Exploring the pathogenesis of severe acute respiratory syndrome (SARS): the tissue distribution of the coronavirus (SARS‐CoV) and its putative receptor, angiotensin‐converting enzyme 2 (ACE2)
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Severe acute respiratory syndrome (SARS) is an emerging infectious disease associated with a new coronavirus, SARS‐CoV. Pulmonary involvement is the dominant clinical feature but extra‐pulmonary manifestations are also common. Factors that account for the wide spectrum of organ system involvement and disease severity are poorly understood and the pathogenesis of SARS‐CoV infection remains unclear. Angiotensin converting enzyme 2 (ACE2) has recently been identified as the functional cellular receptor for SARS‐CoV. Studies of the tissue and cellular distribution of SARS‐CoV, and ACE2 protein expression, reveal new insights into the pathogenesis of this deadly disease. ACE2 is expressed at high level in the primary target cells of SARS‐CoV, namely pneumocytes and surface enterocytes of the small intestine. Despite the fact that SARS‐CoV can infect the lung and intestine, the tissue responses in these two organs are different. All other tissues and cell types expressing ACE2 may be potential targets of SARS‐CoV infection. Remarkably, endothelial cells, which express ACE2 to a high level, have not been shown to be infected by SARS‐CoV. There is also evidence that cell types without detectable ACE2 expression may also be infected by the virus. Furthermore, studies in a new human cell culture model have indicated that the presence of ACE2 alone is not sufficient for maintaining viral infection. Therefore, other virus receptors or co‐receptors may be required in different tissues. Moreover, the interaction between SARS‐CoV and the immunological or lymphoid system remains to be defined. It is clear that we are only at the dawn of our understanding of the pathogenesis of SARS. As our knowledge of the pathogenic mechanisms improves, a more rational approach to therapeutic and vaccine development can be designed in order to combat this new and fatal human disease. Copyright © 2004 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.
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Endothelial cells, which also express high ACE-2 levels, do not display correspondingly high SARS-CoV infection levels.
“However, endothelial cells, which also express high ACE-2 levels do not display correspondingly high SARS-CoV infection levels [173].”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [173]
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
Hamming, I., Timens, W., Bulthuis, M., Lely, A., Navis, G., & van Goor, H. (2004) · The Journal of Pathology · doi:10.1002/path.1570 · Cited by 5,676 · see citing works
A Major Outbreak of Severe Acute Respiratory Syndrome in Hong Kong
Lee, N. L. S., Hui, D. S. C., Wu, A. K. L., Chan, P. K. S., Cameron, P. A., Joynt, G. M., Ahuja, A. T., Yung, M. Y., Leung, C. B., To, K. F., et al. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa030685 · Cited by 2,631 · see citing works
Self-citationCharacterization of a Novel Coronavirus Associated with Severe Acute Respiratory Syndrome
Rota, P. A., Oberste, M. S., Monroe, S. S., Nix, W. A., Campagnoli, R. P., Icenogle, J. P., Peñaranda, S., Bankamp, B., Maher, K., Chen, M., et al. (2003) · Science · doi:10.1126/science.1085952 · Cited by 2,477 · see citing works
The Genome Sequence of the SARS-Associated Coronavirus
Marra, M. A., Jones, S. J. M., Astell, C. R., Holt, R. A., Brooks-Wilson, A. R., Butterfield, Y. S. N., Khattra, J. S., Asano, J. K., Barber, S., Chan, S. Y., et al. (2003) · Science · doi:10.1126/science.1085953 · Cited by 2,017 · see citing works
Plasma inflammatory cytokines and chemokines in severe acute respiratory syndrome
Wong, C. K., LAM, C. W. K., Wu, A. K. L., Ip, W., Lee, N. L. S., Chan, I., Lit, L. C. W., Hui, D. S. C., Chan, M. H. M., CHUNG, S. S. C., et al. (2004) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2004.02415.x · Cited by 1,270 · see citing works
Lung pathology of fatal severe acute respiratory syndrome
Nicholls, J. M., Poon, L. L., Lee, K. C., Ng, W. F., Lai, S. T., Leung, C. Y., Chu, C. M., Hui, P. K., Mak, K. L., Lim, W., et al. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13413-7 · Cited by 1,076 · see citing works
Ding, Y., He, L., Zhang, Q., Huang, Z., Che, X., Hou, J., Wang, H., Shen, H., Qiu, L., Li, Z., et al. (2004) · The Journal of Pathology · doi:10.1002/path.1560 · Cited by 1,068 · see citing works
A Cluster of Cases of Severe Acute Respiratory Syndrome in Hong Kong
TSANG, K. W. T., Ho, P., OOI, G. C., Yee, W. K. S., Wang, T., Chan-Yeung, M. M. W., Lam, W. K., Seto, W., Yam, L. Y.-C., CHEUNG, T. M., et al. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa030666 · Cited by 1,018 · see citing works
Molecular Evolution of the SARS Coronavirus During the Course of the SARS Epidemic in China
