The DOI matches its Crossref record; 50 of the 50 references it cites were found in a registry or an index.
Middle East Respiratory Syndrome Coronavirus Efficiently Infects Human Primary T Lymphocytes and Activates the Extrinsic and Intrinsic Apoptosis Pathways
Open accessAbstract
Middle East respiratory syndrome (MERS) is associated with a mortality rate of >35%. We previously showed that MERS coronavirus (MERS-CoV) could infect human macrophages and dendritic cells and induce cytokine dysregulation. Here, we further investigated the interplay between human primary T cells and MERS-CoV in disease pathogenesis. Importantly, our results suggested that MERS-CoV efficiently infected T cells from the peripheral blood and from human lymphoid organs, including the spleen and the tonsil. We further demonstrated that MERS-CoV infection induced apoptosis in T cells, which involved the activation of both the extrinsic and intrinsic apoptosis pathways. Remarkably, immunostaining of spleen sections from MERS-CoV-infected common marmosets demonstrated the presence of viral nucleoprotein in their CD3(+) T cells. Overall, our results suggested that the unusual capacity of MERS-CoV to infect T cells and induce apoptosis might partly contribute to the high pathogenicity of the virus.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Infection of EC through infected PBMC has been documented for members of several virus families, including bunya, herpes, filo, flavi, toga, and arena viruses (Charrel and de Lamballerie, 2010; Chu et al., 2016; Gowen and Hickerson, 2017; Kunz and de la Torre, 2017; Ma et al., 2013; Mackow and Gavrilovskaya, 2009).”
From Equid Herpesvirus-1 Exploits the Extracellular Matrix of Mononuclear Cells to Ensure Transport to Target Cells (2020) · cites this paper as Chu et al., 2016
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
1 retracted
Siu, K., Yeung, M. L., Kok, K., Yuen, K., Kew, C., Lui, P., Chan, C., Tse, H., Woo, P. C. Y., Yuen, K., et al. (2014) · Journal of Virology · doi:10.1128/jvi.03649-13 · Cited by 179
Self-citationRetractedApoptosis: A Review of Programmed Cell Death
Elmore, S. (2007) · Toxicologic Pathology · doi:10.1080/01926230701320337 · Cited by 13,853
Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation.
Gavrieli, Y., Sherman, Y., & Ben-Sasson, S. A. (1992) · The Journal of cell biology · doi:10.1083/jcb.119.3.493 · Cited by 9,444
Isolation of a Novel Coronavirus from a Man with Pneumonia in Saudi Arabia
Zaki, A. M., van Boheemen, S., Bestebroer, T. M., Osterhaus, A. D. M. E., & Fouchier, R. A. M. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1211721 · Cited by 5,677
Identification of a novel coronavirus in patients with severe acute respiratory syndrome
Drosten, C., Günther, S., Preiser, W., van der Werf, S., Brodt, H.-R., Becker, S., Rabenau, H., Panning, M., Kolesnikova, L., Fouchier, R. A. M., et al. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa030747 · Cited by 4,574
Coronavirus as a possible cause of severe acute respiratory syndrome
Peiris, M. J. S., Lai, S., Poon, L. L. M., Guan, Y., Yam, L., Lim, W., Nicholls, J. M., Yee, W., Yan, W., Cheung, M., et al. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13077-2 · Cited by 2,916
Self-citationDipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC
