Cited by 416SARS-CoV-2 and COVID-19 ResearchImmune responses and vaccinationsT-cell and B-cell Immunology

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Virus-Specific Memory CD8 T Cells Provide Substantial Protection from Lethal Severe Acute Respiratory Syndrome Coronavirus Infection

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Channappanavar, Rudragouda, Fett, Craig, Zhao, Jincun, Meyerholz, David K., Perlman, Stanley·2014·Journal of Virology

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Abstract

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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Canedo-Marroquín, G., Saavedra, F., Andrade, C. A., Berríos-Rojas, R. V., Rodríguez‐Guilarte, L., Opazo, M. C., Riedel, C. A., & Kalergis, A. M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.569760 · Cited by 40
Vaccine Considerations for Multiple Sclerosis in the COVID-19 Era
Coyle, P. K., Gocke, A. R., Vignos, M., & Newsome, S. D. (2021) · Advances in Therapy · doi:10.1007/s12325-021-01761-3 · Cited by 39
“Coronavirus-specific T cells from Middle Eastern respiratory syndrome (MERS) and severe acute respiratory syndrome (SARS) have been shown to have long-term persistence and contribute to protection [176, 180, 181].”
Background
Status of Humoral and Cellular Immune Responses within 12 Months following CoronaVac Vaccination against COVID-19
Zhao, W., Chen, W., Li, J., Chen, M., Li, Q., Lv, M., Zhou, S., Bai, S., Wang, Y., Zhang, L., et al. (2022) · mBio · doi:10.1128/mbio.00181-22 · Cited by 37
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Background
Efficacy of Serology Testing in Predicting Reinfection in Patients With SARS-CoV-2
Chaturvedi, R., Naidu, R., Sheth, S. J., & Chakravarthy, K. V. (2020) · Disaster Medicine and Public Health Preparedness · doi:10.1017/dmp.2020.216 · Cited by 35
Lung Tissue-Resident Memory T cells: The Gatekeeper To Respiratory Viral (Re)-Infection
Tang, J., & Sun, J. (2022) · Current Opinion in Immunology · doi:10.1016/j.coi.2022.102278 · Cited by 39
Protective Immunity against SARS Subunit Vaccine Candidates Based on Spike Protein: Lessons for Coronavirus Vaccine Development
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Rapid GMP-Compliant Expansion of SARS-CoV-2–Specific T Cells From Convalescent Donors for Use as an Allogeneic Cell Therapy for COVID-19
Cooper, R. S., Fraser, A. R., Smith, L. M., Burgoyne, P., Imlach, S. N., JARVIS, L. M., Turner, D. M., Zahra, S., Turner, M. L., & Campbell, J. D. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.598402 · Cited by 33
“This reduced CD8 response may be an advantage for a therapeutic product, as in models there is a clear protective role for CD8 T cells against acute SARS infection (37), but there is evidence that hyperactivation of CD8 T cells can be linked to severity of COVID-19 disease (38).”
Background
Accelerated immune ageing is associated with COVID-19 disease severity
Lord, J. M., Veenith, T., Sullivan, J., Sharma‐Oates, A., Richter, A. G., Greening, N. J., McAuley, H., Evans, R. A., Moss, P. A. H., Moore, S. C., et al. (2024) · Immunity & Ageing · doi:10.1186/s12979-023-00406-z · Cited by 35
“Cytotoxic CD8 T cells play a vital role in immune defence against several viral infections, including coronavirus [25].”
