SARS-CoV-2 productively infects human gut enterocytes
Open accessPublished version of a preprint
Abstract
Intestinal organoids as an infection model: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) causes an influenza-like disease with a respiratory transmission route; however, patients often present with gastrointestinal symptoms such as diarrhea, vomiting, and abdominal pain. Moreover, the virus has been detected in anal swabs, and cells in the inner-gut lining express the receptor that SARS-CoV-2 uses to gain entry to cells. Lamers et al. used human intestinal organoids, a “mini-gut” cultured in a dish, to demonstrate that SARS-CoV-2 readily replicates in an abundant cell type in the gut lining—the enterocyte—resulting in the production of large amounts of infective virus particles in the intestine. This work demonstrates that intestinal organoids can serve as a model to understand SARS-CoV-2 biology and infectivity in the gut. Science , this issue p. 50
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?
Over 2,000 CFTR mutations have been reported, but small molecule therapeutics deployed clinically target only a subset of them.
“Over 2,000 mutations have been reported, yet small molecule therapeutics deployed clinically only target a subset of these185,186.”
From Organoids (2022) · cites this paper as [185]
The retrieved passages from the References section (page unavailable) concern coronavirus research, not CFTR mutation counts or CFTR-targeted therapies. Searches for CFTR, cystic fibrosis, 2,000 mutations, and small-molecule therapeutics found no passage in our copy addressing either part of the claim. (LLM, conf=0.78)
Experimental — accuracy not yet measuredCystic fibrosis is a genetic disorder caused by mutations in CFTR, which encodes a transmembrane chloride and bicarbonate transporter.
“Cystic fibrosis (CF) is a genetic disorder caused by mutations in the gene CFTR, which expresses a transmembrane chloride and bicarbonate transporter.”
From Organoids (2022) · cites this paper as [185]
The supplied Abstract and the passages on airway and gut organoids address SARS-CoV-2 infection, not cystic fibrosis. Searches for CFTR, cystic fibrosis, and chloride and bicarbonate transport found no passage in our copy that addresses the attributed claim. (LLM, conf=0.76)
Experimental — accuracy not yet measuredProductive SARS-CoV-2 infection has been demonstrated in enterocyte organoids in vitro.
“Productive infection has been demonstrated in enterocyte organoids in vitro (Lamers et al., 2020)”
From Viral Infections, the Microbiome, and Probiotics (2021) · cites this paper as Lamers et al., 2020
Low level expression of ACE2 can support CoV-2 cell entry.
“In addition, it has recently been reported that low level expression of ACE2 can support CoV-2 cell entry (86); it is possible, therefore, that ACE2 expression beneath the level of detection in our assays may yet enable CoV-2 infection of apparently ACE2 negative cell types.”
From Non-neuronal expression of SARS-CoV-2 entry genes in the olfactory system suggests mechanisms underlying COVID-19-associated anosmia (2020) · cites this paper as [86]
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
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607 · see citing works
Clinical characteristics of coronavirus disease 2019 in China
Guan, W.-J., Ni, Z.-Y., Hu, Y., Liang, W.-H., Ou, C.-Q., He, J.-X., Liu, L., Shan, H., Lei, C.-L., Hui, D. S. C., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2002032 · Cited by 30,246 · see citing works
A novel coronavirus from patients with pneumonia in China, 2019
Zhu, N., Zhang, D., Wang, W., Li, X., Yang, B., Song, J., Zhao, X., Huang, B., Shi, W., Lu, R., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2001017 · Cited by 28,244 · see citing works
Fast and accurate long-read alignment with Burrows-Wheeler transform.
