Animal origins of the severe acute respiratory syndrome coronavirus: Insight from ACE2-S-protein interactions

Journal of Virology

Volumn 80, Issue 9, 2006, Pages 4211-4219

  Li, Wenhui ^a,b,d   Wong, Swee Kee ^a   Li, Fang ^b   Kuhn, Jens H ^a,c   Huang, I Chueh ^a   Choe, Hyeryun ^b   Farzan, Michael ^a,b,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; CELL SURFACE RECEPTOR; DIPEPTIDYL CARBOXYPEPTIDASE; LYSINE; MICROSOMAL AMINOPEPTIDASE; THREONINE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RECEPTOR; VIRUS S PROTEIN;

ANIMAL; ANIMAL DISEASE; BADGER; BAT; CAT; FERRET; FOX; HOST CELL; HUMAN; MONKEY; NONHUMAN; PALM CIVET; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; SHORT SURVEY; VIRUS TRANSMISSION; ZOONOSIS;

ANIMALS; DNA-BINDING PROTEINS; HUMANS; RECEPTORS, VIRUS; SACCHAROMYCES CEREVISIAE PROTEINS; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; TRANSCRIPTION FACTORS; VIRAL PROTEINS; ZOONOSES;

ANIMALIA; CORONAVIRUS; MUSTELA PUTORIUS FURO; SARS CORONAVIRUS; TAXIDEA TAXUS;

EID: 33646192966     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.9.4211-4219.2006     Document Type: Short Survey

References (114)

1. Arpin, N., and P. J. Talbot. 1990. Molecular characterization of the 229E strain of human coronavirus. Adv. Exp. Med. Biol. 276:73-80.
2. Babcock, G. J., D. J. Esshaki, W. D. Thomas, Jr., and D. M. Ambrosino. 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.
3. Bonavia, A., B. D. Zelus, D. E. Wentworth, P. J. Talbot, and K. V. Holmes. 2003. Identification of a receptor-binding domain of the spike glycoprotein of human coronavirus HCoV-229E. J. Virol. 77:2530-2538.
4. Bosch, B. J., R. van der Zee, C. A. de Haan, and P. J. Rottier. 2003. The coronavirus spike protein is a class I virus fusion protein; structural and functional characterization of the fusion core complex. J. Virol. 77:8801-8811.
5. Breslin, J. J., I. Mork, M. K. Smith, L. K. Vogel, E. M. Hemmila, A. Bonavia, P. J. Talbot, H. Sjostrom, O. Noren, and K. V. Holmes. 2003. Human coronavirus 229E: receptor binding domain and neutralization by soluble receptor at 37°C. J. Virol. 77:4435-4438.
6. Brian, D. A., and R. S. Baric. 2005. Coronavirus genome structure and replication. Curr. Top. Microbiol. Immunol. 287:1-30.
7. Casais, R., B. Dove, D. Cavanagh, and P. Britton. 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.
8. Chan, P. K., K. F. To, A. W. Lo, J. L. Cheung, J. Chu, F. W. Au, J. H. Tong, J. S. Tam, J. J. Sung, and H. K. Ng. 2004. Persistent infection of SARS coronavirus in colonic cells in vitro. J. Med. Virol. 74:1-7.
9. Chandran, K., N. J. Sullivan, U. Felbor, S. P. Whelan, and J. M. Cunningham. 2005. Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308:1643-1645. (First published 14 April 2005; doi: 10.1126/science.1110656.)
10. Chen, Z., L. Zhang, C. Qin, L. Ba, C. E. Yi, F. Zhang, Q. Wei, T. He, W. Yu, J. Yu, H. Gao, X. Tu, A. Gettie, M. Farzan, K. Y. Yuen, and D. D. Ho. 2005. Recombinant modified vaccinia virus Ankara expressing the spike glycoprotein of severe acute respiratory syndrome coronavirus induces protective neutralizing antibodies primarily targeting the receptor binding region. J. Virol. 79:2678-2688.
11. Cherry, J. D. 2004. The chronology of the 2002-2003 SARS mini pandemic. Paediatr. Respir. Rev. 5:262-269.
12. Colman, P. M., and M. C. Lawrence. 2003. The structural biology of type I viral membrane fusion. Nat. Rev. Mol. Cell Biol. 4:309-319.
13. Crackower, M. A., R. Sarao, G. Y. Oudit, C. Yagil, I. Kozieradzki, S. E. Scanga, A. J. Oliveira-dos-Santos, J. da Costa, L. Zhang, Y. Pei, J. Scholey, C. M. Ferrario, A. S. Manoukian, M. C. Chappell, P. H. Backx, Y. Yagil, and J. M. Penninger. 2002. Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature 417:822-828.
14. Delmas, B., J. Gelfi, R. L'Haridon, L. K. Vogel, H. Sjostrom, O. Noren, and H. Laude. 1992. Aminopeptidase N is a major receptor for the enteropathogenic coronavirus TGEV. Nature 357:417-420.