Background
Vaccines for emerging infectious diseases: Lessons from MERS coronavirus and Zika virus
Maslow, J. N. (2017) · Human Vaccines & Immunotherapeutics · doi:10.1080/21645515.2017.1358325 · Cited by 34
“Importantly, mouse studies demonstrated that cytotoxic T-cell immunity against SARS-CoV was required for viral clearance and survival from lethal infection.(51,52) The kinetics of the serologic response against MERS-CoV shows that binding and neutralizing antibodies appear at about day 10 of illness, reaching a peak a…”
Background
Immunoinformatics prediction of overlapping CD8+ T-cell, IFN-γ and IL-4 inducer CD4+ T-cell and linear B-cell epitopes based vaccines against COVID-19 (SARS-CoV-2)
Fatoba, A. J., Maharaj, L., Adeleke, V. T., Okpeku, M., Adeniyi, A. A., & Adeleke, M. A. (2021) · Vaccine · doi:10.1016/j.vaccine.2021.01.003 · Cited by 33
“According to the report of [11], T-cell response is highly immunogenic, dominant and long-lasting against N and S protein of SARS-CoV.”
Background
Cellular Immunity—The Key to Long-Term Protection in Individuals Recovered from SARS-CoV-2 and after Vaccination
Primorac, D., Brlek, P., Matišić, V., Molnar, V., Vrdoljak, K., Zadro, R., & Parčina, M. (2022) · Vaccines · doi:10.3390/vaccines10030442 · Cited by 35
Prevention and Control Strategies for SARS-CoV-2 Infection
Srivastava, N., & Saxena, S. K. (2020) · Medical virology · doi:10.1007/978-981-15-4814-7_11 · Cited by 33
Immune response against epidemic coronaviruses
Pashenkov, M. V., & Khaitov, R. M. (2020) · Immunologiya · doi:10.33029/0206-4952-2020-41-1-5-18 · Cited by 37
Upregulation of CCR4 in activated CD8 + T cells indicates enhanced lung homing in patients with severe acute SARS‐CoV‐2 infection
Spoerl, S., Kremer, A. N., Aigner, M., Eisenhauer, N., Koch, P., Meretuk, L., Löffler, P., Tenbusch, M., Maier, C., Überla, K., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202049135 · Cited by 34
Broad T Cell Targeting of Structural Proteins After SARS-CoV-2 Infection: High Throughput Assessment of T Cell Reactivity Using an Automated Interferon Gamma Release Assay
Brand, I., Gilberg, L., Bruger, J., Garí, M., Wieser, A., Eser, T. M., Frese, J., Ahmed, M. I. M., Rubio‐Acero, R., Noller, J. M. G., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.688436 · Cited by 34
Protective Adaptive Immunity Against Severe Acute Respiratory Syndrome Coronaviruses 2 (SARS-CoV-2) and Implications for Vaccines
Manners, C., Bautista, E. L., Sidoti, H., & López, O. J. (2020) · Cureus · doi:10.7759/cureus.8399 · Cited by 33
CoVaccine HT™ Adjuvant Potentiates Robust Immune Responses to Recombinant SARS-CoV-2 Spike S1 Immunization
Haun, B. K., Lai, C.-Y., Williams, C. A., Wong, T. A. S., Lieberman, M. M., Pessaint, L., Andersen, H., & Lehrer, A. T. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.599587 · Cited by 29
An integrated in silico immuno-genetic analytical platform provides insights into COVID-19 serological and vaccine targets
Ward, D., Higgins, M. K., Phelan, J. E., Hibberd, M. L., Campino, S. G., & Clark, T. G. (2021) · Genome Medicine · doi:10.1186/s13073-020-00822-6 · Cited by 33
Single-dose replicating RNA vaccine induces neutralizing antibodies against SARS-CoV-2 in nonhuman primatesPreprint
Erasmus, J. H., Khandhar, A. P., Walls, A. C., Hemann, E. A., O’Connor, M. A., Murapa, P., Archer, J. F., Leventhal, S. S., Fuller, J., Lewis, T. B., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.28.121640 · Cited by 30
Mitigating Coronavirus Induced Dysfunctional Immunity for At-Risk Populations in COVID-19: Trained Immunity, BCG and “New Old Friends”
Kleen, T. O., Galdon, A. A., MacDonald, A. S., & Dalgleish, A. G. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.02059 · Cited by 29
“Multiple studies have been performed in mouse models describing the importance of type 1 CD4+ and CD8+ T cells in SARS-CoV (128, 129), with one study establishing that virus-specific memory CD8+ T cells provided substantial protection from lethal closely related SARS-CoV infection in a mouse model, emphasizing the imp…”
Background
CD8+ T-cell immune escape by SARS-CoV-2 variants of concern
Kombe, A. J. K., Biteghe, F. A. N., Ndoutoume, Z. N., & Jin, T. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.962079 · Cited by 29
“The CD8 T cells produce numerous toxic substances (perforins, granzyme, and FasL) and cytokines (IFN-g, TNF-a, and IL-2) directly involved in SARS-CoV-2–infected cell death (A) (30, 32).”