Raj, V. S., Mou, H., Smits, S. L., Dekkers, D. H. W., Müller, M. A., Dijkman, R., Muth, D., Demmers, J. A. A., Zaki, A., Fouchier, R. A. M., et al. (2013) · Nature · doi:10.1038/nature12005 · Cited by 2,061
Assiri, A., Al-Tawfiq, J. A., Al-Rabeeah, A. A., Al-Rabiah, F. A., Al-Hajjar, S., Al-Barrak, A., Flemban, H., Al-Nassir, W. N., Balkhy, H. H., Al-Hakeem, R. F., et al. (2013) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(13)70204-4 · Cited by 1,435
Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection
Doitsh, G., Galloway, N. L. K., Geng, X., Yang, Z., Monroe, K. M., Zepeda, O., Hunt, P. W., Hatano, H., Sowinski, S., Muñoz-Arias, I., et al. (2013) · Nature · doi:10.1038/nature12940 · Cited by 1,216
Severe acute respiratory syndrome coronavirus as an agent of emerging and reemerging infection
Cheng, V. C. C., Lau, S. K. P., Woo, P. C. Y., & Yuen, K. Y. (2007) · Clinical Microbiology Reviews · doi:10.1128/cmr.00023-07 · Cited by 1,192
Self-citationSlee, E. A., Adrain, C., & Martin, S. J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m008363200 · Cited by 1,118
Chan, J. F., Lau, S. K. P., To, K. K., Cheng, V. C., Woo, P. C. Y., & Yuen, K. (2015) · Clinical Microbiology Reviews · doi:10.1128/cmr.00102-14 · Cited by 894
Self-citationInterspecies transmission and emergence of novel viruses: lessons from bats and birds
Chan, J. F., To, K. K., Tse, H., Jin, D., & Yuen, K. (2013) · Trends in Microbiology · doi:10.1016/j.tim.2013.05.005 · Cited by 609
Self-citationChan, J. F., Yao, Y., Yeung, M. L., Deng, W., Bao, L., Jia, L., Li, F., Xiao, C., Gao, H., Yü, P., et al. (2015) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiv392 · Cited by 607
Self-citationBermingham, A., Chand, M. A., Brown, C. S., Aarons, E., Tong, C. Y. W., Langrish, C., Höschler, K., Brown, K. E., Galiano, M., Myers, R. E., et al. (2012) · Eurosurveillance · doi:10.2807/ese.17.40.20290-en · Cited by 468
Rapid generation of a mouse model for Middle East respiratory syndrome
Zhao, J., Li, K., Wohlford-Lenane, C., Agnihothram, S., Fett, C., Zhao, J., Gale, M., Baric, R. S., Enjuanes, L., Gallagher, T., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1323279111 · Cited by 453
Zhou, J., Chu, H., Li, C., Wong, B. H., Cheng, Z., Poon, V. K., Sun, T., Lau, C. C.-Y., Wong, K. K. Y., Chan, J. Y. W., et al. (2013) · The Journal of Infectious Diseases · doi:10.1093/infdis/jit504 · Cited by 425
Self-citationLau, S. K. P., Lau, C. C. Y., Chan, K., Li, C. P. Y., Chen, H., Jin, D., Chan, J. F., Woo, P. C. Y., & Yuen, K. (2013) · Journal of General Virology · doi:10.1099/vir.0.055533-0 · Cited by 392
Self-citationBroad-spectrum antivirals for the emerging Middle East respiratory syndrome coronavirus
Chan, J. F., Chan, K., Kao, R. Y. T., To, K. K., Zheng, B.-J., Li, C. P. Y., Li, P. T. W., Dai, J., Mok, F. K. Y., Chen, H., et al. (2013) · Journal of Infection · doi:10.1016/j.jinf.2013.09.029 · Cited by 385
Self-citationde Wilde, A. H., Raj, V. S., Oudshoorn, D., Bestebroer, T. M., van Nieuwkoop, S., Limpens, R. W. A. L., Posthuma, C. C., van der Meer, Y., Bárcena, M., Haagmans, B. L., et al. (2013) · Journal of General Virology · doi:10.1099/vir.0.052910-0 · Cited by 343
Zhao, J., Zhao, J., & Perlman, S. (2010) · Journal of Virology · doi:10.1128/jvi.01049-10 · Cited by 340
