IMMUNE NETWORK

  • 제21권1호
  • /
  • Pages.2.1-2.11
  • /
  • 2021
  • /
  • 1598-2629(pISSN)
  • /
  • 2092-6685(eISSN)
대한면역학회 (The Korean Association of Immunobiologists)
권호 표지
DOI QR코드

DOI QR Code

SARS-CoV-2-Specific T Cell Responses in Patients with COVID-19 and Unexposed Individuals

  • Min-Seok Rha (Laboratory of Immunology and Infectious Diseases, Graduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST)) ;
  • A Reum Kim (Laboratory of Immunology and Infectious Diseases, Graduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST)) ;
  • Eui-Cheol Shin (Laboratory of Immunology and Infectious Diseases, Graduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST))
  • 투고 : 2021.01.16
  • 심사 : 2021.02.07
  • 발행 : 2021.02.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection causes coronavirus disease 2019 (COVID-19), an ongoing pandemic disease. In the current review, we describe SARS-CoV-2-specific CD4+ and CD8+ T-cell responses in acute and convalescent COVID-19 patients. We also discuss the relationships between COVID-19 severity and SARS-CoV-2-specific T-cell responses and summarize recent reports regarding SARS-CoV-2-reactive T cells in SARS-CoV-2-unexposed individuals. These T cells may be cross-reactive cells primed by previous infection with human common-cold coronaviruses. Finally, we outline SARS-CoV-2-specific T-cell responses in the context of vaccination. A better understanding of SARS-CoV-2-specific T-cell responses is needed to develop effective vaccines and therapeutics.

키워드

과제정보

This research was supported by the 2020 Joint Research Project of Institutes of Science and Technology.

