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Functional exhaustion of antiviral lymphocytes in COVID-19 patients
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In December 2019, a novel coronavirus was first reported in Wuhan, China. 1 It was named by the World Health Organization as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and is responsible for coronavirus disease 2019 (COVID-19). Up to 28 February 2020, 79,394 cases have been confirmed according to China’s National Health Commission. Outside China, the virus has spread rapidly to over 36 countries and territories.
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“In ex vivo studies, NK cells from patients with COVID-19 displayed impaired cytotoxicity (64, 65)”
From SARS-CoV-2 variants of concern partially escape humoral but not T cell responses in COVID-19 convalescent donors and vaccine recipients (2021) · cites this paper as [64]
In the citing paper
“NK cells were shown to be decreased in patients with COVID-19 in association with disease severity (64).”
From SARS-CoV-2 variants of concern partially escape humoral but not T cell responses in COVID-19 convalescent donors and vaccine recipients (2021) · cites this paper as [64]
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The deregulated immune reaction and cytokines release storm (CRS) in COVID-19 disease
Pasrija, R., & Naime, M. (2020) · International Immunopharmacology · doi:10.1016/j.intimp.2020.107225 · Cited by 112
“Another report document that, soon after activation, CD8+ cells start expressing repressing receptors like PD1, TIM3, LAG3, CTLA4, NKG2A and CD39, resulting in Tc cell exhaustion [63,64].”
The role of vitamin D in the age of COVID‐19: A systematic review and meta‐analysis
Ghasemian, R., Shamshirian, A., Heydari, K., Malekan, M., Alizadeh‐Navaei, R., Ebrahimzadeh, M. A., Warkiani, M. E., Jafarpour, H., Bazaz, S. R., Shahmirzadi, A. R., et al. (2021) · International Journal of Clinical Practice · doi:10.1111/ijcp.14675 · Cited by 114
Abnormal immunity of non-survivors with COVID-19: predictors for mortality
Zhao, Y., Nie, H., Hu, K., Wu, X., Zhang, Y., Wang, M. E., Wang, T., Zheng, Z., Li, X., & Zeng, S. (2020) · Infectious Diseases of Poverty · doi:10.1186/s40249-020-00723-1 · Cited by 107
Rosa, B. A., Ahmed, M., Singh, D. K., Choreño-Parra, J. A., Cole, J., Jiménez-Álvarez, L. A., Rodríguez-Reyna, T. S., Singh, B., Gonzalez, O., Carrion, R., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-01829-4 · Cited by 106
Contribution of STAT3 to the pathogenesis of COVID-19
Jafarzadeh, A., Nemati, M., & Jafarzadeh, S. (2021) · Microbial Pathogenesis · doi:10.1016/j.micpath.2021.104836 · Cited by 110
Bordoni, V., Sacchi, A., Cimini, E., Notari, S., Grassi, G., Tartaglia, E., Casetti, R., Giancola, M. L., Bevilacqua, N., Maeurer, M. J., et al. (2020) · Clinical Infectious Diseases · doi:10.1093/cid/ciaa577 · Cited by 105
“granzyme content, suggesting an impaired cytotoxic immune response during SARS-CoV-2 infection [6].”
BackgroundThe pathophysiology of SARS-CoV-2: A suggested model and therapeutic approach
Morris, G., Bortolasci, C. C., Puri, B. K., OLIVE, L. S., Marx, W., O'Neil, A. E., Athan, E., Carvalho, A. F., Maes, M. H. J., Walder, K. R., et al. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.118166 · Cited by 107
The pandemic exposes human nature: 10 evolutionary insights
Seitz, B. M., Aktipis, A., Buss, D. M., Alcock, J., Bloom, P. A., Gelfand, M. J., Harris, S., Lieberman, D., Natterson-Horowitz, B., Pinker, S. A., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2009787117 · Cited by 101
Age-related mitochondrial dysfunction as a key factor in COVID-19 disease
Fernández‐Ayala, D. J. M., Navas, P., & López‐Lluch, G. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.111147 · Cited by 110
Coronavirus Disease 2019 (COVID–19): A Short Review on Hematological Manifestations
Słomka, A., Kowalewski, M., & Żekanowska, E. (2020) · Pathogens · doi:10.3390/pathogens9060493 · Cited by 106
“These hypothetical considerations are now supported by the observations that the virus can infect T cells through receptor–dependent, S protein–mediated membrane fusion [57], which results in depletion of the cytotoxic capacity of lymphocytes [58].”