de Wit, E., Rasmussen, A. L., Falzarano, D., Bushmaker, T., Feldmann, F., Brining, D. L., Fischer, E. R., Martellaro, C., Okumura, A., Chang, J., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310744110 · Cited by 308
Alabdallat, M., Payne, D. C., Alqasrawi, S., Rha, B., Tohme, R. A., Abedi, G. R., Nsour, M. A., Iblan, I., Jarour, N., Farag, N. H., et al. (2014) · Clinical Infectious Diseases · doi:10.1093/cid/ciu359 · Cited by 308
Menachery, V. D., Eisfeld, A. J., Schäfer, A., Josset, L., Sims, A. M., Proll, S. C., Fan, S., Li, C., Neumann, G., Tilton, S. C., et al. (2014) · mBio · doi:10.1128/mbio.01174-14 · Cited by 307
Self-citationJosset, L., Menachery, V. D., Gralinski, L. E., Agnihothram, S., Sova, P., Carter, V. S., Yount, B. L., Graham, R. L., Baric, R. S., & Katze, M. G. (2013) · mBio · doi:10.1128/mbio.00165-13 · Cited by 299
Replication and Shedding of MERS-CoV in Upper Respiratory Tract of Inoculated Dromedary Camels
Adney, D. R., van Doremalen, N., Brown, V. R., Bushmaker, T., Scott, D. P., de Wit, E., Bowen, R. A., & Munster, V. J. (2014) · Emerging infectious diseases · doi:10.3201/eid2012.141280 · Cited by 285
Yang, Y., Zhang, L., Geng, H., Deng, Y. L., Huang, B., Yin, G., Zhao, Z., & Tan, W. (2013) · Protein & Cell · doi:10.1007/s13238-013-3096-8 · Cited by 273
He, Z., Zhao, C., Dong, Q., Zhuang, H., Song, S., Peng, G., & Dwyer, D. E. (2005) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2004.07.014 · Cited by 260
Distinct Immune Response in Two MERS-CoV-Infected Patients: Can We Go from Bench to Bedside?
Faure, E., Poissy, J., Goffard, A., Fournier, C., Kipnis, É., Titécat, M., Bortolotti, P., Martinez, L., Dubucquoi, S., Dessein, R., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088716 · Cited by 249
Chan, J. F., Chan, K., Choi, G. K.-Y., To, K. K., Tse, H., Cai, J., Yeung, M. L., Cheng, V. C., Chen, H., Che, X.-Y., et al. (2013) · The Journal of Infectious Diseases · doi:10.1093/infdis/jit123 · Cited by 219
Self-citationInfection with MERS-CoV Causes Lethal Pneumonia in the Common Marmoset
Falzarano, D., de Wit, E., Feldmann, F., Rasmussen, A. L., Okumura, A., Peng, X., Thomas, M. J., van Doremalen, N., Haddock, E., Nagy, L., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004250 · Cited by 209
Müller, M. A., Raj, V. S., Muth, D., Meyer, B., Kallies, S., Smits, S. L., Wollny, R., Bestebroer, T. M., Specht, S., Suliman, T., et al. (2012) · mBio · doi:10.1128/mbio.00515-12 · Cited by 209
Coassociation of CD26 (dipeptidyl peptidase IV) with CD45 on the surface of human T lymphocytes
Torimoto, Y., Dang, N. H., Vivier, É., Tanaka, T., Schlossman, S. F., & Morimoto, C. (1991) · The Journal of Immunology · doi:10.4049/jimmunol.147.8.2514 · Cited by 206
Middle East Respiratory Syndrome Coronavirus Accessory Protein 4a Is a Type I Interferon Antagonist
Niemeyer, D., Zillinger, T., Muth, D., Zielecki, F., Horvath, G. L., Suliman, T., Barchet, W., Weber, F., Drosten, C., & Müller, M. A. (2013) · Journal of Virology · doi:10.1128/jvi.01845-13 · Cited by 190
Chu, H., Zhou, J., Wong, B. H., Li, C., Cheng, Z., Lin, X., Poon, V. K., Sun, T., Lau, C. C.-Y., Chan, J. F., et al. (2014) · Virology · doi:10.1016/j.virol.2014.02.018 · Cited by 180
Self-citationThe costimulatory activity of the CD26 antigen requires dipeptidyl peptidase IV enzymatic activity.
