Structural insights into coronavirus entry

Advances in Virus Research

Volumn 105, Issue , 2019, Pages 93-116

  Tortorici, M Alejandra ^a,b,c   Veesler, David ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b INSTITUT PASTEUR   (France)

^c Institut Pasteur   (France)

Author keywords

Coronavirus; Fusion protein; Membrane fusion; Proteolytic activation; Spike glycoprotein; Vaccine design

Indexed keywords

ANIMAL; CORONAVIRINAE; HOST PATHOGEN INTERACTION; HUMAN; PHYSIOLOGY; ULTRASTRUCTURE; VIRION; VIRUS ENTRY;

ANIMALS; CORONAVIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; VIRION; VIRUS INTERNALIZATION;

EID: 85070931160     PISSN: 00653527     EISSN: 15578399     Source Type: Book Series    
DOI: 10.1016/bs.aivir.2019.08.002     Document Type: Chapter

References (133)

1. Bai, X. C., Fernandez, I. S., McMullan, G., and Scheres, S. H. (2013). Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. Elife 2, e00461.
2. Bakkers, M. J., Lang, Y., Feitsma, L. J., Hulswit, R. J., de Poot, S. A., van Vliet, A. L., Margine, I., de Groot-Mijnes, J. D., van Kuppeveld, F. J., Langereis, M. A., Huizinga, E. G., and de Groot, R. J. (2017). Betacoronavirus Adaptation to Humans Involved Progressive Loss of Hemagglutinin-Esterase Lectin Activity. Cell Host Microbe 21, 356.
3. Bakkers, M. J., Zeng, Q., Feitsma, L. J., Hulswit, R. J., Li, Z., Westerbeke, A., van Kuppeveld, F. J., Boons, G. J., Langereis, M. A., Huizinga, E. G., and de Groot, R. J. (2016). Coronavirus receptor switch explained from the stereochemistry of protein-carbohydrate interactions and a single mutation. Proc Natl Acad Sci U S A 113, E3111.
4. Barlan, A., Zhao, J., Sarkar, M. K., Li, K., McCray, P. B., Perlman, S., and Gallagher, T. (2014). Receptor variation and susceptibility to Middle East respiratory syndrome coronavirus infection. J Virol 88, 4953.
5. Belouzard, S., Chu, V. C., and Whittaker, G. R. (2009). Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites. Proc Natl Acad Sci U S A 106, 5871.
6. Beniac, D. R., Andonov, A., Grudeski, E., and Booth, T. F. (2006). Architecture of the SARS coronavirus prefusion spike. Nat Struct Mol Biol 13, 751.
7. Beniac, D. R., deVarennes, S. L., Andonov, A., He, R., and Booth, T. F. (2007). Conformational reorganization of the SARS coronavirus spike following receptor binding: implications for membrane fusion. PLoS One 2, e1082.
8. Bos, E. C., Heijnen, L., and Spaan, W. J. (1995). Site directed mutagenesis of the murine coronavirus spike protein. Effects on fusion. Adv Exp Med Biol 380, 283.
9. Bosch, B. J., Bartelink, W., and Rottier, P. J. (2008). Cathepsin L functionally cleaves the severe acute respiratory syndrome coronavirus class I fusion protein upstream of rather than adjacent to the fusion peptide. J Virol 82, 8887.
10. Bosch, B. J., de Haan, C. A., Smits, S. L., and Rottier, P. J. (2005). Spike protein assembly into the coronavirion: exploring the limits of its sequence requirements. Virology 334, 306.
11. Bosch, B. J., van der Zee, R., de Haan, C. A., and Rottier, P. J. (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.
12. Brilot, A. F., Chen, J. Z., Cheng, A., Pan, J., Harrison, S. C., Potter, C. S., Carragher, B., Henderson, R., and Grigorieff, N. (2012). Beam-induced motion of vitrified specimen on holey carbon film. J Struct Biol 177, 630.
13. Burkard, C., Verheije, M. H., Wicht, O., van Kasteren, S. I., van Kuppeveld, F. J., Haagmans, B. L., Pelkmans, L., Rottier, P. J., Bosch, B. J., and de Haan, C. A. (2014). Coronavirus cell entry occurs through the endo-/lysosomal pathway in a proteolysis-dependent manner. PLoS Pathog 10, e1004502.
14. Campbell, M. G., Cheng, A., Brilot, A. F., Moeller, A., Lyumkis, D., Veesler, D., Pan, J., Harrison, S. C., Potter, C. S., Carragher, B., and Grigorieff, N. (2012). Movies of ice-embedded particles enhance resolution in electron cryo-microscopy. Structure 20, 1823.
15. Campbell, M. G., Veesler, D., Cheng, A., Potter, C. S., and Carragher, B. (2015). 2.8 Å resolution reconstruction of the Thermoplasma acidophilum 20S proteasome using cryo-electron microscopy. Elife 4.
16. Chang, K. W., Sheng, Y., and Gombold, J. L. (2000). Coronavirus-induced membrane fusion requires the cysteine-rich domain in the spike protein. Virology 269, 212.
