Cryo-electron microscopy structures of the SARS-CoV spike glycoprotein reveal a prerequisite conformational state for receptor binding

Cell Research

Volumn 27, Issue 1, 2017, Pages 119-129

  Gui, Miao ^a   Song, Wenfei ^b   Zhou, Haixia ^b   Xu, Jingwei ^a   Chen, Silian ^a   Xiang, Ye ^a   Wang, Xinquan ^b,c  

^a Tsinghua University   (China)

^b TSINGHUA UNIVERSITY   (China)

^c SICHUAN UNIVERSITY   (China)

Author keywords

cryo EM; receptor binding active state; SARS CoV; spike glycoprotein

Indexed keywords

CELL SURFACE RECEPTOR; CORONAVIRUS SPIKE GLYCOPROTEIN; NEUTRALIZING ANTIBODY; PROTEIN BINDING;

BIOLOGICAL MODEL; CHEMISTRY; CRYOELECTRON MICROSCOPY; HUMAN; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SARS CORONAVIRUS; ULTRASTRUCTURE;

ANTIBODIES, NEUTRALIZING; CRYOELECTRON MICROSCOPY; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RECEPTORS, CELL SURFACE; SARS VIRUS; SPIKE GLYCOPROTEIN, CORONAVIRUS;

EID: 85007247657     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2016.152     Document Type: Article

References (50)

