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. 2006;581:209–218. doi: 10.1007/978-0-387-33012-9_36

Insights from the Association of SARS-CoV S-Protein with its Receptor, ACE2

Wenhui Li 3, Hyeryun Choe 4, Michael Farzan 5
Editors: Stanley Perlman1, Kathryn V Holmes2
PMCID: PMC7123956  PMID: 17037532

The content is available as a PDF (782.7 KB).

Contributor Information

Stanley Perlman, Email: Stanley-Perlman@uiowa.edu

Kathryn V. Holmes, Email: Kathryn.Holmes@ucHSC.edu

References

  • 1.Peiris JS, Lai ST, Poon LL, Guan Y, Yam LY, Lim W, Nicholls J, Yee WK, Yan WW, Cheung MT, Cheng VC, Chan KH, Tsang DN, Yung RW, Ng TK, Yuen KY. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet. 2003;361:1319–1325. doi: 10.1016/S0140-6736(03)13077-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Yu IT, Li Y, Wong TW, Tam W, Chan AT, Lee JH, Leung DY, Ho T. Evidence of airborne transmission of the severe acute respiratory syndrome virus. N. Engl. J. Med. 2004;350:1731–1739. doi: 10.1056/NEJMoa032867. [DOI] [PubMed] [Google Scholar]
  • 3.Zhong N, Ding Y, Mao Y, Wang Q, Wang G, Wang D, Cong Y, Li Q, Liu Y, Ruan L, Chen B, Du X, Yang Y, Zhang Z, Zhang X, Lin J, Zheng J, Zhu Q, Ni D, Xi X, Zeng G, Ma D, Wang C, Wang W, Wang B, Wang J, Liu D, Li X, Liu X, Chen J, Chen R, Min F, Yang P, Zhang Y, Luo H, Lang Z, Hu Y, Ni A, Cao W, Lei J, Wang S, Wang Y, Tong X, Liu W, Zhu M, Chen W, Xhen X, Lin L, Luo Y, Zhong J, Weng W, Peng S, Pan Z, Wang R, Zuo J, Liu B, Zhang N, Zhang J, Zhang B, Chen L, Zhou P, Jiang L, Chao E, Guo L, Tan X, Pan J. Consensus for the management of severe acute respiratory syndrome. Chin. Med. J. (Engl.) 2003;116:1603–1635. [PubMed] [Google Scholar]
  • 4.Lee N, Hui D, Wu A, Chan P, Cameron P, Joynt GM, Ahuja A, Yung MY, Leung CB, To KF, Lui SF, Szeto CC, Chung S, Sung JJ. A major outbreak of severe acute respiratory syndrome in Hong Kong. N. Engl. J. Med. 2003;348:1986–1994. doi: 10.1056/NEJMoa030685. [DOI] [PubMed] [Google Scholar]
  • 5.Cherry JD. The chronology of the 2002-2003 SARS mini pandemic. Paediatr. Respir. Rev. 2004;5:262–269. doi: 10.1016/j.prrv.2004.07.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Drosten C, Gunther S, Preiser W, van der Werf S, Brodt HR, Becker S, Rabenau H, Panning M, Kolesnikova L, Fouchier RA, Berger A, Burguiere AM, Cinatl J, Eickmann M, Escriou N, Grywna K, Kramme S, Manuguerra JC, Muller S, Rickerts V, Sturmer M, Vieth S, Klenk HD, Osterhaus AD, Schmitz H, Doerr HW. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 2003;348:1967–1976. doi: 10.1056/NEJMoa030747. [DOI] [PubMed] [Google Scholar]
  • 7.Fouchier RA, Kuiken T, Schutten M, van Amerongen G, van Doornum GJ, van den Hoogen BG, Peiris M, Lim W, Stohr K, Osterhaus AD. Aetiology: Koch's postulates fulfilled for SARS virus. Nature. 2003;423:240. doi: 10.1038/423240a. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.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. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 2003;348:1953–1966. doi: 10.1056/NEJMoa030781. [DOI] [PubMed] [Google Scholar]
  • 9.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. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet. 2003;362:263–270. doi: 10.1016/S0140-6736(03)13967-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Zhong NS, Zheng BJ, Li YM, Poon, Xie ZH, Chan KH, Li PH, Tan SY, Chang Q, Xie JP, Liu XQ, Xu J, Li DX, Yuen KY, Peiris, Guan Y. Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People's Republic of China, in February, 2003. Lancet. 2003;362:1353–1358. doi: 10.1016/S0140-6736(03)14630-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Peiris JS, Guan Y, Yuen KY. Severe acute respiratory syndrome. Nat. Med. 2004;10:S88–97. doi: 10.1038/nm1143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Zhong N. Management and prevention of SARS in China. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2004;359:1115–1116. doi: 10.1098/rstb.2004.1491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.