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Virus-Specific Memory CD8 T Cells Provide Substantial Protection from Lethal Severe Acute Respiratory Syndrome Coronavirus Infection
Open accessAbstract
UNLABELLED: Severe acute respiratory syndrome coronavirus (SARS-CoV) caused an acute human respiratory illness with high morbidity and mortality in 2002-2003. Several studies have demonstrated the role of neutralizing antibodies induced by the spike (S) glycoprotein in protecting susceptible hosts from lethal infection. However, the anti-SARS-CoV antibody response is short-lived in patients who have recovered from SARS, making it critical to develop additional vaccine strategies. SARS-CoV-specific memory CD8 T cells persisted for up to 6 years after SARS-CoV infection, a time at which memory B cells and antivirus antibodies were undetectable in individuals who had recovered from SARS. In this study, we assessed the ability of virus-specific memory CD8 T cells to mediate protection against infection in the absence of SARS-CoV-specific memory CD4 T or B cells. We demonstrate that memory CD8 T cells specific for a single immunodominant epitope (S436 or S525) substantially protected 8- to 10-month-old mice from lethal SARS-CoV infection. Intravenous immunization with peptide-loaded dendritic cells (DCs) followed by intranasal boosting with recombinant vaccinia virus (rVV) encoding S436 or S525 resulted in accumulation of virus-specific memory CD8 T cells in bronchoalveolar lavage fluid (BAL), lungs, and spleen. Upon challenge with a lethal dose of SARS-CoV, virus-specific memory CD8 T cells efficiently produced multiple effector cytokines (gamma interferon [IFN-γ], tumor necrosis factor alpha [TNF-α], and interleukin 2 [IL-2]) and cytolytic molecules (granzyme B) and reduced lung viral loads. Overall, our results show that SARS-CoV-specific memory CD8 T cells protect susceptible hosts from lethal SARS-CoV infection, but they also suggest that SARS-CoV-specific CD4 T cell and antibody responses are necessary for complete protection. IMPORTANCE: Virus-specific CD8 T cells are required for pathogen clearance following primary SARS-CoV infection. However, the role of SARS-CoV-specific memory CD8 T cells in mediating protection after SARS-CoV challenge has not been previously investigated. In this study, using a prime-boost immunization approach, we showed that virus-specific CD8 T cells protect susceptible 8- to 10-month-old mice from lethal SARS-CoV challenge. Thus, future vaccines against emerging coronaviruses should emphasize the generation of a memory CD8 T cell response for optimal protection.
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“anti-S T-cell responses to the related SARS- and MERS-CoVs contribute toward viral clearance in normal as well as aged mice infected with SARS- or MERS-CoV, respectively (43–45).”
From An Alphavirus -derived replicon RNA vaccine induces SARS-CoV-2 neutralizing antibody and T cell responses in mice and nonhuman primates (2020) · cites this paper as [45]
Experimental — accuracy not yet measuredIn the citing paper
“Memory T cells, particularly those residing at the upper airways might limit disease severity and shorten the duration of disease by rapidly eliminating infected cells and coordinating the production of antibodies [67]”
From The dawn of mRNA vaccines: the COVID-19 case (2021) · cites this paper as [67]
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Resposta imunológica contra o SRAS-CoV-2: uma revisão entre a resposta do hospedeiro e o vírus
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Chen, C. C., Baikoghli, M., & Cheng, R. H. (2020) · ACTA SCIENTIFIC MICROBIOLOGY · doi:10.31080/asmi.2020.03.0741
SARS-CoV-2 Infection in Transplant-Related Biology: Where Do We stand?
Kong, D., Li, M., & Gong, W. (2020) · Annals of Transplantation · doi:10.12659/aot.924768 · Cited by 1
Possible Reinfection with SARS-CoV-2 in a Splenectomized Patient from Kocaeli, Turkey
Deniz, M. T., Akhan, S., Sayan, M., & Barış, S. A. (2021) · Mediterranean Journal of Infection Microbes and Antimicrobials · doi:10.4274/mjima.galenos.2021.2021.29 · Cited by 1
Laboratory and demographic findings among patients with coronavirus disease 2019: A review
Mir, A., Farmanfarma, K. K., Salehiniya, H., Shakiba, A., & Mahdavifar, N. (2021) · Monaldi Archives for Chest Disease · doi:10.4081/monaldi.2021.1694 · Cited by 1
“CD8þ T cells play a vital role in SARS-CoV virus killing in the patients’ lungs (19,20).”
BackgroundPros and Cons for COVID-19 Vaccination and Boost of Young Adults in Light of Recent Literature
Nemunaitis, J. J., Lehmann, P., & Willey, J. C. (2022) · Medical Research Archives · doi:10.18103/mra.v10i8.2943 · Cited by 1
Rakib, A., Sami, S. A., Islam, M. A., Ahmed, S., Faiz, F. B., Khanam, B. H., Uddin, M. M. N., & Emran, T. B. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.16.100206 · Cited by 1
“For a vaccine, it is essential to identify Tcell epitopes that originate from conserved regions of the virus T cell responses against the S and N proteins have been reported to be the most dominant and long-lasting (14).”
