Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC
Open accessAbstract
Most human coronaviruses cause mild upper respiratory tract disease but may be associated with more severe pulmonary disease in immunocompromised individuals. However, SARS coronavirus caused severe lower respiratory disease with nearly 10% mortality and evidence of systemic spread. Recently, another coronavirus (human coronavirus-Erasmus Medical Center (hCoV-EMC)) was identified in patients with severe and sometimes lethal lower respiratory tract infection. Viral genome analysis revealed close relatedness to coronaviruses found in bats. Here we identify dipeptidyl peptidase 4 (DPP4; also known as CD26) as a functional receptor for hCoV-EMC. DPP4 specifically co-purified with the receptor-binding S1 domain of the hCoV-EMC spike protein from lysates of susceptible Huh-7 cells. Antibodies directed against DPP4 inhibited hCoV-EMC infection of primary human bronchial epithelial cells and Huh-7 cells. Expression of human and bat (Pipistrellus pipistrellus) DPP4 in non-susceptible COS-7 cells enabled infection by hCoV-EMC. The use of the evolutionarily conserved DPP4 protein from different species as a functional receptor provides clues about the host range potential of hCoV-EMC. In addition, it will contribute critically to our understanding of the pathogenesis and epidemiology of this emerging human coronavirus, and may facilitate the development of intervention strategies.
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
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?
Preclinical studies showed that GLP-1 receptor agonists reduce cytokine production, attenuate pulmonary inflammation and preserve lung function in rats and mice with experimental lung injury.
“Preclinical studies showed that GLP-1RAs reduce cytokine production, attenuate pulmonary inflammation and preserve lung function in rats and mice with experimental lung injury [8, 32].”
From GLP-1 receptor agonists and renal outcomes in patients with diabetes mellitus type 2 and diabetic kidney disease: state of the art (2022) · cites this paper as [32]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus
Li, W., Moore, M. J., Vasilieva, N., Sui, J., Wong, S. K., Berne, M. A., Somasundaran, M., Sullivan, J. L., Luzuriaga, K., Greenough, T. C., et al. (2003) · Nature · doi:10.1038/nature02145 · Cited by 5,923 · see citing works
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 · see citing works
Self-citationA crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus–induced lung injury
Kuba, K., Imai, Y., Rao, S., Gao, H., Guo, F., Guan, B., Huan, Y., Yang, P., Zhang, Y., Deng, W., et al. (2005) · Nature Medicine · doi:10.1038/nm1267 · Cited by 3,445 · see citing works
Bats Are Natural Reservoirs of SARS-Like Coronaviruses
Li, W., Shi, Z., Yu, M., Ren, W., Smith, C. S., Epstein, J. H., Wang, H., Crameri, G. S., Hú, Z., Zhang, H., et al. (2005) · Science · doi:10.1126/science.1118391 · Cited by 2,571 · see citing works
Angiotensin-converting enzyme 2 protects from severe acute lung failure
Imai, Y., Kuba, K., Rao, S., Huan, Y., Guo, F., Guan, B., Yang, P., Sarao, R., Wada, T., Leong-Poi, H., et al. (2005) · Nature · doi:10.1038/nature03712 · Cited by 2,453 · see citing works
Structure of SARS Coronavirus Spike Receptor-Binding Domain Complexed with Receptor
Li, F., Li, W., Farzan, M., & Harrison, S. C. (2005) · Science · doi:10.1126/science.1116480 · Cited by 2,031 · see citing works
Coronavirus Pathogenesis and the Emerging Pathogen Severe Acute Respiratory Syndrome Coronavirus
Weiss, S. R., & Navas-Martin, S. (2005) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.69.4.635-664.2005 · Cited by 1,256 · see citing works
Severe acute respiratory syndrome
Peiris, M. J. S., Guan, Y., & Yuen, K. (2004) · Nature Medicine · doi:10.1038/nm1143 · Cited by 1,135 · see citing works
Lambeir, A.-M., Durinx, C., Scharpé, S., & De Meester, I. (2003) · Critical Reviews in Clinical Laboratory Sciences · doi:10.1080/713609354 · Cited by 955 · see citing works
Human aminopeptidase N is a receptor for human coronavirus 229E