17. Chen, J., Kovacs, J. M., Peng, H., Rits-Volloch, S., Lu, J., Park, D., Zablowsky, E., Seaman, M. S., and Chen, B. (2015). HIV-1 ENVELOPE. Effect of the cytoplasmic domain on antigenic characteristics of HIV-1 envelope glycoprotein. Science 349, 191.
18. Chen, Y., Rajashankar, K. R., Yang, Y., Agnihothram, S. S., Liu, C., Lin, Y. L., Baric, R. S., and Li, F. (2013). Crystal structure of the receptor-binding domain from newly emerged Middle East respiratory syndrome coronavirus. J Virol 87, 10777.
19. Corti, D., Voss, J., Gamblin, S. J., Codoni, G., Macagno, A., Jarrossay, D., Vachieri, S. G., Pinna, D., Minola, A., Vanzetta, F., Silacci, C., Fernandez-Rodriguez, B. M., Agatic, G., Bianchi, S., Giacchetto-Sasselli, I., Calder, L., Sallusto, F., Collins, P., Haire, L. F., Temperton, N., Langedijk, J. P., Skehel, J. J., and Lanzavecchia, A. (2011). A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333, 850.
20. Corti, D., Zhao, J., Pedotti, M., Simonelli, L., Agnihothram, S., Fett, C., Fernandez-Rodriguez, B., Foglierini, M., Agatic, G., Vanzetta, F., Gopal, R., Langrish, C. J., Barrett, N. A., Sallusto, F., Baric, R. S., Varani, L., Zambon, M., Perlman, S., and Lanzavecchia, A. (2015). Prophylactic and postexposure efficacy of a potent human monoclonal antibody against MERS coronavirus. Proc Natl Acad Sci U S A 112, 10473.
21. Daniel, C., Anderson, R., Buchmeier, M. J., Fleming, J. O., Spaan, W. J., Wege, H., and Talbot, P. J. (1993). Identification of an immunodominant linear neutralization domain on the S2 portion of the murine coronavirus spike glycoprotein and evidence that it forms part of complex tridimensional structure. J Virol 67, 1185.
22. Delmas, B., Gelfi, J., L'Haridon, R., Vogel, L. K., Sjöström, H., Norén, O., and Laude, H. (1992). Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 357, 417.
23. Delmas, B., Gelfi, J., Sjöström, H., Noren, O., and Laude, H. (1993). Further characterization of aminopeptidase-N as a receptor for coronaviruses. Adv Exp Med Biol 342, 293.
24. Dev, J., Park, D., Fu, Q., Chen, J., Ha, H. J., Ghantous, F., Herrmann, T., Chang, W., Liu, Z., Frey, G., Seaman, M. S., Chen, B., and Chou, J. J. (2016). Structural basis for membrane anchoring of HIV-1 envelope spike. Science 353, 172.
25. Du, L., Tai, W., Yang, Y., Zhao, G., Zhu, Q., Sun, S., Liu, C., Tao, X., Tseng, C. K., Perlman, S., Jiang, S., Zhou, Y., and Li, F. (2016). Introduction of neutralizing immunogenicity index to the rational design of MERS coronavirus subunit vaccines. Nat Commun 7, 13473.
26. Duquerroy, S., Vigouroux, A., Rottier, P. J., Rey, F. A., and Bosch, B. J. (2005). Central ions and lateral asparagine/glutamine zippers stabilize the post-fusion hairpin conformation of the SARS coronavirus spike glycoprotein. Virology 335, 276.
27. Dveksler, G. S., Pensiero, M. N., Cardellichio, C. B., Williams, R. K., Jiang, G. S., Holmes, K. V., and Dieffenbach, C. W. (1991). Cloning of the mouse hepatitis virus (MHV) receptor: expression in human and hamster cell lines confers susceptibility to MHV. J Virol 65, 6881.
28. Earnest, J. T., Hantak, M. P., Li, K., McCray, P. B., Perlman, S., and Gallagher, T. (2017). The tetraspanin CD9 facilitates MERS-coronavirus entry by scaffolding host cell receptors and proteases. PLoS Pathog 13, e1006546.
29. Earnest, J. T., Hantak, M. P., Park, J. E., and Gallagher, T. (2015). Coronavirus and influenza virus proteolytic priming takes place in tetraspanin-enriched membrane microdomains. J Virol 89, 6093.
30. Eifart, P., Ludwig, K., Bottcher, C., de Haan, C. A., Rottier, P. J., Korte, T., and Herrmann, A. (2007). Role of endocytosis and low pH in murine hepatitis virus strain A59 cell entry. J Virol 81, 10758.
31. Frana, M. F., Behnke, J. N., Sturman, L. S., and Holmes, K. V. (1985). Proteolytic cleavage of the E2 glycoprotein of murine coronavirus: host-dependent differences in proteolytic cleavage and cell fusion. J Virol 56, 912.
32. Gao, J., Lu, G., Qi, J., Li, Y., Wu, Y., Deng, Y., Geng, H., Li, H., Wang, Q., Xiao, H., Tan, W., Yan, J., and Gao, G. F. (2013). 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 87, 13134.