The Chinese SARS Molecular Epidemiology Consortium (2004) · Science · doi:10.1126/science.1092002 · Cited by 765 · see citing works
The clinical pathology of severe acute respiratory syndrome (SARS): a report from China
Ding, Y., Wang, H., Shen, H., Li, Z., Geng, J., Han, H.-X., Cai, J., Li, X., Kang, W., Weng, D., et al. (2003) · The Journal of Pathology · doi:10.1002/path.1440 · Cited by 765 · see citing works
Enteric involvement of severe acute respiratory syndrome-associated coronavirus infection
Leung, W. K., To, K., Chan, P. K. S., Chan, H. L., Wu, A. K. L., Lee, N. L. S., Yuen, K., & Sung, J. J. �. (2003) · Gastroenterology · doi:10.1016/s0016-5085(03)01215-0 · Cited by 697 · see citing works
Self-citationWong, S. K., Li, W., Moore, M. J., Choe, H., & Farzan, M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.c300520200 · Cited by 690 · see citing works
A DNA vaccine induces SARS coronavirus neutralization and protective immunity in mice
Yang, Z.-Y., Kong, W., Huang, Y., Roberts, A., Murphy, B., Subbarao, K., & Nabel, G. (2004) · Nature · doi:10.1038/nature02463 · Cited by 688 · see citing works
Wong, R., Wu, A., To, K.-F., Lee, N., Lam, C., Wong, C., Chan, P. K., Ng, M., Yu, L., Hui, D., et al. (2003) · British medical journal · doi:10.1136/bmj.326.7403.1358 · Cited by 566 · see citing works
Self-citationSARS — beginning to understand a new virus
Stadler, K., Masignani, V., Eickmann, M., Becker, S., Abrignani, S., Klenk, H., & Rappuoli, R. (2003) · Nature Reviews Microbiology · doi:10.1038/nrmicro775 · Cited by 558 · see citing works
SARS-associated viral hepatitis caused by a novel coronavirus: Report of three cases
Chau, T., Lee, K.-C., Yao, H., Tsang, T. Y. O., Chow, T., Yeung, Y.-C., Choi, K., Tso, Y.-K., Lau, T., Lai, S.-T., et al. (2004) · Hepatology · doi:10.1002/hep.20111 · Cited by 422 · see citing works
Bisht, H., Roberts, A., Vogel, L., Bukreyev, A. A., Collins, P. L., Murphy, B. R., Subbarao, K., & Moss, B. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401939101 · Cited by 415 · see citing works
Franks, T. J., Chong, P. Y., Chui, P., Galvin, J. R., Lourens, R. M., Reid, A. H., Selbs, E., Mcevoy, C. P. L., Hayden, C. D. L., Fukuoka, J., et al. (2003) · Human Pathology · doi:10.1016/s0046-8177(03)00367-8 · Cited by 413 · see citing works
Outcomes and Prognostic Factors in 267 Patients with Severe Acute Respiratory Syndrome in Hong Kong
Choi, K., Chau, T., Tsang, O. T. Y., Tso, E. Y. K., Chiu, M. C., Tong, W., Lee, P. O., Ng, T. K., Ng, W. F., Lee, K. C., et al. (2003) · Annals of Internal Medicine · doi:10.7326/0003-4819-139-9-200311040-00005 · Cited by 392 · see citing works
The SARS-CoV S glycoprotein: expression and functional characterization
Xiao, X., Chakraborti, S., Dimitrov, A., Gramatikoff, K., & Dimitrov, D. S. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2003.11.054 · Cited by 370 · see citing works
ACE2, a new regulator of the renin–angiotensin system
Burrell, L. M., Johnston, C. I., Tikellis, C., & Cooper, M. E. (2004) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2004.03.001 · Cited by 362 · see citing works
Association of HLA class I with severe acute respiratory syndrome coronavirus infection
Lin, M., Tseng, H.-K., Tréjaut, J., Lee, H.-L., Loo, J.-H., Chu, C. C., Chen, P.-J., Su, Y.-W., Lim, K. H., Tsai, Z.-U., et al. (2003) · BMC Medical Genetics · doi:10.1186/1471-2350-4-9 · Cited by 328 · see citing works
Detection of SARS Coronavirus in Patients with Suspected SARS
Chan, K. H., Poon, L. L. M., Cheng, V. C., Guan, Y., Hung, I. F., Kong, J. H. B., Yam, L. Y.-C., Seto, W., Yuen, K., & Peiris, J. S. M. (2004) · Emerging infectious diseases · doi:10.3201/eid1002.030610 · Cited by 313 · see citing works
Chong, P. Y., Chui, P., Ling, A. E., Franks, T. J., Tai, D. Y. H., Leo, Y., Kaw, G. J. L., Wansaicheong, G. K. L., Chan, K. P., Oon, L. L. E., et al. (2004) · Archives of Pathology & Laboratory Medicine · doi:10.5858/2004-128-195-aoddts · Cited by 269 · see citing works
Pulmonary pathological features in coronavirus associated severe acute respiratory syndrome (SARS)
Tse, G. M.-K., To, K., Chan, P. K. S., Lo, A. W. I., Ng, K., Wu, A. K. L., Lee, N. L. S., Wong, H.-C., Mak, S. Y., Chan, K.-F., et al. (2004) · Journal of Clinical Pathology · doi:10.1136/jcp.2003.013276 · Cited by 239 · see citing works
Self-citationTo, K. F., TONG, J. H. M., Chan, P. K. S., Au, F. W. L., Chim, S. S. C., Chan, K. A., Cheung, J. L. K., Liu, E. Y. M., Tse, G. M.-K., Lo, A. W. I., et al. (2004) · The Journal of Pathology · doi:10.1002/path.1510 · Cited by 176 · see citing works
Self-citationKim, T. W., Lee, J. H., Hung, C., Peng, S., Roden, R. B. S., Wang, M., Viscidi, R. P., Tsai, Y.-C., He, L., Chen, P., et al. (2004) · Journal of Virology · doi:10.1128/jvi.78.9.4638-4645.2004 · Cited by 172 · see citing works
Ng, M. H. L., Lau, K., Li, L., Cheng, S., Chan, W. Y., Hui, P. K., Zee, B. C.-Y., Leung, C., & Sung, J. J. �. (2004) · The Journal of Infectious Diseases · doi:10.1086/421523 · Cited by 168 · see citing works
