Student or educator? Sign up with your school email and get 6 months of Pro free.
Cited by 988

The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.

Receptor and viral determinants of SARS‐coronavirus adaptation to human ACE2

Open access
Li, Wenhui, Zhang, Chengsheng, Sui, Jianhua, Kuhn, Jens H, Moore, Michael J, Luo, Shiwen, Wong, Swee‐Kee, Huang, I‐Chueh, Xu, Keming, Vasilieva, Natalya, Murakami, Akikazu, He, Yaqing, Marasco, Wayne A, Guan, Yi, Choe, Hyeryun, Farzan, Michael·2005·The EMBO Journal

Abstract

Human angiotensin‐converting enzyme 2 (ACE2) is a functional receptor for SARS coronavirus (SARS‐CoV). Here we identify the SARS‐CoV spike (S)‐protein‐binding site on ACE2. We also compare S proteins of SARS‐CoV isolated during the 2002–2003 SARS outbreak and during the much less severe 2003–2004 outbreak, and from palm civets, a possible source of SARS‐CoV found in humans. All three S proteins bound to and utilized palm‐civet ACE2 efficiently, but the latter two S proteins utilized human ACE2 markedly less efficiently than did the S protein obtained during the earlier human outbreak. The lower affinity of these S proteins could be complemented by altering specific residues within the S‐protein‐binding site of human ACE2 to those of civet ACE2, or by altering S‐protein residues 479 and 487 to residues conserved during the 2002–2003 outbreak. Collectively, these data describe molecular interactions important to the adaptation of SARS‐CoV to human cells, and provide insight into the severity of the 2002–2003 SARS epidemic.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/sj.emboj.7600640

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Research works printed but not linked: 41