33. Ge, X. Y., Li, J. L., Yang, X. L., Chmura, A. A., Zhu, G., Epstein, J. H., Mazet, J. K., Hu, B., Zhang, W., Peng, C., Zhang, Y. J., Luo, C. M., Tan, B., Wang, N., Zhu, Y., Crameri, G., Zhang, S. Y., Wang, L. F., Daszak, P., and Shi, Z. L. (2013). Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503, 535.
34. Gui, M., Song, W., Zhou, H., Xu, J., Chen, S., Xiang, Y., and Wang, X. (2017). Cryo-electron microscopy structures of the SARS-CoV spike glycoprotein reveal a prerequisite conformational state for receptor binding. Cell Res 27, 119.
35. Haagmans, B. L., Al Dhahiry, S. H., Reusken, C. B., Raj, V. S., Galiano, M., Myers, R., Godeke, G. J., Jonges, M., Farag, E., Diab, A., Ghobashy, H., Alhajri, F., Al-Thani, M., Al-Marri, S. A., Al Romaihi, H. E., Al Khal, A., Bermingham, A., Osterhaus, A. D., AlHajri, M. M., and Koopmans, M. P. (2014). Middle East respiratory syndrome coronavirus in dromedary camels: an outbreak investigation. Lancet Infect Dis 14, 140.
36. Harrison, S. C. (2008). Viral membrane fusion. Nat Struct Mol Biol 15, 690.
37. Heald-Sargent, T., and Gallagher, T. (2012). Ready, set, fuse! The coronavirus spike protein and acquisition of fusion competence. Viruses 4, 557.
38. Hofmann, H., Pyrc, K., van der Hoek, L., Geier, M., Berkhout, B., and 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.
39. Hu, B., Zeng, L. P., Yang, X. L., Ge, X. Y., Zhang, W., Li, B., Xie, J. Z., Shen, X. R., Zhang, Y. Z., Wang, N., Luo, D. S., Zheng, X. S., Wang, M. N., Daszak, P., Wang, L. F., Cui, J., and Shi, Z. L. (2017). Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus. PLoS Pathog 13, e1006698.
40. Hulswit, R. J., de Haan, C. A., and Bosch, B. J. (2016). Coronavirus Spike Protein and Tropism Changes. Adv Virus Res 96, 29.
41. Hulswit, R. J. G., Lang, Y., Bakkers, M. J. G., Li, W., Li, Z., Schouten, A., Ophorst, B., van Kuppeveld, F. J. M., Boons, G. J., Bosch, B. J., Huizinga, E. G., and de Groot, R. J. (2019). Human coronaviruses OC43 and HKU1 bind to 9-O-acetylated sialic acids via a conserved receptor-binding site in spike protein domain A. Proc Natl Acad Sci U S A 116, 2681.
42. Inoue, Y., Tanaka, N., Tanaka, Y., Inoue, S., Morita, K., Zhuang, M., Hattori, T., and Sugamura, K. (2007). Clathrin-dependent entry of severe acute respiratory syndrome coronavirus into target cells expressing ACE2 with the cytoplasmic tail deleted. J Virol 81, 8722.
43. Isaacs, D., Flowers, D., Clarke, J. R., Valman, H. B., and MacNaughton, M. R. (1983). Epidemiology of coronavirus respiratory infections. Arch Dis Child 58, 500.
44. Kirchdoerfer, R. N., Cottrell, C. A., Wang, N., Pallesen, J., Yassine, H. M., Turner, H. L., Corbett, K. S., Graham, B. S., McLellan, J. S., and Ward, A. B. (2016). Pre-fusion structure of a human coronavirus spike protein. Nature 531, 118.
45. Kirchdoerfer, R. N., Wang, N., Pallesen, J., Wrapp, D., Turner, H. L., Cottrell, C. A., Corbett, K. S., Graham, B. S., McLellan, J. S., and Ward, A. B. (2018). Stabilized coronavirus spikes are resistant to conformational changes induced by receptor recognition or proteolysis. Sci Rep 8, 15701.
46. Kong, R., Xu, K., Zhou, T., Acharya, P., Lemmin, T., Liu, K., Ozorowski, G., Soto, C., Taft, J. D., Bailer, R. T., Cale, E. M., Chen, L., Choi, C. W., Chuang, G. Y., Doria-Rose, N. A., Druz, A., Georgiev, I. S., Gorman, J., Huang, J., Joyce, M. G., Louder, M. K., Ma, X., McKee, K., O'Dell, S., Pancera, M., Yang, Y., Blanchard, S. C., Mothes, W., Burton, D. R., Koff, W. C., Connors, M., Ward, A. B., Kwong, P. D., and Mascola, J. R. (2016). Fusion peptide of HIV-1 as a site of vulnerability to neutralizing antibody. Science 352, 828.
47. Krempl, C., Schultze, B., and Herrler, G. (1995). Analysis of cellular receptors for human coronavirus OC43. Adv Exp Med Biol 380, 371.