Li, H., & Durbin, R. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp698 · Cited by 12,063 · see citing works
Lu, R., Zhao, X., Li, J., Niu, P., Yang, B., Wu, H., Wang, W., Song, H., Huang, B., Zhu, N., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)30251-8 · Cited by 11,907 · see citing works
Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation
Wrapp, D., Wang, N., Corbett, K. S., Goldsmith, J. A., Hsieh, C.-L., Abiona, O., Graham, B. S., & McLellan, J. S. (2020) · Science · doi:10.1126/science.abb2507 · Cited by 8,897 · see citing works
Structure, 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
Gorbalenya, A. E., Baker, S. C., Baric, R. S., de Groot, R. J., Drosten, C., Gulyaeva, A. A., Haagmans, B. L., Lauber, C., Leontovich, A. M., Neuman, B. W., et al. (2020) · Nature Microbiology · doi:10.1038/s41564-020-0695-z · Cited by 8,436 · see citing works
Self-citationDetection of 2019 novel coronavirus (2019-nCoV) by real-time RT-PCR
Corman, V. M., Landt, O., Kaiser, M., Molenkamp, R., Meijer, A., Chu, D. K. W., Bleicker, T., Brünink, S., Schneider, J. A., Schmidt, M. L., et al. (2020) · Eurosurveillance · doi:10.2807/1560-7917.es.2020.25.3.2000045 · Cited by 7,266 · see citing works
Self-citationFirst case of 2019 novel coronavirus in the United States
Holshue, M. L., DeBolt, C., Lindquist, S., Lofy, K. H., Wiesman, J., Bruce, H., Spitters, C., Ericson, K., Wilkerson, S., Tural, A., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2001191 · Cited by 6,030 · see citing works
The proximal origin of SARS-CoV-2
Andersen, K. G., Rambaut, A., Lipkin, W. I., Holmes, E. C., & Garry, R. F. (2020) · Nature Medicine · doi:10.1038/s41591-020-0820-9 · Cited by 5,081 · see citing works
Detection of SARS-CoV-2 in Different Types of Clinical Specimens
Wang, W., Xu, Y., Gao, R., Lu, R., Han, K., Wu, G., & Tan, W. (2020) · JAMA · doi:10.1001/jama.2020.3786 · Cited by 5,019 · see citing works
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 · 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
Imbalanced Host Response to SARS-CoV-2 Drives Development of COVID-19
Blanco-Melo, D., Nilsson-Payant, B. E., Liu, W.-C., Uhl, S., Hoagland, D., Møller, R., Jordan, T. X., Oishi, K., Panis, M., Sachs, D., et al. (2020) · Cell · doi:10.1016/j.cell.2020.04.026 · Cited by 4,222 · see citing works
Sato, T., Stange, D. E., Ferrante, M., Vries, R. G. J., van Es, J. H., van den Brink, S., van Houdt, W. J., Pronk, A., van Gorp, J., Siersema, P. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.07.050 · Cited by 3,753 · see citing works
Organoid Models and Applications in Biomedical Research
Xinaris, C., Brizi, V., & Remuzzi, G. (2015) · The Nephron journals/Nephron journals · doi:10.1159/000433566 · Cited by 3,517 · see citing works
A 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
Evidence for gastrointestinal infection of SARS-CoV-2
Xiao, F., Tang, M., Zheng, X., Liu, Y., Li, X., & Shan, H. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.02.055 · Cited by 2,836 · 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
Monteil, V., Kwon, H., Prado, P., Hagelkrüys, A., Wimmer, R. A., Stahl, M., Leopoldi, A., Garreta, E., Hurtado del Pozo, C., Prosper, F., et al. (2020) · Cell · doi:10.1016/j.cell.2020.04.004 · Cited by 2,122 · see citing works
COVID-19: Gastrointestinal Manifestations and Potential Fecal–Oral Transmission
Gu, J., Han, B., & Wang, J. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.02.054 · Cited by 1,505 · see citing works
Replication of human noroviruses in stem cell–derived human enteroids