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 DD, Gu S, Yan X, Liang W, Zhou D, Haynes L, Duan S, Zhang X, Zheng H, Gao Y, Tong S, Li D, Fang L, Qin P, Xu W. Laboratory diagnosis of four recent sporadic cases of community-acquired SARS, Guangdong Province, China. Emerg. Infect. Dis. 2004;10:1774–1781. doi: 10.3201/eid1010.040445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.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. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc. Natl. Acad. Sci. USA. 2005;102:2430–2435. doi: 10.1073/pnas.0409608102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Fleck F. SARS virus returns to China as scientists race to find effective vaccine. Bull. World Health Organ. 2004;82:152–153. [PMC free article] [PubMed] [Google Scholar]
  • 16.Zheng BJ, Wong KH, Zhou J, Wong KL, Young BW, Lu LW, Lee SS. SARS-related virus predating SARS outbreak, Hong Kong. Emerg. Infect. Dis. 2004;10:176–178. doi: 10.3201/eid1002.030533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Normile D. Infectious diseases. Mounting lab accidents raise SARS fears. Science. 2004;304:659–661. doi: 10.1126/science.304.5671.659. [DOI] [PubMed] [Google Scholar]
  • 18.Lim PL, Kurup A, Gopalakrishna G, Chan KP, Wong CW, Ng LC, Se-Thoe SY, Oon L, Bai X, Stanton LW, Ruan Y, Miller LD, Vega VB, James L, Ooi PL, Kai CS, Olsen SJ, Ang B, Leo YS. Laboratory-acquired severe acute respiratory syndrome. N. Engl. J. Med. 2004;350:1740–1745. doi: 10.1056/NEJMoa032565. [DOI] [PubMed] [Google Scholar]
  • 19.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. Isolation and characterization of viruses related to the SARS Coronavirus from animals in Southern China. Science. 2003;302:276–278. doi: 10.1126/science.1087139. [DOI] [PubMed] [Google Scholar]
  • 20.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. Civets are equally susceptible to experimental infection by two different severe acute respiratory syndrome coronavirus isolates. J. Virol. 2005;79:2620–2625. doi: 10.1128/JVI.79.4.2620-2625.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Wang M, Jing HQ, Xu HF, Jiang XG, Kan B, Liu QY, Wan KL, Cui BY, Zheng H, Cui ZG, Yan MY, Liang WL, Wang HX, Qi XB, Li ZJ, Li MC, Chen K, Zhang EM, Zhang SY, Hai R, Yu DZ, Xu JG. Surveillance on severe acute respiratory syndrome associated coronavirus in animals at a live animal market of Guangzhou in 2004. Zhonghua Liu Xing Bing Xue Za Zhi. 2005;26:84–87. [PubMed] [Google Scholar]
  • 22.Li W, Zhang C, Sui J, Kuhn JH, Moore MJ, Luo S, Wong SK, Huang IC, Xu K, Vasilieva N, Murakami A, He Y, Marasco WA, Guan Y, Choe H, Farzan M. Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J. 2005;24:1634. doi: 10.1038/sj.emboj.7600640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Kan B, Wang M, Jing H, Xu H, Jiang X, Yan M, Liang W, Zheng H, Wan K, Liu Q, Cui B, Xu Y, Zhang E, Wang H, Ye J, Li G, Li M, Cui Z, Qi X, Chen K, Du L, Gao K, Zhao Y-T, Zou X-Z, Feng Y-J, Gao Y-F, Hai R, Yu D, Guan Y, Xu J. 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. 2005;79:11892–11900. doi: 10.1128/JVI.79.18.11892-11900.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Tu C, Crameri G, Kong X, Chen J, Sun Y, Yu M, Xiang H, Xia X, Liu S, Ren T, Yu Y, Eaton BT, Xuan H, Wang LF. Antibodies to SARS coronavirus in civets. Emerg. Infect. Dis. 2004;10:2244–2248. doi: 10.3201/eid1012.040520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Poon LL, Chu DK, Chan KH, Wong OK, Ellis TM, Leung YH, Lau SK, Woo PC, Suen KY, Yuen KY, Guan Y, Peiris JS. Identification of a novel coronavirus in bats. J. Virol. 2005;79:2001–2009. doi: 10.1128/JVI.79.4.2001-2009.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang LF. Bats are natural reservoirs of SARS-like coronaviruses. Science. 2005;310:676–679. doi: 10.1126/science.1118391. [DOI] [PubMed] [Google Scholar]