참고문헌

  1. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, Zhang L, Fan G, Xu J, Gu X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020;395:497-506. https://doi.org/10.1016/S0140-6736(20)30183-5
  2. Lee JS, Park S, Jeong HW, Ahn JY, Choi SJ, Lee H, Choi B, Nam SK, Sa M, Kwon JS, et al. Immunophenotyping of COVID-19 and influenza highlights the role of type I interferons in development of severe COVID-19. Sci Immunol 2020;5:eabd1554.
  3. Merad M, Martin JC. Pathological inflammation in patients with COVID-19: a key role for monocytes and macrophages. Nat Rev Immunol 2020;20:355-362. https://doi.org/10.1038/s41577-020-0331-4
  4. Petersen E, Koopmans M, Go U, Hamer DH, Petrosillo N, Castelli F, Storgaard M, Al Khalili S, Simonsen L. Comparing SARS-CoV-2 with SARS-CoV and influenza pandemics. Lancet Infect Dis 2020;20:e238-e244. https://doi.org/10.1016/S1473-3099(20)30484-9
  5. Piroth L, Cottenet J, Mariet AS, Bonniaud P, Blot M, Tubert-Bitter P, Quantin C. Comparison of the characteristics, morbidity, and mortality of COVID-19 and seasonal influenza: a nationwide, population-based retrospective cohort study. Lancet Respir Med 2020. doi: 10.1016/S2213-2600(20)30527-0.
  6. Mathew D, Giles JR, Baxter AE, Oldridge DA, Greenplate AR, Wu JE, Alanio C, Kuri-Cervantes L, Pampena MB, D'Andrea K, et al. Deep immune profiling of COVID-19 patients reveals distinct immunotypes with therapeutic implications. Science 2020;369:eabc8511.
  7. Mazzoni A, Salvati L, Maggi L, Capone M, Vanni A, Spinicci M, Mencarini J, Caporale R, Peruzzi B, Antonelli A, et al. Impaired immune cell cytotoxicity in severe COVID-19 is IL-6 dependent. J Clin Invest 2020;130:4694-4703. https://doi.org/10.1172/JCI138554
  8. Chen G, Wu D, Guo W, Cao Y, Huang D, Wang H, Wang T, Zhang X, Chen H, Yu H, et al. Clinical and immunological features of severe and moderate coronavirus disease 2019. J Clin Invest 2020;130:2620-2629. https://doi.org/10.1172/JCI137244
  9. Kuri-Cervantes L, Pampena MB, Meng W, Rosenfeld AM, Ittner CAG, Weisman AR, Agyekum RS, Mathew D, Baxter AE, Vella LA, et al. Comprehensive mapping of immune perturbations associated with severe COVID-19. Sci Immunol 2020;5:eabd7114.
  10. Zheng HY, Zhang M, Yang CX, Zhang N, Wang XC, Yang XP, Dong XQ, Zheng YT. Elevated exhaustion levels and reduced functional diversity of T cells in peripheral blood may predict severe progression in COVID-19 patients. Cell Mol Immunol 2020;17:541-543. https://doi.org/10.1038/s41423-020-0401-3
  11. De Biasi S, Meschiari M, Gibellini L, Bellinazzi C, Borella R, Fidanza L, Gozzi L, Iannone A, Lo Tartaro D, Mattioli M, et al. Marked T cell activation, senescence, exhaustion and skewing towards TH17 in patients with COVID-19 pneumonia. Nat Commun 2020;11:3434.
  12. Diao B, Wang C, Tan Y, Chen X, Liu Y, Ning L, Chen L, Li M, Liu Y, Wang G, et al. Reduction and functional exhaustion of T cells in patients with coronavirus disease 2019 (COVID-19). Front Immunol 2020;11:827.
  13. Song JW, Zhang C, Fan X, Meng FP, Xu Z, Xia P, Cao WJ, Yang T, Dai XP, Wang SY, et al. Immunological and inflammatory profiles in mild and severe cases of COVID-19. Nat Commun 2020;11:3410.
  14. Zheng M, Gao Y, Wang G, Song G, Liu S, Sun D, Xu Y, Tian Z. Functional exhaustion of antiviral lymphocytes in COVID-19 patients. Cell Mol Immunol 2020;17:533-535. https://doi.org/10.1038/s41423-020-0402-2
  15. Peng Y, Mentzer AJ, Liu G, Yao X, Yin Z, Dong D, Dejnirattisai W, Rostron T, Supasa P, Liu C, et al. Broad and strong memory CD4+ and CD8+ T cells induced by SARS-CoV-2 in UK convalescent individuals following COVID-19. Nat Immunol 2020;21:1336-1345. https://doi.org/10.1038/s41590-020-0782-6