Ettayebi, K., Crawford, S. E., Murakami, K., Broughman, J. R., Karandikar, U., Tenge, V. R., Neill, F. H., Blutt, S. E., Zeng, X.-L., Qu, L., et al. (2016) · Science · doi:10.1126/science.aaf5211 · Cited by 1,305 · see citing works
CEL-seq2: sensitive highly-multiplexed single-cell RNA-Seq
Hashimshony, T., Senderovich, N., Avital, G., Klochendler, A., de Leeuw, Y., Anavy, L., Gennert, D., Li, S., Livak, K. J., Rozenblatt-Rosen, O., et al. (2016) · Genome Biology · doi:10.1186/s13059-016-0938-8 · Cited by 1,125 · see citing works
Long‐term expanding human airway organoids for disease modeling
Sachs, N., Papaspyropoulos, A., Zomer‐van Ommen, D. D., Heo, I., Böttinger, L., Klay, D., Weeber, F., Huelsz‐Prince, G., Iakobachvili, N., Amatngalim, G. D., et al. (2019) · The EMBO Journal · doi:10.15252/embj.2018100300 · Cited by 1,082 · see citing works
Self-citationKnoops, K., Kikkert, M., van den Worm, S. H. E., Zevenhoven-Dobbe, J. C., van der Meer, Y., Koster, A. J., Mommaas, A. M., & Snijder, E. J. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060226 · Cited by 1,015 · see citing works
Self-citationJia, H. P., Look, D. C., Shi, L., Hickey, M. A., Pewe, L. L., Netland, J., Farzan, M., Wohlford-Lenane, C., Perlman, S. M., & McCray, P. B. (2005) · Journal of Virology · doi:10.1128/jvi.79.23.14614-14621.2005 · Cited by 950 · see citing works
Single-Cell RNA Expression Profiling of ACE2, the Receptor of SARS-CoV-2
Zhao, Y., Zhao, Z., Wang, Y., Zhou, Y., Ma, Y., & Zuo, W. (2020) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.202001-0179le · Cited by 916 · see citing works
Qi, F., Qian, S., Zhang, S., & Zhang, Z. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.03.044 · Cited by 905 · see citing works
Single-cell RNA expression profiling of ACE2, the receptor of SARS-CoV-2
Zhao, Y., Zhao, Z., Wang, Y., Zhou, Y., Ma, Y., & Zuo, W. (2020) · doi:10.1101/2020.01.26.919985 · Cited by 860 · see citing works
The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent ‘+4’ cell markers
Muñoz, J., Stange, D. E., Schepers, A. G., van de Wetering, M., Koo, B., Itzkovitz, S., Volckmann, R., Kung, K. S., Köster, J., Radulescu, S., et al. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.166 · Cited by 758 · see citing works
Self-citationEnteric 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
Kristiansen, K., Hagen, S., Kollevold, T., TORVIK, A., Holme, I., Stat, M. A., Nesbakken, R., Hatlevoll, R., Lindgren, M., Brun, A., et al. (1981) · Cancer · doi:10.1002/1097-0142(19810215)47:4 · Cited by 424 · see citing works
Kaimal, V., Bardes, E. E., Tabar, S., Jegga, A. G., & Aronow, B. J. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq418 · Cited by 375 · see citing works
Jiang, S., Du, L., & Shi, Z. (2020) · Emerging Microbes & Infections · doi:10.1080/22221751.2020.1723441 · Cited by 330 · see citing works
Enteroendocrine cells switch hormone expression along the crypt-to-villus BMP signalling gradient
Beumer, J., Artegiani, B., Post, Y., Reimann, F. M., Gribble, F. M., Nguyen, T. N., Zeng, H., van den Born, M., van Es, J. H., & Clevers, H. C. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0143-y · Cited by 280 · see citing works
Self-citationA Single-Cell RNA Expression Map of Human Coronavirus Entry Factors
Singh, M., Bansal, V., & Feschotte, C. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108175 · Cited by 239 · see citing works
Cholankeril, G. T., Podboy, A. J., Aivaliotis, V. I., Tarlow, B., Pham, E. A., Spencer, S. P., Kim, D., Hsing, A. W., & Ahmed, A. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.04.008 · Cited by 208 · see citing works