Tanaka, T., Kameoka, J., Yaron, A., Schlossman, S. F., & Morimoto, C. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.10.4586 · Cited by 176
Ishii, T., Ohnuma, K., Murakami, A., Takasawa, N., Kobayashi, S., Dang, N. H., Schlossman, S. F., & Morimoto, C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.211439098 · Cited by 172
Chan, J. F., Li, K. S. M., To, K. K., Cheng, V. C., Chen, H., & Yuen, K. (2012) · Journal of Infection · doi:10.1016/j.jinf.2012.10.002 · Cited by 162
Self-citationYang, X., Chen, X., Bian, G., Tu, J., Xing, Y., Wang, Y., & Chen, Z. (2013) · Journal of General Virology · doi:10.1099/vir.0.059014-0 · Cited by 155
Zhao, J., Zhao, J., van Rooijen, N., & Perlman, S. M. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000636 · Cited by 151
Che, X.-Y., Qiu, L., Pan, Y.-X., Wen, K., Hao, W., Zhang, L.-Y., Wang, Y.-D., Liao, Z.-Y., Xu, H., Cheng, V. C., et al. (2004) · Journal of Clinical Microbiology · doi:10.1128/jcm.42.6.2629-2635.2004 · Cited by 128
Self-citationDetection of SARS Coronavirus in Plasma by Real-Time RT-PCR
Grant, P. R., Garson, J. A., Tedder, R. S., Chan, P. K. S., Tam, J. S., & Sung, J. J. �. (2003) · New England Journal of Medicine · doi:10.1056/nejm200312183492522 · Cited by 126
An Animal Model of MERS Produced by Infection of Rhesus Macaques With MERS Coronavirus
Yao, Y., Bao, L., Deng, W., Xu, L., Li, F., Lv, Q., Yü, P., Chen, T., Xu, Y., Zhu, H., et al. (2013) · The Journal of Infectious Diseases · doi:10.1093/infdis/jit590 · Cited by 125
Self-citationEckerle, I., Müller, M. A., Kallies, S., Gotthardt, D. N., & Drosten, C. (2013) · Virology Journal · doi:10.1186/1743-422x-10-359 · Cited by 118
Chan, J. F., Choi, G. K.-Y., Tsang, A. K. L., Tee, K., Lam, H., Yip, C. C., To, K. K., Cheng, V. C., Yeung, M. L., Lau, S. K. P., et al. (2015) · Journal of Clinical Microbiology · doi:10.1128/jcm.01224-15 · Cited by 89
Self-citationChu, H., Wang, J.-J., Qi, M., Yoon, J.-J., Chen, X., Wen, X., Hammonds, J. E., Ding, L., & Spearman, P. W. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.07.011 · Cited by 85
Self-citationKinetics and pattern of viral excretion in biological specimens of two MERS-CoV cases
Poissy, J., Goffard, A., Parmentier-Decrucq, E., Favory, R., Kauv, M., Kipnis, É., Mathieu, D., & Guery, B. P. (2014) · Journal of Clinical Virology · doi:10.1016/j.jcv.2014.07.002 · Cited by 82
Kapoor, M., Pringle, K. D., Kumar, A., Dearth, S. M., Liu, L., Lovchik, J. C., Perez, O., Pontones, P., Richards, S. M., Yeadon-Fagbohun, J., et al. (2014) · Clinical Infectious Diseases · doi:10.1093/cid/ciu635 · Cited by 77
Kraaij‐Dirkzwager, M., Timen, A., Dirksen, K., Gelinck, L. B. S., Leyten, E. M. S., Groeneveld, P. H. P., Jansen, C. L., Jonges, M., Raj, V. S., Thurkow, I., et al. (2014) · Eurosurveillance · doi:10.2807/1560-7917.es2014.19.21.20817 · Cited by 75
Tao, X., Hill, T. E., Morimoto, C., Peters, C. J., Ksiazek, T. G., & Tseng, C.-T. K. (2013) · Journal of Virology · doi:10.1128/jvi.01562-13 · Cited by 73
Cited by
Sorted by citations