  16. Sekine T, Perez-Potti A, Rivera-Ballesteros O, Stralin K, Gorin JB, Olsson A, Llewellyn-Lacey S, Kamal H, Bogdanovic G, Muschiol S, et al. Robust T Cell Immunity in Convalescent Individuals with Asymptomatic or Mild COVID-19. Cell 2020;183:158-168.e14. https://doi.org/10.1016/j.cell.2020.08.017
  17. Schulien I, Kemming J, Oberhardt V, Wild K, Seidel LM, Killmer S, Sagar , Daul F, Salvat Lago M, Decker A, et al. Characterization of pre-existing and induced SARS-CoV-2-specific CD8+ T cells. Nat Med 2021;27:78-85. https://doi.org/10.1038/s41591-020-01143-2
  18. Habel JR, Nguyen TH, van de Sandt CE, Juno JA, Chaurasia P, Wragg K, Koutsakos M, Hensen L, Jia X, Chua B, et al. Suboptimal SARS-CoV-2-specific CD8+ T cell response associated with the prominent HLA-A*02:01HLA-A*02:01 phenotype. Proc Natl Acad Sci U S A 2020;117:24384-24391. https://doi.org/10.1073/pnas.2015486117
  19. Rha MS, Jeong HW, Ko JH, Choi SJ, Seo IH, Lee JS, Sa M, Kim AR, Joo EJ, Ahn JY, et al. PD-1-expressing SARS-CoV-2-specific CD8+ T cells are not exhausted, but functional in patients with COVID-19. Immunity 2021;54:44-52.e3. https://doi.org/10.1016/j.immuni.2020.12.002
  20. Shomuradova AS, Vagida MS, Sheetikov SA, Zornikova KV, Kiryukhin D, Titov A, Peshkova IO, Khmelevskaya A, Dianov DV, Malasheva M, et al. SARS-CoV-2 epitopes are recognized by a public and diverse repertoire of human T cell receptors. Immunity 2020;53:1245-1257.e5. https://doi.org/10.1016/j.immuni.2020.11.004
  21. Ferretti AP, Kula T, Wang Y, Nguyen DM, Weinheimer A, Dunlap GS, Xu Q, Nabilsi N, Perullo CR, Cristofaro AW, et al. Unbiased screens show CD8+ T cells of COVID-19 patients recognize shared epitopes in SARS-CoV-2 that largely reside outside the spike protein. Immunity 2020;53:1095-1107.e3. https://doi.org/10.1016/j.immuni.2020.10.006
  22. Meckiff BJ, Ramirez-Suastegui C, Fajardo V, Chee SJ, Kusnadi A, Simon H, Eschweiler S, Grifoni A, Pelosi E, Weiskopf D, et al. Imbalance of regulatory and cytotoxic SARS-CoV-2-reactive CD4+ T cells in COVID-19. Cell 2020;183:1340-1353.e16. https://doi.org/10.1016/j.cell.2020.10.001
  23. Ni L, Ye F, Cheng ML, Feng Y, Deng YQ, Zhao H, Wei P, Ge J, Gou M, Li X, et al. Detection of SARS-CoV-2-specific humoral and cellular immunity in COVID-19 convalescent individuals. Immunity 2020;52:971-977.e3. https://doi.org/10.1016/j.immuni.2020.04.023
  24. Le Bert N, Tan AT, Kunasegaran K, Tham CY, Hafezi M, Chia A, Chng MH, Lin M, Tan N, Linster M, et al. SARS-CoV-2-specific T cell immunity in cases of COVID-19 and SARS, and uninfected controls. Nature 2020;584:457-462. https://doi.org/10.1038/s41586-020-2550-z
  25. 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
  26. Zhou R, To KK, Wong YC, Liu L, Zhou B, Li X, Huang H, Mo Y, Luk TY, Lau TT, et al. Acute SARS-CoV-2 infection impairs dendritic cell and T cell responses. Immunity 2020;53:864-877.e5. https://doi.org/10.1016/j.immuni.2020.07.026
  27. Rydyznski Moderbacher C, Ramirez SI, Dan JM, Grifoni A, Hastie KM, Weiskopf D, Belanger S, Abbott RK, Kim C, Choi J, et al. Antigen-specific adaptive immunity to SARS-CoV-2 in acute COVID-19 and associations with age and disease severity. Cell 2020;183:996-1012.e19. https://doi.org/10.1016/j.cell.2020.09.038
  28. Kim J, Chang DY, Lee HW, Lee H, Kim JH, Sung PS, Kim KH, Hong SH, Kang W, Lee J, et al. Innate-like cytotoxic function of bystander-activated CD8+ T cells is associated with liver injury in acute hepatitis A. Immunity 2018;48:161-173.e5. https://doi.org/10.1016/j.immuni.2017.11.025
