Coronavirus Spike Protein and Tropism Changes

Advances in Virus Research

Volumn 96, Issue , 2016, Pages 29-57

  Hulswit, R J G ^a   de Haan, C A M ^a   Bosch, B J ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Coronavirus spike; Cross species transmission; Cryo EM structure; Membrane fusion; Receptor interaction; Tropism

Indexed keywords

CORONAVIRUS SPIKE GLYCOPROTEIN; PROTEIN SUBUNIT; VIRUS RECEPTOR;

ANIMAL; CHEMISTRY; GENE EXPRESSION; GENETIC VARIATION; GENETICS; HUMAN; METABOLISM; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MOLECULAR MODEL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN SUBUNIT; SARS CORONAVIRUS; ULTRASTRUCTURE; VIRAL TROPISM; VIRION; VIRUS ENTRY;

ANIMALS; GENE EXPRESSION; GENETIC VARIATION; HUMANS; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN DOMAINS; PROTEIN SUBUNITS; PROTEOLYSIS; RECEPTORS, VIRUS; SARS VIRUS; SPIKE GLYCOPROTEIN, CORONAVIRUS; VIRAL TROPISM; VIRION; VIRUS INTERNALIZATION;

EID: 84994888248     PISSN: 00653527     EISSN: 15578399     Source Type: Book Series    
DOI: 10.1016/bs.aivir.2016.08.004     Document Type: Chapter

References (133)

1. Aït-Slimane, T., Galmes, R., Trugnan, G., Maurice, M., Basolateral internalization of GPI-anchored proteins occurs via a clathrin-independent flotillin-dependent pathway in polarized hepatic cells. Mol. Biol. Cell 20:17 (2009), 3792–3800, 10.1091/mbc.E09-04-0275.
2. Akimkin, V., Beer, M., Blome, S., Hanke, D., Höper, D., Jenckel, M., Pohlmann, A., New chimeric porcine coronavirus in swine feces, Germany, 2012. Emerg. Infect. Dis. 22:7 (2016), 1314–1315, 10.3201/eid2207.160179.
3. Alagaili, A.N., Briese, T., Mishra, N., Kapoor, V., Sameroff, S.C., Burbelo, P.D., et al. Middle East respiratory syndrome coronavirus infection in dromedary camels in Saudi Arabia. mBio, 5(2), 2014, 10.1128/mBio.00884-14 e00884-14.
4. Annan, A., Baldwin, H.J., Corman, V.M., Klose, S.M., Owusu, M., Nkrumah, E.E., et al. Human betacoronavirus 2c EMC/2012-related viruses in bats, Ghana and Europe. Emerg. Infect. Dis. 19:3 (2013), 456–459, 10.3201/eid1903.121503.
5. Azhar, E.I., El-Kafrawy, S.A., Farraj, S.A., Hassan, A.M., Al-Saeed, M.S., Hashem, A.M., Madani, T.A., Evidence for camel-to-human transmission of MERS coronavirus. N. Engl. J. Med. 26:26 (2014), 2499–2505, 10.1056/NEJMoa1401505.
6. Baker, K.A., Dutch, R.E., Lamb, R.A., Jardetzky, T.S., Structural basis for paramyxovirus-mediated membrane fusion. Mol. Cell 3:3 (1999), 309–319, 10.1016/S1097-2765(00)80458-X.
7. Bank-Wolf, B.R., Stallkamp, I., Wiese, S., Moritz, A., Tekes, G., Thiel, H.J., Mutations of 3c and spike protein genes correlate with the occurrence of feline infectious peritonitis. Vet. Microbiol. 173:3–4 (2014), 177–188, 10.1016/j.vetmic.2014.07.020.
8. Baric, R.S., Sullivan, E., Hensley, L., Yount, B., Chen, W., Persistent infection promotes cross-species transmissibility of mouse hepatitis virus. J. Virol. 73:1 (1999), 638–649.
9. Barlan, A., Zhao, J., Sarkar, M.K., Li, K., McCray, P.B., Perlman, S., Gallagher, T., Receptor variation and susceptibility to Middle East respiratory syndrome coronavirus infection. J. Virol. 88:9 (2014), 4953–4961, 10.1128/JVI.00161-14.