Background
Overview of the current promising approaches for the development of an effective severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccine
Mirzaei, R., Mohammadzadeh, R., Mahdavi, F., Badrzadeh, F., Kazemi, S., Ebrahimi, M., soltani, F., Kazemi, S., Jeda, A. S., Darvishmotevalli, M., et al. (2020) · International Immunopharmacology · doi:10.1016/j.intimp.2020.106928 · Cited by 29
“been reported to be the most dominant and long-lasting immune reaction [105].”
Vaccines for COVID-19: perspectives from nucleic acid vaccines to BCG as delivery vector system
de Queiroz, N. M. G. P., Marinho, F. V., Chagas, M., Leite, L. C. C., Homan, E. J., de Magalhães, M. T. Q., & Oliveira, S. C. (2020) · Microbes and Infection · doi:10.1016/j.micinf.2020.09.004 · Cited by 27
“CTL mediated protection through increased production of IFN-g and cytotoxicity [40].”
Rapid detection of SARS‐CoV‐2‐specific memory T‐cell immunity in recovered COVID‐19 cases
Lineburg, K. E., Srihari, S., Altaf, M., Swaminathan, S., Panikkar, A., Raju, J., Crooks, P., Ambalathingal, G. R., Martins, J. P., Matthews, K. K., et al. (2020) · Clinical & Translational Immunology · doi:10.1002/cti2.1219 · Cited by 27
“Based on observations in other coronavirus infections, particularly in animal models, it is also likely that this T-cell response plays a critical role in disease prevention.(32) Ongoing studies in patients with acute infection and symptomatic disease should help to further define the role of T cells in the prevention…”
A vaccine platform targeting lung-resident memory CD4+ T-cells provides protection against heterosubtypic influenza infections in mice and ferrets
Ko, K. H., Bae, H. S., Park, J. W., Lee, J.-S., Park, S., Heo, J., Park, H., Choi, J., Bae, E., Na, W., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-54620-4 · Cited by 27
Exploring the SARS-CoV-2 structural proteins for multi-epitope vaccine development: an in-silico approach
Kumar, A., Kumar, P., Saumya, K. U., Kapuganti, S. K., Bhardwaj, T., & Giri, R. (2020) · Expert Review of Vaccines · doi:10.1080/14760584.2020.1813576 · Cited by 29
“Similarly, T C cell response against the structural proteins S and N are long-lasting [22].”
Background
Dynamic SARS-CoV-2-Specific Immunity in Critically Ill Patients With Hypertension
Zeng, Q., Li, Y., Dong, S.-Y., Chen, Z., Gao, X., Zhang, H., Huang, G., & Xu, Y. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.596684 · Cited by 27
“(35) first reported that SARS-CoVspecific memory CD8 T cells persisted for up to 6 years after SARS-CoV infection.”
Background
Emerging Human Coronavirus Infections (SARS, MERS, and COVID-19): Where They Are Leading Us
Kumar, V. (2020) · International Reviews of Immunology · doi:10.1080/08830185.2020.1800688 · Cited by 29
Immune Correlates of COVID-19 Control
Poonia, B., & Kottilil, S. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.569611 · Cited by 26
Key Considerations for the Development of Safe and Effective SARS‐CoV‐2 Subunit Vaccine: A Peptide‐Based Vaccine Alternative
Shalash, A. O., Hussein, W. M., Skwarczyński, M., & Tóth, I. (2021) · Advanced Science · doi:10.1002/advs.202100985 · Cited by 25
Immunopathology and Immunosenescence, the Immunological Key Words of Severe COVID-19. Is There a Role for Stem Cell Transplantation?