  1. Babcock GJ, Esshaki DJ, Thomas Jr WD, Ambrosino DM (2004) Amino acids 270 to 510 of the severe acute respiratory syndrome coronavirus spike protein are required for interaction with receptor. J Virol 78: 4552–4560 · DOI
  2. Casais R, Dove B, Cavanagh D, Britton P (2003) Recombinant avian infectious bronchitis virus expressing a heterologous spike gene demonstrates that the spike protein is a determinant of cell tropism. J Virol 77: 9084–9089 · DOI · Paper page
  3. Chan PK, To KF, Lo AW, Cheung JL, Chu I, Au FW, Tong JH, Tam JS, Sung JJ, Ng HK (2004) Persistent infection of SARS coronavirus in colonic cells in vitro. J Med Virol 74: 1–7 · DOI
  4. Dales NA, Gould AE, Brown JA, Calderwood EF, Guan B, Minor CA, Gavin JM, Hales P, Kaushik VK, Stewart M, Tummino PJ, Vickers CS, Ocain TD, Patane MA (2002) Substrate‐based design of the first class of angiotensin‐converting enzyme‐related carboxypeptidase (ACE2) inhibitors. J Am Chem Soc 124: 11852–11853 · DOI
  5. Ding Y, He L, Zhang Q, Huang Z, Che X, Hou J, Wang H, Shen H, Qiu L, Li Z, Geng J, Cai J, Han H, Li X, Kang W, Weng D, Liang P, Jiang S (2004) Organ distribution of severe acute respiratory syndrome (SARS) associated coronavirus (SARS‐CoV) in SARS patients: implications for pathogenesis and virus transmission pathways. J Pathol 203: 622–630 · DOI · Paper page
  6. Fouchier RA, Kuiken T, Schutten M, van Amerongen G, van Doornum GJ, van den Hoogen BG, Peiris M, Lim W, Stohr K, Osterhaus AD (2003) Aetiology: Koch's postulates fulfilled for SARS virus. Nature 423: 240 · DOI · Paper page
  7. Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX, Cheung CL, Luo SW, Li PH, Zhang LJ, Guan YJ, Butt KM, Wong KL, Chan KW, Lim W, Shortridge KF, Yuen KY, Peiris JS, Poon LL (2003) Isolation and characterization of viruses related to the SARS coronavirus from animals in Southern China. Science 4: 4
  8. Haijema BJ, Volders H, Rottier PJ (2003) Switching species tropism: an effective way to manipulate the feline coronavirus genome. J Virol 77: 4528–4538 · DOI
  9. Hamming I, Timens W, Bulthuis ML, Lely AT, Navis GJ, van Goor H (2004) Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol 203: 631–637 · DOI · Paper page
  10. Harmer D, Gilbert M, Borman R, Clark KL (2002) Quantitative mRNA expression profiling of ACE 2, a novel homologue of angiotensin converting enzyme. FEBS Lett 532: 107–110 · DOI · Paper page
  11. He JF, Peng GW, Min J, Yu DW, Liang WJ, Zhang SY, Xu RH, Zheng HY, Wu XW, Xu J, Wang ZH, Fang L, Zhang X, Li H, Yan XG, Lu JH, Hu ZH, Huang JC, Wan XW (2004) Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 303: 1666–1669, Epub 2004 Jan 29 · DOI · Paper page
  12. Hofmann H, Geier M, Marzi A, Krumbiegel M, Peipp M, Fey GH, Gramberg T, Pohlmann S (2004) Susceptibility to SARS coronavirus S protein‐driven infection correlates with expression of angiotensin converting enzyme 2 and infection can be blocked by soluble receptor. Biochem Biophys Res Commun 319: 1216–1221 · DOI · Paper page
  13. Hofmann H, Pohlmann S (2004) Cellular entry of the SARS coronavirus. Trends Microbiol 12: 466–472 · DOI
  14. Jeffers SA, Tusell SM, Gillim‐Ross L, Hemmila EM, Achenbach JE, Babcock GJ, Thomas Jr WD, Thackray LB, Young MD, Mason RJ, Ambrosino DM, Wentworth DE, Demartini JC, Holmes KV (2004) CD209L (L‐SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc Natl Acad Sci USA 101: 15748–15753, Epub 2004 Oct 20 · DOI · Paper page
  15. Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T, Emery S, Tong S, Urbani C, Comer JA, Lim W, Rollin PE, Dowell SF, Ling AE, Humphrey CD, Shieh WJ, Guarner J, Paddock CD, Rota P, Fields B, DeRisi J, Yang JY, Cox N, Hughes JM, LeDuc JW, Bellini WJ, Anderson LJ (2003) A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med 348: 1953–1966 · DOI · Paper page
  16. Kuiken T, Fouchier RA, Schutten M, Rimmelzwaan GF, van Amerongen G, van Riel D, Laman JD, de Jong T, van Doornum G, Lim W, Ling AE, Chan PK, Tam JS, Zambon MC, Gopal R, Drosten C, van der Werf S, Escriou N, Manuguerra JC, Stohr K, Peiris JS, Osterhaus AD (2003) Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362: 263–270 · DOI · Paper page