10. Bartesaghi, A., Merk, A., Borgnia, M.J., Milne, J.L.S., Subramaniam, S., Prefusion structure of trimeric HIV-1 envelope glycoprotein determined by cryo-electron microscopy. Nat. Struct. Mol. Biol. 20:12 (2013), 1352–1357, 10.1038/nsmb.2711.
11. Becker, M.M., Graham, R.L., Donaldson, E.F., Rockx, B., Sims, A.C., Sheahan, T., et al. Synthetic recombinant bat SARS-like coronavirus is infectious in cultured cells and in mice. Proc. Natl. Acad. Sci. U.S.A. 105:50 (2008), 19944–19949, 10.1073/pnas.0808116105.
12. Bolles, M., Donaldson, E., Baric, R., SARS-CoV and emergent coronaviruses: viral determinants of interspecies transmission. Curr. Opin. Virol. 1:6 (2011), 624–634, 10.1016/j.coviro.2011.10.012.
13. Bonavia, A., Zelus, B.D., Wentworth, D.E., Talbot, P.J., Holmes, K.V., Identification of a receptor-binding domain of the spike glycoprotein of human coronavirus HCoV-229E. J. Virol. 77:4 (2003), 2530–2538, 10.1128/JVI.77.4.2530-2538.2003.
14. Boniotti, M.B., Papetti, A., Lavazza, A., Alborali, G., Sozzi, E., Chiapponi, C., et al. Porcine epidemic diarrhea virus and discovery of a recombinant swine enteric coronavirus, Italy. Emerg. Infect. Dis. 22:1 (2016), 83–87, 10.3201/eid2201.
15. Bosch, B.J., Rottier, P.J.M., Nidovirus entry into cells. Perlman, S., Gallagher, T., Snijder, E., (eds.) Nidoviruses, 2008, American Society of Microbiology, Washington, DC, 157–178 http://dx.doi.org/10.1128/9781555815790.ch11.
16. Bosch, B.J., Van Der Zee, R., de Haan, C.A.M., Rottier, P.J.M., The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J. Virol. 77:16 (2003), 8801–8811, 10.1128/JVI.77.16.8801.
17. Bosch, B.J., Martina, B.E.E., Van Der Zee, R., Lepault, J., Haijema, B.J., Versluis, C., et al. Severe acute respiratory syndrome coronavirus (SARS-CoV) infection inhibition using spike protein heptad repeat-derived peptides. Proc. Natl. Acad. Sci. U.S.A. 101:22 (2004), 8455–8460, 10.1073/pnas.0400576101.
18. Bosch, B.J., Smits, S.L., Haagmans, B.L., Membrane ectopeptidases targeted by human coronaviruses. Curr. Opin. Virol. 6:1 (2014), 55–60, 10.1016/j.coviro.2014.03.011.
19. Briese, T., Mishra, N., Jain, K., East, M., Syndrome, R., Quasispecies, C., et al. Dromedary camels in Saudi Arabia include homologues of human isolates revealed through whole-genome analysis etc. mBio 5:3 (2014), 1–5, 10.1128/mBio.01146-14 Editor.
20. Burkard, C., Verheije, M.H., Wicht, O., van Kasteren, S.I., van Kuppeveld, F.J., Haagmans, B.L., et al. Coronavirus cell entry occurs through the endo-/lysosomal pathway in a proteolysis-dependent manner. PLoS Pathog., 10(11), 2014, e1004502, 10.1371/journal.ppat.1004502.
21. Chambers, P., Pringle, C.R., Easton, A.J., Heptad repeat sequences are located adjacent to hydrophobic regions in several types of virus fusion glycoproteins. J. Gen. Virol. 71:12 (1990), 3075–3080, 10.1099/0022-1317-71-12-3075.
22. Chan, F.J., To, K.K., Tse, H., Jin, D.-Y., Yuen, K.-Y., Interspecies transmission and emergence of novel viruses: lessons from bats and birds. Trends Microbiol. 21:10 (2013), 544–555, 10.1016/j.tim.2013.05.005.
