Crystal structure of the receptor-binding domain from newly emerged middle east respiratory syndrome coronavirus

Journal of Virology

Volumn 87, Issue 19, 2013, Pages 10777-10783

  Chen, Yaoqing ^a   Rajashankar, Kanagalaghatta R ^b   Yang, Yang ^a   Agnihothram, Sudhakar S ^c   Liu, Chang ^a   Lin, Yi Lun ^a   Baric, Ralph S ^c   Li, Fang ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c IL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS SPIKE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CORONAVIRUS; CRYSTAL STRUCTURE; CRYSTALLIZATION; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; RECEPTOR BINDING; SARS CORONAVIRUS; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS; VIRUS IDENTIFICATION; VIRUS TRANSMISSION;

CORONAVIRUS;

EID: 84886007720     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01756-13     Document Type: Article

References (46)

1. de Groot RJ, Baker SC, Baric RS, Brown CS, Drosten C, Enjuanes L, Fouchier RA, Galiano M, Gorbalenya AE, Memish Z, Perlman S, Poon LL, Snijder EJ, Stephens GM, Woo PC, Zaki AM, Zambon M, Ziebuhro J. 2013. Middle East respiratory syndrome coronavirus (MERS-CoV); announcement of the Coronavirus Study Group. J. Virol. 87:7790-7792.
2. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus A, Fouchier RAM. 2012. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med. 367:1814-1820.
3. Annan A, Baldwin HJ, Corman VM, Klose SM, Owusu M, Nkrumah EE, Badu EK, Anti P, Agbenyega O, Meyer B, Oppong S, Sarkodie YA, Kalko EK, Lina PH, Godlevska EV, Reusken C, Seebens A, Gloza-Rausch F, Vallo P, Tschapka M, Drosten C, Drexler JF. 2013. Human betacoronavirus 2c EMC/2012-related viruses in bats, Ghana and Europe. Emerg. Infect. Dis. 19:456-459.
4. Holmes KV, Dominguez SR. 2013. The new age of virus discovery: genomic analysis of a novel human betacoronavirus isolated from a fatal case of pneumonia. mBio 4:e00548-12. doi:10.1128/mBio.00548-12.
5. Lau SK, Li KS, Tsang AK, Lam CS, Ahmed S, Chen H, Chan KH, Woo PC, Yuen KY. 2013. Genetic characterization of betacoronavirus lineage C viruses in bats reveals marked sequence divergence in the spike protein of Pipistrellus bat coronavirus HKU5 in Japanese pipistrelle: implications for the origin of the novel Middle East respiratory syndrome coronavirus. J. Virol. 87:8638-8650.
6. Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T, Emery S, Tong SX, 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.
7. Peiris JSM, Lai ST, Poon LLM, Guan Y, Yam LYC, Lim W, Nicholls J, Yee WKS, Yan WW, Cheung MT, Cheng VCC, Chan KH, Tsang DNC, Yung RWH, Ng TK, Yuen KY. 2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319-1325.
8. Perlman S, Netland J. 2009. Coronaviruses post-SARS: update on replication and pathogenesis. Nat. Rev. Microbiol. 7:439-450.
9. Hofmann H, Pyrc K, van der Hoek L, Geier M, Berkhout B, Pohlmann S. 2005. Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proc. Natl. Acad. Sci. U.S.A. 102:7988-7993.
10. Li WH, Moore MJ, Vasilieva N, Sui JH, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzuriaga K, Greenough TC, Choe H, Farzan M. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450-454.
11. Delmas B, Gelfi J, Lharidon R, Vogel LK, Sjostrom H, Noren O, Laude H. 1992. Aminopeptidase-N is a major receptor for the enteropathogenic coronavirus TGEV. Nature 357:417-420.
12. Yeager CL, Ashmun RA, Williams RK, Cardellichio CB, Shapiro LH, Look AT, Holmes KV. 1992. Human aminopeptidase-N is a receptor for human coronavirus-229E. Nature 357:420-422.
13. Dveksler GS, Pensiero MN, Cardellichio CB, Williams RK, Jiang GS, Holmes KV, Dieffenbach CW. 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.
14. Williams RK, Jiang GS, Holmes KV. 1991. Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc. Natl. Acad. Sci. U.S.A. 88:5533-5536.
15. Watanabe R, Matsuyama S, Taguchi F. 2006. Receptor-independent infection of murine coronavirus: Analysis by spinoculation. J. Virol. 80: 4901-4908.
16. Watanabe R, Sawicki SG, Taguchi F. 2007. Heparan sulfate is a binding molecule but not a receptor for CEACAM1-independent infection of murine coronavirus. Virology 366:16-22.
17. Cavanagh D, Davis PJ. 1986. Coronavirus IBV-removal of spike glycopolypeptide-S1 by urea abolishes infectivity and hemagglutination but not attachment to cells. J. Gen. Virol. 67:1443-1448.
18. Schultze B, Cavanagh D, Herrler G. 1992. Neuraminidase treatment of avian infectious-bronchitis coronavirus reveals a hemagglutinating activity that is dependent on sialic acid-containing receptors on erythrocytes. Virology 189:792-794.
19. Schultze B, Gross HJ, Brossmer R, Herrler G. 1991. The S-protein of bovine coronavirus is a hemagglutinin recognizing 9-O-acetylated sialic acid as a receptor determinant. J. Virol. 65:6232-6237.
20. Schwegmann-Wessels C, Herrler G. 2006. Sialic acids as receptor determinants for coronaviruses. Glycoconj. J. 23:51-58.