  17. Kuo L, Godeke GJ, Raamsman MJ, Masters PS, Rottier PJ (2000) Retargeting of coronavirus by substitution of the spike glycoprotein ectodomain: crossing the host cell species barrier. J Virol 74: 1393–1406 · DOI · Paper page
  18. Li W, Greenough TC, Moore MJ, Vasilieva N, Somasundaran M, Sullivan JL, Farzan M, Choe H (2004) Efficient replication of severe acute respiratory syndrome coronavirus in mouse cells is limited by murine angiotensin‐converting enzyme 2. J Virol 78: 11429–11433 · DOI
  19. Liang G, Chen Q, Xu J, Liu Y, Lim W, Peiris JS, Anderson LJ, Ruan L, Li H, Kan B, Di B, Cheng P, Chan KH, Erdman D, Gu S, Xinge Y, Liang W, Zhou D, Haynes L (2004) Laboratory diagonosis of four recent sporadic cases of community‐acquired SARS, Guangdong Province, China. Emerg Infect Dis 10: 1774–1781 · DOI
  20. Marra MA, Jones SJ, Astell CR, Holt RA, Brooks‐Wilson A, Butterfield YS, Khattra J, Asano JK, Barber SA, Chan SY, Cloutier A, Coughlin SM, Freeman D, Girn N, Griffith OL, Leach SR, Mayo M, McDonald H, Montgomery SB, Pandoh PK, Petrescu AS, Robertson AG, Schein JE, Siddiqui A, Smailus DE, Stott JM, Yang GS, Plummer F, Andonov A, Artsob H, Bastien N, Bernard K, Booth TF, Bowness D, Czub M, Drebot M, Fernando L, Flick R, Garbutt M, Gray M, Grolla A, Jones S, Feldmann H, Meyers A, Kabani A, Li Y, Normand S, Stroher U, Tipples GA, Tyler S, Vogrig R, Ward D, Watson B, Brunham RC, Krajden M, Petric M, Skowronski DM, Upton C, Roper RL (2003) The genome sequence of the SARS‐associated coronavirus. Science 300: 1399–1404 · DOI · Paper page
  21. Marzi A, Gramberg T, Simmons G, Moller P, Rennekamp AJ, Krumbiegel M, Geier M, Eisemann J, Turza N, Saunier B, Steinkasserer A, Becker S, Bates P, Hofmann H, Pohlmann S (2004) DC‐SIGN and DC‐SIGNR interact with the glycoprotein of Marburg virus and the S protein of severe acute respiratory syndrome coronavirus. J Virol 78: 12090–12095 · DOI · Paper page
  22. Moore MJ, Dorfman T, Li W, Wong SK, Li Y, Kuhn JH, Coderre J, Vasilieva N, Han Z, Greenough TC, Farzan M, Choe H (2004) Retroviruses pseudotyped with the severe acute respiratory syndrome coronavirus spike protein efficiently infect cells expressing angiotensin‐converting enzyme 2. J Virol 78: 10628–10635 · DOI
  23. Nie Y, Wang P, Shi X, Wang G, Chen J, Zheng A, Wang W, Wang Z, Qu X, Luo M, Tan L, Song X, Yin X, Ding M, Deng H (2004) Highly infectious SARS‐CoV pseudotyped virus reveals the cell tropism and its correlation with receptor expression. Biochem Biophys Res Commun 321: 994–1000 · DOI
  24. Normile D (2004) Infectious diseases. Mounting lab accidents raise SARS fears. Science 304: 659–661 · DOI
  25. Peiris JS, Guan Y, Yuen KY (2004) Severe acute respiratory syndrome. Nat Med 10: S88–97 · DOI · Paper page
  26. Rota PA, Oberste MS, Monroe SS, Nix WA, Campagnoli R, Icenogle JP, Penaranda S, Bankamp B, Maher K, Chen MH, Tong S, Tamin A, Lowe L, Frace M, DeRisi JL, Chen Q, Wang D, Erdman DD, Peret TC, Burns C, Ksiazek TG, Rollin PE, Sanchez A, Liffick S, Holloway B, Limor J, McCaustland K, Olsen‐Rasmussen M, Fouchier R, Gunther S, Osterhaus AD, Drosten C, Pallansch MA, Anderson LJ, Bellini WJ (2003) Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300: 1394–1399 · DOI
  27. Schickli JH, Thackray LB, Sawicki SG, Holmes KV (2004) The N‐terminal region of the murine coronavirus spike glycoprotein is associated with the extended host range of viruses from persistently infected murine cells. J Virol 78: 9073–9083 · DOI
  28. Song HD, Tu CC, Zhang GW, Wang SY, Zheng K, Lei LC, Chen QX, Gao YW, Zhou HQ, Xiang H, Zheng HJ, Chern SW, Cheng F, Pan CM, Xuan H, Chen SJ, Luo HM, Zhou DH, Liu YF, He JF, Qin PZ, Li LH, Ren YQ, Liang WJ, Yu YD, Anderson L, Wang M, Xu RH, Wu XW, Zheng HY, Chen JD, Liang G, Gao Y, Liao M, Fang L, Jiang LY, Li H, Chen F, Di B, He LJ, Lin JY, Tong S, Kong X, Du L, Hao P, Tang H, Bernini A, Yu XJ, Spiga O, Guo ZM, Pan HY, He WZ, Manuguerra JC, Fontanet A, Danchin A, Niccolai N, Li YX, Wu CI, Zhao GP (2005) Cross‐host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc Natl Acad Sci USA 102: 2430–2435, Epub 2005 Feb 04 · DOI · Paper page