23. Chang, H.W., Egberink, H.F., Halpin, R., Spiro, D.J., Rottier, P.J.M., Spike protein fusion peptide and feline coronavirus virulence. Emerg. Infect. Dis. 18:7 (2012), 1089–1095, 10.3201/eid1807.120143.
24. Corman, V.M., Baldwin, H.J., Tateno, A.F., Zerbinati, R.M., Annan, A., Owusu, M., et al. Evidence for an ancestral association of human coronavirus 229E with bats. J. Virol. 89:23 (2015), 11858–11870, 10.1128/JVI.01755-15.
25. Crossley, B.M., Mock, R.E., Callison, S.A., Hietala, S.K., Identification and characterization of a novel alpaca respiratory coronavirus most closely related to the human coronavirus 229E. Viruses 4:12 (2012), 3689–3700, 10.3390/v4123689.
26. Dalziel, R.G., Lampert, P.W., Talbot, P.J., Buchmeier, M.J., Site-specific alteration of murine hepatitis virus type 4 peplomer glycoprotein E2 results in reduced neurovirulence. J. Virol. 59:2 (1986), 463–471 Retrieved from http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=3016306.
27. de Haan, C.A.M., Li, Z., te Lintelo, E., Bosch, B.J., Haijema, B.J., Rottier, P.J.M., Murine coronavirus with an extended host range uses heparan sulfate as an entry receptor. J. Virol. 79:22 (2005), 14451–14456, 10.1128/JVI.79.22.14451-14456.2005.
28. de Haan, C.A.M., te Lintelo, E., Li, Z., Raaben, M., Wurdinger, T., Bosch, B.J., Rottier, P.J.M., Cooperative involvement of the S1 and S2 subunits of the murine coronavirus spike protein in receptor binding and extended host range. J. Virol. 80:22 (2006), 10909–10918, 10.1128/JVI.00950-06.
29. de Haan, C.A.M., Haijema, B.J., Masters, P.S., Rottier, P.J.M., Manipulation of the coronavirus genome using targeted RNA recombination with interspecies chimeric coronaviruses. Methods Mol. Biol. 454 (2008), 229–236, 10.1007/978-1-59745-181-9_17.
30. Delmas, B., Gelfi, J., L'Haridon, R., Vogel, L.K., Sjöström, H., Norén, O., Laude, H., Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 357:6377 (1992), 417–420, 10.1038/357417a0.
31. Desmarets, L.M.B., Theuns, S., Roukaerts, I.D.M., Acar, D.D., Nauwynck, H.J., Role of sialic acids in feline enteric coronavirus infections. J. Gen. Virol. 95:9 (2014), 1911–1918, 10.1099/vir.0.064717-0.
32. Desmarets, L.M.B., Vermeulen, B.L., Theuns, S., Conceição-Neto, N., Zeller, M., Roukaerts, I.D.M., et al. Experimental feline enteric coronavirus infection reveals an aberrant infection pattern and shedding of mutants with impaired infectivity in enterocyte cultures. Sci. Rep., 6, 2016, 20022, 10.1038/srep20022.
33. Drexler, J.F., Gloza-Rausch, F., Glende, J., Corman, V.M., Muth, D., Goettsche, M., et al. Genomic characterization of severe acute respiratory syndrome-related coronavirus in European bats and classification of coronaviruses based on partial RNA-dependent RNA polymerase gene sequences. J. Virol. 84:21 (2010), 11336–11349, 10.1128/JVI.00650-10.
34. Duquerroy, B.S., Vigouroux, A., Rottier, P.J.M., Rey, F.A., Berend, T., Bosch, J., Central ions and lateral asparagine/glutamine zippers stabilize the post-fusion hairpin conformation of the SARS coronavirus spike glycoprotein. Virology 335:2 (2005), 276–285, 10.1016/j.virol.2005.02.022.
35. Eckerle, I., Corman, V.M., Müller, M.A., Lenk, M., Ulrich, R.G., Drosten, C., Replicative capacity of MERS coronavirus in livestock cell lines. Emerg. Infect. Dis. 20:2 (2014), 276–279, 10.3201/eid2002.131182.