  • 27.Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, Wong SS, Leung SY, Chan KH, Yuen KY. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. USA. 2005;102:14040–14045. doi: 10.1073/pnas.0506735102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Gonzalez JM, Gomez-Puertas P, Cavanagh D, Gorbalenya AE, Enjuanes L. A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae. Arch. Virol. 2003;148:2207–2235. doi: 10.1007/s00705-003-0162-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Brian DA, Baric RS. Coronavirus genome structure and replication. Curr. Top. Microbiol. Immunol. 2005;287:1–30. doi: 10.1007/3-540-26765-4_1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.McIntosh K. Coronaviruses in the limelight. J. Infect. Dis. 2005;191:489–491. doi: 10.1086/428510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Esper F, Weibel C, Ferguson D, Landry ML, Kahn JS. Evidence of a novel human coronavirus that is associated with respiratory tract disease in infants and young children. J. Infect. Dis. 2005;191:492–498. doi: 10.1086/428138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Fouchier RA, Hartwig NG, Bestebroer TM, Niemeyer B, de Jong JC, Simon JH, Osterhaus AD. A previously undescribed coronavirus associated with respiratory disease in humans. Proc. Natl. Acad. Sci. USA. 2004;101:6212–6216. doi: 10.1073/pnas.0400762101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.van der Hoek L, Pyrc K, Jebbink MF, Vermeulen-Oost W, Berkhout RJ, Wolthers KC, Wertheim-van Dillen PM, Kaandorp J, Spaargaren J, Berkhout B. Identification of a new human coronavirus. Nat. Med. 2004;10:368–373. doi: 10.1038/nm1024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Hofmann H, Pyrc K, van der Hoek L, Geier M, Berkhout B, Pohlmann S. Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proc. Natl. Acad. Sci. USA. 2005;102:7988–7983. doi: 10.1073/pnas.0409465102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Woo PC, Lau SK, Chu CM, Chan KH, Tsoi HW, Huang Y, Wong BH, Poon RW, Cai JJ, Luk WK, Poon LL, Wong SS, Guan Y, Peiris JS, Yuen KY. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 2005;79:884–895. doi: 10.1128/JVI.79.2.884-895.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Gorbalenya AE, Snijder EJ, Spaan WJ. Severe acute respiratory syndrome coronavirus phylogeny: toward consensus. J. Virol. 2004;78:7863–7866. doi: 10.1128/JVI.78.15.7863-7866.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Snijder EJ, Bredenbeek PJ, Dobbe JC, Thiel V, Ziebuhr J, Poon LL, Guan Y, Rozanov M, Spaan WJ, Gorbalenya AE. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus Group 2 lineage. J. Mol. Biol. 2003;331:991–1004. doi: 10.1016/S0022-2836(03)00865-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Gibbs AJ, Gibbs MJ, Armstrong JS. The phylogeny of SARS coronavirus. Arch. Virol. 2004;149:621–624. doi: 10.1007/s00705-003-0244-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Delmas B, Gelfi J, L'Haridon R, Vogel LK, Sjostrom H, Noren O, Laude H. Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature. 1992;357:417–420. doi: 10.1038/357417a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Yeager CL, Ashmun RA, Williams RK, Cardellichio CB, Shapiro LH, Look AT, Holmes KV. Human aminopeptidase N is a receptor for human coronavirus 229E. Nature. 1992;357:420–422. doi: 10.1038/357420a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Dveksler GS, Dieffenbach CW, Cardellichio CB, McCuaig K, Pensiero MN, Jiang GS, Beauchemin N, Holmes KV. Several members of the mouse carcinoembryonic antigen-related glycoprotein family are functional receptors for the coronavirus mouse hepatitis virus-A59. J. Virol. 1993;67:1–8. doi: 10.1128/jvi.67.1.1-8.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Dveksler GS, Pensiero MN, Cardellichio CB, Williams RK, Jiang GS, Holmes KV, Dieffenbach CW. Cloning of the mouse hepatitis virus (MHV) receptor: expression in human and hamster cell lines confers susceptibility to MHV. J. Virol. 