Yeager, C. L., Ashmun, R. A., Williams, R. K., Cardellichio, C. B., Shapiro, L. H., Look, A. T., & Holmes, K. V. (1992) · Nature · doi:10.1038/357420a0 · Cited by 941 · see citing works
van Boheemen, S., de Graaf, M., Lauber, C., Bestebroer, T. M., Raj, V. S., Zaki, A. M., Osterhaus, A. D. M. E., Haagmans, B. L., Gorbalenya, A. E., Snijder, E. J., et al. (2012) · mBio · doi:10.1128/mbio.00473-12 · Cited by 911 · see citing works
Self-citationGraham, R. L., & Baric, R. S. (2009) · Journal of Virology · doi:10.1128/jvi.01394-09 · Cited by 738 · see citing works
Aminopeptidase N is a major receptor for the enteropathogenic coronavirus TGEV
Delmas, B., Gelfi, J., L'Haridon, R., Vogel, L. K., Sjöström, H., Norén, & Laude, H. (1992) · Nature · doi:10.1038/357417a0 · Cited by 632 · see citing works
An Oct4-Centered Protein Interaction Network in Embryonic Stem Cells
van den Berg, D. L. C., Snoek, T., Mullin, N. P., Yates, A., Bezstarosti, K., Demmers, J., Chambers, I., & Poot, R. A. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.02.014 · Cited by 542 · see citing works
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 · see citing works
Self-citationWilliams, R. K., Jiang, G. S., & Holmes, K. V. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.13.5533 · Cited by 406 · see citing works
Drexler, J. F., Gloza‐Rausch, F., Glende, J., Corman, V. M., Muth, D., Göttsche, M., Seebens-Hoyer, A., Niedrig, M., Pfefferle, S., Yordanov, S., et al. (2010) · Journal of Virology · doi:10.1128/jvi.00650-10 · Cited by 393 · see citing works
Self-citationThe multifunctional or moonlighting protein CD26/DPPIV
Boonacker, E., & Noorden, C. J. F. V. (2003) · European Journal of Cell Biology · doi:10.1078/0171-9335-00302 · Cited by 337 · see citing works
Evidence Supporting a Zoonotic Origin of Human Coronavirus Strain NL63
Huynh, J., Li, S. R., Yount, B. L., Smith, A., Sturges, L., Olsen, J. C., Nagel, J. J., Johnson, J. B., Agnihothram, S., Gates, J. E., et al. (2012) · Journal of Virology · doi:10.1128/jvi.00906-12 · Cited by 288 · see citing works
Mechanisms of Host Receptor Adaptation by Severe Acute Respiratory Syndrome Coronavirus
Wu, K., Peng, G., Wilken, M. S., Geraghty, R. J., & Li, F. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.325803 · Cited by 246 · see citing works
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 206 · see citing works
Self-citationDijkman, R., Jebbink, M. F., Koekkoek, S. M., Deijs, M., Jónsdóttir, H. R., Molenkamp, R., Ieven, M. M., Goossens, H., Thiel, V., & van der Hoek, L. (2013) · Journal of Virology · doi:10.1128/jvi.03368-12 · Cited by 155 · see citing works
Self-citationSchultze, B., & Herrler, G. (1992) · Journal of General Virology · doi:10.1099/0022-1317-73-4-901 · Cited by 119 · see citing works
SARS-CoV replication and pathogenesis in an in vitro model of the human conducting airway epithelium
Sims, A. M., Burkett, S. E., Yount, B. L., & Pickles, R. J. (2007) · Virus Research · doi:10.1016/j.virusres.2007.03.013 · Cited by 118 · see citing works
Bosch, B., Bodewes, R., de Vries, R. P., Kreijtz, J. H. C. M., Bartelink, W., van Amerongen, G., Rimmelzwaan, G. F., de Haan, C. A. M., Osterhaus, A. D. M. E., & Rottier, P. J. M. (2010) · Journal of Virology · doi:10.1128/jvi.01035-10 · Cited by 115 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Hoffmann, M., Kleine-Weber, H., Schroeder, S., Krüger, N., Herrler, T., Erichsen, S., Schiergens, T. S., Herrler, G., Wu, N.-H., Nitsche, A., et al. (2020) · Cell · doi:10.1016/j.cell.2020.02.052 · Cited by 20,286 · see citing works
Self-citationStructure, function and antigenicity of the SARS-CoV-2 spike glycoprotein
Walls, A. C., Park, Y.-J., Tortorici, M. A., Wall, A., McGuire, A. T., & Veesler, D. (2020) · doi:10.1101/2020.02.19.956581 · Cited by 8,586 · see citing works
Origin and evolution of pathogenic coronaviruses
Cui, J., Li, F., & Shi, Z. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0118-9 · Cited by 5,543 · see citing works
Wan, Y., Shang, J., Graham, R., Baric, R. S., & Li, F. (2020) · Journal of Virology · doi:10.1128/jvi.00127-20 · Cited by 4,341 · see citing works
“3C), and yet they recognize the same 124 receptor dipeptidyl peptidase 4 (DPP4) (27, 28).”