21. Raj VS, Mou HH, Smits SL, Dekkers DHW, Muller MA, Dijkman R, Muth D, Demmers JAA, Zaki A, Fouchier RAM, Thiel V, Drosten C, Rottier PJM, Osterhaus A, Bosch BJ, Haagmans BL. 2013. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495:251-254.
22. Bosch BJ, van der Zee R, de Haan CAM, Rottier PJM. 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.
23. Li F. 2012. Evidence for a common evolutionary origin of coronavirus spike protein receptor-binding subunits. J. Virol. 86:2856-2858.
24. Li F, Li WH, Farzan M, Harrison SC. 2005. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309:1864-1868.
25. Peng GQ, Sun DW, Rajashankar KR, Qian ZH, Holmes KV, Li F. 2011. Crystal structure of mouse coronavirus receptor-binding domain complexed with its murine receptor. Proc. Natl. Acad. Sci. U.S.A. 108:10696-10701.
26. Peng GQ, Xu LQ, Lin YL, Chen L, Pasquarella JR, Holmes KV, Li F. 2012. Crystal structure of bovine coronavirus spike protein lectin domain. J. Biol. Chem. 287:41931-41938.
27. Reguera J, Santiago C, Mudgal G, Ordoño D, Enjuanes L, Casasnovas JM. 2012. Structural bases of coronavirus attachment to host aminopeptidase N and its inhibition by neutralizing antibodies. PLoS Pathog. 8:e1002859. doi:10.1371/journal.ppat.1002859.
28. Wu KL, Li WK, Peng GQ, Li F. 2009. Crystal structure of NL63 respiratory coronavirus receptor-binding domain complexed with its human receptor. Proc. Natl. Acad. Sci. U.S.A. 106:19970-19974.
29. Li F. 2008. Structural analysis of major species barriers between humans and palm civets for severe acute respiratory syndrome coronavirus infections. J. Virol. 82:6984-6991.
30. Wu KL, Peng GQ, Wilken M, Geraghty RJ, Li F. 2012. Mechanisms of host receptor adaptation by severe acute respiratory syndrome coronavirus. J. Biol. Chem. 287:8904-8911.
31. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
32. Grosse-Kunstleve RW, Adams PD. 2003. Substructure search procedures for macromolecular structures. Acta Crystallogr. D Biol. Crystallogr. 59: 1966-1973.
33. Terwilliger TC. 2000. Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56:965-972.
34. Murshudov GN, Vagin AA, Lebedev A, Wilson KS, Dodson EJ. 1999. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr. D Biol. Crystallogr. 55:247-255.
35. Josset L, Menachery VD, Gralinski LE, Agnihothram S, Sova P, Carter VS, Yount BL, Graham RL, Baric RS, Katze MG. 2013. Cell host response to infection with novel human coronavirusEMCpredicts potential antivirals and important differences with SARS coronavirus. mBio 4:e00165-13. doi:10.1128/mBio.00165-13.
36. Wu K, Chen L, Peng G, Zhou W, Pennell CA, Mansky LM, Geraghty RJ, Li F. 2011. A virus-binding hot spot on human angiotensin-converting enzyme 2 is critical for binding of two different coronaviruses. J. Virol. 85:5331-5337.
37. Dauter Z, Dauter M, Rajashankar KR. 2000. Novel approach to phasing proteins: derivatization by short cryo-soaking with halides. Acta Crystallogr. D Biol. Crystallogr. 56:232-237.
38. Holm L, Sander C. 1998. Touring protein fold space with Dali/FSSP. Nucleic Acids Res. 26:316-319.
39. Li F, Berardi M, Li WH, Farzan M, Dormitzer PR, Harrison SC. 2006. Conformational states of the severe acute respiratory syndrome coronavirus spike protein ectodomain. J. Virol. 80:6794-6800.
40. He YX, Lu H, Siddiqui P, Zhou YS, Jiang SB. 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.
41. He YX, Zhou YS, Wu H, Luo BJ, Chen JM, Li WB, Jiang SB. 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.
42. Du L, Zhao G, Kou Z, Ma C, Sun S, Poon VK, Lu L, Wang L, Debnath AK, Zheng BJ, Zhou Y, Jiang S. 2013. Identification of receptor-binding domain in S protein of the novel human coronavirus MERS-CoV as an essential target for vaccine development. J. Virol. [Epub ahead of print.] doi:10.1128/JVI.01048-13.
43. Mou H, Raj VS, van Kuppeveld FJ, Rottier PJ, Haagmans BL, Bosch BJ. 2013. The receptor binding domain of the newMERScoronavirus maps to a 231-residue region in the spike protein that efficiently elicits neutralizing antibodies. J. Virol. [Epub ahead of print.] doi:10.1128/JVI.01277-13.
44. Lu G, Hu Y, Wang Q, Qi J, Gao F, Li Y, Zhang Y, Zhang W, Yuan Y, Bao J, Zhang B, Shi Y, Yan J, Gao GF. 2013. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature [Epub ahead of print.] doi:10.1038/nature12328.
45. Wang N, Shi X, Jiang L, Zhang S, Wang D, Tong P, Guo D, Fu L, Cui Y, Liu X, Arledge KC, Chen YH, Zhang L, Wang X. 2013. Structure of MERS-CoV spike receptor-binding domain complexed with human receptor DPP4. Cell Res. [Epub ahead of print.] doi:10.1038/cr.2013.92.
46. Prabakaran P, Gan JH, Feng Y, Zhu ZY, Choudhry V, Xiao XD, Ji XH, Dimitrov DS. 2006. Structure of severe acute respiratory syndrome coronavirus receptor-binding domain complexed with neutralizing antibody. J. Biol. Chem. 281:15829-15836.