48. Krempl, C., Schultze, B., Laude, H., and Herrler, G. (1997). Point mutations in the S protein connect the sialic acid binding activity with the enteropathogenicity of transmissible gastroenteritis coronavirus. J Virol 71, 3285.
49. Krokhin, O., Li, Y., Andonov, A., Feldmann, H., Flick, R., Jones, S., Stroeher, U., Bastien, N., Dasuri, K. V., Cheng, K., Simonsen, J. N., Perreault, H., Wilkins, J., Ens, W., Plummer, F., and Standing, K. G. (2003). Mass spectrometric characterization of proteins from the SARS virus: a preliminary report. Mol Cell Proteomics 2, 346.
50. Lang, S., Xie, J., Zhu, X., Wu, N. C., Lerner, R. A., and Wilson, I. A. (2017). Antibody 27F3 Broadly Targets Influenza A Group 1 and 2 Hemagglutinins through a Further Variation in VH1-69 Antibody Orientation on the HA Stem. Cell Rep 20, 2935.
51. Li, F., Li, W., Farzan, M., and Harrison, S. C. (2005a). Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309, 1864.
52. Li, W., Hulswit, R. J. G., Kenney, S. P., Widjaja, I., Jung, K., Alhamo, M. A., van Dieren, B., van Kuppeveld, F. J. M., Saif, L. J., and Bosch, B. J. (2018). Broad receptor engagement of an emerging global coronavirus may potentiate its diverse cross-species transmissibility. Proc Natl Acad Sci U S A 115, E5135.
53. Li, W., Hulswit, R. J. G., Widjaja, I., Raj, V. S., McBride, R., Peng, W., Widagdo, W., Tortorici, M. A., van Dieren, B., Lang, Y., van Lent, J. W. M., Paulson, J. C., de Haan, C. A. M., de Groot, R. J., van Kuppeveld, F. J. M., Haagmans, B. L., and Bosch, B. J. (2017). Identification of sialic acid-binding function for the Middle East respiratory syndrome coronavirus spike glycoprotein. Proc Natl Acad Sci U S A 114, E8508.
54. Li, W., Moore, M. J., Vasilieva, N., Sui, J., Wong, S. K., Berne, M. A., Somasundaran, M., Sullivan, J. L., Luzuriaga, K., Greenough, T. C., Choe, H., and Farzan, M. (2003). Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426, 450.
55. Li, W., Wicht, O., van Kuppeveld, F. J., He, Q., Rottier, P. J., and Bosch, B. J. (2015). A Single Point Mutation Creating a Furin Cleavage Site in the Spike Protein Renders Porcine Epidemic Diarrhea Coronavirus Trypsin Independent for Cell Entry and Fusion. J Virol 89, 8077.
56. Li, W., Zhang, C., Sui, J., Kuhn, J. H., Moore, M. J., Luo, S., Wong, S. K., Huang, I. C., Xu, K., Vasilieva, N., Murakami, A., He, Y., Marasco, W. A., Guan, Y., Choe, H., and Farzan, M. (2005b). Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J 24, 1634.
57. Li, X., Mooney, P., Zheng, S., Booth, C. R., Braunfeld, M. B., Gubbens, S., Agard, D. A., and Cheng, Y. (2013). Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat Methods 10, 584.
58. Liu, C., Tang, J., Ma, Y., Liang, X., Yang, Y., Peng, G., Qi, Q., Jiang, S., Li, J., Du, L., and Li, F. (2015). Receptor usage and cell entry of porcine epidemic diarrhea coronavirus. J Virol 89, 6121.
59. Lontok, E., Corse, E., and Machamer, C. E. (2004). Intracellular targeting signals contribute to localization of coronavirus spike proteins near the virus assembly site. J Virol 78, 5913.
60. 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., and Gao, G. F. (2013). Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature 500, 227.
61. McCoy, L. E., van Gils, M. J., Ozorowski, G., Messmer, T., Briney, B., Voss, J. E., Kulp, D. W., Macauley, M. S., Sok, D., Pauthner, M., Menis, S., Cottrell, C. A., Torres, J. L., Hsueh, J., Schief, W. R., Wilson, I. A., Ward, A. B., Sanders, R. W., and Burton, D. R. (2016). Holes in the Glycan Shield of the Native HIV Envelope Are a Target of Trimer-Elicited Neutralizing Antibodies. Cell Rep 16, 2327.
62. McLellan, J. S., Chen, M., Leung, S., Graepel, K. W., Du, X., Yang, Y., Zhou, T., Baxa, U., Yasuda, E., Beaumont, T., Kumar, A., Modjarrad, K., Zheng, Z., Zhao, M., Xia, N., Kwong, P. D., and Graham, B. S. (2013). Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340, 1113.
63. McLellan, J. S., Yang, Y., Graham, B. S., and Kwong, P. D. (2011). Structure of respiratory syncytial virus fusion glycoprotein in the postfusion conformation reveals preservation of neutralizing epitopes. J Virol 85, 7788.