  29. Kim TS, Shin EC. The activation of bystander CD8+ T cells and their roles in viral infection. Exp Mol Med 2019;51:1-9. https://doi.org/10.1038/s12276-019-0316-1
  30. Xu Z, Shi L, Wang Y, Zhang J, Huang L, Zhang C, Liu S, Zhao P, Liu H, Zhu L, et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med 2020;8:420-422. https://doi.org/10.1016/S2213-2600(20)30076-X
  31. Kang CK, Han GC, Kim M, Kim G, Shin HM, Song KH, Choe PG, Park WB, Kim ES, Kim HB, et al. Aberrant hyperactivation of cytotoxic T-cell as a potential determinant of COVID-19 severity. Int J Infect Dis 2020;97:313-321. https://doi.org/10.1016/j.ijid.2020.05.106
  32. Chang JT, Wherry EJ, Goldrath AW. Molecular regulation of effector and memory T cell differentiation. Nat Immunol 2014;15:1104-1115. https://doi.org/10.1038/ni.3031
  33. Kaech SM, Wherry EJ. Heterogeneity and cell-fate decisions in effector and memory CD8+ T cell differentiation during viral infection. Immunity 2007;27:393-405. https://doi.org/10.1016/j.immuni.2007.08.007
  34. Sette A, Crotty S. Pre-existing immunity to SARS-CoV-2: the knowns and unknowns. Nat Rev Immunol 2020;20:457-458. https://doi.org/10.1038/s41577-020-0389-z
  35. Braun J, Loyal L, Frentsch M, Wendisch D, Georg P, Kurth F, Hippenstiel S, Dingeldey M, Kruse B, Fauchere F, et al. SARS-CoV-2-reactive T cells in healthy donors and patients with COVID-19. Nature 2020;587:270-274. https://doi.org/10.1038/s41586-020-2598-9
  36. Mateus J, Grifoni A, Tarke A, Sidney J, Ramirez SI, Dan JM, Burger ZC, Rawlings SA, Smith DM, Phillips E, et al. Selective and cross-reactive SARS-CoV-2 T cell epitopes in unexposed humans. Science 2020;370:89-94. https://doi.org/10.1126/science.abd3871
  37. Nelde A, Bilich T, Heitmann JS, Maringer Y, Salih HR, Roerden M, Lubke M, Bauer J, Rieth J, Wacker M, et al. SARS-CoV-2-derived peptides define heterologous and COVID-19-induced T cell recognition. Nat Immunol 2021;22:74-85. https://doi.org/10.1038/s41590-020-00808-x
  38. Klenerman P, Zinkernagel RM. Original antigenic sin impairs cytotoxic T lymphocyte responses to viruses bearing variant epitopes. Nature 1998;394:482-485. https://doi.org/10.1038/28860
  39. Sagar M, Reifler K, Rossi M, Miller NS, Sinha P, White LF, Mizgerd JP. Recent endemic coronavirus infection is associated with less-severe COVID-19. J Clin Invest 2021;131:e143380.
  40. Anderson EJ, Rouphael NG, Widge AT, Jackson LA, Roberts PC, Makhene M, Chappell JD, Denison MR, Stevens LJ, Pruijssers AJ, et al. Safety and immunogenicity of SARS-CoV-2 mRNA-1273 vaccine in older adults. N Engl J Med 2020;383:2427-2438. https://doi.org/10.1056/NEJMoa2028436
  41. Sahin U, Muik A, Derhovanessian E, Vogler I, Kranz LM, Vormehr M, Baum A, Pascal K, Quandt J, Maurus D, et al. COVID-19 vaccine BNT162b1 elicits human antibody and TH1 T cell responses. Nature 2020;586:594-599. https://doi.org/10.1038/s41586-020-2814-7
  42. Ewer KJ, Barrett JR, Belij-Rammerstorfer S, Sharpe H, Makinson R, Morter R, Flaxman A, Wright D, Bellamy D, Bittaye M, et al. T cell and antibody responses induced by a single dose of ChAdOx1 nCoV-19 (AZD1222) vaccine in a phase 1/2 clinical trial. Nat Med 2020. doi: 10.1038/s41591-020-01194-5.
  43. Keech C, Albert G, Cho I, Robertson A, Reed P, Neal S, Plested JS, Zhu M, Cloney-Clark S, Zhou H, et al. Phase 1-2 trial of a SARS-CoV-2 recombinant spike protein nanoparticle vaccine. N Engl J Med 2020;383:2320-2332. https://doi.org/10.1056/NEJMoa2026920
  44. McMahan K, Yu J, Mercado NB, Loos C, Tostanoski LH, Chandrashekar A, Liu J, Peter L, Atyeo C, Zhu A, et al. Correlates of protection against SARS-CoV-2 in rhesus macaques. Nature 2020. doi: 10.1038/s41586-020-03041-6.