Skip to main content
NCBI home page
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2020 Oct 5;14(6):746–751. doi: 10.1007/s11684-020-0822-5

Durability of neutralizing antibodies and T-cell response post SARS-CoV-2 infection

Yun Tan 1,#, Feng Liu 1,#, Xiaoguang Xu 1,#, Yun Ling 2,#, Weijin Huang 3,#, Zhaoqin Zhu 2,#, Mingquan Guo 2,#, Yixiao Lin 2,#, Ziyu Fu 1, Dongguo Liang 1, Tengfei Zhang 2, Jian Fan 2, Miao Xu 3, Hongzhou Lu 2,✉, Saijuan Chen 1,✉
PMCID: PMC7533664  PMID: 33017040

Abstract

The ongoing pandemic of Coronavirus disease 19 (COVID-19) is caused by a newly discovered β Coronavirus named severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). How long the adaptive immunity triggered by SARS-CoV-2 can last is of critical clinical relevance in assessing the probability of second infection and efficacy of vaccination. Here we examined, using ELISA, the IgG antibodies in serum specimens collected from 17 COVID-19 patients at 6–7 months after diagnosis and the results were compared to those from cases investigated 2 weeks to 2 months post-infection. All samples were positive for IgGs against the S- and N-proteins of SARS-CoV-2. Notably, 14 samples available at 6–7 months post-infection all showed significant neutralizing activities in a pseudovirus assay, with no difference in blocking the cell-entry of the 614D and 614G variants of SARS-CoV-2. Furthermore, in 10 blood samples from cases at 6–7 months post-infection used for memory T-cell tests, we found that interferon γ-producing CD4+ and CD8+ cells were increased upon SARS-CoV-2 antigen stimulation. Together, these results indicate that durable anti-SARS-CoV-2 immunity is common in convalescent population, and vaccines developed from 614D variant may offer protection from the currently predominant 614D variant of SARS-CoV-2.

Keywords: SARS-CoV-2, neutralizing antibodies, T-cell response

Acknowledgements

This work was supported by grant from Double First-Class Project (No. WF510162602) from the Ministry of Education, State Key Laboratory of Medical Genomics, Overseas Expertise Introduction Project for Discipline Innovation (111 Project, No. B17029) and National Key R&D Program of China (No. 2019YFA0905902), the Shanghai Guangci Translational Medical Research Development Foundation.

Compliance with ethics guidelines

Yun Tan, Feng Liu, Xiaoguang Xu, Yun Ling, Weijin Huang, Zhaoqin Zhu, Mingquan Guo, Yixiao Lin, Ziyu Fu, Dongguo Liang, Tengfei Zhang, Jian Fan, Miao Xu, Hongzhou Lu, and Saijuan Chen declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000 (5). Informed consent was obtained from all patients for being included in the study.

Footnotes

Yun Tan, Feng Liu, Xiaoguang Xu, Yun Ling, Weijin Huang, Zhaoqin Zhu, Mingquan Guo, and Yixiao Lin contributed equally to this study.

Contributor Information

Hongzhou Lu, Email: luhongzhou@shphc.org.cn.

Saijuan Chen, Email: sjchen@stn.sh.cn.