1991;65:6881–6891. doi: 10.1128/jvi.65.12.6881-6891.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Williams RK, Jiang GS, Holmes KV. Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc. Natl. Acad. Sci. USA. 1991;88:5533–5536. doi: 10.1073/pnas.88.13.5533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Schultze B, Herrler G. Bovine coronavirus uses N-acetyl-9-O-acetylneuraminic acid as a receptor determinant to initiate the infection of cultured cells. J. Gen. Virol. 1992;73:901–906. doi: 10.1099/0022-1317-73-4-901. [DOI] [PubMed] [Google Scholar]
  • 45.Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzeriaga C, Greenough TC, Choe H, Farzan M. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature. 2003;426:450–454. doi: 10.1038/nature02145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Moore MJ, Dorfman T, Li W, Wong SK, Li Y, Kuhn JH, Coderre J, Vasilieva N, Han Z, Greenough TC, Farzan M, Choe H. Retroviruses pseudotyped with the severe acute respiratory syndrome coronavirus spike protein efficiently infect cells expressing angiotensin-converting enzyme 2. J. Virol. 2004;78:10628–10635. doi: 10.1128/JVI.78.19.10628-10635.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Chan PK, To KF, Lo AW, Cheung JL, Chu I, Au FW, Tong JH, Tam JS, Sung JJ, Ng HK. Persistent infection of SARS coronavirus in colonic cells in vitro. J. Med. Virol. 2004;74:1–7. doi: 10.1002/jmv.20138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.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. Organ distribution of severe acute respiratory syndrome (SARS) associated coronavirus (SARS-CoV) in SARS patients: implications for pathogenesis and virus transmission pathways. J. Pathol. 2004;203:622–630. doi: 10.1002/path.1560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Hamming I, Timens W, Bulthuis ML, Lely AT, Navis GJ, van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J. Pathol. 2004;203:631–637. doi: 10.1002/path.1570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Harmer D, Gilbert M, Borman R, Clark KL. Quantitative mRNA expression profiling of ACE 2, a novel homologue of angiotensin converting enzyme. FEBS Lett. 2002;532:107–110. doi: 10.1016/S0014-5793(02)03640-2. [DOI] [PubMed] [Google Scholar]
  • 51.Li W, Greenough TC, Moore MJ, Vasilieva N, Somasundaran M, Sullivan JL, Farzan M, Choe H. Efficient replication of severe acute respiratory syndrome coronavirus in mouse cells is limited by murine Angiotensin-converting enzyme 2. J. Virol. 2004;78:11429–11433. doi: 10.1128/JVI.78.20.11429-11433.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Subbarao K, McAuliffe J, Vogel L, Fahle G, Fischer S, Tatti K, Packard M, Shieh WJ, Zaki S, Murphy B. Prior infection and passive transfer of neutralizing antibody prevent replication of severe acute respiratory syndrome coronavirus in the respiratory tract of mice. J. Virol. 2004;78:3572–3577. doi: 10.1128/JVI.78.7.3572-3577.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Wentworth DE, Gillim-Ross L, Espina N, Bernard KA. Mice susceptible to SARS coronavirus. Emerg. Infect. Dis. 2004;10:1293–1296. doi: 10.3201/eid1007.031119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.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. 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. 2004;101:2536–2541. doi: 10.1073/pnas.0307140101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Hofmann H, Geier M, Marzi A, Krumbiegel M, Peipp M, Fey GH, Gramberg T, Pohlmann S. 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. 2004;319:1216–1221. doi: 10.1016/j.bbrc.2004.05.114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.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. Highly infectious SARS-CoV pseudotyped virus reveals the cell tropism and its correlation with receptor expression. Biochem. Biophys. Res. Commun. 