Yang, X., Yu, Y., Xu, J., Shu, H., Xia, J., Liu, H., Wu, Y., Zhang, L., Yu, Z., Fang, M., et al. (2020) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(20)30079-5 · Cited by 10,066
Clinical and immunological features of severe and moderate coronavirus disease 2019
Chen, G., Wu, D., Guo, W., Cao, Y., Huang, D., Wang, H., Wang, T., Zhang, X., Chen, H., Yu, H., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci137244 · Cited by 4,750
Extrapulmonary manifestations of COVID-19
Gupta, A., Madhavan, M. V., Sehgal, K., Nair, N., Mahajan, S., Sehrawat, T. S., Bikdeli, B., Ahluwalia, N., Ausiello, J. C., Wan, E. Y., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-0968-3 · Cited by 3,185
Channappanavar, R., & Perlman, S. (2017) · Seminars in Immunopathology · doi:10.1007/s00281-017-0629-x · Cited by 2,524
Cytokine release syndrome in severe COVID-19
Moore, J. B., & June, C. H. (2020) · Science · doi:10.1126/science.abb8925 · Cited by 1,912
Metadata
- Authors
- Chu, H., Zhou, J., Wong, B. H.-Y., Li, C., Chan, J. F.-W., Cheng, Z.-S., Yang, D., Wang, D., Lee, A. C.-Y., Li, C., Yeung, M.-L., Cai, J.-P., Chan, I. H.-Y., Ho, W.-K., To, K. K.-W., Zheng, B.-J., Yao, Y., Qin, C., & Yuen, K.-Y.
- Affiliations
- University of Hong Kong (HK)
- Chinese Academy of Medical Sciences & Peking Union Medical College (CN)
- Zhejiang University (CN)
- Corresponding author
- Chu, Hin
- ORCID
- Venue
- Journal of Infectious Diseases
- Publisher
- Oxford University Press (OUP)
- Published
- 2015-07-22
- Volume
- 213
- Issue
- 6
- Pages
- 904-914
- ISSN
- 0022-1899 (ISSN-L)
- 1537-6613
- PMC
- PMC7107330
- OpenAlex
- W1947409115
- Cited by
- 448
- References
- 50
- Citations by year
- 2026: 4 · 2025: 16 · 2024: 19 · 2023: 22 · 2022: 50 · 2021: 117 · 2020: 149 · 2019: 14 · 2018: 15 · 2017: 12 · 2016: 14 · 2015: 4
- FWCI
- 11.68
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Infectious Diseases (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- The HKU Scholars Hub (University of Hong Kong) (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Research Grants Council of the Hong Kong Special Administrative Region (T11/707/15)
- Providence Foundation Limited
- University of Hong Kong Small Project Funding (201409176024)
- Hong Kong Health and Medical Research Fund (14131392)
- Hong Kong Research Grants Council (N_HKU728/14)
- National Science and Technology Major Projects of Infectious Disease (2012ZX10004501-004)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Health Sciences › Medicine › Infectious Diseases › Viral Infections and Outbreaks Research
- Keywords
- MERS-CoV, T cells, T cell infection, apoptosis, extrinsic apoptotic pathway, mitochondrial apoptosis, spleen, tonsil, marmoset, viral pathogenicity, lymphoid organs
- MeSH terms
- Animals, Antibodies, Viral, Callithrix, Cells, Cultured, Gene Expression Regulation, Humans, Spleen, T-Lymphocytes, Palatine Tonsil, Apoptosis, Dipeptidyl Peptidase 4, Severe acute respiratory syndrome-related coronavirus, Middle East Respiratory Syndrome Coronavirus
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review