BackgroundCharacterization of humoral and SARS-CoV-2 specific T cell responses in people living with HIV
Alrubayyi, A., Gea‐Mallorquí, E., Touizer, E., Hameiri‐Bowen, D., Kopycinski, J. T., Charlton, B. G., Fisher-Pearson, N., Muir, L., Rosa, A., Roustan, C., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26137-7 · Cited by 107
Herpes zoster might be an indicator for latent COVID 19 infection
Elsaie, M. L., Youssef, E. A., & Nada, H. (2020) · Dermatologic Therapy · doi:10.1111/dth.13666 · Cited by 102
“Lower percentages of T cell functional markers is also observed with in the T Lymphocytes population as COVID-19 patients showed decreased percentages of CD107a+ CD8+, IFN-γ+CD8+, and IL-2+CD8+ T cells and MFI of granzyme B+CD8+ T cells when compared to normal controls (13).”
BackgroundNon‐steroidal anti‐inflammatory drugs, prostaglandins, and COVID‐19
Robb, C. T., Goepp, M., Rossi, A. G., & Yao, C. (2020) · British Journal of Pharmacology · doi:10.1111/bph.15206 · Cited by 104
“Like T cells, NK cells are also depleted in peripheral blood of severe but not mild COVID-19 patients (Zheng et al., 2020; Wen et al., 2020; Wilk et al., 2020).”
BackgroundInfluentialImmune Response and COVID-19: A mirror image of Sepsis
López‐Collazo, E., Ortiz, J. A., Martín‐Quirós, A., & Aguirre, L. A. (2020) · International Journal of Biological Sciences · doi:10.7150/ijbs.48400 · Cited by 103
“NK cell levels have been found to be reduced and to present an anergic status in patients with COVID-19 [90].”
BackgroundLongitudinal transcriptome analyses show robust T cell immunity during recovery from COVID-19
Zheng, H., Xu, M., Yang, C.-X., Tian, R.-R., Zhang, M., Li, J. J., Wang, X.-C., Ding, Z.-L., Li, G.-M., Li, X., et al. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00457-4 · Cited by 103
“A large number of studies have shown that SARS-CoV-2 infection can cause a more pronounced lymphocytopenia in patients with moderate and severe COVID-19, as reflected by the decreased level of T cells, including Th1, Treg, and CD8 T cells.(1,39,40) In addition, neutrophils increased and monocytes decreased in COVID-19…”
ResultKreutmair, S., Unger, S., Núñez, N. G., Ingelfinger, F., Alberti, C., Feo, D. D., Krishnarajah, S., Kauffmann, M., Friebel, E., Babaei, S., et al. (2021) · Immunity · doi:10.1016/j.immuni.2021.05.002 · Cited by 109
“Multiple studies have shown differences in the proportions of immune cell populations in the peripheral blood of COVID-19 patients compared with healthy individuals, in particular a marked lymphopenia that is accompanied by changes to the lymphocyte activation and exhaustion phenotypes, some of which are partly associ…”
Age-severity matched cytokine profiling reveals specific signatures in Covid-19 patients
Angioni, R., Sánchez‐Rodríguez, R., Munari, F., Bertoldi, N., Arcidiacono, D., Cavinato, S., Marturano, D., Zaramella, A., Realdon, S., Cattelan, A. M., et al. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-03151-z · Cited by 101
The immunology of SARS-CoV-2 infections and vaccines
Grigoryan, L., & Pulendran, B. (2020) · Seminars in Immunology · doi:10.1016/j.smim.2020.101422 · Cited by 102
Zhang, Y.-Y., Li, B.-R., & Ning, B. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.02033 · Cited by 103
Calming the Storm: Natural Immunosuppressants as Adjuvants to Target the Cytokine Storm in COVID-19
Peter, A. E., Sandeep, B. V., Rao, B. G., & Kalpana, V. L. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.583777 · Cited by 106
Parallels in Sepsis and COVID-19 Conditions: Implications for Managing Severe COVID-19
Olwal, C. O., Nganyewo, N. N., Tapela, K., Zune, A. L. D., Owoicho, O., Bediako, Y., & Duodu, S. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.602848 · Cited by 97
“Increased T lymphopenia, particularly CD4+ and CD8+ T cells have been shown to decrease markedly in COVID-19 patients, implying damage of lymphocytes by the SARS-CoV-2 virus (13, 20, 21).”
BackgroundObesity and its impact on COVID-19
de Leeuw, A. J. M., Luttikhuis, M. A. M. O., Wellen, A. C., Müller, C., & Calkhoven, C. F. (2021) · Journal of Molecular Medicine · doi:10.1007/s00109-021-02072-4 · Cited by 115
Early Differences in Cytokine Production by Severity of Coronavirus Disease 2019
Tjan, L. H., Furukawa, K., Nagano, T., Kiriu, T., Nishimura, M., Arii, J., Hino, Y., Iwata, S., Nishimura, Y., & Mori, Y. (2021) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiab005 · Cited by 96
“Interestingly, several studies showed that the numbers of peripheral NK cells were significantly lower in patients with severe COVID-19 than in healthy individuals [2, 8] or patients with mild COVID-19 [2].”