Virtual nanoscopy: Generation of ultra-large high resolution electron microscopy maps
Faas, F. G. A., Avramut, M. C., van den Berg, B. M., Mommaas, A. M., Koster, A. J., & Ravelli, R. B. G. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201201140 · Cited by 169 · see citing works
Self-citationDrummond, C., Bolock, A. M., Ma, C., Luke, C. J., Good, M. L., & Coyne, C. B. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1617363114 · Cited by 150 · see citing works
Saxena, K., Simon, L. M., Zeng, X., Blutt, S. E., Crawford, S. E., Sastri, N. P., Karandikar, U. C., Ajami, N. J., Zachos, N. C., Kovbasnjuk, O. N., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1615422114 · Cited by 120 · see citing works
Transformation of intestinal stem cells into gastric stem cells on loss of transcription factor Cdx2
Simmini, S., Bialecka, M., Huch, M., Kester, L. A., van de Wetering, M., Sato, T., Beck, F., van Oudenaarden, A., Clevers, H. C., & Deschamps, J. (2014) · Nature Communications · doi:10.1038/ncomms6728 · Cited by 105 · see citing works
Self-citationType III interferon signaling restricts enterovirus 71 infection of goblet cells
Good, C. A., Wells, A. I., & Coyne, C. B. (2019) · Science Advances · doi:10.1126/sciadv.aau4255 · Cited by 99 · see citing works
Hosmillo, M. D. T., Chaudhry, Y., Nayak, K., Sorgeloos, F., Koo, B., Merenda, A., Lillestøl, R., Drumright, L. N., Zilbauer, M., & Goodfellow, I. (2020) · mBio · doi:10.1128/mbio.00215-20 · Cited by 91 · see citing works
Clevers, H. C. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0258-4 · Cited by 75 · see citing works
Self-citationPublishing and sharing multi-dimensional image data with OMERO
Burel, J.-M., Besson, S., Blackburn, C., Carroll, M., Ferguson, R. K., Flynn, H., Gillen, K., Leigh, R., Li, S., Lindner, D., et al. (2015) · Mammalian Genome · doi:10.1007/s00335-015-9587-6 · Cited by 62 · 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
Features of enteric disease from human coronaviruses: Implications for COVID‐19
Cimolai, N. (2020) · Journal of Medical Virology · doi:10.1002/jmv.26066 · Cited by 33 · see citing works
Successful management of the first reported case in Austria of COVID-19 with ARDS
Seitz, T., Hoepler, W., Weseslindtner, L., Aberle, J. H., Aberle, S. W., Puchhammer-Stoeckl, E., Baumgartner, S., Traugott, M. T., Karolyi, M., Pawelka, E., et al. (2020) · Infection · doi:10.1007/s15010-020-01458-9 · Cited by 15 · see citing works
Activation of the SARS-CoV-2 Receptor Ace2 by Cytokines Through Pan JAK-STAT EnhancersPreprint
Hennighausen, L. G., & Lee, H. (2020) · SSRN Electronic Journal · doi:10.2139/ssrn.3601827 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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 · see citing works
Human organoids: model systems for human biology and medicine
Kim, J., Koo, B.-K., & Knoblich, J. A. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0259-3 · Cited by 2,187 · see citing works
Evolution of antibody immunity to SARS-CoV-2
Gaebler, C., Wang, Z., Lorenzi, J. C. C., Muecksch, F., Finkin, S., Tokuyama, M., Cho, A., Jankovic, M., Schaefer-Babajew, D., Oliveira, T. Y., et al. (2021) · Nature · doi:10.1038/s41586-021-03207-w · Cited by 1,674 · see citing works
Long COVID or post-COVID-19 syndrome: putative pathophysiology, risk factors, and treatments
Yong, S. J. (2021) · Infectious Diseases · doi:10.1080/23744235.2021.1924397 · Cited by 1,339 · see citing works