1. Su S, Wong G, Shi W, et al. Epidemiology, genetic recombination, and pathogenesis of coronaviruses. Trends Microbiol 2016; 24:490-502.
2. Ksiazek TG, Erdman D, Goldsmith CS, et al. A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med 2003; 348:1953-1966.
3. Drosten C, Gunther S, Preiser W, et al. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 2003; 348:1967-1976.
4. Peiris JS, Lai ST, Poon LL, et al. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 2003; 361:1319-1325.
5. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 2012; 367:1814-1820.
6. de Groot RJ, Baker SC, Baric RS, et al. Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus Study Group. J Virol 2013; 87:7790-7792.
7. Du L, He Y, Zhou Y, Liu S, Zheng BJ, Jiang S. The spike protein of SARS-CoV-a target for vaccine and therapeutic development. Nat Rev Microbiol 2009; 7:226-236.
8. de Wit E, van Doremalen N, Falzarano D, Munster VJ. SARS and MERS: recent insights into emerging coronaviruses. Nat Rev Microbiol 2016; 14:523-534.
9. Chan JF, Lau SK, To KK, Cheng VC, Woo PC, Yuen KY. Middle East respiratory syndrome coronavirus: another zoonotic betacoronavirus causing SARS-like disease. Clin Microbiol Rev 2015; 28:465-522.
10. Vijay R, Perlman S. Middle East respiratory syndrome and severe acute respiratory syndrome. Curr Opin Virol 2016; 16:70-76.
11. Millet JK, Whittaker GR. Host cell proteases: critical determinants of coronavirus tropism and pathogenesis. Virus Res 2015; 202:120-134.
12. Li F. Receptor recognition mechanisms of coronaviruses: a decade of structural studies. J Virol 2015; 89:1954-1964.
13. Li F. Structure, function, and evolution of coronavirus spike proteins. Annu Rev Virol 2016; 3:237-261.
14. Lu G, Wang Q, Gao GF. Bat-to-human: spike features determining 'host jump' of coronaviruses SARS-CoV, MERS-CoV, and beyond. Trends Microbiol 2015; 23:468-478.
15. Graham RL, Baric RS. Recombination, reservoirs, and the modular spike: mechanisms of coronavirus cross-species transmission. J Virol 2010; 84:3134-3146.
16. Beniac DR, Andonov A, Grudeski E, Booth TF. Architecture of the SARS coronavirus prefusion spike. Nat Struct Mol Biol 2006; 13:751-752.
17. Hofmann H, Pohlmann S. Cellular entry of the SARS coronavirus. Trends Microbiol 2004; 12:466-472.
18. Li F, Li W, Farzan M, Harrison SC. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 2005; 309:1864-1868.
19. Lu G, Hu Y, Wang Q, et al. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature 2013; 500:227-231.
20. Wang N, Shi X, Jiang L, et al. Structure of MERS-CoV spike receptor-binding domain complexed with human receptor DPP4. Cell Res 2013; 23:986-993.
21. Gao J, Lu G, Qi J, et al. Structure of the fusion core and inhibition of fusion by a heptad repeat peptide derived from the S protein of Middle East respiratory syndrome coronavirus. J Virol 2013; 87:13134-13140.
22. Lu L, Liu Q, Zhu Y, et al. Structure-based discovery of Middle East respiratory syndrome coronavirus fusion inhibitor. Nat Commun 2014; 5:3067.
23. Supekar VM, Bruckmann C, Ingallinella P, Bianchi E, Pessi A, Carfi A. Structure of a proteolytically resistant core from the severe acute respiratory syndrome coronavirus S2 fusion protein. Proc Natl Acad Sci USA 2004; 101:17958-17963.
24. Walls AC, Tortorici MA, Bosch BJ, et al. Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature 2016; 531:114-117.
25. Kirchdoerfer RN, Cottrell CA, Wang N, et al. Pre-fusion structure of a human coronavirus spike protein. Nature 2016; 531:118-121.
26. Walls AC, Tortorici MA, Frenz B, et al. Glycan shield and epitope masking of a coronavirus spike protein observed bycryo-electron microscopy. Nat Struct Mol Biol 2016; 23:899-905.
27. Belouzard S, Chu VC, Whittaker GR. Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites. Proc Natl Acad Sci USA 2009; 106:5871-5876.
28. Li W, Moore MJ, Vasilieva N, et al. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 2003; 426:450-454.
29. Hwang WC, Lin Y, Santelli E, et al. Structural basis of neutralization by a human anti-severe acute respiratory syndrome spike protein antibody, 80R. J Biol Chem 2006; 281:34610-34616.
30. Prabakaran P, Gan J, Feng Y, et al. Structure of severe acute respiratory syndrome coronavirus receptor-binding domain complexed with neutralizing antibody. J Biol Chem 2006; 281:15829-15836.
31. Pak JE, Sharon C, Satkunarajah M, et al. Structural insights into immune recognition of the severe acute respiratory syndrome coronavirus S protein receptor binding domain. J Mol Biol 2009; 388:815-823.
32. Huang X, Dong W, Milewska A, et al. Human coronavirus HKU1 spike protein uses O-acetylated sialic acid as an attachment receptor determinant and employs hemagglutinin-esterase protein as a receptor-destroying enzyme. J Virol 2015; 89:7202-7213.
33. Peng G, Sun D, Rajashankar KR, Qian Z, Holmes KV, Li F. Crystal structure of mouse coronavirus receptor-binding domain complexed with its murine receptor. Proc Natl Acad Sci USA 2011; 108:10696-10701.
34. Wang Q, Qi J, Yuan Y, et al. Bat origins of MERS-CoV supported by bat coronavirus HKU4 usage of human receptor CD26. Cell Host Microbe 2014; 16:328-337.
35. Raj VS, Mou H, Smits SL, et al. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 2013; 495:251-254.
36. Yang Y, Du L, Liu C, et al. Receptor usage and cell entry of bat coronavirus HKU4 provide insight into bat-to-human transmission of MERS coronavirus. Proc Natl Acad Sci USA 2014; 111:12516-12521.
37. Li X, Zheng S, Agard DA, Cheng Y. Asynchronous data acquisition and on-the-fly analysis of dose fractionated cryoEM images by UCSFImage. J Struct Biol 2015; 192:174-178.
38. Tang G, Peng L, Baldwin PR, et al. EMAN2: an extensible image processing suite for electron microscopy. J Struct Biol 2007; 157:38-46.
39. Li X, Mooney P, Zheng S, et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat Methods 2013; 10:584-590.
40. Rohou A, Grigorieff N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J Struct Biol 2015; 192:216-221.
41. Scheres SH. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J Struct Biol 2012; 180:519-530.
42. Kucukelbir A, Sigworth FJ, Tagare HD. Quantifying the local resolution of cryo-EM density maps. Nat Methods 2014; 11:63-65.
43. Pettersen EF, Goddard TD, Huang CC, et al. UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 2004; 25:1605-1612.
44. Larkin MA, Blackshields G, Brown NP, et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947-2948.
45. Song Y, DiMaio F, Wang RY, et al. High-resolution comparative modeling with RosettaCM. Structure 2013; 21:1735-1742.
46. DiMaio F, Tyka MD, Baker ML, Chiu W, Baker D. Refinement of protein structures into low-resolution density maps using rosetta. J Mol Biol 2009; 392:181-190.
47. Adams PD, Afonine PV, Bunkoczi G, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 2010; 66:213-221.
48. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 2010; 66:486-501.
49. Brown A, Long F, Nicholls RA, Toots J, Emsley P, Murshudov G. Tools for macromolecular model building and refinement into electron cryo-microscopy reconstructions. Acta Crystallogr D Biol Crystallogr 2015; 71:136-153.
50. Amunts A, Brown A, Bai XC, et al. Structure of the yeast mitochondrial large ribosomal subunit. Science 2014; 343:1485-1489.