15. Dimitrov, D. S. 2004. Virus entry: molecular mechanisms and biomedical applications. Nat. Rev. Microbiol. 2:109-122.
16. Ding, Y., L. He, Q. Zhang, Z. Huang, X. Che, J. Hou, H. Wang, H. Shen, L. Qiu, Z. Li, J. Geng, J. Cai, H. Han, X. Li, W. Kang, D. Weng, P. Liang, and S. Jiang. 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.
17. Donoghue, M., F. Hsieh, E. Baronas, K. Godbout, M. Gosselin, N. Stagliano, M. Donovan, B. Woolf, K. Robison, R. Jeyaseelan, R. E. Breitbart, and S. Acton. 2000. A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ. Res. 87:E1-E9.
18. Drosten, C., S. Gunther, W. Preiser, S. van der Werf, H. R. Brodt, S. Becker, H. Rabenau, M. Panning, L. Kolesnikova, R. A. Fouchier, A. Berger, A. M. Burgulere, J. Cinatl, M. Eickmann, N. Escriou, K. Grywna, S. Kramme, J. C. Manuguerra, S. Muller, V. Rickerts, M. Sturmer, S. Vieth, H. D. Klenk, A. D. Osterhaus, H. Schmitz, and H. W. Doerr. 2003. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348:1967-1976.
19. Dveksler, G. S., C. W. Dieffenbach, C. B. Cardellichio, K. McCuaig, M. N. Pensiero, G. S. Jiang, N. Beauchemin, and K. V. Holmes. 1993. Several members of the mouse carcinoembryonic antigen-related glycoprotein family are functional receptors for the coronavirus mouse hepatitis virus-A59. J. Virol. 67:1-8.
20. Dveksler, G. S., M. N. Pensiero, C. B. Cardellichio, R. K. Williams, G. S. Jiang, K. V. Holmes, and C. W. Dieffenbach. 1991. Cloning of the mouse hepatitis virus (MHV) receptor: expression in human and hamster cell lines confers susceptibility to MHV. J. Virol. 65:6881-6891.
21. Esper, F., C. Weibel, D. Ferguson, M. L. Landry, and J. S. Kahn. 2005. Evidence of a novel human coronavirus that is associated with respiratory tract disease in infants and young children. J. Infect. Dis. 191:492-498. [Online.]
22. Fleck, F. 2004. SARS virus returns to China as scientists race to find effective vaccine. Bull. W. H. O. 82:152-153.
23. Fouchier, R. A., N. G. Hartwig, T. M. Bestebroer, B. Niemeyer, J. C. de Jong, J. H. Simon, and A. D. Osterhaus. 2004. A previously undescribed coronavirus associated with respiratory disease in humans. Proc. Natl. Acad. Sci. USA 101:6212-6216.
24. Fouchier, R. A., T. Kuiken, M. Schutten, G. van Amerongen, G. J. van Doornum, B. G. van den Hoogen, M. Peiris, W. Lim, K. Stohr, and A. D. Osterhaus. 2003. Aetiology: Koch's postulates fulfilled for SARS virus. Nature 423:240.
25. Gallagher, T. M., and M. J. Buchmeier. 2001. Coronavirus spike proteins in viral entry and pathogenesis. Virology 279:371-374.
26. Gibbs, A. J., M. J. Gibbs, and J. S. Armstrong. 2004. The phylogeny of SARS coronavirus. Arch. Virol. 149:621-624.
27. Gonzalez, J. M., P. Gomez-Puertas, D. Cavanagh, A. E. Gorbalenya, and L. Enjuanes. 2003. A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae. Arch. Virol. 148:2207-2235.
28. Gorbalenya, A. E., E. J. Snijder, and W. J. Spaan. 2004. Severe acute respiratory syndrome coronavirus phylogeny: toward consensus. J. Virol. 78:7863-7866.
29. Gramberg, T., H. Hofmann, P. Moller, P. F. Lalor, A. Marzi, M. Geier, M. Krumbiegel, T. Winkler, F. Kirchhoff, D. H. Adams, S. Becker, J. Munch, and S. Pohlmann. 2005. LSECtin interacts with filovirus glycoproteins and the spike protein of SARS coronavirus. Virology 340:224-236.
30. Greenough, T. C., G. J. Babcock, A. Roberts, H. J. Hernandez, W. D. Thomas, Jr., J. A. Coccia, R. F. Graziano, M. Srinivasan, I. Lowy, R. W. Finberg, K. Subbarao, L. Vogel, M. Somasundaran, K. Luzuriaga, J. L. Sullivan, and D. M. Ambrosino. 2005. Development and characterization of a severe acute respiratory syndrome-associated coronavirus-neutralizing human monoclonal antibody that provides effective immunoprophylaxis in mice. J. Infect. Dis. 191:507-514.