Brann, D. H., Tsukahara, T., Weinreb, C., Lipovsek, M., Van den Berge, K., Gong, B., Chance, R., Macaulay, I. C., Chou, H.-J., Fletcher, R. B., et al. (2020) · Science Advances · doi:10.1126/sciadv.abc5801 · Cited by 1,198 · see citing works
Hofer, M., & Lutolf, M. P. (2021) · Nature Reviews Materials · doi:10.1038/s41578-021-00279-y · Cited by 1,184 · 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
Zhao, Z., Chen, X., Dowbaj, A. M., Sljukic, A., Bratlie, K., Lin, L., Fong, E. L. S., Balachander, G. M., Chen, Z., Soragni, A., et al. (2022) · Nature Reviews Methods Primers · doi:10.1038/s43586-022-00174-y · Cited by 1,001 · see citing works
TMPRSS2 and TMPRSS4 promote SARS-CoV-2 infection of human small intestinal enterocytes
Zang, R., Castro, M. F. G., McCune, B. T., Zeng, Q., Rothlauf, P. W., Sonnek, N. M., Liu, Z., Brulois, K. F., Wang, X., Greenberg, H. B., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.abc3582 · Cited by 982 · see citing works
SARS-CoV-2: Structure, Biology, and Structure-Based Therapeutics Development
Wang, M.-Y., Zhao, R., Gao, L.-J., Gao, X.-F., Wang, D.-P., & Cao, J.-M. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.587269 · Cited by 874 · see citing works
Viable SARS-CoV-2 in the air of a hospital room with COVID-19 patients
Lednicky, J. A., Lauzardo, M., Fan, Z. H., Jutla, A., Tilly, T. B., Gangwar, M., Usmani, M., Shankar, S. N., Mohamed, K., Eiguren-Fernandez, A., et al. (2020) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2020.09.025 · Cited by 683 · see citing works
Identification of SARS-CoV-2 inhibitors using lung and colonic organoids
Han, Y., Duan, X., Yang, L., Nilsson-Payant, B. E., Wang, P., Duan, F., Tang, X., Yaron, T. M., Zhang, T., Uhl, S., et al. (2021) · Nature · doi:10.1038/s41586-020-2901-9 · Cited by 530 · see citing works
SARS‐CoV‐2 targets neurons of 3D human brain organoids
Ramani, A., Müller, L., Ostermann, P. N., Gabriel, E., Abida‐Islam, P., Müller‐Schiffmann, A., Mariappan, A., Goureau, O., Gruell, H., Walker, A., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2020106230 · Cited by 518 · see citing works
Interplay between SARS-CoV-2 and the type I interferon response
Sa Ribero, M., Jouvenet, N., Dreux, M., & Nisole, S. (2020) · PLOS Pathogens · doi:10.1371/journal.ppat.1008737 · Cited by 443 · see citing works
Carter, M. J., Fish, M., Jennings, A., Doores, K. J., Wellman, P., Seow, J., Acors, S., Graham, C., Timms, E., Kenny, J., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-1054-6 · Cited by 419 · see citing works
Progenitor identification and SARS-CoV-2 infection in human distal lung organoids
Salahudeen, A. A., Choi, S. S., Rustagi, A., Zhu, J., van Unen, V., de la O, S. M., Flynn, R. A., Margalef-Català, M., Santos, A. J. M., Ju, J., et al. (2020) · Nature · doi:10.1038/s41586-020-3014-1 · Cited by 416 · see citing works
Katsura, H., Sontake, V., Tata, A., Kobayashi, Y., Edwards, C. E., Heaton, B. E., Konkimalla, A., Asakura, T., Mikami, Y., Fritch, E. J., et al. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.10.005 · Cited by 416 · see citing works
SARS-CoV-2 Orf9b suppresses type I interferon responses by targeting TOM70
Jiang, H.-W., Zhang, H.-N., Meng, Q.-F., Xie, J., Li, Y., Chen, H., Zheng, Y.-X., Wang, X.-N., Qi, H., Zhang, J., et al. (2020) · Cellular & Molecular Immunology · doi:10.1038/s41423-020-0514-8 · Cited by 351 · see citing works
Three-dimensional human alveolar stem cell culture models reveal infection response to SARS-CoV-2
Youk, J., Kim, T., Evans, K. V., Jeong, Y.-I., Hur, Y., Hong, S. P., Kim, J. H., Yi, K., Kim, S. Y., Na, K. J., et al. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.10.004 · Cited by 266 · see citing works