36. Eifart, P., Ludwig, K., Böttcher, C., de Haan, C.A.M., Rottier, P.J.M., Korte, T., Herrmann, A., Role of endocytosis and low pH in murine hepatitis virus strain A59 cell entry. J. Virol. 81:19 (2007), 10758–10768, 10.1128/JVI.00725-07.
37. Falzarano, D., de Wit, E., Feldmann, F., Rasmussen, A.L., Okumura, A., Peng, X., et al. Infection with MERS-CoV causes lethal pneumonia in the common marmoset. PLoS Pathog., 10(8), 2014, e1004250, 10.1371/journal.ppat.1004250.
38. Farsani, S.M.J., Dijkman, R., Jebbink, M.F., Goossens, H., Ieven, M., Deijs, M., et al. The first complete genome sequences of clinical isolates of human coronavirus 229E. Virus Genes 45:3 (2012), 433–439, 10.1007/s11262-012-0807-9.
39. Forni, D., Filippi, G., Cagliani, R., De Gioia, L., Pozzoli, U., Al-Daghri, N., et al. The heptad repeat region is a major selection target in MERS-CoV and related coronaviruses. Sci. Rep., 5, 2015, 14480, 10.1038/srep14480.
40. Frana, M.F., Behnke, J.N., Sturman, L.S., Holmes, K.V., Proteolytic cleavage of the E2 glycoprotein of murine coronavirus: host-dependent differences in proteolytic cleavage and cell fusion. J. Virol. 56:3 (1985), 912–920 Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=252664&tool=pmcentrez&rendertype=abstract.
41. Gallagher, T.M., Buchmeier, M.J., Coronavirus spike proteins in viral entry and pathogenesis. Virology 279:2 (2001), 371–374, 10.1006/viro.2000.0757.
42. Gallagher, T.M., Buchmeier, M.J., Perlman, S., Cell receptor-independent infection by a neurotropic murine coronavirus. Virology 19:1 (1992), 517–522 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1413526.
43. Gallagher, T.M., Buchmeier, M.J., Perlman, S., Dissemination of MHV4 (strain JHM) infection does not require specific coronavirus receptors. Adv. Exp. Med. Biol. 342 (1993), 279–284 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/8209743.
44. Gao, J., Lu, G., Qi, J., Li, Y., Wu, Y., Deng, Y., 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. 87:24 (2013), 13134–13140, 10.1128/JVI.02433-13.
45. Ge, X.Y., Li, J.L., Yang, X.L., Chmura, A.A., Zhu, G., Epstein, J.H., et al. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503:7477 (2013), 535–538, 10.1038/nature12711.
46. Guan, Y., Zheng, B.J., He, Y.Q., Liu, X.L., Zhuang, Z.X., Cheung, C.L., et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302:5643 (2003), 276–278, 10.1126/science.1087139.
47. Haijema, B.J., Volders, H., Rottier, P.J.M., Switching species tropism: an effective way to manipulate the feline coronavirus genome. J. Virol. 77:8 (2003), 4528–4538, 10.1128/JVI.77.8.4528-4538.2003.
48. Herrewegh, A.A.P.M., Vennema, H., Horzinek, M.C., Rottier, P.J.M., de Groot, R.J., The molecular genetics of feline coronaviruses: comparative sequence analysis of the ORF7a/7b transcription unit of different biotypes. Virology 212:2 (1995), 622–631.
49. Hofmann, H., Hattermann, K., Marzi, A., Gramberg, T., Geier, M., Krumbiegel, M., et al. S protein of severe acute respiratory syndrome-associated coronavirus mediates entry into hepatoma cell lines and is targeted by neutralizing antibodies in infected patients. J. Virol. 78:12 (2004), 6134–6142, 10.1128/JVI.78.12.6134-6142.2004.
50. Hu, B., Ge, X., Wang, L.-F., Shi, Z., Bat origin of human coronaviruses. Virol. J., 12(1), 2015, 221, 10.1186/s12985-015-0422-1.