Expression cloning of functional receptor used by SARS coronavirus
Wang, P., Chen, J., Zheng, A., Nie, Y., Shi, X., Wang, W., Wang, G., Luo, M., Liu, H., Tan, L., et al. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.01.076 · Cited by 145 · see citing works
Induction of SARS-nucleoprotein-specific immune response by use of DNA vaccine
Zhu, M. (2004) · Immunology Letters · doi:10.1016/j.imlet.2004.01.001 · Cited by 96 · see citing works
Persistent infection of SARS coronavirus in colonic cells in vitro
Chan, P. K. S., To, K., Lo, A. W. I., Cheung, J. L. K., Chu, I. M., Au, F. W. L., TONG, J. H. M., Tam, J. S., Sung, J. J. �., & Ng, H. (2004) · Journal of Medical Virology · doi:10.1002/jmv.20138 · Cited by 91 · see citing works
Self-citationInflammatory Cytokine Profile in Children With Severe Acute Respiratory Syndrome
Ng, P. C., Lam, C. W. K., Li, A. M., Wong, C. K., Cheng, F. W. T., Leung, T. F., Hon, E. K. L., Chan, I. H. S., Li, C. K., Fung, K. S. C., et al. (2004) · PEDIATRICS · doi:10.1542/peds.113.1.e7 · Cited by 90 · see citing works
Chim, S. S. C., Tsui, S. K., Chan, K., Au, T. C. C., Hung, E., Tong, Y., Chiu, R., Ng, E. K. W., Chan, P., Chu, C., et al. (2003) · The Lancet · doi:10.1016/s0140-6736(03)14901-x · Cited by 63 · see citing works
Pathological study on severe acute respiratory syndrome.
郎振为, 张立洁, Zhang, S., 孟忻, 李俊强, 宋晨朝, 孙琳, & 周育森 (2003) · PubMed · Cited by 57 · see citing works
Detection of Severe Acute Respiratory Syndrome-Associated Coronavirus in Pneumocytes of the Lung
Chow, K., Hsiao, C.-H., Lin, T., Chen, C., & Chiou, S.-H. (2004) · American Journal of Clinical Pathology · doi:10.1309/c0ed-u0ra-qbtx-bhce · Cited by 55 · see citing works
Detection of Severe Acute Respiratory Syndrome–Associated Coronavirus in Pneumocytes of the Lung
Chow, K., Hsiao, C.-H., Lin, T., et al. (2004) · American Journal of Clinical Pathology · doi:10.1309/c0edu0raqbtxbhce · Cited by 49 · see citing works
Severe acute respiratory syndrome in children
Wong, G., Li, A. M., Ng, P. C., & Fok, T. F. (2003) · Pediatric Pulmonology · doi:10.1002/ppul.10367 · Cited by 45 · see citing works
SARS Coronavirus-Infected Cells in Lung Detected by New In Situ Hybridization Technique
Nakajima, N., Asahi‐Ozaki, Y., Nagata, N., Sato, Y., Dizon, F., Paladin, F. J., Olveda, R. M., Odagiri, T., Tashiro, M., & Sata, T. (2003) · Japanese Journal of Infectious Diseases · doi:10.7883/yoken.jjid.2003.139 · Cited by 33 · see citing works
Chen, P. C.-H., & Hsiao, C.-H. (2004) · The Journal of Pathology · doi:10.1002/path.1575 · Cited by 12 · see citing works
Digestive system manifestations in patients with severe acute respiratory syndrome.
詹俊, 陈为宪, 李楚强, 伍卫, 李建军, 江山平, 王景峰, 曾志勇, 黄子通, & 黄洪章 (2003) · PubMed · Cited by 7 · see citing works
Inadequate plumbing systems probably contributed to SARS transmission.
(2003) · PubMed · Cited by 6 · see citing works
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The Severe Acute Respiratory Syndrome
Peiris, J. S. M., Yuen, K., Osterhaus, A. D. M. E., & Stöhr, K. (2003) · New England Journal of Medicine · doi:10.1056/nejmra032498 · Cited by 1,377 · see citing works
Wu, P., Duan, F., Luo, C., Liu, Q., Qu, X., Liang, L., & Wu, K. (2020) · JAMA Ophthalmology · doi:10.1001/jamaophthalmol.2020.1291 · Cited by 1,235 · see citing works
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Peiris, M. J. S., Guan, Y., & Yuen, K. (2004) · Nature Medicine · doi:10.1038/nm1143 · Cited by 1,135 · 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 882 · see citing works
Matsuyama, S., Nagata, N., Shirato, K., Kawase, M., Takeda, M., & Taguchi, F. (2010) · Journal of Virology · doi:10.1128/jvi.01542-10 · Cited by 778 · see citing works
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Jeffers, S. A., Tusell, S. M., Gillim-Ross, L., Hemmila, E. M., Achenbach, J. E., Babcock, G. J., Thomas, W. D., Thackray, L. B., Young, M. D., Mason, R. J., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403812101 · Cited by 606 · see citing works
Iba, T., Levy, J. H., Levi, M. M., & Thachil, J. V. (2020) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.14975 · Cited by 594 · see citing works
Kawase, M., Shirato, K., van der Hoek, L., Taguchi, F., & Matsuyama, S. (2012) · Journal of Virology · doi:10.1128/jvi.00094-12 · Cited by 517 · see citing works
Glowacka, I., Bertram, S., Herzog, P., Pfefferle, S., Steffen, I., Muench, M. O., Simmons, G., Hofmann, H., Kuri, T., Weber, F., et al. (2009) · Journal of Virology · doi:10.1128/jvi.01248-09 · Cited by 495 · see citing works
Chemokine up-regulation in SARS-coronavirus–infected, monocyte-derived human dendritic cells
Law, H., Cheung, C. Y., Ng, H. Y., Sia, S. F., Chan, Y. O., Luk, W., Nicholls, J. M., Peiris, M. J. S., & Lau, Y. (2005) · Blood · doi:10.1182/blood-2004-10-4166 · Cited by 467 · see citing works
What are the risks of COVID-19 infection in pregnant women?