SARS-CoV-2 infects the human kidney and drives fibrosis in kidney organoids
Jansen, J., Reimer, K. C., Nagai, J. S., Varghese, F. S., Overheul, G. J., de Beer, M., Roverts, R., Daviran, D., Fermin, L. A. S., Willemsen, B., et al. (2022) · Cell Stem Cell · doi:10.1016/j.stem.2021.12.010 · Cited by 259 · see citing works
Lamers, M. M., van der Vaart, J., Knoops, K., Riesebosch, S., Breugem, T. I., Mykytyn, A. Z., Beumer, J., Schipper, D., Bezstarosti, K., Koopman, C. D., et al. (2021) · The EMBO Journal · doi:10.15252/embj.2020105912 · Cited by 227 · see citing works
Self-citationOral Microbiome and SARS-CoV-2: Beware of Lung Co-infection
Bao, L., Zhang, C., Dong, J., Zhao, L., Li, Y., & Sun, J. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01840 · Cited by 207 · see citing works
Heer, C. D., Sanderson, D. J., Voth, L. S., Alhammad, Y. M. O., Schmidt, M. S., Trammell, S. A. J., Perlman, S., Cohen, M. S., Fehr, A. R., & Brenner, C. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra120.015138 · Cited by 192 · see citing works
SARS-CoV-2 Infects Human Engineered Heart Tissues and Models COVID-19 Myocarditis
Bailey, A. L., Dmytrenko, O., Greenberg, L., Bredemeyer, A. L., Ma, P., Liu, J., Penna, V., Winkler, E. S., Sviben, S., Brooks, E., et al. (2021) · JACC: Basic to Translational Science · doi:10.1016/j.jacbts.2021.01.002 · Cited by 193 · see citing works
Zhou, Y., Hou, Y., Shen, J., Mehra, R., Kallianpur, A., Culver, D. A., Gack, M. U., Farha, S., Zein, J., Comhair, S., et al. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000970 · Cited by 180 · see citing works
Viral Infections, the Microbiome, and Probiotics
Harper, A., Vijayakumar, V., Ouwehand, A. C., ter Haar, J., Obis, D., Espadaler, J., Binda, S., Desiraju, S., & Day, R. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.596166 · Cited by 177 · see citing works
Antigenic cartography of SARS-CoV-2 reveals that Omicron BA.1 and BA.2 are antigenically distinct
Mykytyn, A. Z., Rissmann, M., Kok, A., Rosu, M. E., Schipper, D., Breugem, T. I., van den Doel, P. B., Chandler, F., Bestebroer, T., de Wit, M., et al. (2022) · Science Immunology · doi:10.1126/sciimmunol.abq4450 · Cited by 153 · see citing works
Self-citationReorganisation of Faecal Microbiota Transplant Services During the COVID-19 Pandemic
Ianiro, G., Mullish, B. H., Kelly, C. R., Kassam, Z., Kuijper, E. J., Ng, S. C., Iqbal, T. H., Allegretti, J. R., Bibbò, S., Sokol, H., et al. (2020) · Gut · doi:10.1136/gutjnl-2020-321829 · Cited by 147 · see citing works
Bein, A., Kim, S., Goyal, G., Cao, W., Fadel, C., Naziripour, A., Sharma, S., Swenor, B., LoGrande, N., Nurani, A., et al. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.718484 · Cited by 83 · see citing works
Advanced human developmental toxicity and teratogenicity assessment using human organoid models
Li, M., Gong, J., Gao, L., Zou, T., Kang, J., & Xu, H. (2022) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2022.113429 · Cited by 84 · see citing works
Enabling peristalsis of human colon tumor organoids on microfluidic chips
Fang, G., Lu, H., Al-Nakashli, R., Chapman, R., Zhang, Y., Ju, L. A., Lin, G., Stenzel, M. H., & Jin, D. (2022) · Biofabrication · doi:10.1088/1758-5090/ac2ef9 · Cited by 77 · see citing works
Feeding intolerance in critically ill patients with COVID-19
Liu, R., Paz, M., Siraj, L., Boyd, T., Salamone, S., Lite, T.-L. V., Leung, K. M., Chirinos, J. D., Shang, H. H., Townsend, M. J., et al. (2022) · Clinical Nutrition · doi:10.1016/j.clnu.2021.03.033 · Cited by 54 · see citing works