31. Guan, Y., B. J. Zheng, Y. Q. He, X. L. Liu, Z. X. Zhuang, C. L. Cheung, S. W. Luo, P. H. Li, L. J. Zhang, Y. J. Guan, K. M. Butt, K. L. Wong, K. W. Chan, W. Lim, K. F. Shortridge, K. Y. Yuen, J. S. Peins, and L. L. Poon. 2003. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302:276-278.
32. Haijema, B. J., H. Volders, and P. J. Rottier. 2003. Switching species tropism: an effective way to manipulate the feline coronavirus genome. J. Virol. 77:4528-4538.
33. Hamming, I., W. Timens, M. L. Bulthuis, A. T.Lely, G. J. Navis, and H. van Goor. 2004. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus, A first step in understanding SARS pathogenesis. J. Pathol. 203:631-637.
34. Harmer, D., M. Gilbert, R. Borman, and K. L. Clark. 2002. Quantitative mRNA expression profiling of ACE 2, a novel homologue of angiotensin converting enzyme. FEBS Lett. 532:107-110.
35. He, J. F., G. W. Peng, J. Min, D. W. Yu, W. J. Liang, S. Y. Zhang, R. H. Xu, H. Y. Zheng, X. W. Wu, J. Xu, Z. H. Wang, L. Fang, X. Zhang, H. Li, X.-G. Yan, J. H. Lu, Z. H. Hu, J. C. Huang, and X. W. Wan. 2004. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 303:1666-1669.
36. He, Y., H. Lu, P. Siddiqui, Y. Zhou, and S. Jiang. 2005. Receptor-binding domain of severe acute respiratory syndrome coronavirus spike protein contains multiple conformation-dependent epitopes that induce highly potent neutralizing antibodies. J. Immunol. 174:4908-4915.
37. He, Y., Y. Zhou, S. Liu, Z. Kou, W. Li, M. Farzan, and S. Jiang. 2004. Receptor-binding domain of SARS-CoV spike protein induces highly potent neutralizing antibodies: implication for developing subunit vaccine. Biochem. Biophys. Res. Commun. 324:773-781.
38. He, Y., Y. Zhou, H. Wu, B. Luo, J. Chen, W. Li, and S. Jiang. 2004. Identification of immunodominant sites on the spike protein of severe acute respiratory syndrome (SARS) coronavirus: implication for developing SARS diagnostics and vaccines. J. Immunol. 173:4050-4057.
39. Hofmann, H., M. Geier, A. Marzi, M. Krumbiegel, M. Peipp, G. H. Fey, T. Gramberg, and S. Pohlmann. 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.
40. Hofmann, H., K. Pyre, L. van der Hoek, M. Geier, B. Berkhout, and S. Pohlmann. 2005. Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proc. Natl. Acad. Sci. USA 102:7988-7993.
41. Holmes, E. C., and A. Rambaut. 2004. Viral evolution and the emergence of SARS coronavirus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359:1059-1065.
42. Holmes, K. V. 2003. SARS coronavirus: a new challenge for prevention and therapy. J. Clin. Investig. 111:1605-1609.
43. 42a. Huang, I. C., B. J. Bosch, F. Li, W. Li, K. H. Lee, S. Ghiran, N. Vasilieva, T. S. Dermody, S. C. Harrison, P. R. Dormitzer, M. Farzan, P. J. Rottier, and H. Choe. 2006. SARS coronavirus, but not human coronavirus NL63, utilizes cathepsin L to infect ACE2-expressing cells. J. Biol. Chem. 281: 3198-3203.
44. Imai, Y., K. Kuba, S. Rao, Y. Huan, F. Guo, B. Guan, P. Yang, R. Sarao, T. Wada, H. Leong-Poi, M. A. Crackower, A. Fukamizu, C. C. Hui, L. Hein, S. Uhlig, A. S. Slutsky, C. Jiang, and J. M. Penninger. 2005. Angiotensin- converting enzyme 2 protects from severe acute lung failure. Nature 436: 112-116.
45. Jackwood, M. W., D. A. Hilt, S. A. Callison, C. W. Lie, H. Plaza, and E. Wade. 2001. Spike glycoprotein cleavage recognition site analysis of infectious bronchitis virus. Avian Dis. 45:366-372.
46. Jeffers, S. A., S. M. Tusell, L. Gillim-Ross, E. M. Hemmila, J. E. Achenbach, G. J. Babcock, W. D. Thomas, Jr., L. B. Thackray, M. D. Young, R. J. Mason, D. M. Ambrosino, D. E. Wentworth, J. C. Demartini, and K. V. Holmes. 2004. CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA 101:15748-15753.
47. Kan, B., M. Wang, H. Jing, H. Xu, X. Jiang, M. Yan, W. Liang, H. Zheng, K. Wan, Q. Liu, B. Cui, Y. Xu, E. Zhang, H. Wang, J. Ye, G. Li, M. Li, Z. Cui, X. Qi, K. Chen, L. Du, K. Gao, Y.-T. Zhao, X.-Z. Zou, Y.-J. Feng, Y.-F. Gao, R. Hai, D. Yu, Y. Guan, and J. Xu. 2005. Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms. J. Virol. 79:11892-11900.
