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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]
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“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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BackgroundInfluentialAntibody Response and Disease Severity in Healthcare Worker MERS Survivors
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“Although T cells have persisted up to 6 years in SARS survivors (2), whether these patients would have been protected if infected a second time with SARS-CoV is unknown.”
BackgroundInfluentialPersistent cellular immunity to SARS-CoV-2 infection
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“avian influenza, SARS, and Middle East respiratory syndrome (MERS) (Channappanavar et al., 2014; Wang et al., 2015; Wang et al., 2018; Zhao et al., 2017) and persist long-term as cross-reactive memory pools (Koutsakos et al.”
Does infection with or vaccination against SARS-CoV-2 lead to lasting immunity?
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Vaccine-induced systemic and mucosal T cell immunity to SARS-CoV-2 viral variants
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Memory CD8 T cells mediate severe immunopathology following respiratory syncytial virus infection
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Immune system and COVID-19 by sex differences and age
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“Yang et al. also proposed a nucleocapsid based vaccine for SARS-CoV-1 (61).”
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“[33] [34] [35] [36] In this study, we found that the route of rAd vector delivery critically impacted both systemic and mucosal immunity.”
BackgroundT cell immunity to SARS-CoV-2 following natural infection and vaccination
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“following lethal Severe Acute Respiratory Syndrome (SARS)-CoV challenge [15].”
SARS-CoV-2 infections in children and young people
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What Does Plant-Based Vaccine Technology Offer to the Fight against COVID-19?
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“It should also be considered that CTL responses are relevant to cope with COVID-19 [85].”
BackgroundImmunoinformatic identification of B cell and T cell epitopes in the SARS-CoV-2 proteome
Crooke, S. N., Ovsyannikova, I. G., Kennedy, R. B., & Poland, G. A. (2020) · Scientific Reports · doi:10.1038/s41598-020-70864-8 · Cited by 104
“It is currently unknown which epitopes in the SARS-CoV-2 proteome are recognized by the 98 human immune system, although studies of SARS-CoV immune responses suggest that both cellular and 99 humoral responses against structural proteins mediate protection against disease (19, 22, 25-27).”
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“hCoVs induce protective lung- and airway-resident CD69+ TRM T cells in young mice (124, 125).”
BackgroundPotential T-cell and B-cell Epitopes of 2019-nCoVPreprint
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“143 This is consistent with the role of CD8 T-cell in clearing 144 infected cells and mutations supporting the evasion of immune 145 surveillance (27).”
ResultMaruggi, G., Mallett, C. P., Westerbeck, J. W., Chen, T., Lofano, G., Friedrich, K., Qu, L., Sun, J., McAuliffe, J., Kanitkar, A. P., et al. (2022) · Molecular Therapy · doi:10.1016/j.ymthe.2022.01.001 · Cited by 88
“The vaccine also induced high levels of spike-speci fi c polyfunctional cytotoxic CD8 + T cells, which could contribute to viral clearance upon infection, as suggested by previous reports on mouse infection models of SARS-CoV and MERS-CoV, and more importantly, by recent reports on better recovery from COVID-19.”
The CD4 T cell response to respiratory syncytial virus infection
Christiaansen, A. F., Knudson, C. J., Weiss, K. A., & Varga, S. M. (2014) · Immunologic Research · doi:10.1007/s12026-014-8540-1 · Cited by 90
The clinical and immunological features of pediatric COVID-19 patients in China
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“However, it could also induce immune injury by inflammation cytokines.(16,17) In another study about SARS-CoV, depletion of CD4þ T cells led to reduced capability of lymphocytes recruitment and cytokine production, which resulted in immune mediated delayed clearance of SARS-CoV.”
Structure-guided T cell vaccine design for SARS-CoV-2 variants and sarbecoviruses
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“, 2016), and vaccine-induced CD8 T cells protect against lethal SARS-CoV-1 challenge in mice (Channappanavar et al., 2014).”
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An Effective COVID-19 Vaccine Needs to Engage T Cells
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SARS-CoV-2 infection: The role of PD-1/PD-L1 and CTLA-4 axis
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“Virus-specific T cells may thus play a role in eradicating virus-infected cells or inhibiting viral replication and spread via noncytotoxic effects (38, 39).”
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Multiscale PHATE identifies multimodal signatures of COVID-19
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“30,31 ), we tried to determine the differing states present in CD8 + T cells and their role in disease pathogenesis.”
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“It is also possible that CD8 T cells might mediate or contribute to rapid termination of infection as described for SARS-CoV [45, 46] and other viral infection diseases [47, 48].”
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“SARS-CoV-2–specific cellular immunity is comparable in previously infected and vaccinated transplant recipients Virus-specific CD8+ T cells reduce disease severity and promote recovery in many respiratory infections, including those driven by coronaviruses (25, 26), by eliminating infected cells.”
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“This is probably followed by a CD8 cytotoxic T cell response that is generated within days of infection (Channappanavar et al., 2014; Prompetchara et al., 2020; Thevarajan et al., 2020).”
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“These mouse models serve complementary roles in the evaluation of medical countermeasures (Channappanavar et al., 2014a, 2014b), MERS-CoV respiratory disease (Agrawal et al., 2015) and lung pathology (Pascal et al., 2015).”
BackgroundInfluentialRole of iBALT in Respiratory Immunity
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“2003), SARS coronavirus (Channappanavar et al. 2014) and adenovirus (Jericho et al.”
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In silico T cell epitope identification for SARS-CoV-2: Progress and perspectives
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“Surprisingly, the other structural proteins (M, N and E), also reported to be immunogenic in SARS-CoV-2 [6] as well as SARS-CoV [173,174], were analyzed by only a few studies.”
The BCG Vaccine for COVID-19: First Verdict and Future Directions
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“Overall, T-cell responses against the S, N, and M antigens have been reported to be the most dominant and long lasting (51).”
BackgroundGittelman, R. M., Lavezzo, E., Snyder, T. M., Zahid, H. J., Carty, C. L., Elyanow, R., Dalai, S. C., Kirsch, I. R., Baldo, L., Manuto, L., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.151849 · Cited by 78
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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