2004;321:994–1000. doi: 10.1016/j.bbrc.2004.07.060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Greenough TC, Babcock GJ, Roberts A, Hernandez HJ, Thomas WD, Jr., Coccia JA, Graziano RF, Srinivasan M, Lowy I, Finberg RW, Subbarao K, Vogel L, Somasundaran M, Luzuriaga K, Sullivan JL, Ambrosino DM. Development and characterization of a severe acute respiratory syndrome-associated coronavirus-neutralizing human monoclonal antibody that provides effective immunoprophylaxis in mice. J. Infect. Dis. 2005;191:507–514. doi: 10.1086/427242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.J. Sui, W. Li, A. Roberts, L. J. Matthews, A. Murakami, L. Vogel, S. K. Wong, K. Subbarao, M. Farzan, and W. A. Marasco, Evaluation of human mAb 80R in immunoprophylaxis of SARS by an animal study, epitope mapping and analysis of spike variants, J. Virol. in press, 2005. [DOI] [PMC free article] [PubMed]
  • 59.He Y, Lu H, Siddiqui P, Zhou Y, Jiang S. Receptor-binding domain of severe acute respiratory syndrome coronavirus spike protein contains multiple conformation-dependent epitopes that induce highly potent neutralizing antibodies. J. Immunol. 2005;174:4908–4915. doi: 10.4049/jimmunol.174.8.4908. [DOI] [PubMed] [Google Scholar]
  • 60.He Y, Zhou Y, Wu H, Luo B, Chen J, Li W, Jiang S. Identification of immunodominant sites on the spike protein of severe acute respiratory syndrome (SARS) coronavirus: implication for developing SARS diagnostics and vaccines. J. Immunol. 2004;173:4050–4057. doi: 10.4049/jimmunol.173.6.4050. [DOI] [PubMed] [Google Scholar]
  • 61.Kuba K, Imai Y, Rao S, Gao H, Guo F, Guan B, Huan Y, Yang P, Zhang Y, Deng W, Bao L, Zhang B, Liu G, Wang Z, Chappell M, Liu Y, Zheng D, Leibbrandt A, Wada T, Slutsky AS, Liu D, Qin C, Jiang C, Penninger JM. A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury. Nat. Med. 2005;11:875–879. doi: 10.1038/nm1267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Gramberg T, Hofmann H, Moller P, Lalor PF, Marzi A, Geier M, Krumbiegel M, Winkler T, Kirchhoff F, Adams DH, Becker S, Munch J, Pohlmann S. LSECtin interacts with filovirus glycoproteins and the spike protein of SARS coronavirus. Virology. 2005;340:224–236. doi: 10.1016/j.virol.2005.06.026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Jeffers SA, Tusell SM, Gillim-Ross L, Hemmila EM, Achenbach JE, Babcock GJ, Thomas WD, Jr., Thackray LB, Young MD, Mason RJ, Ambrosino DM, Wentworth DE, Demartini JC, Holmes KV. CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA. 2004;101:15748–15753. doi: 10.1073/pnas.0403812101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.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. DC-SIGN and DC-SIGNR interact with the glycoprotein of Marburg virus and the S protein of severe acute respiratory syndrome coronavirus. J. Virol. 2004;78:12090–12095. doi: 10.1128/JVI.78.21.12090-12095.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Yang ZY, Huang Y, Ganesh L, Leung K, Kong WP, Schwartz O, Subbarao K, Nabel GJ. 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. 2004;78:5642–5650. doi: 10.1128/JVI.78.11.5642-5650.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66.Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, Donovan M, Woolf B, Robison K, Jeyaseelan R, Breitbart RE, Acton S. A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ. Res. 2000;87:E1–9. doi: 10.1161/01.res.87.5.e1. [DOI] [PubMed] [Google Scholar]
  • 67.Tipnis SR, Hooper NM, Hyde R, Karran E, Christie G, Turner AJ. A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J. Biol. Chem. 2000;275:33238–33243. doi: 10.1074/jbc.M002615200. [DOI] [PubMed] [Google Scholar]
  • 68.Vickers C, Hales P, Kaushik V, Dick L, Gavin J, Tang J, Godbout K, Parsons T, Baronas E, Hsieh F, Acton S, Patane M, Nichols A, Tummino P. Hydrolysis of biological peptides by human angiotensinconverting enzyme-related carboxypeptidase. J. Biol. Chem. 2002;277:14838–14843. doi: 10.1074/jbc.M200581200. [DOI] [PubMed] [Google Scholar]