48. Ksiazek, T. G., D. Erdman, C. S. Goldsmith, S. R. Zaki, T. Peret, S. Emery, S. Tong, C. Urbani, J. A. Comer, W. Lim, P. E. Rollin, S. F. Dowell, A. E. Ling, C. D. Humphrey, W. J. Shieh, J. Guarner, C. D. Paddock, P. Rota, B. Fields, J. DeRisi, J. Y. Yang, N. Cox, J. M. Hughes, J. W. LeDuc, W. J. Bellini, and L. J. Anderson. 2003. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348:1953-1966.
49. Kuba, K., Y. Imai, S. Rao, H. Gao, F. Guo, B. Guan, Y. Huan, P. Yang, Y. Zhang, W. Deng, L. Bao, B. Zhang, G. Liu, Z. Wang, M. Chappell, Y. Liu, D. Zheng, A. Leibbrandt, T. Wada, A. S. Slutsky, D. Liu, C. Qin, C. Jiang, and J. M. Penninger. 2005. A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury. Nat. Med. 11:875-879.
50. Kubo, H., Y. K. Yamada, and F. Taguchi. 1994. Localization of neutralizing epitopes and the receptor-binding site within the amino-terminal 330 amino acids of the murine coronavirus spike protein. J. Virol. 68:5403-5410.
51. Kuiken, T., R. A. Fouchier, M. Schutten, G. F. Rimmelzwaan, G. van Amerongen, D. van Kiel, J. D. Laman, T. de Jong, G. van Doornum, W. Lim, A. E. Ling, P. K. Chan, J. S. Tam, M. C. Zambon, R. Gopal, C. Drosten, S. van der Werf, N. Escriou, J. C. Manuguerra, K. Stohr, J. S. Peiris, and A. D. Osterhaus. 2003. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362:263-270.
52. Kuo, L., G. J. Godeke, M. J. Raamsman, P. S. Masters, and P. J. Rottier. 2000. Retargeting of coronavirus by substitution of the spike glycoprotein ectodomain: crossing the host cell species barrier. J. Virol. 74:1393-1406.
53. Lai, M. M., and D. Cavanagh. 1997. The molecular biology of coronaviruses. Adv. Virus Res. 48:1-100.
54. Lau, S. K., P. C. Woo, K. S. Li, Y. Huang, H. W. Tsoi, B. H. Wong, S. S. Wong, S. Y. Leung, K. H. Chan, and K. Y. Yuen. 2005. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. USA 102:14040-14045.
55. Lee, N., D. Hui, A. Wu, P. Chan, P. Cameron, G. M. Joynt, A. Ahuja, M. Y. Yung, C. B. Leung, K. F. To, S. F. Lui, C. C. Szeto, S. Chung, and J. J. Sung. 2003. A major outbreak of severe acute respiratory syndrome in Hong Kong. N. Engl. J. Med. 348:1986-1994.
56. Leparc-Goffart, I., S. T. Hingley, M. M. Chua, J. Phillips, E. Lavi, and S. R. Weiss. 1998, Targeted recombination within the spike gene of murine coronavirus mouse hepatitis virus-A59: Q159 is a determinant of hepatotropism. J. Virol. 72:9628-9636.
57. Li, F., W. Li, M. Farzan, and S. C. Harrison. 2005. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309:1864-1868.
58. Li, W., T. C. Greenough, M. J. Moore, N. Vasilieva, M. Somasundaran, J. L. Sullivan, M. Farzan, and H. Choe. 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.
59. Li, W., M. J. Moore, N. Vasilieva, J. Sui, S. K. Wong, M. A. Berne, M. Somasundaran, J. L. Sullivan, C. Luzeriaga, T. C. Greenough, H. Choe, and M. Farzan. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450-454.
60. Li, W., Z. Shi, M. Yu, W. Ren, C. Smith, J. H. Epstein, H. Wang, G. Crameri, Z. Hu, H. Zhang, J. Zhang, J. McEachern, H. Field, P. Daszak, B. T. Eaton, S. Zhang, and L. F. Wang. 2005. Bats are natural reservoirs of SARS-like coronaviruses. Science 310:676-679.
61. Li, W., C. Zhang, J. Sui, J. H. Kuhn, M. J. Moore, S. Luo, S. K. Wong, I. C. Huang, K. Xu, N. Vasilieva, A. Murakami, Y. He, W. A. Marasco, Y. Guan, H. Choe, and M. Farzan. 2005. Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J. 24:1634-1643.