  29. Subbarao K, McAuliffe J, Vogel L, Fahle G, Fischer S, Tatti K, Packard M, Shieh WJ, Zaki S, Murphy B (2004) Prior infection and passive transfer of neutralizing antibody prevent replication of severe acute respiratory syndrome coronavirus in the respiratory tract of mice. J Virol 78: 3572–3577 · DOI · Paper page
  30. Sui J, Li W, Murakami A, Tamin A, Matthews LJ, Wong SK, Moore MJ, St Clair Tallarico A, Olurinde M, Choe H, Anderson LJ, Bellini WJ, Farzan M, Marasco WA (2004) Potent neutralization of severe acute respiratory syndrome (SARS) coronavirus by a human mAb to S1 protein that blocks receptor association. Proc Natl Acad Sci USA 101: 2536–2541 · DOI · Paper page
  31. Sui J, Li W, Roberts A, Matthews LJ, Murakami A, Vogel L, Wong SK, Subbarao K, Farzan M, Marasco WA (2005) Evaluation of human mAb 80R in immunoprophylaxis of SARS by an animal study, epitope mapping and analysis of spike variants. J Virol in press · DOI
  32. Towler P, Staker B, Prasad SG, Menon S, Tang J, Parsons T, Ryan D, Fisher M, Williams D, Dales NA, Patane MA, Pantoliano MW (2004) ACE2 X‐ray structures reveal a large hinge‐bending motion important for inhibitor binding and catalysis. J Biol Chem 279: 17996–18007, Epub 2004 Jan 30 · DOI · Paper page
  33. Webby R, Hoffmann E, Webster R (2004) Molecular constraints to interspecies transmission of viral pathogens. Nat Med 10: S77–S81 · DOI
  34. Wentworth DE, Gillim‐Ross L, Espina N, Bernard KA (2004) Mice susceptible to SARS coronavirus. Emerg Infect Dis 10: 1293–1296 · DOI
  35. Wong SK, Li W, Moore MJ, Choe H, Farzan M (2004) A 193‐amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin‐converting enzyme 2. J Biol Chem 279: 3197–3201, Epub 2003 Dec 11 · DOI · Paper page
  36. Wu D, Tu C, Xin C, Xuan H, Meng Q, Liu Y, Yu Y, Guan Y, Jiang Y, Yin X, Crameri G, Wang M, Li C, Liu S, Liao M, Feng L, Xiang H, Sun J, Chen J, Sun Y, Gu S, Liu N, Fu D, Eaton BT, Wang LF, Kong X (2005) Civets are equally susceptible to experimental infection by two different severe acute respiratory syndrome coronavirus isolates. J Virol 79: 2620–2625 · DOI
  37. Xiao X, Chakraborti S, Dimitrov AS, Gramatikoff K, Dimitrov DS (2003) The SARS‐CoV S glycoprotein: expression and functional characterization. Biochem Biophys Res Commun 312: 1159–1164 · DOI · Paper page
  38. Yang ZY, Huang Y, Ganesh L, Leung K, Kong WP, Schwartz O, Subbarao K, Nabel GJ (2004) pH‐dependent entry of severe acute respiratory syndrome coronavirus is mediated by the spike glycoprotein and enhanced by dendritic cell transfer through DC‐SIGN. J Virol 78: 5642–5650 · DOI · Paper page
  39. Zhang H, Wada J, Hida K, Tsuchiyama Y, Hiragushi K, Shikata K, Wang H, Lin S, Kanwar YS, Makino H (2001) Collectrin, a collecting duct‐specific transmembrane glycoprotein, is a novel homolog of ACE2 and is developmentally regulated in embryonic kidneys. J Biol Chem 276: 17132–17139 · DOI
  40. Zhang Y, Zheng N, Hao P, Zhong Y (2004) Reconstruction of the most recent common ancestor sequences of SARS‐CoV S gene and detection of adaptive evolution in the spike protein. Chinese Sci Bull 49: 1311–1313 · DOI
  41. Zhong N (2004) Management and prevention of SARS in China. Philos Trans R Soc London B 359: 1115–1116 · DOI

Cited by

See all 988

Metadata

Authors
Li, W., Zhang, C., Sui, J., Kuhn, J. H., Moore, M. J., Luo, S., Wong, S., Huang, I., Xu, K., Vasilieva, N., Murakami, A., He, Y., Marasco, W. A., Guan, Y., Choe, H., & Farzan, M.
Venue
The EMBO Journal
Published
2005-03-24
Volume
24
Issue
8
Pages
1634-1643
ISSN
  • 0261-4189 (ISSN-L)
  • 1460-2075
OpenAlex
W2038918691
Cited by
988
References
4
FWCI
19.61
Type
journal article
Language
en
Open access
green
Licence

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

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.