BackgroundResultNKG2A and COVID-19: another brick in the wall
Antonioli, L., Fornai, M., Pellegrini, C., & Blandizzi, C. (2020) · Cellular and Molecular Immunology · doi:10.1038/s41423-020-0450-7 · Cited by 97
“expression was markedly reduced.(14) These findings allow to hypothesize that the functional exhaustion of cytotoxic lymphocytes associated with COVID-19 infection breaks down the antiviral immunity, and that the enhanced expression of NKG2A, as specifically observed in CD8 and NK cells, could contribute to the mainte…”
BackgroundResultMorris, G., Bortolasci, C. C., Puri, B. K., Marx, W., O'Neil, A. E., Athan, E., Walder, K. R., Berk, M., OLIVE, L. S., Carvalho, A. F., et al. (2021) · Cytokine · doi:10.1016/j.cyto.2021.155593 · Cited by 101
Gagiannis, D., Steinestel, J., Hackenbroch, C., Schreiner, B., Hannemann, M., Bloch, W., Umathum, V. G., Gebauer, N., Rother, C., Stahl, M., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.587517 · Cited by 101
“Coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has caused or contributed to hundreds of thousands of deaths and led to almost complete shutdown of social and economic life in many countries (1).”
BackgroundXu, R., Zhou, Y., Cai, L., Wang, L., Han, J.-B., Yang, X., Chen, J., Chen, J., Ma, C., & Shen, L.-L. (2020) · British Journal of Dermatology · doi:10.1111/bjd.19484 · Cited by 95
Notz, Q., Schmalzing, M., Wedekink, F., Schlesinger, T., Gernert, M., Herrmann, J., Sorger, L., Weismann, D., Schmid, B., Sitter, M., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.581338 · Cited by 98
“Exhaustion of NK cells and CD8+ T cells has been previously described in COVID-19 and was associated with reduced CD107a degranulation and granzyme B production (34).”
BackgroundNazerian, Y., Ghasemi, M., Yassaghi, Y., Nazerian, A., & Hashemi, S. M. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.109428 · Cited by 96
“significantly higher in COVID-19 patients, especially in severe conditions [38-40].”
BackgroundCOVID‐19: Current knowledge in clinical features, immunological responses, and vaccine development
Singh, R., Kang, A., Luo, X., Jeyanathan, M., Gillgrass, A. E., Afkhami, S., & Xing, Z. (2021) · The FASEB Journal · doi:10.1096/fj.202002662r · Cited by 101
Helal, M. A., Shouman, S., Abdelwaly, A., Elmehrath, A. O., Essawy, M., Sayed, S. M., Saleh, A. H., & El‐Badri, N. (2020) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2020.1822208 · Cited by 96
“, 2020), especially in the CD8þ, CD4þ, and CD3þ T lymphocyte populations (Zeng, 2020; Zheng et al., 2020).”
BackgroundImmunobiology and immunotherapy of COVID‐19: A clinically updated overview
Esmaeilzadeh, A., & Elahi, R. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.30076 · Cited by 94
“The upregulated expression of NKG2A reduces the production of proinflammatory cytokine by NK cells and T lymphocytes (Zheng et al., 2020).”
BackgroundThe Effects of COVID-19 on the Placenta During Pregnancy
Sadeghirad, H., Röhl, J., Stylianou, N., Allenby, M. C., Bazaz, S. R., Warkiani, M. E., Souza-Fonseca-Guimarães, F., Clifton, V. L., & Kulasinghe, A. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.743022 · Cited by 94
Metadata
- Authors
- Zheng, M., Gao, Y., Wang, G., Song, G., Liu, S., Sun, D., Xu, Y., & Tian, Z.
- Affiliations
- First Affiliated Hospital of Anhui Medical University (CN)
- Anhui Medical University (CN)
- University of Science and Technology of China (CN)
- Corresponding author
- Zheng, Meijuan
- Xu, Yuanhong
- Tian, Zhigang
- Venue
- Cellular & Molecular Immunology
- Published
- 2020-03-19
- Volume
- 17
- Issue
- 5
- Pages
- 533-535
- ISSN
- 1672-7681 (ISSN-L)
- 2042-0226
- PMC
- PMC7091858
- OpenAlex
- W3011508332
- Cited by
- 1,768
- References
- 11
- Citations by year
- 2026: 26 · 2025: 63 · 2024: 119 · 2023: 186 · 2022: 329 · 2021: 514 · 2020: 531
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Cellular and Molecular Immunology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (81788101, 81771685)
- Chinese Academy of Sciences (XDB29030000, 81788101)
- Anhui Medical University (YJGG202002)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- COVID-19 pandemic, SARS-CoV-2, T cell exhaustion, T cell dysfunction
- MeSH terms
- Betacoronavirus, COVID-19, SARS-CoV-2, Antiviral Agents, Hepatitis C, Humans, Killer Cells, Natural, Pneumonia, Viral, Coronavirus Infections, Pandemics
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