62. Liang, G., Q. Chen, J. Xu, Y. Liu, W. Lim, J. S. Peiris, L. J. Anderson, L. Ruan, H. Li, B. Kan, B. Di, P. Cheng, K. H. Chan, D. D. Erdman, S. Gu, X. Yan, W. Liang, D. Zhou, L. Haynes, S. Duan, X. Zhang, H. Zheng, Y. Gao, S. Tong, D. Li, L. Fang, P. Qin, and W. Xu. 2004. Laboratory diagnosis of four recent sporadic cases of community-acquired SARS, Guangdong province, China. Emerg. Infect. Dis. 10:1774-1781.
63. Lim, P. L., A. Kurup, G. Gopalakrishna, K. P. Chan, C. W. Wong, L. C. Ng, S. Y. Se-Thoe, L. Oon, X. Bai, L. W. Stanton, Y. Ruan, L. D. Miller, V. B. Vega, L. James, P. L. Ooi, C. S. Kai, S. J. Olsen, B. Ang, and Y. S. Leo. 2004. Laboratory-acquired severe acute respiratory syndrome. N. Engl. J. Med. 350:1740-1745.
64. Marra, M. A., S. J. Jones, C. R. Astell, R. A. Holt, A. Brooks-Wilson, Y. S. Butterfield, J. Khattra, J. K. Asano, S. A. Barber, S. Y. Chan, A. Cloutier, S. M. Coughlin, D. Freeman, N. Girn, O. L. Griffith, S. R. Leach, M. Mayo, H. McDonald, S. B. Montgomery, P. K. Pandoh, A. S. Petrescu, A. G. Robertson, J. E. Schein, A. Siddiqui, D. E. Smailus, J. M. Stott, G. S. Yang, F. Plummer, A. Andonov, H. Artsob, N. Bastien, K. Bernard, T. F. Booth, D. Bowness, M. Czub, M. Drebot, L. Fernando, R. Flick, M. Garbutt, M. Gray, A. Grolla, S. Jones, H. Feldmann, A. Meyers, A. Kabani, Y. Li, S. Normand, U. Stroher, G. A. Tipples, S. Tyler, R. Vogrig, D. Ward, B. Watson, R. C. Brunham, M. Krajden, M. Petric, D. M. Skowronski, C. Upton, and R. L. Roper. 2003. The genome sequence of the SARS-associated coronavirus. Science 300:1399-1404.
65. Martina, B. E., B. L. Haagmans, T. Kuiken, R. A. Fouchier, G. F. Rimmelzwaan, G. Van Amerongen, J. S. Peiris, W. Lim, and A. D. Osterhaus. 2003. Virology: SARS virus infection of cats and ferrets. Nature 425:915.
66. Marzi, A., T. Gramberg, G. Simmons, P. Moller, A. J. Rennekamp, M. Krumbiegel, M. Geier, J. Eisemann, N. Turza, B. Saunier, A. Steinkasserer, S. Becker, P. Bates, H. Hofmann, and S. Pohlmann. 2004. DC-SIGN and DC-SIGNR interact with the glycoprotein of Marburg virus and the S protein of severe acule respiratory syndrome coronavirus. J. Virol. 78: 12090-12095.
67. Matsuyama, S., M. Ujike, S. Morikawa, M. Tashiro, and F. Taguchi. 2005. Protease-mediated enhancement of severe acute respiratory syndrome coronavirus infection. Proc. Natl. Acad. Sci. USA 102:12543-12547.
68. McIntosh, K. 2005. Coronaviruses in the limelight. J Infect. Dis. 191:489-491.
69. Moore, M. J., T. Dorfman, W. Li, S. K. Wong, Y. Li, J. H. Kuhn, J. Coderre, N. Vasilieva, Z. Han, T. C. Greenough, M. Farzan, and H. Choe. 2004. Retroviruses pseudotyped with the severe acule respiratory syndrome coronavirus spike protein efficiently infect cells expressing angiotensin-converting enzyme 2. J. Virol. 78:10628-10635.
70. Nie, Y., P. Wang, X. Shi, G. Wang, J. Chen, A. Zheng, W. Wang, Z. Wang, X. Qu, M. Luo, L. Tan, X. Song, X. Yin, M. Ding, and H. Deng. 2004. Highly infectious SARS-CoV pseudotyped virus reveals the cell tropism and its correlation with receptor expression. Biochem. Biophys. Res. Commun. 321:994-1000.
71. Normile, D. 2004. Infectious diseases. Mounting lab accidents raise SARS fears. Science 304:659-661.
72. Peiris, J. S., Y. Guan, and K. Y. Yuen. 2004. Severe acute respiratory syndrome. Nat. Med. 10:S88-S97.
73. Peiris, J. S., S. T. Lai, L. L. Poon, Y. Guan, L. Y. Yam, W. Lim, J. Nicholls, W. K. Yee, W. W. Yan, M. T. Cheung, V. C. Cheng, K. H. Chan, D. N. Tsang, R. W. Yung, T. K. Ng, and K. Y. Yuen. 2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319-1325.