  • 69.Yagil Y, Yagil C. Hypothesis: ACE2 modulates blood pressure in the mammalian organism. Hypertension. 2003;41:871–873. doi: 10.1161/01.HYP.0000063886.71596.C8. [DOI] [PubMed] [Google Scholar]
  • 70.Crackower MA, Sarao R, Oudit GY, Yagil C, Kozieradzki I, Scanga SE, Oliveira-dos-Santos AJ, da Costa J, Zhang L, Pei Y, Scholey J, Ferrario CM, Manoukian AS, Chappell MC, Backx PH, Yagil Y, Penninger JM. Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature. 2002;417:822–828. doi: 10.1038/nature00786. [DOI] [PubMed] [Google Scholar]
  • 71.Imai Y, Kuba K, Rao S, Huan Y, Guo F, Guan B, Yang P, Sarao R, Wada T, Leong-Poi H, Crackower MA, Fukamizu A, Hui CC, Hein L, Uhlig S, Slutsky AS, Jiang C, Penninger JM. Angiotensin-converting enzyme 2 protects from severe acute lung failure. Nature. 2005;436:112–116. doi: 10.1038/nature03712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Kubo H, Yamada YK, Taguchi F. Localization of neutralizing epitopes and the receptor-binding site within the amino-terminal 330 amino acids of the murine coronavirus spike protein. J. Virol. 1994;68:5403–5410. doi: 10.1128/jvi.68.9.5403-5410.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73.Bonavia A, Zelus BD, Wentworth DE, Talbot PJ, Holmes KV. Identification of a receptor-binding domain of the spike glycoprotein of human coronavirus HCoV-229E. J. Virol. 2003;77:2530–2538. doi: 10.1128/JVI.77.4.2530-2538.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 74.Breslin JJ, Mork I, Smith MK, Vogel LK, Hemmila EM, Bonavia A, Talbot PJ, Sjostrom H, Noren O, Holmes KV. Human coronavirus 229E: receptor binding domain and neutralization by soluble receptor at 37 degrees C. J. Virol. 2003;77:4435–4438. doi: 10.1128/JVI.77.7.4435-4438.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 75.Babcock GJ, Esshaki DJ, Thomas WD, Jr., Ambrosino DM. Amino acids 270 to 510 of the severe acute respiratory syndrome coronavirus spike protein are required for interaction with receptor. J. Virol. 2004;78:4552–4560. doi: 10.1128/JVI.78.9.4552-4560.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Wong SK, Li W, Moore MJ, Choe H, Farzan M. A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2. J. Biol. Chem. 2004;279:3197–3201. doi: 10.1074/jbc.C300520200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Xiao X, Chakraborti S, Dimitrov AS, Gramatikoff K, Dimitrov DS. The SARS-CoV S glycoprotein: expression and functional characterization. Biochem. Biophys. Res. Commun. 2003;312:1159–1164. doi: 10.1016/j.bbrc.2003.11.054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 78.Li F, Li W, Farzan M, Harrison SC. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science. 2005;309:1864–1868. doi: 10.1126/science.1116480. [DOI] [PubMed] [Google Scholar]
  • 79.Qu XX, Hao P, Song XJ, Jiang SM, Liu YX, Wang PG, Rao X, Song HD, Wang SY, Zuo Y, Zheng AH, Luo M, Wang HL, Deng F, Wang HZ, Hu ZH, Ding MX, Zhao GP, Deng HK. 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. 2005;280:29588–29595. doi: 10.1074/jbc.M500662200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80.Yang ZY, Werner HC, Kong WP, Leung K, Traggiai E, Lanzavecchia A, Nabel GJ. Evasion of antibody neutralization in emerging severe acute respiratory syndrome coronaviruses. Proc. Natl. Acad. Sci. USA. 2005;102:797–801. doi: 10.1073/pnas.0409065102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.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. The genome sequence of the SARS-associated coronavirus. Science. 2003;300:1399–1404. doi: 10.1126/science.1085953. [DOI] [PubMed] [Google Scholar]
  • 82.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. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science. 2004;303:1666–1669. doi: 10.1126/science.1092002. [DOI] [PubMed] [Google Scholar]

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