Qiao, J. (2020) · The Lancet · doi:10.1016/s0140-6736(20)30365-2 · Cited by 475 · see citing works
Emerging COVID-19 variants and their impact on SARS-CoV-2 diagnosis, therapeutics and vaccines
Fernandes, Q., Inchakalody, V. P., Merhi, M., Mestiri, S., Taib, N., El-Ella, D. M. A., Bedhiafi, T., Raza, A., Al-Zaidan, L., Mohsen, M. O., et al. (2022) · Annals of Medicine · doi:10.1080/07853890.2022.2031274 · Cited by 446 · see citing works
Colmenero, I., Santonja, C., Alonso, M., Noguera‐Morel, L., Hernández‐Martín, A., Martínez, D. A., Wiesner, T., Rodriguez-Peralto, J., Requena, L., & Torrelo, A. (2020) · British Journal of Dermatology · doi:10.1111/bjd.19327 · Cited by 416 · see citing works
Bertram, S., Heurich, A., Lavender, H., Gierer, S., Danisch, S., Perin, P. M., Lucas, J. M., Nelson, P. S., Pöhlmann, S., & Soilleux, E. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035876 · Cited by 398 · see citing works
Huang, I., Bosch, B., Li, F., Li, W., Lee, K. H., Ghiran, S., Vasilieva, N. Y., Dermody, T. S., Harrison, S. C., Dormitzer, P. R., et al. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508381200 · Cited by 373 · see citing works
Bertram, S., Glowacka, I., Müller, M. A., Lavender, H., Gnirß, K., Nehlmeier, I., Niemeyer, D., He, Y., Simmons, G., Drosten, C., et al. (2011) · Journal of Virology · doi:10.1128/jvi.05300-11 · Cited by 330 · see citing works
Protease-mediated enhancement of severe acute respiratory syndrome coronavirus infection
Matsuyama, S., Ujike, M., Morikawa, S., Tashiro, M., & Taguchi, F. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503203102 · Cited by 314 · see citing works
Qian, Z., Travanty, E. A., Oko, L. M., Edeen, K. E., Berglund, A., Wang, J., Ito, Y., Holmes, K. V., & Mason, R. J. (2013) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2012-0339oc · Cited by 314 · see citing works
Potential intestinal infection and faecal–oral transmission of SARS-CoV-2
Guo, M., Tao, W., Flavell, R. A., & Zhu, S. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-021-00416-6 · Cited by 305 · see citing works
Camargo, S. M. R., Singer, D., Makrides, V., Huggel, K., Pos, K. M., Wagner, C. A., Kuba, K., Danilczyk, U. G., Skovby, F., Kleta, R., et al. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.10.055 · Cited by 282 · see citing works
ACE2, TMPRSS2 distribution and extrapulmonary organ injury in patients with COVID-19
Dong, M., Zhang, J., Ma, X., Tan, J., Chen, L., Liu, S., Xin, Y., & Zhuang, L. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110678 · Cited by 259 · see citing works
Wang, W., Ye, L., Li, Y., Li, B., Gao, B., Zeng, Y., Kong, L., Fang, X., Zheng, H., Wu, Z., et al. (2007) · Virus Research · doi:10.1016/j.virusres.2007.02.007 · Cited by 247 · see citing works
Tang, N. L. S., Chan, P. K. S., Wong, C.-K., To, K., Wu, A. K. L., Sung, Y.-M., Hui, D. S. C., Sung, J. J. �., & Lam, C. W. (2005) · Clinical Chemistry · doi:10.1373/clinchem.2005.054460 · Cited by 231 · see citing works
Self-citationNicotinamide Riboside—The Current State of Research and Therapeutic Uses
Mehmel, M., Jovanović, N. D., & Spitz, U. P. (2020) · Nutrients · doi:10.3390/nu12061616 · Cited by 225 · see citing works
Matricardi, P. M., Negro, R. W. D., & Nisini, R. (2020) · Pediatric Allergy and Immunology · doi:10.1111/pai.13271 · Cited by 212 · see citing works
Organ-specific distribution of ACE2 mRNA and correlating peptidase activity in rodents
Gembardt, F., Sterner‐Kock, A., Imboden, H., Spalteholz, M., Reibitz, F., Schultheiß, H., Siems, W., & Walther, T. (2005) · Peptides · doi:10.1016/j.peptides.2005.01.009 · Cited by 190 · see citing works
Neuropathology and virus in brain of SARS-CoV-2 infected non-human primates
Rutkai, I., Mayer, M. G., Hellmers, L., Ning, B., Huang, Z. J., Monjure, C. J., Coyne, C., Silvestri, R., Golden, N., Hensley, K., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29440-z · Cited by 188 · see citing works
Endothelium Infection and Dysregulation by SARS-CoV-2: Evidence and Caveats in COVID-19
Bernard, I., Limonta, D., Mahal, L. K., & Hobman, T. C. (2020) · Viruses · doi:10.3390/v13010029 · Cited by 182 · see citing works
Davidson, A. M., Wysocki, J. A., & BATLLE, D. C. (2020) · Hypertension · doi:10.1161/hypertensionaha.120.15256 · Cited by 180 · see citing works
Predictors of COVID-19 severity: a systematic review and meta-analysis