64. Menachery, V. D., Yount, B. L., Debbink, K., Agnihothram, S., Gralinski, L. E., Plante, J. A., Graham, R. L., Scobey, T., Ge, X. Y., Donaldson, E. F., Randell, S. H., Lanzavecchia, A., Marasco, W. A., Shi, Z. L., and Baric, R. S. (2015). A SARS-like cluster of circulating bat coronaviruses shows potential for human emergence. Nat Med 21, 1508.
65. Menachery, V. D., Yount, B. L., Sims, A. C., Debbink, K., Agnihothram, S. S., Gralinski, L. E., Graham, R. L., Scobey, T., Plante, J. A., Royal, S. R., Swanstrom, J., Sheahan, T. P., Pickles, R. J., Corti, D., Randell, S. H., Lanzavecchia, A., Marasco, W. A., and Baric, R. S. (2016). SARS-like WIV1-CoV poised for human emergence. Proc Natl Acad Sci U S A 113, 3048.
66. Milewska, A., Zarebski, M., Nowak, P., Stozek, K., Potempa, J., and Pyrc, K. (2014). Human coronavirus NL63 utilizes heparan sulfate proteoglycans for attachment to target cells. J Virol 88, 13221.
67. Millet, J. K., and Whittaker, G. R. (2014). Host cell entry of Middle East respiratory syndrome coronavirus after two-step, furin-mediated activation of the spike protein. Proc Natl Acad Sci U S A 111, 15214.
68. Millet, J. K., and Whittaker, G. R. (2015). Host cell proteases: Critical determinants of coronavirus tropism and pathogenesis. Virus Res 202, 120.
69. Ng, M. L., Tan, S. H., See, E. E., Ooi, E. E., and Ling, A. E. (2003). Proliferative growth of SARS coronavirus in Vero E6 cells. J Gen Virol 84, 3291.
70. Nomura, R., Kiyota, A., Suzaki, E., Kataoka, K., Ohe, Y., Miyamoto, K., Senda, T., and Fujimoto, T. (2004). Human coronavirus 229E binds to CD13 in rafts and enters the cell through caveolae. J Virol 78, 8701.
71. Owczarek, K., Szczepanski, A., Milewska, A., Baster, Z., Rajfur, Z., Sarna, M., and Pyrc, K. (2018). Early events during human coronavirus OC43 entry to the cell. Sci Rep 8, 7124.
72. Pallesen, J., Wang, N., Corbett, K. S., Wrapp, D., Kirchdoerfer, R. N., Turner, H. L., Cottrell, C. A., Becker, M. M., Wang, L., Shi, W., Kong, W. P., Andres, E. L., Kettenbach, A. N., Denison, M. R., Chappell, J. D., Graham, B. S., Ward, A. B., and McLellan, J. S. (2017). Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen. Proc Natl Acad Sci U S A 114, E7348.
73. Park, J. E., Li, K., Barlan, A., Fehr, A. R., Perlman, S., McCray, P. B., and Gallagher, T. (2016). Proteolytic processing of Middle East respiratory syndrome coronavirus spikes expands virus tropism. Proc Natl Acad Sci U S A 113, 12262.
74. Peng, G., Sun, D., Rajashankar, K. R., Qian, Z., Holmes, K. V., and 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.
75. Peng, G., Xu, L., Lin, Y. L., Chen, L., Pasquarella, J. R., Holmes, K. V., and Li, F. (2012). Crystal structure of bovine coronavirus spike protein lectin domain. J Biol Chem 287, 41931.
76. Petit, C. M., Melancon, J. M., Chouljenko, V. N., Colgrove, R., Farzan, M., Knipe, D. M., and Kousoulas, K. G. (2005). Genetic analysis of the SARS-coronavirus spike glycoprotein functional domains involved in cell-surface expression and cell-to-cell fusion. Virology 341, 215.
77. Prabakaran, P., Gan, J., Feng, Y., Zhu, Z., Choudhry, V., Xiao, X., Ji, X., and Dimitrov, D. S. (2006). Structure of severe acute respiratory syndrome coronavirus receptor-binding domain complexed with neutralizing antibody. J Biol Chem 281, 15829.
78. Punjani, A., Rubinstein, J. L., Fleet, D. J., and Brubaker, M. A. (2017). cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat Methods 14, 290.
79. Raj, V. S., Mou, H., Smits, S. L., Dekkers, D. H., Muller, M. A., Dijkman, R., Muth, D., Demmers, J. A., Zaki, A., Fouchier, R. A., Thiel, V., Drosten, C., Rottier, P. J., Osterhaus, A. D., Bosch, B. J., and Haagmans, B. L. (2013). Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495, 251.
80. Regan, A. D., Shraybman, R., Cohen, R. D., and Whittaker, G. R. (2008). Differential role for low pH and cathepsin-mediated cleavage of the viral spike protein during entry of serotype II feline coronaviruses. Vet Microbiol 132, 235.
81. Reguera, J., Santiago, C., Mudgal, G., Ordoño, D., Enjuanes, L., and Casasnovas, J. M. (2012). Structural bases of coronavirus attachment to host aminopeptidase N and its inhibition by neutralizing antibodies. PLoS Pathog 8, e1002859.