BackgroundCoronaviruses: An Overview of Their Replication and Pathogenesis
Fehr, A. R., & Perlman, S. M. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2438-7_1 · Cited by 3,784 · see citing works
COVID-19 infection: Emergence, transmission, and characteristics of human coronaviruses
Shereen, M. A., Khan, S., Kazmi, A., Bashir, N., & Siddique, R. (2020) · Journal of Advanced Research · doi:10.1016/j.jare.2020.03.005 · Cited by 3,591 · see citing works
SARS and MERS: recent insights into emerging coronaviruses
de Wit, E., van Doremalen, N., Falzarano, D., & Munster, V. J. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.81 · Cited by 3,510 · see citing works
Letko, M., Marzi, A., & Munster, V. (2020) · Nature Microbiology · doi:10.1038/s41564-020-0688-y · Cited by 3,109 · see citing works
Ou, X., Liu, Y., Lei, X., Li, P., Mi, D., Ren, L., Guo, L., Guo, R., Chen, T., Hu, J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15562-9 · Cited by 3,097 · see citing works
Mechanisms of SARS-CoV-2 entry into cells
Jackson, C. B., Farzan, M., Chen, B., & Choe, H. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00418-x · Cited by 3,082 · see citing works
Structural and Functional Basis of SARS-CoV-2 Entry by Using Human ACE2
Wang, Q., Zhang, Y., Wu, L., Niu, S., Song, C., Zhang, Z., Lu, G., Qiao, C., Hu, Y., Yuen, K.-Y., et al. (2020) · Cell · doi:10.1016/j.cell.2020.03.045 · Cited by 2,892 · see citing works
“In light of the determinant role of SARS-RBD and MERS-RBD in receptor recognition (Li et al., 2003, 2005; Lu et al., 2013; Raj et al., 2013), the majority of neutralizing antibodies have been shown to target the RBD, exerting neutralization activity by disrupting virus/receptor engagement (Du et al.”
Structure, Function, and Evolution of Coronavirus Spike Proteins
Li, F. (2016) · Annual Review of Virology · doi:10.1146/annurev-virology-110615-042301 · Cited by 2,740 · see citing works
HCA Lung Biological Network, Sungnak, W., Huang, N., Bécavin, C., Berg, M., Queen, R., Litvinukova, M., Talavera-López, C., Maatz, H., Reichart, D., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-0868-6 · Cited by 2,501 · see citing works
Xu, X., Chen, P., Wang, J., Feng, J., Zhou, H., Li, X., Zhong, W., & Hao, P. (2020) · Science China Life Sciences · doi:10.1007/s11427-020-1637-5 · Cited by 2,202 · see citing works
Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor
Ge, X.-Y., Li, J.-L., Yang, X.-L., Chmura, A. A., Zhu, G., Epstein, J. H., Mazet, J. K., Hu, B., Zhang, W., Peng, C., et al. (2013) · Nature · doi:10.1038/nature12711 · Cited by 1,778 · see citing works
Molecular immune pathogenesis and diagnosis of COVID-19
Li, X., Geng, M., Peng, Y., Meng, L., & Lu, S. (2020) · Journal of Pharmaceutical Analysis · doi:10.1016/j.jpha.2020.03.001 · Cited by 1,723 · see citing works
Coronaviruses — drug discovery and therapeutic options
Zumla, A. I., Chan, J. F., Azhar, E. I., Hui, D. S. C., & Yuen, K. (2016) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2015.37 · Cited by 1,689 · see citing works
Tai, W., He, L., Zhang, X., Pu, J., Voronin, D., Jiang, S., Zhou, Y., & Du, L. (2020) · Cellular & Molecular Immunology · doi:10.1038/s41423-020-0400-4 · Cited by 1,654 · see citing works
Okba, N. M. A., Müller, M. A., Li, W., Wang, C., GeurtsvanKessel, C. H., Corman, V. M., Lamers, M. M., Sikkema, R. S., de Bruin, E., Chandler, F. D., et al. (2020) · Emerging Infectious Diseases · doi:10.3201/eid2607.200841 · Cited by 1,614 · see citing works
Self-citationGuzik, T. J., MOHIDDIN, S. A., Dimarco, A. D., Patel, V., Savvatis, K., Marelli‐Berg, F. M., Madhur, M. S., Tomaszewski, M., Maffia, P., D’Acquisto, F., et al. (2020) · Cardiovascular Research · doi:10.1093/cvr/cvaa106 · Cited by 1,451 · see citing works
Middle East respiratory syndrome