Mudatsir, M., Fajar, J. K., Wulandari, L., Soegiarto, G., Ilmawan, M., Purnamasari, Y., Mahdi, B. A., Jayanto, G. D., Suhendra, S., Setianingsih, Y. A., et al. (2020) · F1000Research · doi:10.12688/f1000research.26186.2 · Cited by 209 · see citing works
Surface vimentin is critical for the cell entry of SARS-CoV
Yu, Y. T.-C., Chien, S.-C., Chen, I.-Y., Lai, C.-T., Tsay, Y., Chang, S. C., & Chang, M. (2016) · Journal of Biomedical Science · doi:10.1186/s12929-016-0234-7 · Cited by 160 · see citing works
van den Brand, J. M. A., Haagmans, B. L., van Riel, D. A. J., Osterhaus, A. D. M. E., & Kuiken, T. (2014) · Journal of Comparative Pathology · doi:10.1016/j.jcpa.2014.01.004 · Cited by 158 · see citing works
Severe Acute Respiratory Syndrome (SARS)
Cleri, D. J., Ricketti, A. J., & Vernaleo, J. R. (2010) · Infectious Disease Clinics of North America · doi:10.1016/j.idc.2009.10.005 · Cited by 160 · see citing works
Han, D. P., Lohani, M., & Cho, M. W. (2007) · Journal of Virology · doi:10.1128/jvi.00315-07 · Cited by 156 · see citing works
Cytokine regulation in SARS coronavirus infection compared to other respiratory virus infections
Okabayashi, T., Kariwa, H., Yokota, S.-I., Iki, S., Indoh, T., Yokosawa, N., Takashima, I., Tsutsumi, H., & Fujii, N. (2006) · Journal of Medical Virology · doi:10.1002/jmv.20556 · Cited by 147 · see citing works
COVID‐19 and comorbidities: A role for dipeptidyl peptidase 4 ( DPP4 ) in disease severity?
Bassendine, M. F., Bridge, S. H., McCaughan, G. W., & Gorrell, M. D. (2020) · Journal of Diabetes · doi:10.1111/1753-0407.13052 · Cited by 147 · see citing works
SARS-CoV-2 and nervous system: From pathogenesis to clinical manifestation
Keyhanian, K., Umeton, R. P., Mohit, B., Davoudi, V., Hajighasemi, F., & Ghasemi, M. (2020) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2020.577436 · Cited by 143 · see citing works
Systematic analysis of SARS-CoV-2 infection of an ACE2-negative human airway cell
Puray‐Chavez, M., LaPak, K. M., Schrank, T. P., Elliott, J. L., Bhatt, D. P., Agajanian, M. J., Jasuja, R., Lawson, D. Q., Davis, K., Rothlauf, P. W., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109364 · Cited by 131 · see citing works
SARS-CoV-2 productively infects primary human immune system cells in vitro and in COVID-19 patients
Pontelli, M. C., Castro, Í. A., Júnior, R. B. M., Serra, L. L., Veras, F. P., Nascimento, D. C., Silva, C. M. S., Cardoso, R. D. S., Rosales, R., Gomes, R., et al. (2022) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjac021 · Cited by 140 · see citing works
Cell-free DNA maps COVID-19 tissue injury and risk of death and can cause tissue injury
Andargie, T. E., Tsuji, T., Seifuddin, F., Jang, M. K., Yuen, P. S. T., Kong, H., Tunc, I., Singh, K., Charya, A. V., Wilkins, K. J., et al. (2021) · JCI Insight · doi:10.1172/jci.insight.147610 · Cited by 137 · see citing works
Nițulescu, G. M., Păunescu, H., Moschos, S. A., Petrakis, D., Nițulescu, G., Ion, D., Spandidos, D. A., Νikolouzakis, Τ. Κ., Drakoulis, N., & Tsatsakis, A. M. (2020) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2020.4608 · Cited by 131 · see citing works
Pathology of Experimental SARS Coronavirus Infection in Cats and Ferrets
van den Brand, J. M. A., Haagmans, B. L., Leijten, L. M. E., van Riel, D. A. J., Martina, B. E. E., Osterhaus, A. D. M. E., & Kuiken, T. (2008) · Veterinary Pathology · doi:10.1354/vp.45-4-551 · Cited by 113 · see citing works
Alsaied, T., Aboulhosn, J., Cotts, T. B., Daniels, C. J., Etheridge, S. P., Feltes, T. F., Gurvitz, M. Z., Lewin, M., Oster, M. E., & Saidi, A. S. (2020) · Journal of the American Heart Association · doi:10.1161/jaha.120.017224 · Cited by 118 · see citing works
Greenough, T. C., Carville, A., Coderre, J. A., Somasundaran, M., Sullivan, J. L., Luzuriaga, K., & Mansfield, K. G. (2005) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)62989-6 · Cited by 111 · see citing works
Covid-19, Coronavirus, SARS-CoV-2 and the small bowel
M�nkemüller, K., Fry, L. C., & Rickes, S. (2020) · Revista Española de Enfermedades Digestivas · doi:10.17235/reed.2020.7137/2020 · Cited by 105 · see citing works
Cardinale, V., Capurso, G., Ianiro, G., Gasbarrini, A., Arcidiacono, P. G., & Alvaro, D. (2020) · Digestive and Liver Disease · doi:10.1016/j.dld.2020.09.009 · Cited by 108 · see citing works