Ligotti, M. E., Pojero, F., Accardi, G., Aiello, A., Caruso, C., Duro, G., & Candore, G. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.725606 · Cited by 26
Simultaneous CD8+ T-Cell Immune Response against SARS-Cov-2 S, M, and N Induced by Endogenously Engineered Extracellular Vesicles in Both Spleen and Lungs
Ferrantelli, F., Chiozzini, C., Manfredi, F., Giovannelli, A., Leone, P., & Federico, M. (2021) · Vaccines · doi:10.3390/vaccines9030240 · Cited by 24
“showed that CD8+ T-cells specific for a single SARS-CoV immunodominant epitope protected mice from an otherwise lethal dose of virus in the absence of neutralizing antibodies [76].”
Background
Considerations for Novel COVID-19 Mucosal Vaccine Development
Alturaiki, W. (2022) · Vaccines · doi:10.3390/vaccines10081173 · Cited by 25
Vaccination against SARS-CoV-2 and disease enhancement – knowns and unknowns
Zellweger, R. M., Wartel, T. A., Marks, F., Song, M., & Kim, J. H. (2020) · Expert Review of Vaccines · doi:10.1080/14760584.2020.1800463 · Cited by 24
“of the Th2/Th1 balance (either increased Th2 or decreased Th1) and sub-optimal CD8 responses have all been postulated to explain vaccine-induced disease enhancement [26,27,40,43,44].”
Background
Treatment and prognosis of COVID‑19: Current scenario and prospects (Review)
Li, X., Li, T., & Wang, H. (2020) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2020.9435 · Cited by 24
“In addition, it is reported that depletion of CD8+ T cells does not affect and delay viral replication in SARS‐CoV infection (71), but loss of CD4+ T cells is accom‐ panied by reduced production of lymphocytes neutralizing antibody and cytokine, resulting in interstitial pneumonitis and delayed clearance of SARS‐CoV‐2…”
Background
Does common cold coronavirus infection protect against severe SARS-CoV-2 disease?
Meyerholz, D. K., & Perlman, S. M. (2020) · Journal of Clinical Investigation · doi:10.1172/jci144807 · Cited by 22
“In animal models, T cells (both CD4+ and CD8+) have been shown to provide effective and protective immunity against coronavirus infection (9, 10).”
Background
Immunoinformatics Analysis of SARS-CoV-2 ORF1ab Polyproteins to Identify Promiscuous and Highly Conserved T-Cell Epitopes to Formulate Vaccine for Indonesia and the World Population
Gustiananda, M., Sulistyo, B. P., Agustriawan, D., & Andarini, S. (2021) · Vaccines · doi:10.3390/vaccines9121459 · Cited by 27
AI Aided Design of Epitope-Based Vaccine for the Induction of Cellular Immune Responses Against SARS-CoV-2
Mazzocco, G., Niemiec, I., Myronov, A., Skoczylas, P., Kaczmarczyk, J., Sanecka-Duin, A., Gruba, K., Król, P., Drwal, M., Szczepanik, M., et al. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.602196 · Cited by 22
“The importance of both CD8+ and CD4+ T-cell activation has been reported in several SARS-CoV studies for both animal models and humans (Channappanavar et al. 2014).”
Background
SARS-CoV-2 infection paralyzes cytotoxic and metabolic functions of the immune cells
Singh, Y., Trautwein, C., Fendel, R., Krickeberg, N., Berezhnoy, G., Bissinger, R., Ossowski, S., Salker, M. S., Casadei, N., Rieß, O., et al. (2021) · Heliyon · doi:10.1016/j.heliyon.2021.e07147 · Cited by 24
“Interestingly, patients with mild symptoms were also shown to have increased T and B cells compared with severely affected patients [26, 29, 30, 31].”