Zumla, A. I., Hui, D. S. C., & Perlman, S. M. (2015) · The Lancet · doi:10.1016/s0140-6736(15)60454-8 · Cited by 1,281 · see citing works
From SARS to MERS, Thrusting Coronaviruses into the Spotlight
Song, Z., Xu, Y., Bao, L., Zhang, L., Yü, P., Qu, Y., Zhu, H., Zhao, W., Han, Y., & Qin, C. (2019) · Viruses · doi:10.3390/v11010059 · Cited by 1,268 · see citing works
Sungnak, W., Huang, N., Bécavin, C., & Berg, M. (2020) · PubMed · Cited by 1,196 · see citing works
Role of angiotensin-converting enzyme 2 (ACE2) in COVID-19
Ni, W., Yang, X., Yang, D., Bao, J., Li, R., Xiao, Y., Hou, C., Wang, H., Liu, J., Yang, D., et al. (2020) · Critical Care · doi:10.1186/s13054-020-03120-0 · Cited by 1,175 · see citing works
Coronavirus disease 2019 (COVID-19): current status and future perspectives
Li, H., Liu, S., Yu, X.-H., Tang, S., & Tang, C. (2020) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2020.105951 · Cited by 1,174 · see citing works
A human monoclonal antibody blocking SARS-CoV-2 infection
Wang, C., Li, W., Drabek, D., Okba, N. M. A., van Haperen, R., Osterhaus, A. D. M. E., van Kuppeveld, F. J. M., Haagmans, B. L., Grosveld, F. G., & Bosch, B. (2020) · Nature Communications · doi:10.1038/s41467-020-16256-y · Cited by 1,115 · see citing works
Self-citationCoronavirus Infections in Children Including COVID-19
Zimmermann, P., & Curtis, N. C. (2020) · The Pediatric Infectious Disease Journal · doi:10.1097/inf.0000000000002660 · Cited by 1,104 · see citing works
Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen
Pallesen, J., Wang, N., Corbett, K. S., Wrapp, D., Kirchdoerfer, R. N., Turner, H. L., Cottrell, C. A., Becker, M. M., Wang, L., Shi, W., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707304114 · Cited by 1,073 · see citing works
The deadly coronaviruses: The 2003 SARS pandemic and the 2020 novel coronavirus epidemic in China
Yang, Y., Peng, F., Wang, R., Guan, K., Jiang, T., Xu, G., Sun, J., & Chang, C. C.-C. (2020) · Journal of Autoimmunity · doi:10.1016/j.jaut.2020.102434 · Cited by 1,073 · see citing works
COVID-19: Transmission, prevention, and potential therapeutic opportunities
Lotfi, M., Hamblin, M. R., & Rezaei, N. (2020) · Clinica Chimica Acta · doi:10.1016/j.cca.2020.05.044 · Cited by 1,029 · see citing works
COVID-19 and diabetes mellitus: from pathophysiology to clinical management
Lim, S. K., Bae, J. H., Kwon, H., & Nauck, M. A. (2020) · Nature Reviews Endocrinology · doi:10.1038/s41574-020-00435-4 · Cited by 1,024 · see citing works
Ahn, D., Shin, H.-J., Kim, M.-H., Lee, S.-H., Kim, H.-S., Myoung, J., Kim, B., & Kim, S. (2020) · Journal of Microbiology and Biotechnology · doi:10.4014/jmb.2003.03011 · Cited by 997 · see citing works
Lamers, M. M., & Haagmans, B. L. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00713-0 · Cited by 986 · see citing works
Self-citationPractical recommendations for the management of diabetes in patients with COVID-19
Bornstein, S. R., Rubino, F., Khunti, K., Mingrone, G., Hopkins, D., Birkenfeld, A. L., Boehm, B. O., Amiel, S. A., Holt, R. I. G., Skyler, J. S., et al. (2020) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(20)30152-2 · Cited by 964 · see citing works
Diabetes in COVID-19: Prevalence, pathophysiology, prognosis and practical considerations
Singh, A. K., Gupta, R., Ghosh, A., & Misra, A. (2020) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2020.04.004 · Cited by 940 · see citing works
COVID-19 pandemic, coronaviruses, and diabetes mellitus
Muniyappa, R., & Gubbi, S. (2020) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00124.2020 · Cited by 913 · see citing works
Lin, L., Lu, L., Cao, W., & Li, T. (2020) · Emerging Microbes & Infections · doi:10.1080/22221751.2020.1746199 · Cited by 909 · see citing works
COVID-19 in people with diabetes: understanding the reasons for worse outcomes