The therapeutic potential of apelin in kidney disease
Chapman, F. A., Nyimanu, D., Maguire, J. J., Davenport, A. P., Newby, D. E., & Dhaun, N. (2021) · Nature Reviews Nephrology · doi:10.1038/s41581-021-00461-z · Cited by 105 · see citing works
Molecular Biology of the SARS-Coronavirus
Lal, S. K. (2010) · Springer eBooks · doi:10.1007/978-3-642-03683-5 · Cited by 102 · see citing works
Damiano, R. F., Guedes, B. F., de Rocca, C. C., de Pádua Serafim, A., Castro, L. H. M., Munhoz, C. D., Nitrini, R., Filho, G. B., Miguel, E. C., Lucchetti, G., et al. (2022) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-021-01286-4 · Cited by 98 · see citing works
Temporal omics analysis in Syrian hamsters unravel cellular effector responses to moderate COVID-19
Nouailles, G., Wyler, E., Pennitz, P., Postmus, D., Vladimirova, D., Kazmierski, J., Pott, F., Dietert, K., Mülleder, M., Farztdinov, V. M., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25030-7 · Cited by 98 · see citing works
Thoughts on the alveolar phase of COVID-19
Mason, R. J. (2020) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00126.2020 · Cited by 96 · see citing works
Szczepański, A., Owczarek, K., Bzowska, M., Gula, K., Drebot, I., Ochman, M., Maksym, B., Rajfur, Z., Mitchell, J. A., & Pyrć, K. (2019) · Viruses · doi:10.3390/v11040328 · Cited by 96 · see citing works
Ballout, R. A., Sviridov, D., Bukrinsky, M., & Remaley, A. T. (2020) · The FASEB Journal · doi:10.1096/fj.202000654r · Cited by 94 · see citing works
Neurological consequences of COVID-19: what have we learned and where do we go from here?
Jarrahi, A., Ahluwalia, M., Khodadadi, H., Salles, É. L., Kolhe, R. B., Hess, D. C., Vale, F. Ĺ., Kumar, M., Baban, B., Vaibhav, K., et al. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01957-4 · Cited by 86 · see citing works
Orsini, A. A., Corsi, M., Santangelo, A., Riva, A., Peroni, D. G., Foiadelli, T., Savasta, S., & Striano, P. (2020) · Neurological Sciences · doi:10.1007/s10072-020-04544-w · Cited by 86 · see citing works
Zhang, L., Dong, L., Lei, M., Wei, M., Li, J., Hu, R., & Yang, J. (2020) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-020-03026-3 · Cited by 80 · see citing works
Venkatakrishnan, A., Puranik, A., Anand, A., Zemmour, D., Yao, X., Wu, X., Chilaka, R., Murakowski, D. K., Standish, K., Raghunathan, B., et al. (2020) · eLife · doi:10.7554/elife.58040 · Cited by 78 · see citing works
Overview of the pathogenesis of COVID‑19 (Review)
Li, C., He, Q., Qian, H., & Liu, J. (2021) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2021.10444 · Cited by 76 · see citing works
COVID-19: Coronavirus replication, pathogenesis, and therapeutic strategies
Bergmann, C. C., & Silverman, R. H. (2020) · Cleveland Clinic Journal of Medicine · doi:10.3949/ccjm.87a.20047 · Cited by 73 · see citing works
Briguglio, M., Bona, A. R., Porta, M., Dell’Osso, B. M., Pregliasco, F. E., & Banfi, G. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00671 · Cited by 69 · see citing works
Endothelial contribution to COVID-19: an update on mechanisms and therapeutic implications
Ma, Z., Yang, Y., Huang, Y., & Lui, K. O. (2021) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2021.11.010 · Cited by 68 · see citing works
Maric, S., Restin, T., Muff, J. L., Camargo, S. M. R., Guglielmetti, L. C., Holland-Cunz, S. G., Crenn, P. P., & Vuille-dit-Bille, R. N. (2021) · Nutrients · doi:10.3390/nu13082794 · Cited by 68 · see citing works
Liu, X., Cao, W., & Li, T. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01660 · Cited by 66 · see citing works
Coronaviruses, Toroviruses, and Arteriviruses
Siddell, S. G., Ziebuhr, J., & Snijder, E. J. (2010) · doi:10.1002/9780470688618.taw0245 · Cited by 64 · see citing works
Network perturbation analysis in human bronchial epithelial cells following SARS-CoV2 infection
Nunnari, G., Sanfilippo, C., Castrogiovanni, P., Imbesi, R., Volti, G. L., Barbagallo, I. A., Musumeci, G., & Rosa, M. D. (2020) · Experimental Cell Research · doi:10.1016/j.yexcr.2020.112204 · Cited by 60 · see citing works
SARS-CoV-2, More than a Respiratory Virus: Its Potential Role in Neuropathogenesis
Singal, C. M. S., Jaiswal, P., & Seth, P. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00251 · Cited by 58 · see citing works
Findings of Hepatic Severe Acute Respiratory Syndrome Coronavirus-2 Infection