74. Phillips, J. J., M. M. Chua, E. Lavi, and S. R. Weiss. 1999. Pathogenesis of chimeric MHV4/MHV-A59 recombinant viruses: the murine coronavirus spike protein is a major determinant of neurovirulence. J. Virol. 73:7752-7760.
75. Poon, L. L., D. K. Chu, K. H. Chan, O. K. Wong, T. M. Ellis, Y. H. Leung, S. K. Lau, P. C. Woo, K. Y. Suen, K. Y. Yuen, Y. Guan, and J. S. Peiris. 2005. Identification of a novel coronavirus in bats. J. Virol. 79:2001-2009.
76. Qin, C., J. Wang, Q. Wei, M. She, W. A. Marasco, H. Jiang, X. Tu, H. Zhu, L. Ren, H. Gao, L. Guo, L. Huang, R. Yang, Z. Cong, Y. Wang, Y. Liu, Y. Sun, S. Duan, J. Qu, L. Chen, W. Tong, L. Ruan, P. Liu, H. Zhang, J. Zhang, D. Liu, Q. Liu, T. Hong, and W. He. 2005. An animal model of SARS produced by infection of Macaca mulatta with SARS coronavirus. J. Pathol. 206:251-259.
77. Qu, X. X., P. Hao, X. J. Song, S. M. Jiang, Y. X. Liu, P. G. Wang, X. Rao, H. D. Song, S. Y. Wang, Y. Zuo, A. H. Zheng, M. Luo, H. L. Wang, F. Deng, H. Z. Wang, Z. H. Hu, M. X. Ding, G. P. Zhao, and H. K. Deng. 2005. Identification of two critical amino acid residues of the severe acute respiratory syndrome coronavirus spike protein for its variation in zoonotic tropism transition via a double substitution strategy. J. Biol. Chem. 280: 29588-29595.
78. Roberts, A., L. Vogel, J. Guarner, N. Hayes, B. Murphy, S. Zaki, and K. Subbarao. 2005. Severe acute respiratory syndrome coronavirus infection of golden Syrian hamsters. J. Virol. 79:503-511.
79. Rowe, T., G. Gao, R. J. Hogan, R. G. Crystal, T. G. Voss, R. L. Grant, P. Bell, G. P. Kobinger, N. A. Wivel, and J. M. Wilson. 2004. Macaque model for severe acute respiratory syndrome. J. Virol. 78:11401-11404.
80. Sanchez, C. M., A. Izeta, J. M. Sanchez-Morgado, S. Alonso, I. Sola, M. Balasch, J. Plana-Duran, and L. Enjuanes. 1999. Targeted recombination demonstrates that the spike gene of transmissible gastroenteritis coronavirus is a determinant of its enteric tropism and virulence. J. Virol. 73:7607-7618.
81. Schickli, J. H., L. B. Thackray, S. G. Sawicki, and K. V. Holmes. 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.
82. Schultze, B., and G. Herrler. 1992. Bovine coronavirus uses N-acetyl-9-O-acetylneuraminic acid as a receptor determinant to initiate the infection of cultured cells. J. Gen. Virol. 73:901-906.
83. Simmons, G., D. N. Gosalia, A. J. Rennekamp, J. D. Reeves, S. L. Diamond, and P. Bates. 2005. Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc. Natl. Acad. Sci. USA 102:11876-11881.
84. Snijder, E. J., P. J. Bredenbeek, J. C. Dobbe, V. Thiel, J. Ziebuhr, L. L. Poon, Y. Guan, M. Rozanov, W. J. Spaan, and A. E. Gorbalenya. 2003. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J. Mol. Biol. 331:991-1004.
85. Song, H. D., C. C. Tu, G. W. Zhang, S. Y. Wang, K. Zheng, L. C. Lei, Q. X. Chen, Y. W. Gao, H. Q. Zhou, H. Xiang, H. J. Zheng, S. W. Chern, F. Cheng, C. M. Pan, H. Xuan, S. J. Chen, H. M. Luo, D. H. Zhou, Y. F. Liu, J. F. He, P. Z. Qin, L. H. Li, Y. Q. Ren, W. J. Liang, Y. D. Yu, L. Anderson, M. Wang, R. H. Xu, X. W. Wu, H. Y. Zheng, J. D. Chen, G. Liang, Y. Gao, M. Liao, L. Fang, L. Y. Jiang, H. Li, F. Chen, B. Di, L. J. He, J. Y. Lin, S. Tong, X. Kong, L. Du, P. Hao, H. Tang, A. Bernini, X. J. Yu, O. Spiga, Z. M. Guo, H. Y. Pan, W. Z. He, J. C. Manuguerra, A. Fontanet, A. Danchin, N. Niccolai, Y. X. Li, C. I. Wu, and G. P. Zhao. 2005. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc. Natl. Acad. Sci. USA 102:2430-2435.