Apicella, M., Campopiano, M. C., Mantuano, M., Mazoni, L., Coppelli, A., & Prato, S. D. (2020) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(20)30238-2 · Cited by 905 · see citing works
Comparative pathogenesis of COVID-19, MERS, and SARS in a nonhuman primate model
Rockx, B., Kuiken, T., Herfst, S., Bestebroer, T., Lamers, M. M., Oude Munnink, B. B., de Meulder, D., van Amerongen, G., van den Brand, J., Okba, N. M. A., et al. (2020) · Science · doi:10.1126/science.abb7314 · Cited by 901 · see citing works
Self-citationHost cell proteases: Critical determinants of coronavirus tropism and pathogenesis
Millet, J. K., & Whittaker, G. R. (2014) · Virus Research · doi:10.1016/j.virusres.2014.11.021 · Cited by 887 · see citing works
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 876 · see citing works
Heurich, A., Hofmann-Winkler, H., Gierer, S., Liepold, T., Jahn, O., & Pöhlmann, S. (2013) · Journal of Virology · doi:10.1128/jvi.02202-13 · Cited by 871 · see citing works
Liver injury during highly pathogenic human coronavirus infections
Xu, L., Liu, J., Lu, M., Yang, D., & Zheng, X. (2020) · Liver International · doi:10.1111/liv.14435 · Cited by 855 · see citing works
COVID-19: what has been learned and to be learned about the novel coronavirus disease
Ye, Y., Lagniton, P. N. P., Ye, S., Li, E., & Xu, R.-H. (2020) · International Journal of Biological Sciences · doi:10.7150/ijbs.45134 · Cited by 836 · see citing works
Barnes, C. O., West, A. P., Huey-Tubman, K. E., Hoffmann, M. A. G., Sharaf, N. G., Hoffman, P. R., Koranda, N., Gristick, H. B., Gaebler, C., Muecksch, F., et al. (2020) · Cell · doi:10.1016/j.cell.2020.06.025 · Cited by 795 · see citing works
Structural insights into coronavirus entry
(2019) · Advances in Virus Research · doi:10.1016/bs.aivir.2019.08.002 · Cited by 769 · see citing works
Adaptation of SARS-CoV-2 in BALB/c mice for testing vaccine efficacy
Gu, H., Chen, Q., Yang, G., He, L., Fan, H., Deng, Y.-Q., Wang, Y., Teng, Y., Zhao, Z., Cui, Y., et al. (2020) · Science · doi:10.1126/science.abc4730 · Cited by 762 · see citing works
Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin
Zhou, P., Fan, H., Lan, T., Yang, X., Shi, W., Zhang, W., Zhu, Y., Zhang, Y., Xie, Q., Mani, S., et al. (2018) · Nature · doi:10.1038/s41586-018-0010-9 · Cited by 755 · see citing works
Coronavirus membrane fusion mechanism offers a potential target for antiviral development
Tang, T., Bidon, M. K., Jaimes, J. A., Whittaker, G. R., & Daniel, S. (2020) · Antiviral Research · doi:10.1016/j.antiviral.2020.104792 · Cited by 750 · see citing works
Casagrande, M., Favieri, F., Tambelli, R., & Forte, G. (2020) · Sleep Medicine · doi:10.1016/j.sleep.2020.05.011 · Cited by 735 · see citing works
Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26
Lu, G., Hu, Y., Wang, Q., Qi, J., Gao, F., Li, Y., Zhang, Y., Zhang, W., Yuan, Y., Bao, J., et al. (2013) · Nature · doi:10.1038/nature12328 · Cited by 732 · see citing works
de Wilde, A. H., Jochmans, D., Posthuma, C. C., Zevenhoven-Dobbe, J. C., van Nieuwkoop, S., Bestebroer, T. M., van den Hoogen, B. G., Neyts, J. H., & Snijder, E. J. (2014) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.03011-14 · Cited by 727 · see citing works
Reusken, C. B. E. M., Haagmans, B. L., Müller, M. A., Gutiérrez, C., Godeke, G.-J., Meyer, B., Muth, D., Raj, V. S., Vries, L. S.-D., Corman, V. M., et al. (2013) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(13)70164-6 · Cited by 726 · see citing works
Self-citationStructure of MERS-CoV spike receptor-binding domain complexed with human receptor DPP4
Wang, N., Shi, X., Jiang, L., Zhang, S., Wang, D., Tong, P., Guo, D., Fu, L., Cui, Y., Liu, X., et al. (2013) · Cell Research · doi:10.1038/cr.2013.92 · Cited by 717 · see citing works
Helmy, Y. A., Fawzy, M., Elaswad, A., Sobieh, A., Kenney, S. P., & Shehata, A. A. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9041225 · Cited by 687 · see citing works