82. Ritchie, G., Harvey, D. J., Feldmann, F., Stroeher, U., Feldmann, H., Royle, L., Dwek, R. A., and Rudd, P. M. (2010). Identification of N-linked carbohydrates from severe acute respiratory syndrome (SARS) spike glycoprotein. Virology 399, 257.
83. Rockx, B., Corti, D., Donaldson, E., Sheahan, T., Stadler, K., Lanzavecchia, A., and Baric, R. (2008). Structural basis for potent cross-neutralizing human monoclonal antibody protection against lethal human and zoonotic severe acute respiratory syndrome coronavirus challenge. J Virol 82, 3220.
84. Rosenthal, P. B., Zhang, X., Formanowski, F., Fitz, W., Wong, C. H., Meier-Ewert, H., Skehel, J. J., and Wiley, D. C. (1998). Structure of the haemagglutinin-esterase-fusion glycoprotein of influenza C virus. Nature 396, 92.
85. Sabir, J. S., Lam, T. T., Ahmed, M. M., Li, L., Shen, Y., Abo-Aba, S. E., Qureshi, M. I., Abu-Zeid, M., Zhang, Y., Khiyami, M. A., Alharbi, N. S., Hajrah, N. H., Sabir, M. J., Mutwakil, M. H., Kabli, S. A., Alsulaimany, F. A., Obaid, A. Y., Zhou, B., Smith, D. K., Holmes, E. C., Zhu, H., and Guan, Y. (2016). Co-circulation of three camel coronavirus species and recombination of MERS-CoVs in Saudi Arabia. Science 351, 81.
86. Scheres, S. H. (2012). RELION: implementation of a Bayesian approach to cryo-EM structure determination. J Struct Biol 180, 519.
87. Schroth-Diez, B., Ludwig, K., Baljinnyam, B., Kozerski, C., Huang, Q., and Herrmann, A. (2000). The role of the transmembrane and of the intraviral domain of glycoproteins in membrane fusion of enveloped viruses. Biosci Rep 20, 571.
88. Schwegmann-Wessels, C., Zimmer, G., Schröder, B., Breves, G., and Herrler, G. (2003). Binding of transmissible gastroenteritis coronavirus to brush border membrane sialoglycoproteins. J Virol 77, 11846.
89. Shang, J., Zheng, Y., Yang, Y., Liu, C., Geng, Q., Luo, C., Zhang, W., and Li, F. (2018a). Cryo-EM structure of infectious bronchitis coronavirus spike protein reveals structural and functional evolution of coronavirus spike proteins. PLoS Pathog 14, e1007009.
90. Shang, J., Zheng, Y., Yang, Y., Liu, C., Geng, Q., Tai, W., Du, L., Zhou, Y., Zhang, W., and Li, F. (2018b). Cryo-Electron Microscopy Structure of Porcine Deltacoronavirus Spike Protein in the Prefusion State. J Virol 92.
91. Shulla, A., Heald-Sargent, T., Subramanya, G., Zhao, J., Perlman, S., and Gallagher, T. (2011). A transmembrane serine protease is linked to the severe acute respiratory syndrome coronavirus receptor and activates virus entry. J Virol 85, 873.
92. Simmons, G., Gosalia, D. N., Rennekamp, A. J., Reeves, J. D., Diamond, S. L., and Bates, P. (2005). Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc Natl Acad Sci U S A 102, 11876.
93. Song, W., Gui, M., Wang, X., and Xiang, Y. (2018). Cryo-EM structure of the SARS coronavirus spike glycoprotein in complex with its host cell receptor ACE2. PLoS Pathog 14, e1007236.
94. Stertz, S., Reichelt, M., Spiegel, M., Kuri, T., Martínez-Sobrido, L., García-Sastre, A., Weber, F., and Kochs, G. (2007). The intracellular sites of early replication and budding of SARS-coronavirus. Virology 361, 304.
95. Su, S., Wong, G., Shi, W., Liu, J., Lai, A. C. K., Zhou, J., Liu, W., Bi, Y., and Gao, G. F. (2016). Epidemiology, Genetic Recombination, and Pathogenesis of Coronaviruses. Trends Microbiol 24, 490.
96. Supekar, V. M., Bruckmann, C., Ingallinella, P., Bianchi, E., Pessi, A., and Carfí, A. (2004). Structure of a proteolytically resistant core from the severe acute respiratory syndrome coronavirus S2 fusion protein. Proc Natl Acad Sci U S A 101, 17958.
97. Swanson, K., Wen, X., Leser, G. P., Paterson, R. G., Lamb, R. A., and Jardetzky, T. S. (2010). Structure of the Newcastle disease virus F protein in the post-fusion conformation. Virology 402, 372.
98. Swanson, K. A., Settembre, E. C., Shaw, C. A., Dey, A. K., Rappuoli, R., Mandl, C. W., Dormitzer, P. R., and Carfi, A. (2011). Structural basis for immunization with postfusion respiratory syncytial virus fusion F glycoprotein (RSV F) to elicit high neutralizing antibody titers. Proc Natl Acad Sci U S A 108, 9619.
