD-reactive antibodies in pre-pandemic plasma samples from elderly people in ACE2-mediated pseudovirus infection. Front Immunol 2022;12:813240. https://doi.org/10.3389/fimmu.2021.813240
  5. Guo L, Wang Y, Kang L, Hu Y, Wang L, Zhong J, Chen H, Ren L, Gu X, Wang G, et al. Cross-reactive antibody against human coronavirus OC43 spike protein correlates with disease severity in COVID-19 patients: a retrospective study. Emerg Microbes Infect 2021;10:664-676. https://doi.org/10.1080/22221751.2021.1905488
  6. Lapp SA, Edara VV, Lu A, Lai L, Hussaini L, Chahroudi A, Anderson LJ, Suthar MS, Anderson EJ, Rostad CA. Original antigenic sin responses to betacoronavirus spike proteins are observed in a mouse model, but are not apparent in children following SARS-CoV-2 infection. PLoS One 2021;16:e0256482.
  7. Lin CY, Wolf J, Brice DC, Sun Y, Locke M, Cherry S, Castellaw AH, Wehenkel M, Crawford JC, Zarnitsyna VI, et al. Pre-existing humoral immunity to human common cold coronaviruses negatively impacts the protective SARS-CoV-2 antibody response. Cell Host Microbe 2022;30:83-96.e4. https://doi.org/10.1016/j.chom.2021.12.005
  8. Yamaguchi T, Shinagawa T, Kobata H, Nakagawa H. Immunity against seasonal human coronavirus OC43 mitigates fatal deterioration of COVID-19. Int J Infect Dis 2021;109:261-268. https://doi.org/10.1016/j.ijid.2021.07.015
  9. Loyal L, Braun J, Henze L, Kruse B, Dingeldey M, Reimer U, Kern F, Schwarz T, Mangold M, Unger C, et al. Cross-reactive CD4+ T cells enhance SARS-CoV-2 immune responses upon infection and vaccination. Science 2021;374:eabh1823.
  10. Kundu R, Narean JS, Wang L, Fenn J, Pillay T, Fernandez ND, Conibear E, Koycheva A, Davies M, Tolosa-Wright M, et al. Cross-reactive memory T cells associate with protection against SARS-CoV-2 infection in COVID-19 contacts. Nat Commun 2022;13:80.
  11. Abreu RB, Kirchenbaum GA, Clutter EF, Sautto GA, Ross TM. Preexisting subtype immunodominance shapes memory B cell recall response to influenza vaccination. JCI Insight 2022;5:e132155.
  12. Elias G, Meysman P, Bartholomeus E, De Neuter N, Keersmaekers N, Suls A, Jansens H, Souquette A, De Reu H, Emonds MP, et al. Preexisting memory CD4 T cells in naive individuals confer robust immunity upon hepatitis B vaccination. Elife 2022;11:e68388.
  13. Mongkolsapaya J, Dejnirattisai W, Xu XN, Vasanawathana S, Tangthawornchaikul N, Chairunsri A, Sawasdivorn S, Duangchinda T, Dong T, Rowland-Jones S, et al. Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med 2003;9:921-927. https://doi.org/10.1038/nm887
  14. Olson MR, Chua BY, Good-Jacobson KL, Doherty PC, Jackson DC, Turner SJ. Competition within the virus-specific CD4 T-cell pool limits the T follicular helper response after influenza infection. Immunol Cell Biol 2016;94:729-740. https://doi.org/10.1038/icb.2016.42
  15. Johnson LR, Weizman OE, Rapp M, Way SS, Sun JC. Epitope-specific vaccination limits clonal expansion of heterologous naive T cells during viral challenge. Cell Reports 2016;17:636-644. https://doi.org/10.1016/j.celrep.2016.09.019
  16. Lee TY, Kim CU, Lee P, Seo SH, Bae EH, Kim YS, Kim SH, Kim DJ. Outer membrane vesicle increases the efficacy of an influenza vaccine in a diet-induced obese mouse model. Immunol Lett 2020;219:27-33. https://doi.org/10.1016/j.imlet.2019.12.009
  17. de Vries RD. SARS-CoV-2-specific T-cells in unexposed humans: presence of cross-reactive memory cells does not equal protective immunity. Signal Transduct Target Ther 2020;5:224.
  18. Jacomy H, Talbot PJ. Vacuolating encephalitis in mice infected by human coronavirus OC43. Virology 2003;315:20-33. https://doi.org/10.1016/S0042-6822(03)00323-4
  19. Liu DX, Liang JQ, Fung TS. Human coronavirus-229E, -OC43, -NL63, and -HKU1 (coronaviridae). In: Encyclopedia of Virology. 4th ed. Bamford DH, Zuckerman M, eds. San Diego, CA: Academic Press; 2021. p.428-440.
  20. Khoury DS, Cromer D, Reynaldi A, Schlub TE, Wheatley AK, Juno JA, Subbarao K, Kent SJ, Triccas JA, Davenport MP. Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection. Nat Med 2021;27:1205-1211. https://doi.org/10.1038/s41591-021-01377-8
  21. Steiner S, Sotzny F, Bauer S, Na IK, Schmueck-Henneresse M, Corman VM, Schwarz T, Drosten C, Wendering DJ, Behrends U, et al. HCoV- and SARS-CoV-2 cross-reactive T cells in CVID patients. Front Immunol 2020;11:607918.