Fiel, M. I., Jamal, S. M. E., Paniz‐Mondolfi, A., Gordon, R. E., Reidy, J., Bandovic, J., Advani, R. R., Kilaru, S. M., Pourmand, K., Ward, S. C., et al. (2020) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2020.09.015 · Cited by 57 · see citing works
Impact of COVID-19 on Alzheimer’s Disease Risk: Viewpoint for Research Action
Abate, G., Memo, M., & Uberti, D. (2020) · Healthcare · doi:10.3390/healthcare8030286 · Cited by 56 · see citing works
Yoshikawa, N., Yoshikawa, T., Hill, T. E., Huang, C., Watts, D. M., Makino, S., Milligan, G. N., Chan, T., Peters, C. J., & Tseng, C.-T. K. (2009) · Journal of Virology · doi:10.1128/jvi.02272-08 · Cited by 56 · see citing works
The Role of Extracellular Vesicles as Allies of HIV, HCV and SARS Viruses
Giannessi, F., Aiello, A., Franchi, F., Percario, Z. A., & Affabris, E. (2020) · Viruses · doi:10.3390/v12050571 · Cited by 56 · see citing works
Pathogenesis‐directed therapy of 2019 novel coronavirus disease
Stratton, C. W., Tang, Y., & Lu, H. (2020) · Journal of Medical Virology · doi:10.1002/jmv.26610 · Cited by 55 · see citing works
Chan, W. S., Wu, C. F., Chow, S. C. S., Cheung, T., To, K., Leung, W. K., Chan, P. K. S., Lee, K.-C., Ng, H., Au, D., et al. (2005) · Modern Pathology · doi:10.1038/modpathol.3800439 · Cited by 53 · see citing works
Self-citationCarnevale, S., Beretta, P., & Morbini, P. (2020) · Journal of Medical Virology · doi:10.1002/jmv.26119 · Cited by 52 · see citing works
Plasma mediators in patients with severe COVID-19 cause lung endothelial barrier failure
Michalick, L., Weidenfeld, S., Grimmer, B., Fatykhova, D., Solymosi, P., Behrens, F., Dohmen, M., Brack, M. C., Schulz, S., Thomasch, E., et al. (2020) · European Respiratory Journal · doi:10.1183/13993003.02384-2020 · Cited by 50 · see citing works
Post COVID-19 Ophthalmic Manifestations in an Asian Indian Male
Sanjay, S., Srinivasan, P., Jayadev, C., Mahendradas, P., Gupta, A., Kawali, A., & Shetty, R. (2021) · Ocular Immunology and Inflammation · doi:10.1080/09273948.2020.1870147 · Cited by 49 · see citing works
Susceptibility of human and rat neural cell lines to infection by SARS-coronavirus
Yamashita, M., Yamate, M., Li, G., & Ikuta, K. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.06.061 · Cited by 48 · see citing works
Diemer, C., Schneider, M., Seebach, J., Quaas, J., Frösner, G., Schätzl, H. M., & Gilch, S. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.11.081 · Cited by 48 · see citing works
New Corona Virus (COVID-19) Management in Pregnancy and Childbirth
Asadi, L., Tabatabaei, R. S., Safinejad, H., & Mohammadi, M. (2020) · Archives of Clinical Infectious Diseases · doi:10.5812/archcid.102938 · Cited by 48 · see citing works
Severe Acute Respiratory Syndrome (SARS)
Peiris, M. J. S. (2003) · Journal of Clinical Virology · doi:10.1016/j.jcv.2003.08.005 · Cited by 47 · see citing works
SARS‐CoV‐2 and the possible connection to ERs, ACE2, and RAGE: Focus on susceptibility factors
Stilhano, R. S., Costa, A. J., Nishino, M. S., Shams, S., Bartolomeo, C. S., Breithaupt‐Faloppa, A. C., Silva, E. A., Ramirez, A. L., Prado, C. M., & Ureshino, R. P. (2020) · The FASEB Journal · doi:10.1096/fj.202001394rr · Cited by 47 · see citing works
Tang, J. W.-T., To, K., Lo, A. W. I., Sung, J. J. �., Ng, H., & Chan, P. K. S. (2007) · Journal of Medical Virology · doi:10.1002/jmv.20873 · Cited by 44 · see citing works
Self-citationVimentin as a target for the treatment of COVID-19
Li, Z., Paulin, D., Lacolley, P. J., Coletti, D., & Agbulut, O. (2020) · BMJ Open Respiratory Research · doi:10.1136/bmjresp-2020-000623 · Cited by 40 · see citing works
Acute Viral Illnesses and Ischemic Stroke
Bahouth, M. N., & Venkatesan, A. (2021) · Stroke · doi:10.1161/strokeaha.120.030630 · Cited by 40 · see citing works
Age-Associated Neurological Complications of COVID-19: A Systematic Review and Meta-Analysis
Sullivan, B. N., & Fischer, T. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.653694 · Cited by 39 · see citing works
Suresh, V., Parida, D., Minz, A. P., Sethi, M., Sahoo, B. S., & Senapati, S. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.579330 · Cited by 38 · see citing works
Sanjay, S., Gowda, P. B., Rao, B., Mutalik, D., Mahendradas, P., Kawali, A., & Shetty, R. (2021) · Journal of Ophthalmic Inflammation and Infection · doi:10.1186/s12348-021-00244-4 · Cited by 37 · see citing works