51. Huynh, J., Li, S., Yount, B., Smith, A., Sturges, L., Olsen, J.C., et al. Evidence supporting a zoonotic origin of human coronavirus strain NL63. J. Virol. 86:23 (2012), 12816–12825, 10.1128/JVI.00906-12.
52. Inoue, Y., Tanaka, N., Tanaka, Y., Inoue, S., Morita, K., Zhuang, M., et al. Clathrin-dependent entry of severe acute respiratory syndrome coronavirus into target cells expressing ACE2 with the cytoplasmic tail deleted. J. Virol. 81:16 (2007), 8722–8729, 10.1128/JVI.00253-07.
53. Kirchdoerfer, R.N., Cottrell, C.A., Wang, N., Pallesen, J., Yassine, H.M., Turner, H.L., et al. Pre-fusion structure of a human coronavirus spike protein. Nature 531:7592 (2016), 118–121, 10.1038/nature17200.
54. Kolb, A.F., Hegyi, A., Siddell, S.G., Identification of residues critical for the human coronavirus 229E receptor function of human aminopeptidase N. J. Gen. Virol. 78:11 (1997), 2795–2802.
55. Krempl, C., Schultze, B., Laude, H., Point mutations in the S protein connect the sialic acid binding activity with the enteropathogenicity of transmissible gastroenteritis coronavirus. J. Virol. 71:4 (1997), 3285–3287.
56. Krueger, D.K., Kelly, S.M., Lewicki, D.N., Ruffolo, R., Gallagher, T.M., Variations in disparate regions of the murine coronavirus spike protein impact the initiation of membrane fusion. J. Virol. 75:6 (2001), 2792–2802, 10.1128/JVI.75.6.2792-2802.2001.
57. Künkel, F., Herrler, G., Structural and functional analysis of the surface protein of human coronavirus OC43. Virology 195:1 (1993), 195–202.
58. Kuo, L., Godeke, G.J., Raamsman, M.J., Masters, P.S., Rottier, P.J., Retargeting of coronavirus by substitution of the spike glycoprotein ectodomain: crossing the host cell species barrier. J. Virol. 74:3 (2000), 1393–1406, 10.1128/JVI.74.3.1393-1406.2000.
59. Langereis, M.A., van Vliet, A.L.W., Boot, W., de Groot, R.J., Attachment of mouse hepatitis virus to O-acetylated sialic acid is mediated by hemagglutinin-esterase and not by the spike protein. J. Virol. 84:17 (2010), 8970–8974, 10.1128/JVI.00566-10.
60. Lau, S.K.P., Woo, P.C.Y., Li, K.S.M., Huang, Y., Wang, M., Lam, C.S.F., et al. Complete genome sequence of bat coronavirus HKU2 from Chinese horseshoe bats revealed a much smaller spike gene with a different evolutionary lineage from the rest of the genome. Virology 367:2 (2007), 428–439, 10.1016/j.virol.2007.06.009.
61. Lee, C., Porcine epidemic diarrhea virus: an emerging and re-emerging epizootic swine virus. Virol. J., 12(1), 2015, 193, 10.1186/s12985-015-0421-2.
62. Lee, J.E., Fusco, M.L., Hessell, A.J., Oswald, W.B., Burton, D.R., Saphire, E.O., Structure of the ebola virus glycoprotein bound to an antibody from a human survivor. Nature 454:7201 (2008), 177–182, 10.1038/nature07082.
63. Levis, R., Cardellichio, C.B., Scanga, C.A., Compton, S.R., Holmes, K.V., Multiple receptor-dependent steps determine the species specificity of HCV-229E infection. Adv. Exp. Med. Biol. 380 (1995), 337–343 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/8830504.
64. Lewis, C.S., Porter, E., Matthews, D., Kipar, A., Tasker, S., Helps, C.R., Siddell, S.G., Genotyping coronaviruses associated with feline infectious peritonitis. J. Gen. Virol. 96:Pt. 6 (2015), 1358–1368, 10.1099/vir.0.000084.
65. Li, F., Evidence for a common evolutionary origin of coronavirus spike protein receptor-binding subunits. J. Virol. 86:5 (2012), 2856–2858, 10.1128/JVI.06882-11.