  22. Johansson AM, Malhotra U, Kim YG, Gomez R, Krist MP, Wald A, Koelle DM, Kwok WW. Cross-reactive and mono-reactive SARS-CoV-2 CD4+ T cells in prepandemic and COVID-19 convalescent individuals. PLoS Pathog 2021;17:e1010203.
  23. Kutzler MA, Weiner DB. DNA vaccines: ready for prime time? Nat Rev Genet 2008;9:776-788. https://doi.org/10.1038/nrg2432
  24. Wheatley AK, Fox A, Tan HX, Juno JA, Davenport MP, Subbarao K, Kent SJ. Immune imprinting and SARS-CoV-2 vaccine design. Trends Immunol 2021;42:956-959. https://doi.org/10.1016/j.it.2021.09.001
  25. Focosi D, Genoni A, Lucenteforte E, Tillati S, Tamborini A, Spezia PG, Azzi L, Baj A, Maggi F. Previous humoral immunity to the endemic seasonal alphacoronaviruses NL63 and 229E is associated with worse clinical outcome in COVID-19 and suggests original antigenic sin. Life (Basel) 2021;11:298.
  26. Aydillo T, Rombauts A, Stadlbauer D, Aslam S, Abelenda-Alonso G, Escalera A, Amanat F, Jiang K, Krammer F, Carratala J, et al. Immunological imprinting of the antibody response in COVID-19 patients. Nat Commun 2021;12:3781.
  27. Aguilar-Bretones M, Westerhuis BM, Raadsen MP, de Bruin E, Chandler FD, Okba NM, Haagmans BL, Langerak T, Endeman H, van den Akker JP, et al. Seasonal coronavirus-specific B cells with limited SARS-CoV-2 cross-reactivity dominate the IgG response in severe COVID-19. J Clin Invest 2021;131:e150613.
  28. Yamashita T, Shimakami T, Nio K, Terashima T, Okajima M, Taniguchi T, Wada T, Honda M, Gabata T, Ota K, et al. Preexisting humoral immunity cross-reacting with SARS-CoV-2 might prevent death due to COVID-19 in critical patients. J Clin Med 2022;11:3870.
  29. Chalkias S, Harper C, Vrbicky K, Walsh SR, Essink B, Brosz A, McGhee N, Tomassini JE, Chen X, Chang Y, et al. A bivalent omicron-containing booster vaccine against COVID-19. N Engl J Med 2022;387:1279-1291. https://doi.org/10.1056/NEJMoa2208343
  30. Scheaffer SM, Lee D, Whitener B, Ying B, Wu K, Liang CY, Jani H, Martin P, Amato NJ, Avena LE, et al. Bivalent SARS-CoV-2 mRNA vaccines increase breadth of neutralization and protect against the ba.5 omicron variant in mice. Nat Med 2023;29:247-257. https://doi.org/10.1038/s41591-022-02092-8
  31. Rehman MF, Fariha C, Anwar A, Shahzad N, Ahmad M, Mukhtar S, Farhan Ul Haque M. Novel coronavirus disease (COVID-19) pandemic: a recent mini review. Comput Struct Biotechnol J 2021;19:612-623. https://doi.org/10.1016/j.csbj.2020.12.033
  32. Grifoni A, Weiskopf D, Ramirez SI, Mateus J, Dan JM, Moderbacher CR, Rawlings SA, Sutherland A, Premkumar L, Jadi RS, et al. Targets of T cell responses to SARS-CoV-2 coronavirus in humans with COVID-19 disease and unexposed individuals. Cell 2020;181:1489-1501.e15. https://doi.org/10.1016/j.cell.2020.05.015
  33. Howard FH, Kwan A, Winder N, Mughal A, Collado-Rojas C, Muthana M. Understanding immune responses to viruses-do underlying Th1/Th2 cell biases predict outcome? Viruses 2022;14:1493.
  34. Jin H, Xiao C, Chen Z, Kang Y, Ma Y, Zhu K, Xie Q, Tu Y, Yu Y, Wang B. Induction of Th1 type response by DNA vaccinations with N, M, and E genes against SARS-CoV in mice. Biochem Biophys Res Commun 2005;328:979-986. https://doi.org/10.1016/j.bbrc.2005.01.048
  35. Fonseca DM, Bonato VL, Silva CL, Sartori A. Th1 polarized response induced by intramuscular DNA-HSP65 immunization is preserved in experimental atherosclerosis. Braz J Med Biol Res 2007;40:1495-1504. https://doi.org/10.1590/S0100-879X2007001100010
  36. Alamri SS, Alluhaybi KA, Alhabbab RY, Basabrain M, Algaissi A, Almahboub S, Alfaleh MA, Abujamel TS, Abdulaal WH, ElAssouli MZ, et al. Synthetic SARS-CoV-2 spike-based DNA vaccine elicits robust and long-lasting th1 humoral and cellular immunity in mice. Front Microbiol 2021;12:727455.
  37. Xie P, Fang Y, Baloch Z, Yu H, Zhao Z, Li R, Zhang T, Li R, Zhao J, Yang Z, et al. A mouse-adapted model of HCoV-OC43 and its usage to the evaluation of antiviral drugs. Front Microbiol 2022;13:845269.