99. Thorp, E. B., Boscarino, J. A., Logan, H. L., Goletz, J. T., and Gallagher, T. M. (2006). Palmitoylations on murine coronavirus spike proteins are essential for virion assembly and infectivity. J Virol 80, 1280.
100. Tortorici, M. A., Walls, A. C., Lang, Y., Wang, C., Li, Z., Koerhuis, D., Boons, G. J., Bosch, B. J., Rey, F. A., de Groot, R. J., and Veesler, D. (2019). Structural basis for human coronavirus attachment to sialic acid receptors. Nat Struct Mol Biol 26, 481.
101. Traggiai, E., Becker, S., Subbarao, K., Kolesnikova, L., Uematsu, Y., Gismondo, M. R., Murphy, B. R., Rappuoli, R., and Lanzavecchia, A. (2004). An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus. Nat Med 10, 871.
102. Van Hamme, E., Dewerchin, H. L., Cornelissen, E., Verhasselt, B., and Nauwynck, H. J. (2008). Clathrin- and caveolae-independent entry of feline infectious peritonitis virus in monocytes depends on dynamin. J Gen Virol 89, 2147.
103. Vlasak, R., Luytjes, W., Spaan, W., and Palese, P. (1988). Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses. Proc Natl Acad Sci U S A 85, 4526.
104. Walls, A., Tortorici, M. A., Bosch, B. J., Frenz, B., Rottier, P. J., DiMaio, F., Rey, F. A., and Veesler, D. (2017a). Crucial steps in the structure determination of a coronavirus spike glycoprotein using cryo-electron microscopy. Protein Sci 26, 113.
105. Walls, A. C., Tortorici, M. A., Bosch, B. J., Frenz, B., Rottier, P. J. M., DiMaio, F., Rey, F. A., and Veesler, D. (2016a). Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature 531, 114.
106. Walls, A. C., Tortorici, M. A., Frenz, B., Snijder, J., Li, W., Rey, F. A., DiMaio, F., Bosch, B. J., and Veesler, D. (2016b). Glycan shield and epitope masking of a coronavirus spike protein observed by cryo-electron microscopy. Nat Struct Mol Biol 23, 899.
107. Walls, A. C., Tortorici, M. A., Snijder, J., Xiong, X., Bosch, B. J., Rey, F. A., and Veesler, D. (2017b). Tectonic conformational changes of a coronavirus spike glycoprotein promote membrane fusion. Proc Natl Acad Sci U S A 114, 11157.
108. Walls, A. C., Xiong, X., Park, Y. J., Tortorici, M. A., Snijder, J., Quispe, J., Cameroni, E., Gopal, R., Dai, M., Lanzavecchia, A., Zambon, M., Rey, F. A., Corti, D., and Veesler, D. (2019). Unexpected Receptor Functional Mimicry Elucidates Activation of Coronavirus Fusion. Cell 176, 1026.
109. Wang, N., Shi, X., Jiang, L., Zhang, S., Wang, D., Tong, P., Guo, D., Fu, L., Cui, Y., Liu, X., Arledge, K. C., Chen, Y. H., Zhang, L., and Wang, X. (2013). Structure of MERS-CoV spike receptor-binding domain complexed with human receptor DPP4. Cell Res 23, 986.
110. Wang, Q., Qi, J., Yuan, Y., Xuan, Y., Han, P., Wan, Y., Ji, W., Li, Y., Wu, Y., Wang, J., Iwamoto, A., Woo, P. C., Yuen, K. Y., Yan, J., Lu, G., and Gao, G. F. (2014). Bat origins of MERS-CoV supported by bat coronavirus HKU4 usage of human receptor CD26. Cell Host Microbe 16, 328.
111. Wang, S., Guo, F., Liu, K., Wang, H., Rao, S., Yang, P., and Jiang, C. (2008). Endocytosis of the receptor-binding domain of SARS-CoV spike protein together with virus receptor ACE2. Virus Res 136, 8.
112. Wicht, O., Li, W., Willems, L., Meuleman, T. J., Wubbolts, R. W., van Kuppeveld, F. J., Rottier, P. J., and Bosch, B. J. (2014). Proteolytic activation of the porcine epidemic diarrhea coronavirus spike fusion protein by trypsin in cell culture. J Virol 88, 7952.
113. Wickramasinghe, I. N., de Vries, R. P., Grone, A., de Haan, C. A., and Verheije, M. H. (2011). Binding of avian coronavirus spike proteins to host factors reflects virus tropism and pathogenicity. J Virol 85, 8903.
114. Williams, R. K., Jiang, G. S., and Holmes, K. V. (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.
115. Wong, A. H. M., Tomlinson, A. C. A., Zhou, D., Satkunarajah, M., Chen, K., Sharon, C., Desforges, M., Talbot, P. J., and Rini, J. M. (2017). Receptor-binding loops in alphacoronavirus adaptation and evolution. Nat Commun 8, 1735.