References

  • 1.Zhou G, Chen S, Chen Z. Back to the spring of 2020: facts and hope of COVID-19 outbreak. Front Med. 2020;14(2):113–116. doi: 10.1007/s11684-020-0758-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Zhou G, Chen S, Chen Z. Advances in COVID-19: the virus, the pathogenesis, and evidence-based control and therapeutic strategies. Front Med. 2020;14(2):117–125. doi: 10.1007/s11684-020-0773-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Zhou M, Zhang X, Qu J. Coronavirus disease 2019 (COVID-19): a clinical update. Front Med. 2020;14(2):126–135. doi: 10.1007/s11684-020-0767-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Le Bert N, Tan AT, Kunasegaran K, Tham CYL, Hafezi M, Chia A, Chng MHY, Lin M, Tan N, Linster M, Chia WN, Chen MI, Wang LF, Ooi EE, Kalimuddin S, Tambyah PA, Low JG, Tan YJ, Bertoletti A. SARS-CoV-2-specific T cell immunity in cases of COVID-19 and SARS, and uninfected controls. Nature. 2020;584(7821):457–462. doi: 10.1038/s41586-020-2550-z. [DOI] [PubMed] [Google Scholar]
  • 5.Grifoni A, Weiskopf D, Ramirez SI, Mateus J, Dan JM, Moderbacher CR, Rawlings SA, Sutherland A, Premkumar L, Jadi RS, Marrama D, de Silva AM, Frazier A, Carlin AF, Greenbaum JA, Peters B, Krammer F, Smith DM, Crotty S, Sette A. Targets of T cell responses to SARS-CoV-2 coronavirus in humans with COVID-19 disease and unexposed individuals. Cell. 2020;181(7):1489–1501.e15. doi: 10.1016/j.cell.2020.05.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.To KK, Tsang OT, Leung WS, Tam AR, Wu TC, Lung DC, Yip CC, Cai JP, Chan JM, Chik TS, Lau DP, Choi CY, Chen LL, Chan WM, Chan KH, Ip JD, Ng AC, Poon RW, Luo CT, Cheng VC, Chan JF, Hung IF, Chen Z, Chen H, Yuen KY. Temporal profiles of viral load in posterior oropharyngeal saliva samples and serum antibody responses during infection by SARS-CoV-2: an observational cohort study. Lancet Infect Dis. 2020;20(5):565–574. doi: 10.1016/S1473-3099(20)30196-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Robbiani DF, Gaebler C, Muecksch F, Lorenzi JCC, Wang Z, Cho A, Agudelo M, Barnes CO, Gazumyan A, Finkin S, Hägglöf T, Oliveira TY, Viant C, Hurley A, Hoffmann HH, Millard KG, Kost RG, Cipolla M, Gordon K, Bianchini F, Chen ST, Ramos V, Patel R, Dizon J, Shimeliovich I, Mendoza P, Hartweger H, Nogueira L, Pack M, Horowitz J, Schmidt F, Weisblum Y, Michailidis E, Ashbrook AW, Waltari E, Pak JE, Huey-Tubman KE, Koranda N, Hoffman PR, West AP, Jr., Rice CM, Hatziioannou T, Bjorkman PJ, Bieniasz PD, Caskey M, Nussenzweig MC. Convergent antibody responses to SARS-CoV-2 in convalescent individuals. Nature. 2020;584(7821):437–442. doi: 10.1038/s41586-020-2456-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Ibarrondo FJ, Fulcher JA, Goodman-Meza D, Elliott J, Hofmann C, Hausner MA, Ferbas KG, Tobin NH, Aldrovandi GM, Yang OO. Rapid decay of anti-SARS-CoV-2 antibodies in persons with mild Covid-19. N Engl J Med. 2020;383(11):1085–1087. doi: 10.1056/NEJMc2025179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Gudbjartsson DF, Norddahl GL, Melsted P, Gunnarsdottir K, Holm H, Eythorsson E, Arnthorsson AO, Helgason D, Bjarnadottir K, Ingvarsson RF, Thorsteinsdottir B, Kristjansdottir S, Birgisdottir K, Kristinsdottir AM, Sigurdsson MI, Arnadottir GA, Ivarsdottir EV, Andresdottir M, Jonsson F, Agustsdottir AB, Berglund J, Eiriks-dottir B, Fridriksdottir R, Gardarsdottir EE, Gottfredsson M, Gretarsdottir OS, Gudmundsdottir S, Gudmundsson KR, Gunnars-dottir TR, Gylfason A, Helgason A, Jensson BO, Jonasdottir A, Jonsson H, Kristjansson T, Kristinsson KG, Magnusdottir DN, Magnusson OT, Olafsdottir LB, Rognvaldsson S, le Roux L, Sigmundsdottir G, Sigurdsson A, Sveinbjornsson G, Sveinsdottir KE, Sveinsdottir M, Thorarensen EA, Thorbjornsson B, Thordar-dottir M, Saemundsdottir J, Kristjansson SH, Josefsdottir KS, Masson G, Georgsson G, Kristjansson M, Moller A, Palsson R, Gudnason T, Thorsteinsdottir U, Jonsdottir I, Sulem P, Stefansson K. Humoral immune response to SARS-CoV-2 in Iceland. N Engl J Med 2020; [Epub ahead of print] doi: 10.1056/NEJMoa2026116
  • 10.AlterG, SederR. The power ofantibody-based surveillance. N Engl J Med 2020; [Epub ahead of print] doi: 10.1056/NEJMe2028079