A decade after SARS: strategies for controlling emerging coronaviruses
Graham, R. L., Donaldson, E., & Baric, R. S. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro3143 · Cited by 676 · see citing works
Millet, J. K., & Whittaker, G. R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1407087111 · Cited by 673 · see citing works
Lymphopenia in severe coronavirus disease-2019 (COVID-19): systematic review and meta-analysis
Huang, I., & Pranata, R. (2020) · Journal of Intensive Care · doi:10.1186/s40560-020-00453-4 · Cited by 662 · see citing works
Molecular Mechanism for Antibody-Dependent Enhancement of Coronavirus Entry
Wan, Y., Shang, J., Sun, S., Tai, W., Chen, J., Geng, Q., He, L., Chen, Y., Wu, J., Shi, Z., et al. (2019) · Journal of Virology · doi:10.1128/jvi.02015-19 · Cited by 662 · see citing works
Dyall, J., Coleman, C. M., Hart, B. J., Venkataraman, T., Holbrook, M. R., Kindrachuk, J., Johnson, R. F., Olinger, G. G., Jahrling, P. B., Laidlaw, M., et al. (2014) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.03036-14 · Cited by 653 · see citing works
The Novel Coronavirus 2019 epidemic and kidneys
Naicker, S., Yang, C.-W., Hwang, S., Liu, B., Chen, J., & Jha, V. (2020) · Kidney International · doi:10.1016/j.kint.2020.03.001 · Cited by 653 · see citing works
Unoh, Y., Uehara, S., Nakahara, K., Nobori, H., Yamatsu, Y., Yamamoto, S., Maruyama, Y., Taoda, Y., Kasamatsu, K., Suto, T., et al. (2022) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.2c00117 · Cited by 635 · see citing works
Damas, J., Hughes, G. M., Keough, K. C., Painter, C. A., Persky, N. S., Corbo, M., Hiller, M., Koepfli, K.-P., Pfenning, A. R., Zhao, H., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2010146117 · Cited by 633 · see citing works
Structural Basis for Potent Neutralization of Betacoronaviruses by Single-Domain Camelid Antibodies
Wrapp, D., De Vlieger, D., Corbett, K. S., Torres, G. M., Wang, N., Van Breedam, W., Roose, K., van Schie, L., Hoffmann, M., Pöhlmann, S., et al. (2020) · Cell · doi:10.1016/j.cell.2020.04.031 · Cited by 610 · see citing works
Interspecies 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 · see citing works
Ashour, H. M., Elkhatib, W. F., Rahman, M. M., & Elshabrawy, H. A. (2020) · Pathogens · doi:10.3390/pathogens9030186 · Cited by 603 · see citing works
Bat-to-human: spike features determining ‘host jump’ of coronaviruses SARS-CoV, MERS-CoV, and beyond
Lu, G., Wang, Q., & Gao, G. F. (2015) · Trends in Microbiology · doi:10.1016/j.tim.2015.06.003 · Cited by 600 · see citing works
Unexpected Receptor Functional Mimicry Elucidates Activation of Coronavirus Fusion
Walls, A. C., Xiong, X., Park, Y.-J., Tortorici, M. A., Snijder, J., Quispe, J., Cameroni, E., Gopal, R., Dai, M., Lanzavecchia, A., et al. (2019) · Cell · doi:10.1016/j.cell.2018.12.028 · Cited by 582 · see citing works
Gui, M., Song, W., Zhou, H., Xu, J., Chen, S., Xiang, Y., & Wang, X. (2016) · Cell Research · doi:10.1038/cr.2016.152 · Cited by 577 · see citing works
Receptor Recognition Mechanisms of Coronaviruses: a Decade of Structural Studies
Li, F. (2014) · Journal of Virology · doi:10.1128/jvi.02615-14 · Cited by 569 · see citing works
Structural basis for human coronavirus attachment to sialic acid receptors
Tortorici, M. A., Walls, A. C., Lang, Y., Wang, C., Li, Z., Koerhuis, D., Boons, G., Bosch, B., Rey, F. A., de Groot, R. J., et al. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0233-y · Cited by 568 · see citing works
Self-citationGenome-wide CRISPR Screens Reveal Host Factors Critical for SARS-CoV-2 Infection
Wei, J., Alfajaro, M. M., DeWeirdt, P. C., Hanna, R. E., Lu-Culligan, W. J., Cai, W. L., Strine, M. S., Zhang, S.-M., Graziano, V. R., Schmitz, C. O., et al. (2020) · Cell · doi:10.1016/j.cell.2020.10.028 · Cited by 559 · see citing works