116. Wong, J. J., Paterson, R. G., Lamb, R. A., and Jardetzky, T. S. (2016). Structure and stabilization of the Hendra virus F glycoprotein in its prefusion form. Proc Natl Acad Sci U S A 113, 1056.
117. Wu, K., Li, W., Peng, G., and 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.
118. Xiong, X., Coombs, P. J., Martin, S. R., Liu, J., Xiao, H., McCauley, J. W., Locher, K., Walker, P. A., Collins, P. J., Kawaoka, Y., Skehel, J. J., and Gamblin, S. J. (2013). Receptor binding by a ferret-transmissible H5 avian influenza virus. Nature 497, 392.
119. Xiong, X., Tortorici, M. A., Snijder, J., Yoshioka, C., Walls, A. C., Li, W., McGuire, A. T., Rey, F. A., Bosch, B. J., and Veesler, D. (2018). Glycan Shield and Fusion Activation of a Deltacoronavirus Spike Glycoprotein Fine-Tuned for Enteric Infections. J Virol 92.
120. Xu, K., Chan, Y. P., Bradel-Tretheway, B., Akyol-Ataman, Z., Zhu, Y., Dutta, S., Yan, L., Feng, Y., Wang, L. F., Skiniotis, G., Lee, B., Zhou, Z. H., Broder, C. C., Aguilar, H. C., and Nikolov, D. B. (2015). Crystal Structure of the Pre-fusion Nipah Virus Fusion Glycoprotein Reveals a Novel Hexamer-of-Trimers Assembly. PLoS Pathog 11, e1005322.
121. Xu, Y., Liu, Y., Lou, Z., Qin, L., Li, X., Bai, Z., Pang, H., Tien, P., Gao, G. F., and Rao, Z. (2004a). Structural basis for coronavirus-mediated membrane fusion. Crystal structure of mouse hepatitis virus spike protein fusion core. J Biol Chem 279, 30514.
122. Xu, Y., Su, N., Qin, L., Bai, Z., Gao, G. F., and Rao, Z. (2004b). Crystallization and preliminary crystallographic analysis of the heptad-repeat complex of SARS coronavirus spike protein. Acta Crystallogr D Biol Crystallogr 60, 2377.
123. Yamada, Y., and Liu, D. X. (2009). Proteolytic activation of the spike protein at a novel RRRR/S motif is implicated in furin-dependent entry, syncytium formation, and infectivity of coronavirus infectious bronchitis virus in cultured cells. J Virol 83, 8744.
124. Yang, Y., Liu, C., Du, L., Jiang, S., Shi, Z., Baric, R. S., and Li, F. (2015). Two Mutations Were Critical for Bat-to-Human Transmission of Middle East Respiratory Syndrome Coronavirus. J Virol 89, 9119.
125. Ye, R., Montalto-Morrison, C., and Masters, P. S. (2004). Genetic analysis of determinants for spike glycoprotein assembly into murine coronavirus virions: distinct roles for charge-rich and cysteine-rich regions of the endodomain. J Virol 78, 9904.
126. Yeager, C. L., Ashmun, R. A., Williams, R. K., Cardellichio, C. B., Shapiro, L. H., Look, A. T., and Holmes, K. V. (1992). Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357, 420.
127. Yin, H. S., Paterson, R. G., Wen, X., Lamb, R. A., and Jardetzky, T. S. (2005). Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc Natl Acad Sci U S A 102, 9288.
128. Yin, H. S., Wen, X., Paterson, R. G., Lamb, R. A., and Jardetzky, T. S. (2006). Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439, 38.
129. Youn, S., Collisson, E. W., and Machamer, C. E. (2005). Contribution of trafficking signals in the cytoplasmic tail of the infectious bronchitis virus spike protein to virus infection. J Virol 79, 13209.
130. Yu, X., Zhang, S., Jiang, L., Cui, Y., Li, D., Wang, D., Wang, N., Fu, L., Shi, X., Li, Z., Zhang, L., and Wang, X. (2015). Structural basis for the neutralization of MERS-CoV by a human monoclonal antibody MERS-27. Sci Rep 5, 13133.
131. Yuan, Y., Cao, D., Zhang, Y., Ma, J., Qi, J., Wang, Q., Lu, G., Wu, Y., Yan, J., Shi, Y., Zhang, X., and Gao, G. F. (2017). Cryo-EM structures of MERS-CoV and SARS-CoV spike glycoproteins reveal the dynamic receptor binding domains. Nat Commun 8, 15092.
132. Zhang, H., Wang, G., Li, J., Nie, Y., Shi, X., Lian, G., Wang, W., Yin, X., Zhao, Y., Qu, X., Ding, M., and Deng, H. (2004). Identification of an antigenic determinant on the S2 domain of the severe acute respiratory syndrome coronavirus spike glycoprotein capable of inducing neutralizing antibodies. J Virol 78, 6938.
133. Zheng, Q., Deng, Y., Liu, J., van der Hoek, L., Berkhout, B., and Lu, M. (2006). Core structure of S2 from the human coronavirus NL63 spike glycoprotein. Biochemistry 45, 15205.