86. Sturman, L. S., and K. V. Holmes. 1984. Proteolytic cleavage of peplomeric glycoprotein E2 of MHV yields two 90K subunits and activates cell fusion. Adv. Exp. Med. Biol. 173:25-35.
87. Sturman, L. S., C. S. Ricard, and K. V. Holmes. 1985. Proteolylic cleavage of the E2 glycoprotein of murine coronavirus: activation of cell-fusing activity of virions by trypsin and separation of two different 90K cleavage fragments. J. Virol. 56:904-911.
88. Subbarao, K., J. McAuliffe, L. Vogel, G. Fahle, S. Fischer, K. Tatti, M. Packard, W. J. Shieh, S. Zaki, and B. Murphy. 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.
89. Sui, J., W. Li, A. Murakami, A. Tamin, L. J. Matthews, S. K. Wong, M. J. Moore, A. St. Clair Tallarico, M. Olurinde, H. Choe, L. J. Anderson, W. J. Bellini, M. Farzan, and W. A. Marasco. 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.
90. Sui, J., W. Li, A. Roberts, L. J. Matthews, A. Murakami, L. Vogel, S. K. Wong, K. Subbarao, M. Farzan, and W. A. Marasco. 2005. Evaluation of human monoclonal antibody 80R for immunoprophylaxis of severe acute respiratory syndrome by an animal study, epitope mapping, and analysis of spike variants. J. Virol. 79:5900-5906.
91. Tipnis, S. R., N. M. Hooper, R. Hyde, E. Karran, G. Christie, and A. J. Turner. 2000. A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J. Biol. Chem. 275:33238-33243.
92. Traggiai, E., S. Becker, K. Subbarao, L. Kolesnikova, Y. Uematsu, M. R. Gismondo, B. R. Murphy, R. Rappuoli, and A. Lanzavecchia. 2004. An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus. Nat. Med. 10:871-875.
93. Tu, C., G. Crameri, X. Kong, J. Chen, Y. Sun, M. Yu, H. Xiang, X. Xia, S. Liu, T. Ren, Y. Yu, B. T. Eaton, H. Xuan, and L. F. Wang. 2004. Antibodies to SARS coronavirus in civets. Emerg. Infect. Dis. 10:2244-2248.
94. van den Brink, E. N., J. Ter Meulen, F. Cox, M. A. Jongeneelen, A. Thijsse, M. Throsby, W. E. Marissen, P. M. Rood, A. B. Bakker, H. R. Gelderblom, B. E. Martina, A. D. Osterhaus, W. Preiser, H. W. Doerr, J. de Kruif, and J. Goudsmit. 2005. Molecular and biological characterization of human monoclonal antibodies binding to the spike and nucleocapsid proteins of severe acute respiratory syndrome coronavirus. J. Virol. 79:1635-1644.
95. van der Hoek, L., K. Pyre, M. F. Jebbink, W. Vermeulen-Oost, R. J. Berkhout, K. C. Wolthers, P. M. Wertheim-van Dillen, J. Kaandorp, J. Spaargaren, and B. Berkhout. 2004. Identification of a new human coronavirus. Nat. Med. 10:368-373.
96. Vickers, C., P. Hales, V. Kaushik, L. Dick, J. Gavin, J. Tang, K. Godbout, T. Parsons, E. Baronas, F. Hsieh, S. Acton, M. Patane, A. Nichols, and P. Tummino. 2002. Hydrolysis of biological peptides by human angiotensin-converting enzyme-related carboxypeptidase. J. Biol. Chem. 277:14838-14843.
97. Wang, M., H. Q. Jing, H. F. Xu, X. G. Jiang, B. Kan, Q. Y. Liu, K. L. Wan, B. Y. Cui, H. Zheng, Z. G. Cui, M. Y. Yan, W. L. Liang, H. X. Wang, X. B. Qi, Z. J. Li, M. C. Li, K. Chen, E. M. Zhang, S. Y. Zhang, R. Hai, D. Z. Yu, and J. G. Xu. 2005. Surveillance on severe acute respiratory syndrome associated coronavirus in animals at a live animal market of Guangzhou in 2004. Zhonghua Liuxingbingxue Zazhi 26:84-87. (In Chinese.)
98. Wang, S., T. H. Chou, P. V. Sakhatskyy, S. Huang, J. M. Lawrence, H. Cao, X. Huang, and S. Lu. 2005. Identification of two neutralizing regions on the severe acute respiratory syndrome coronavirus spike glycoprotein produced from the mammalian expression system. J. Virol. 79:1906-1910.
99. Wentworth, D. E., L. Gillim-Ross, N. Espina, and K. A. Bernard. 2004. Mice susceptible to SARS coronavirus. Emerg. Infect. Dis. 10:1293-1296.
100. Williams, R. K., G. S. Jiang, and K. V. Holmes. 1991. Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc. Natl. Acad. Sci. USA 88:5533-5536.