  • 11.Zhang NN, Li XF, Deng YQ, Zhao H, Huang YJ, Yang G, Huang WJ, Gao P, Zhou C, Zhang RR, Guo Y, Sun SH, Fan H, Zu SL, Chen Q, He Q, Cao TS, Huang XY, Qiu HY, Nie JH, Jiang Y, Yan HY, Ye Q, Zhong X, Xue XL, Zha ZY, Zhou D, Yang X, Wang YC, Ying B, Qin CF. A thermostable mRNA vaccine against COVID-19. Cell. 2020;182(5):1271–1283.e16. doi: 10.1016/j.cell.2020.07.024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Nie J, Li Q, Wu J, Zhao C, Hao H, Liu H, Zhang L, Nie L, Qin H, Wang M, Lu Q, Li X, Sun Q, Liu J, Fan C, Huang W, Xu M, Wang Y. Establishment and validation of a pseudovirus neutralization assay for SARS-CoV-2. Emerg Microbes Infect. 2020;9(1):680–686. doi: 10.1080/22221751.2020.1743767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Shi H, Ye J, Teng J, Yin Y, Hu Q, Wu X, Liu H, Cheng X, Su Y, Liu M, Gu J, Lu T, Chen H, Zheng H, Sun Y, Yang C. Elevated serum autoantibodies against co-inhibitory PD-1 facilitate T cell proliferation and correlate with disease activity in new-onset systemic lupus erythematosus patients. Arthritis Res Ther. 2017;19(1):52. doi: 10.1186/s13075-017-1258-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Goudot C, Coillard A, Villani AC, Gueguen P, Cros A, Sarkizova S, Tang-Huau TL, Bohec M, Baulande S, Hacohen N, Amigorena S, Segura E. Aryl hydrocarbon receptor controls monocyte differentiation into dendritic cells versus macrophages. Immunity. 2017;47(3):582–596.e6. doi: 10.1016/j.immuni.2017.08.016. [DOI] [PubMed] [Google Scholar]
  • 15.Korber B, Fischer WM, Gnanakaran S, Yoon H, Theiler J, Abfalterer W, Hengartner N, Giorgi EE, Bhattacharya T, Foley B, Hastie KM, Parker MD, Partridge DG, Evans CM, Freeman TM, de Silva TI, Sheffield C-G, McDanal C, Perez LG, Tang H, Moon-Walker A, Whelan SP, LaBranche CC, Saphire EO, Montefiori DC. Tracking changes in SARS-CoV-2 spike: evidence that D614G increases infectivity of the COVID-19 virus. Cell. 2020;182(4):812–827.e19. doi: 10.1016/j.cell.2020.06.043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Zhang X, Tan Y, Ling Y, Lu G, Liu F, Yi Z, Jia X, Wu M, Shi B, Xu S, Chen J, Wang W, Chen B, Jiang L, Yu S, Lu J, Wang J, Xu M, Yuan Z, Zhang Q, Zhang X, Zhao G, Wang S, Chen S, Lu H. Viral and host factors related to the clinical outcome of COVID-19. Nature. 2020;583(7816):437–440. doi: 10.1038/s41586-020-2355-0. [DOI] [PubMed] [Google Scholar]
  • 17.Rogers TF, Zhao F, Huang D, Beutler N, Burns A, He WT, Limbo O, Smith C, Song G, Woehl J, Yang L, Abbott RK, Callaghan S, Garcia E, Hurtado J, Parren M, Peng L, Ramirez S, Ricketts J, Ricciardi MJ, Rawlings SA, Wu NC, Yuan M, Smith DM, Nemazee D, Teijaro JR, Voss JE, Wilson IA, Andrabi R, Briney B, Landais E, Sok D, Jardine JG, Burton DR. Isolation of potent SARS-CoV-2 neutralizing antibodies and protection from disease in a small animal model. Science. 2020;369(6506):956–963. doi: 10.1126/science.abc7520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Peng H, Yang LT, Li J, Lu ZQ, Wang LY, Koup RA, Bailer RT, Wu CY. Human memory T cell responses to SARS-CoV E protein. Microbes Infect. 2006;8(9–10):2424–2431. doi: 10.1016/j.micinf.2006.05.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Peng H, Yang LT, Wang LY, Li J, Huang J, Lu ZQ, Koup RA, Bailer RT, Wu CY. Long-lived memory T lymphocyte responses against SARS coronavirus nucleocapsid protein in SARS-recovered patients. Virology. 2006;351(2):466–475. doi: 10.1016/j.virol.2006.03.036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Ng OW, Chia A, Tan AT, Jadi RS, Leong HN, Bertoletti A, Tan YJ. Memory T cell responses targeting the SARS coronavirus persist up to 11 years post-infection. Vaccine. 2016;34(17):2008–2014. doi: 10.1016/j.vaccine.2016.02.063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Yang L, Peng H, Zhu Z, Li G, Huang Z, Zhao Z, Koup RA, Bailer RT, Wu C. Persistent memory CD4+ and CD8+ T-cell responses in recovered severe acute respiratory syndrome (SARS) patients to SARS coronavirus M antigen. J Gen Virol. 2007;88(Pt10):2740–2748. doi: 10.1099/vir.0.82839-0. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Frontiers of Medicine are provided here courtesy of Nature Publishing Group

RESOURCES