BackgroundBaker, D., Roberts, C., Pryce, G., Kang, A. S., Marta, M., Reyes, S., Schmierer, K., Giovannoni, G., & Amor, S. (2020) · doi:10.22541/au.159292858.82650822 · Cited by 1
Exploit T cell Immunity for Rapid, Safe and Effective COVID-19 Vaccines
Moise, L., Ross, T. M., Hoft, D. F., Martin, W. D., & Groot, A. S. D. (2020) · Expert Review of Vaccines · doi:10.1080/14760584.2020.1825946 · Cited by 1
Sterilizing immunity against SARS-CoV-2 in hamsters conferred by a novel recombinant subunit vaccinePreprint
Wu, Y., Huang, X., Yuan, L., Wang, S., Zhang, Y., Xiong, H., Chen, R., Ma, J., Qi, R., Nie, M., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.18.423552 · Cited by 1
“Moreover, the functional antibody may not completely block viruses from invading cells; virus-specific T cells may play a remedial role in eradicating virus-infected cells or inhibiting viral replication and spread via non-cytotoxic effects (37, 38).”
BackgroundPredicting SARS-CoV-2 epitope-specific TCR recognition using pre-trained protein embeddingsPreprint
Han, Y., & Lee, A. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.17.468929 · Cited by 1
“T-cells circulating in the blood lead the first response to any virus in the adaptive immune system: they detect infected cells and mount an immune response or directly clear the infected cells, often before symptoms appear [3-6].”
BackgroundWang, C. Y., Peng, W., Kuo, B.-S., Liu, H., Ho, Y.-H., Wang, M.-S., Yang, Y.-T., Chang, P.-Y., Shen, Y.-H., & Hwang, K. (2022) · medRxiv · doi:10.1101/2022.08.26.22279232 · Cited by 1
“The facts that potent memory CD4 and CD8 T cell memory can protect against SARS-CoV-2 infection in the absence of immune neutralizing antibodies (52, 53, 61) raises concerns over the fact that humoral antibody response has long been used as a sole bridging metric of protective immunity (62), which lacks full understan…”
BackgroundAntonio, E. C., Meireles, M. R., Bragatte, M. A. D. S., & Vieira, G. F. (2020) · medRxiv · doi:10.1101/2020.06.15.20131987
Zeng, Q., Huang, G., Li, Y., Xu, G., Dong, S.-Y., Zhong, T., Chen, Z., & Xu, Y. (2020) · medRxiv · doi:10.1101/2020.07.29.20164681
T-Zellantworten gegen SARS-CoV-2 und die Rolle präexistierender Gedächtniszellen
Scheffold, A., & Bächer, P. (2020) · Trillium Immunologie · doi:10.47184//ti.2020.03.03
Aktueller Stand der Impfstoff-Entwicklung gegen SARS-CoV-2
Kamradt, T. (2020) · Trillium Immunologie · doi:10.47184//ti.2020.03.06
COVID-19 bei Kindern und Jugendlichen
Felsenstein, S., & Hedrich, C. M. (2020) · Arthritis und Rheuma · doi:10.1055/a-1255-8937
Robuste T-Zell-Antwort schützt vor SARS-CoV-2-Re-Infektion
Gesierich, W. (2020) · Pneumo News · doi:10.1007/s15033-020-1936-9
Daouda, T., Dumont-Lagacé, M., Feghaly, A., & Villani, A. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.04.429819
Шиловский, И. П., Валерьевич, Ю. К., Никольский, А. А., Vishniakova, L. I., & Khaitov, M. R. (2021) · Biochemistry (Moscow) · doi:10.31857/s0320972521030052
SARS-CoV-2 re-positivity within the first 3 months of COVID-19 recovery; probable re-infectionPreprint
Sadr, S., Bafrani, M. A., Abdollahi, A., SeyedAlinaghi, S., Mohammadnejad, E., Hossienzade, R., Golestan, F. S., Ahmadinejad, Z., Salehi, M., Javaherian, M., et al. (2021) · doi:10.22541/au.162117445.56254867/v1
T Cell Predominant Response to AAV-Spike Protects hACE2 Mice from SARS-CoV-2 PneumoniaPreprint
Greer, C. D., Kasden, C. M., Morales, L., Lundgreen, K. A., Hicks, P. D., Carpenter, L. J., Salas-Quinchucua, C., Tichy, E. D., Maguire, A. M., Hoffman, J. G., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.16.456441 · Cited by 1
Clinical Manifestations of Cytokine Storm and Immune Response to COVID-19: Literature Review
Kowsarnia, S. (2021) · Open Journal of Internal Medicine · doi:10.4236/ojim.2021.113012
Zhao, W., Chen, W., Li, J., Cheng, M., Li, Q., Lv, M., Zhou, S., Bai, S., Wang, Y., Zhang, L., et al. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3945456
C 4 H 6 O, C 4 H 6 S与XF (X＝F, Cl, Br)分子间卤键的电子密度拓扑研究
曾艳丽, 吉丽婷, 郑世钧, & 孟令鹏 (2011) · 化学学报
The Association of MHC Molecules with COVID-19
Oğuz, S. R. (2021) · Flora the Journal of Infectious Diseases and Clinical Microbiology · doi:10.5578/flora.20219601
Clonal diversity determines persistence of SARS-CoV-2 epitope-specific T cell responsePreprint
Zornikova, K. V., Khmelevskaya, A. A., Sheetikov, S. A., Kiryukhin, D. O., Shcherbakova, O. V., Titov, A., Zvyagin, I. V., & Efimov, G. A. (2022) · medRxiv · doi:10.1101/2022.04.18.22273961
“A beneficial role of T cells has also been shown in mice: in the absence of antibodies, T cells were able to eliminate SARS-CoV infection, and immunization with a single immunodominant CD8+ T cell epitope protected against lethal disease (Zhao et al., 2010; Channappanavar et al., 2014).”