COVID-19 as a trigger for type 1 diabetes
Wang, Y., Guo, H., Wang, G., Zhai, J., & Du, B. (2023) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgad165 · Cited by 50 · see citing works
Tao, W., Wang, X., Zhang, G., Guo, M., Ma, H., Zhao, D., Sun, Y., He, J., Liu, L., Zhang, K., et al. (2021) · Protein & Cell · doi:10.1007/s13238-020-00778-8 · Cited by 42 · see citing works
Mini organs reveal how the coronavirus ravages the body
Mallapaty, S. (2020) · Nature · doi:10.1038/d41586-020-01864-x · Cited by 24 · see citing works
Yantiss, R. K., Qin, L., He, B., Crawford, C. V., Seshan, S., Patel, S., Wahid, N., & Jessurun, J. (2022) · American Journal of Surgical Pathology · doi:10.1097/pas.0000000000001755 · Cited by 23 · see citing works
Severe COVID-19 initially presenting as mesenteric adenopathy
Noda, S., Ma, J., Romberg, E. K., Hernandez, R. E., & Ferguson, M. R. (2021) · Pediatric Radiology · doi:10.1007/s00247-020-04789-9 · Cited by 19 · see citing works
- Authors
- Lamers, M. M., Beumer, J., van der Vaart, J., Knoops, K., Puschhof, J., Breugem, T. I., Ravelli, R. B. G., Paul van Schayck, J., Mykytyn, A. Z., Duimel, H. Q., van Donselaar, E., Riesebosch, S., Kuijpers, H. J. H., Schipper, D., van de Wetering, W. J., de Graaf, M., Koopmans, M., Cuppen, E., Peters, P. J., Haagmans, B. L., & Clevers, H.
- Affiliations
- Erasmus MC (NL)
- Royal Netherlands Academy of Arts and Sciences (NL)
- Oncode Institute, Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences and University Medical Center, Utrecht, Netherlands.
- Maastricht University (NL)
- The Maastricht Multimodal Molecular Imaging Institute, Maastricht University, Maastricht, Netherlands.
- Viroscience Department, Erasmus Medical Center, Rotterdam, Netherlands.
- University Medical Center Utrecht (NL)
- Corresponding author
- Lamers, Mart M.
- Beumer, Joep
- Haagmans, Bart L.
- Clevers, Hans
- ORCID
- Venue
- Science
- Published
- 2020-07-03
- Volume
- 369
- Issue
- 6499
- Pages
- 50-54
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC7199907
- OpenAlex
- W3020909574
- Cited by
- 1,573
- References
- 51
- Citations by year
- 2026: 62 · 2025: 79 · 2024: 120 · 2023: 194 · 2022: 286 · 2021: 476 · 2020: 353 · 2018: 1 · 2017: 1
- FWCI
- 42.97
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Science (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, cc-by)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion, other-oa)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, cc-by)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, other-oa)
- RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- Funders
- European Research Council (67013)
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (022.005.032, 184.034.019 (X-omics))
- Dutch Technology Foundation STW (14207)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Health Sciences › Medicine › Infectious Diseases › Viral gastroenteritis research and epidemiology
- Keywords
- SARS-CoV-2, COVID-19 pandemic, enterocytes, intestinal epithelium, ACE2 receptor, small intestinal organoids, viral replication, viral shedding, experimental infection model
- MeSH terms
- Betacoronavirus, Angiotensin-Converting Enzyme 2, SARS-CoV-2, Cell Differentiation, Culture Media, Humans, Ileum, Peptidyl-Dipeptidase A, Lung, Male, Organoids, Receptors, Virus, RNA, Messenger, Virus Replication, Gene Expression, Cell Culture Techniques, Cell Lineage, Respiratory Mucosa, Enterocytes, Severe acute respiratory syndrome-related coronavirus, Cell Proliferation
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