101. Wong, S. K., W. Li, M. J. Moore, H. Choe, and M. Farzan. 2004. A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2. J. Biol. Chem. 279:3197-3201.
102. Woo, P. C., S. K. Lau, C. M. Chu, K. H. Chan, H. W. Tsoi, Y. Huang, B. H. Wong, R. W. Poon, J. J. Cai, W. K. Luk, L. L. Poon, S. S. Wong, Y. Guan, J. S. Peiris, and K. Y. Yuen. 2005. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 79:884-895.
103. Wu, D., C. Tu, C. Xin, H. Xuan, Q. Meng, Y. Lin, Y. Yu, Y. Guan, Y. Jiang, X. Yin, G. Crameri, M. Wang, C. Li, S. Liu, M. Liao, L. Feng, H. Xiang, J. Sun, J. Chen, Y. Sun, S. Gu, N. Liu, D. Fu, B. T. Eaton, L. F. Wang, and X. Kong. 2005. Civets are equally susceptible to experimental infection by two different severe acute respiratory syndrome coronavirus isolates. J. Virol. 79:2620-2625.
104. Xiao, X., S. Chakraborti, A. S. Dimitrov, K. Gramatikoff, and D. S. Dimitrov. 2003. The SARS-CoV S glycoprotein: expression and functional characterization. Biochem. Biophys. Res. Commun. 312:1159-1164.
105. Yagil, Y., and C. Yagil. 2003. Hypothesis: ACE2 modulates blood pressure in the mammalian organism. Hypertension 41:871-873.
106. Yang, Z. Y., Y. Huang, L. Ganesh, K. Leung, W. P. Kong, O. Schwartz, K. Subbarao, and G. J. Nabel. 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.
107. Yang, Z. Y., H. C. Werner, W. P. Kong, K. Leung, E. Traggiai, A. Lanzavecchia, and G. J. Nabel. 2005. Evasion of antibody neutralization in emerging severe acute respiratory syndrome coronaviruses. Proc. Natl. Acad. Sci. USA 102:797-801.
108. Yeager, C. L., R. A. Ashmun, R. K. Williams, C. B. Cardellichio, L. H. Shapiro, A. T. Look, and K. V. Holmes. 1992. Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357:420-422.
109. Yu, I. T., Y. Li, T. W. Wong, W. Tam, A. T. Chan, J. H. Lee, D. Y. Leung, and T. Ho. 2004. Evidence of airborne transmission of the severe acute respiratory syndrome virus. N. Engl. J. Med. 350:1731-1739.
110. Zheng, B. J., K. H. Wong, J. Zhou, K. L. Wong, B. W. Young, L. W. Lu, and S. S. Lee. 2004. SARS-related virus predating SARS outbreak, Hong Kong. Emerg. Infect. Dis. 10:176-178.
111. Zhong, N. 2004. Management and prevention of SARS in China, Philos. Trans. R. Soc. Lond. B. Biol. Sci. 359:1115-1116.
112. Zhong, N., Y. Ding, Y. Mao, Q. Wang, G. Wang, D. Wang, Y. Cong, Q. Li, Y. Liu, L. Ruan, B. Chen, X. Du, Y. Yang, Z. Zhang, X. Zhang, J. Lin, J. Zheng, Q. Zhu, D. Ni, X. Xi, G. Zeng, D. Ma, C. Wang, W. Wang, B. Wang, J. Wang, D. Liu, X. Li, X. Liu, J. Chen, R. Chen, F. Min, P. Yang, Y. Zhang, H. Luo, Z. Lang, Y. Hu, A. Ni, W. Cao, J. Lei, S. Wang, Y. Wang, X. Tong, W. Liu, M. Zhu, W. Chen, X. Xhen, L. Lin, Y. Luo, J. Zhong, W. Weng, S. Peng, Z. Pan, R. Wang, J. Zuo, B. Liu, N. Zhang, J. Zhang, B. Zhang, L. Chen, P. Zhou, L. Jiang, E. Chao, L. Guo, X. Tan, and J. Pan. 2003. Consensus for the management of severe acute respiratory syndrome. Chin. Med. J. (Engl. Ed.). 116:1603-1635.
113. Zhong, N. S., B. J. Zheng, Y. M. Li, L. Poon, Z. H. Xie, K. H. Chan, P. H. Li, S. Y. Tan, Q. Chang, J. P. Xie, X. Q. Liu, J. Xu, D. X. Li, K. Y. Yuen, and Y. Guan. 2003. Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People's Republic of China, in February, 2003. Lancet 362:1353-1358.
114. Zhou, T., H. Wang, D. Luo, T. Rowe, Z. Wang, R. J. Hogan, S. Qiu, R. J. Bunzel, G. Huang, V. Mishra, T. G. Voss, R. Kimberly, and M. Luo. 2004. An exposed domain in the severe acute respiratory syndrome coronavirus spike protein induces neutralizing antibodies. J. Virol. 78:7217-7226.