BackgroundРОЛЬ КЛЕТОЧНОГО ЗВЕНА ИММУНИТЕТА В ФОРМИРОВАНИИ ИММУННОГО ОТВЕТА ПРИ КОРОНАВИРУСНЫХ ИНФЕКЦИЯХPreprint
Ia, I., Omelchenko, N. D., Filippenko, A. V., Trufanova, A. A., & Носков, А. К. (2021) · doi:10.21055/preprints-3111935
Uvarova, E. A., Belavin, P. A., & Дейнеко, Е. В. (2022) · Vavilov Journal of Genetics and Breeding · doi:10.18699/vjgb-22-39
“Toll-like and NOD-like receptors constitute the main group of receptors during the development of nonspecific protection (Takeuchi, Akira, 2010; Channappanavar et al., 2014).”
BackgroundCould veterinarians be immune to contracting SARS-CoV-2?
Kozłowska-Geller, M. A., Lewitowicz, P., Węgierek-Ciuk, A., Adamus-Białek, W., Piechowska, A., & Głuszek, S. (2022) · Central European Journal of Immunology · doi:10.5114/ceji.2022.119893
“The recurrent contact with pathogens may work as immune mobilization against SARS-CoV-2 in many different paths [13].”
BackgroundBarral, A. M. P., & Barral‐Netto, M. (2023) · Revista de estudios brasileños · doi:10.14201/reb20229194556
Perlman, S. M., & Denison, M. R. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-79058-1.00017-7 · Cited by 2
Li, C., Xu, D., Lu, L., Zhao, H., Zeng, C., Hu, L., Guo, X., Liu, L., Tang, L., Huo, F., et al. (2023) · SSRN Electronic Journal · doi:10.2139/ssrn.4632955
Desarrollo de una vacuna a base de nanopartículas
Rizzo, G. (2023) · doi:10.35537/10915/161626
Qin, T., Shen, B., Li, E., Jin, S., Luo, R., Zhang, Y., Qi, J., Deng, X., Shi, Z., Wang, T., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22671341
Qin, T., Shen, B., Li, E., Jin, S., Luo, R., Zhang, Y., Qi, J., Deng, X., Shi, Z., Wang, T., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22671344
As vacinas para COVID-19 e suas tecnologias: potencial e perspectivas
Nunes, V. A., Chambergo, F. S., Akamatsu, M. A., & Ho, P. L. (2022) · Cadernos de História da Ciência · doi:10.47692/cadhistcienc.2021.v15.36516
Metadata
- Authors
- Channappanavar, R., Fett, C., Zhao, J., Meyerholz, D. K., & Perlman, S.
- Affiliations
- University of Iowa (US)
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2014-10
- Volume
- 88
- Issue
- 19
- Pages
- 11034-11044
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC4178831
- OpenAlex
- W2004583429
- Cited by
- 411
- References
- 53
- Citations by year
- 2026: 8 · 2025: 14 · 2024: 14 · 2023: 39 · 2022: 51 · 2021: 117 · 2020: 142 · 2019: 3 · 2018: 6 · 2017: 4 · 2016: 6 · 2015: 3 · 2014: 3
- FWCI
- 3.75
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Virology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (AI060699)
- National Institute of Allergy and Infectious Diseases (AI091322, R01AI091322, AI060699, P01AI060699)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK054759)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- SARS-CoV, memory CD8+ T cells, T cell immunity, immunodominant epitopes, spike protein, prime-boost vaccination, peptide-loaded dendritic cells, vaccinia virus vector, lung viral load, cytokine production, granzyme B
- MeSH terms
- Animals, Antibodies, Viral, Antigens, Viral, Dendritic Cells, Female, Humans, Immunity, Active, Immunity, Cellular, Immunization, Immunologic Memory, Peptides, CD4-Positive T-Lymphocytes, Gene Expression, Survival Analysis, CD8-Positive T-Lymphocytes, Epitopes, T-Lymphocyte, Severe Acute Respiratory Syndrome, Severe acute respiratory syndrome-related coronavirus, Mice, Immunity, Humoral
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