A Review of Routine Laboratory Biomarkers for the Detection of Severe COVID-19 Disease
Keykavousi, K., Nourbakhsh, F., Abdollahpour, N., Fazeli, F., Sedaghat, A., Soheili, V., & Sahebkar, A. (2022) · International Journal of Analytical Chemistry · doi:10.1155/2022/9006487 · Cited by 24
Potential protective role of the anti-PD-1 blockade against SARS-CoV-2 infection
Awadasseid, A., Yin, Q., Wu, Y., & Zhang, W. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.111957 · Cited by 24
Immune features of COVID-19 convalescent individuals revealed by a single-cell RNA sequencing
Zhao, P., Zou, J., Zhou, F., Zhu, Y., Song, Q., Yu, D., & Li, X. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.108767 · Cited by 21
“In line with antibody, memory B cell responses tend to be short lived after infection with SARS-CoV-1 [21,22].”
Convalescent plasma (hyperimmune immunoglobulin) for COVID-19 management: An update
Chavda, V. P., Bezbaruah, R., Dolia, S., Shah, N., Verma, S., Savale, S. S., & Ray, S. (2023) · Process Biochemistry · doi:10.1016/j.procbio.2023.01.018 · Cited by 25
“Virus-specific memory CD4 and CD8 T cells are responsible for protecting the infected person from mortality [36,37].”
Background
Divergent SARS-CoV-2-specific T and B cell responses in severe but not mild COVID-19Preprint
Oja, A. E., Saris, A., Ghandour, C. A., Kragten, N. A. M., Hogema, B. M., Nossent, E. J., Heunks, L. M. A., Cuvalay, S., Slot, E., Swaneveld, F. H., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.18.159202 · Cited by 22
Expected immune recognition of COVID-19 virus by memory from earlier infections with common coronaviruses in a large part of the world population
Dijkstra, J. M., & Hashimoto, K. (2020) · F1000Research · doi:10.12688/f1000research.23458.1 · Cited by 20
CD8 T cell epitope generation toward the continually mutating SARS-CoV-2 spike protein in genetically diverse human population: Implications for disease control and prevention
Guo, E., & Guo, H. (2020) · PLoS ONE · doi:10.1371/journal.pone.0239566 · Cited by 21
Emerging Roles of Coronavirus in Autoimmune Diseases
Zhou, S.-Y., Zhang, C., Shu, W.-J., Chong, L.-Y., He, J., Xu, Z., & Pan, H. (2021) · Archives of Medical Research · doi:10.1016/j.arcmed.2021.03.012 · Cited by 23
Exosomal Vaccine Loading T Cell Epitope Peptides of SARS-CoV-2 Induces Robust CD8+ T Cell Response in HLA-A Transgenic Mice
Shen, A.-R., Jin, X.-X., Tang, T.-T., Ding, Y., Liu, X.-T., Zhong, X., Wu, Y.-D., Han, X.-L., Zhao, G.-Y., Shen, C.-L., et al. (2022) · International Journal of Nanomedicine · doi:10.2147/ijn.s367494 · Cited by 19
“In contrast, the life-span of memory B cells is significantly shorter in the host.(34,36) Therefore, T cell epitope-based vaccines are expected to provide long-lasting preventive and therapeutic effects against SARS-CoV-2 infection by inducing specific T cell responses.”
Background

Authors: Channappanavar, R., Fett, C., Zhao, J., Meyerholz, D. K., & Perlman, S.
Affiliations: University of Iowa (US)
ORCID: Channappanavar, Rudragouda
Zhao, Jincun
Meyerholz, David K.
Perlman, Stanley
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
DOI: 10.1128/jvi.01505-14
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
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
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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Virus-Specific Memory CD8 T Cells Provide Substantial Protection from Lethal Severe Acute Respiratory Syndrome Coronavirus Infection

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