Bat-borne virus diversity, spillover and emergence
Letko, M. C., Seifert, S. N., Olival, K. J., Plowright, R. K., & Munster, V. J. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-020-0394-z · Cited by 558 · see citing works
Host Factors in Coronavirus Replication
de Wilde, A. H., Snijder, E. J., Kikkert, M., & van Hemert, M. J. (2017) · Current topics in microbiology and immunology · doi:10.1007/82_2017_25 · Cited by 542 · see citing works
Rapkiewicz, A., Mai, X., Carsons, S. E., Pittaluga, S., Kleiner, D. E., Berger, J. S., Thomas, S., Adler, N., Charytan, D. M., Gasmi, B., et al. (2020) · EClinicalMedicine · doi:10.1016/j.eclinm.2020.100434 · Cited by 532 · see citing works
T cell-mediated immune response to respiratory coronaviruses
Channappanavar, R., Zhao, J., & Perlman, S. (2014) · Immunologic Research · doi:10.1007/s12026-014-8534-z · Cited by 512 · see citing works
Tian, J.-H., Patel, N., Haupt, R., Zhou, H., Weston, S., Hammond, H., Logue, J., Portnoff, A. D., Norton, J., Guebre-Xabier, M., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20653-8 · Cited by 508 · see citing works
Obesity and diabetes as high‐risk factors for severe coronavirus disease 2019 ( Covid ‐19)
Zhou, Y., Chi, J., Lv, W., & Wang, Y. (2020) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.3377 · Cited by 496 · see citing works
Bat origin of human coronaviruses
Hu, B., Ge, X., Wang, L., & Shi, Z. (2015) · Virology Journal · doi:10.1186/s12985-015-0422-1 · Cited by 492 · see citing works
Shanmugaraj, B., Siriwattananon, K., Wangkanont, K., & Phoolcharoen, W. (2020) · Asian Pacific Journal of Allergy and Immunology · doi:10.12932/ap-200220-0773 · Cited by 487 · see citing works
Rapid reconstruction of SARS-CoV-2 using a synthetic genomics platform
Thao, T. T. N., Labroussaa, F., Ebert, N., V’kovski, P., Stalder, H., Portmann, J., Kelly, J. N., Steiner, S., Holwerda, M., Kratzel, A., et al. (2020) · Nature · doi:10.1038/s41586-020-2294-9 · Cited by 485 · see citing works
Self-citationMiddle East respiratory syndrome
Memish, Z. A., Perlman, S. M., Kerkhove, M. D. V., & Zumla, A. I. (2020) · The Lancet · doi:10.1016/s0140-6736(19)33221-0 · Cited by 484 · see citing works
Devaux, C. A., Rolain, J., & Raoult, D. (2020) · Journal of Microbiology Immunology and Infection · doi:10.1016/j.jmii.2020.04.015 · Cited by 477 · see citing works
A SARS-CoV-2 Infection Model in Mice Demonstrates Protection by Neutralizing Antibodies
Hassan, A. O., Case, J. B., Winkler, E. S., Thackray, L. B., Kafai, N. M., Bailey, A. L., McCune, B. T., Fox, J. M., Chen, R. E., Alsoussi, W. B., et al. (2020) · Cell · doi:10.1016/j.cell.2020.06.011 · Cited by 477 · see citing works
A Universal Design of Betacoronavirus Vaccines against COVID-19, MERS, and SARS
Dai, L., Zheng, T., Xu, K., Han, Y., Xu, L., Huang, E., An, Y., Cheng, Y., Li, S., Liu, M., et al. (2020) · Cell · doi:10.1016/j.cell.2020.06.035 · Cited by 476 · see citing works
Middle East Respiratory Syndrome Coronavirus Infection in Dromedary Camels in Saudi Arabia
Alagaili, A. N., Briese, T., Mishra, N., Kapoor, V., Sameroff, S. C., de Wit, E., Munster, V. J., Hensley, L. E., Zalmout, I. S., Kapoor, A., et al. (2014) · mBio · doi:10.1128/mbio.00884-14 · Cited by 474 · see citing works
Jothimani, D. K., Venugopal, R., Abedin, M. F., Kaliamoorthy, I., & Rela, M. (2020) · Journal of Hepatology · doi:10.1016/j.jhep.2020.06.006 · Cited by 471 · see citing works
Overview of Immune Response During SARS-CoV-2 Infection: Lessons From the Past
Shah, V. K., Firmal, P., Alam, A., Ganguly, D., & Chattopadhyay, S. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01949 · Cited by 471 · see citing works