Bioinformatic characterization of angiotensin-converting enzyme 2, the entry receptor for SARS-CoV-2
Barker, H. R., & Parkkila, S. (2020) · PLoS ONE · doi:10.1371/journal.pone.0240647 · Cited by 35 · see citing works
Chow, S. C. S., Ho, C. Y. S., Tam, T., Wu, C. F., Cheung, T. T., Chan, P. K. S., Ng, M. H. L., Hui, P. K., Ng, H., Au, D. M. Y., et al. (2006) · Journal of Clinical Pathology · doi:10.1136/jcp.2005.029868 · Cited by 36 · see citing works
Self-citationGai, W., Zou, W., Lei, L., Luo, J., Tu, H., Zhang, Y., Wang, K., Tien, P., & Yan, H. (2008) · Viral Immunology · doi:10.1089/vim.2007.0079 · Cited by 35 · see citing works
Heteromeric Solute Carriers: Function, Structure, Pathology and Pharmacology
Fairweather, S. J., Shah, N., & Bröer, S. (2020) · Advances in experimental medicine and biology · doi:10.1007/5584_2020_584 · Cited by 36 · see citing works
Obstetric Management of COVID-19 in Pregnant Women
Mei, Y., Luo, D., Wei, S., Liao, X., Pan, Y., Yang, X., & Lin, Y. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01186 · Cited by 34 · see citing works
A Comprehensive Summary of the Knowledge on COVID-19 Treatment
Peng, Y., Tao, H., Satyanarayanan, S. K., Jin, K., & Su, H. (2021) · Aging and Disease · doi:10.14336/ad.2020.1124 · Cited by 35 · see citing works
Yeung, K. S., Yamanaka, G. A., & Meanwell, N. A. (2006) · Medicinal Research Reviews · doi:10.1002/med.20055 · Cited by 31 · see citing works
Mithal, A., Hume, A. J., Lindstrom-Vautrin, J., Villacorta-Martín, C., Olejnik, J., Bullitt, E., Hinds, A., Mühlberger, E., & Mostoslavsky, G. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.02.019 · Cited by 32 · see citing works
Characteristics of a COVID-19 Cohort With Large Vessel Occlusion: A Multicenter International Study
Jabbour, P. M., Dmytriw, A. A., Sweid, A., Piotin, M., Bekelis, K., Sourour, N. A., Raz, E., Linfante, I., Dabus, G., Kole, M., et al. (2022) · Neurosurgery · doi:10.1227/neu.0000000000001902 · Cited by 32 · see citing works
Immunity after COVID-19 Recovery and Vaccination: Similarities and Differences
Kamińska, D., Dęborska−Materkowska, D., Kościelska−Kasprzak, K., Mazanowska, O., Remiorz, A., Poznański, P., Durlik, M., & Krajewska, M. (2022) · Vaccines · doi:10.3390/vaccines10071068 · Cited by 32 · see citing works
He, Z., Chin, Y., Yu, S., Huang, J. V., Zhang, C. J. P., Ke, Z., Azarakhsh, N., Sheng, J., He, Y., Jayavanth, P., et al. (2020) · JMIR Public Health and Surveillance · doi:10.2196/20495 · Cited by 31 · see citing works
Identification, Mechanism, and Treatment of Skin Lesions in COVID-19: A Review
Fernández‐Lázaro, D., & Garrosa, M. (2021) · Viruses · doi:10.3390/v13101916 · Cited by 31 · see citing works
Goblet Cell Hyperplasia Increases SARS-CoV-2 Infection in Chronic Obstructive Pulmonary Disease
Osan, J. K., Talukdar, S. N., Feldmann, F., DeMontigny, B. A., Jerome, K., Bailey, K. L., Feldmann, H., & Mehedi, M. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.00459-22 · Cited by 38 · see citing works
- Authors
- To, K., & Lo, A. W.
- Affiliations
- Chinese University of Hong Kong (HK)
- ORCID
- Lo, Anthony WI
- Venue
- The Journal of Pathology
- Publisher
- Wiley
- Published
- 2004-06-21
- Volume
- 203
- Issue
- 3
- Pages
- 740-743
- ISSN
- 0022-3417 (ISSN-L)
- 1096-9896
- PMC
- PMC7167902
- OpenAlex
- W2086347780
- Cited by
- 226
- References
- 42
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 9 · 2023: 8 · 2022: 25 · 2021: 47 · 2020: 77 · 2019: 1 · 2018: 1 · 2016: 2 · 2014: 3 · 2013: 3 · 2012: 2
- FWCI
- 4.68
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Pathology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Chinese University of Hong Kong
- 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 › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Keywords
- SARS, SARS-CoV, angiotensin-converting enzyme 2, viral receptor, tissue distribution, pathogenesis, pulmonary infection, intestinal infection, alveolar epithelial cells, enterocytes, endothelial cells, co-receptors, lymphoid system, vaccine development, therapeutic target
- MeSH terms
- Angiotensin-Converting Enzyme 2, Carboxypeptidases, Humans, Peptidyl-Dipeptidase A, Tissue Distribution, Severe Acute Respiratory Syndrome, Severe acute respiratory syndrome-related coronavirus
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