Li, K., Wohlford-Lenane, C., Perlman, S., Zhao, J., Jewell, A. K., Reznikov, L. R., Gibson-Corley, K. N., Meyerholz, D. K., & McCray, P. B. (2016) · Journal of Infectious Diseases · doi:10.1093/infdis/jiv499 · Cited by 459 · see citing works
Coronavirus Spike Protein and Tropism Changes
Hulswit, R. J. G., de Haan, C. A. M., & Bosch, B. (2016) · Advances in virus research · doi:10.1016/bs.aivir.2016.08.004 · Cited by 457 · see citing works
Self-citationThe structure and functions of coronavirus genomic 3′ and 5′ ends
Yang, D., & Leibowitz, J. L. (2015) · Virus Research · doi:10.1016/j.virusres.2015.02.025 · Cited by 453 · see citing works
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 · see citing works
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., et al. (2016) · Journal of Infectious Diseases · doi:10.1093/infdis/jiv380 · Cited by 448 · see citing works
Shirato, K., Kawase, M., & Matsuyama, S. (2013) · Journal of Virology · doi:10.1128/jvi.01890-13 · Cited by 448 · see citing works
Smith, E. C., Blanc, H., Vignuzzi, M., & Denison, M. R. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003565 · Cited by 428 · see citing works
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 · see citing works
Subunit Vaccines Against Emerging Pathogenic Human Coronaviruses
Wang, N., Shang, J., Jiang, S., & Du, L. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00298 · Cited by 424 · see citing works
Virus–Receptor Interactions: The Key to Cellular Invasion
Maginnis, M. S. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.06.024 · Cited by 415 · see citing works
Thrombocytopathy and endotheliopathy: crucial contributors to COVID-19 thromboinflammation
Gu, S. X., Tyagi, T., Jain, K., Gu, V. W., Lee, S. H., Hwa, J. M., Kwan, J. M., Krause, D. S., Lee, A. I., Halene, S., et al. (2020) · Nature Reviews Cardiology · doi:10.1038/s41569-020-00469-1 · Cited by 414 · see citing works
Case, J. B., Rothlauf, P. W., Chen, R. E., Liu, Z., Zhao, H., Kim, A. S., Bloyet, L.-M., Zeng, Q., Tahan, S., Droit, L., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.06.021 · Cited by 410 · see citing works
- Authors
- 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., Thiel, V., Drosten, C., Rottier, P. J. M., Osterhaus, A. D. M. E., Bosch, B. J., & Haagmans, B. L.
- Affiliations
- Erasmus MC (NL)
- Utrecht University (NL)
- University of Bonn (DE)
- Kantonsspital St. Gallen (CH)
- Soliman Fakeeh Hospital (SA)
- University of Zurich (CH)
- Corresponding author
- Bosch, Berend Jan
- Haagmans, Bart L.
- ORCID
- Venue
- Nature
- Published
- 2013-03
- Volume
- 495
- Issue
- 7440
- Pages
- 251-254
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC7095326
- OpenAlex
- W2119111857
- Cited by
- 2,061
- References
- 25
- Citations by year
- 2026: 41 · 2025: 64 · 2024: 97 · 2023: 130 · 2022: 199 · 2021: 358 · 2020: 609 · 2019: 74 · 2018: 59 · 2017: 61 · 2016: 93 · 2015: 101 · 2014: 86 · 2013: 87 · 2012: 1
- FWCI
- 89.49
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, other-oa)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Funders
- National Science Foundation
- European Commission (223498, 278976)
- Deutsche Forschungsgemeinschaft (DR 772/3-1, KA1241/18-1, 772/3)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (132898)
- Bundesministerium für Bildung und Forschung
- China Scholarship Council
- Stiftung Forschung 3R (128-11)
- 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 › COVID-19 Clinical Research Studies
- Keywords
- MERS-CoV, dipeptidyl peptidase IV, CD26, viral receptor, host range, lower respiratory tract infection, SARS-CoV, receptor binding domain, Huh7 cells, bronchial epithelial cells
- MeSH terms
- Animals, Chlorocebus aethiops, Chiroptera, Epithelial Cells, Humans, Molecular Sequence Data, Receptors, Virus, Coronavirus, Coronavirus Infections, Dipeptidyl Peptidase 4, COS Cells, Bronchioles, Host Specificity
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