66. Li, F., Receptor recognition mechanisms of coronaviruses: a decade of structural studies. J. Virol. 89:4 (2015), 1954–1964, 10.1128/JVI.02615-14.
67. Li, F., Li, W., Farzan, M., Harrison, S.C., Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309:5742 (2005), 1864–1868, 10.1126/science.1116480.
68. Li, W., Zhang, C., Sui, J., Kuhn, J.H., Moore, M.J., Luo, S., et al. Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J. 24:8 (2005), 1634–1643, 10.1038/sj.emboj.7600640.
69. Li, W., Wong, S.-K., Li, F., Kuhn, J.H., Huang, I.-C., Choe, H., Farzan, M., Animal origins of the severe acute respiratory syndrome coronavirus: insight from ACE2-S-protein interactions. J. Virol. 80:9 (2006), 4211–4219, 10.1128/JVI.80.9.4211-4219.2006.
70. Li, W., Wicht, O., van Kuppeveld, F.J.M., He, Q., Rottier, P.J.M., Bosch, B.-J., 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. 89:15 (2015), 8077–8081, 10.1128/JVI.00356-15.
71. Licitra, B.N., Millet, J.K., Regan, A.D., Hamilton, B.S., Rinaldi, V.D., Duhamel, G.E., Whittaker, G.R., Mutation in spike protein cleavage site and pathogenesis of feline coronavirus. Emerg. Infect. Dis. 19:7 (2013), 1066–1073, 10.3201/eid1907.121094.
72. Lin, X., Eddy, N.R., Noel, J.K., Whitford, P.C., Wang, Q., Ma, J., Onuchic, J.N., Order and disorder control the functional rearrangement of influenza hemagglutinin. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 12049–12054, 10.1073/pnas.1412849111.
73. Lu, G., Hu, Y., Wang, Q., Qi, J., Gao, F., Li, Y., et al. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature 500:7461 (2013), 227–231, 10.1038/nature12328.
74. Lu, L., Liu, Q., Zhu, Y., Chan, K.-H., Qin, L., Li, Y., et al. Structure-based discovery of Middle East respiratory syndrome coronavirus fusion inhibitor. Nat. Commun., 5, 2014, 3067, 10.1038/ncomms4067.
75. Matsuyama, S., Taguchi, F., Two-step conformational changes in a coronavirus envelope glycoprotein mediated by receptor binding and proteolysis. J. Virol. 83:21 (2009), 11133–11141, 10.1128/JVI.00959-09.
76. McRoy, W.C., Baric, R.S., Amino acid substitutions in the S2 subunit of mouse hepatitis virus variant V51 encode determinants of host range expansion. J. Virol. 82:3 (2008), 1414–1424, 10.1128/JVI.01674-07.
77. Millet, J.K., Whittaker, G.R., Host cell proteases: critical determinants of coronavirus tropism and pathogenesis. Virus Res. 202 (2015), 120–134, 10.1016/j.virusres.2014.11.021.
78. Mou, H., Raj, V.S., van Kuppeveld, F.J.M., Rottier, P.J.M., Haagmans, B.L., Bosch, B.J., The receptor binding domain of the new Middle East respiratory syndrome coronavirus maps to a 231-residue region in the spike protein that efficiently elicits neutralizing antibodies. J. Virol. 87:16 (2013), 9379–9383, 10.1128/JVI.01277-13.
79. Müller, M.A., Raj, V.S., Muth, D., Meyer, B., Kallies, S., Smits, S.L., et al. Human coronavirus EMC does not require the SARS-coronavirus receptor and maintains broad replicative capability in mammalian cell lines. mBio, 3(6), 2012, 10.1128/mBio.00515-12 e00515-12.
80. Myrrha, L.W., Silva, F.M.F., de Oliveira Peternelli, E.F., Junior, A.S., Resende, M., de Almeida, M.R., The paradox of feline coronavirus pathogenesis: a review. Adv. Virol., 2011, 2011, 109849, 10.1155/2011/109849.
81. Navas-Martin, S., Hingley, S.T., Weiss, S.R., Murine coronavirus evolution in vivo: functional compensation of a detrimental amino acid substitution in the receptor binding domain of the spike glycoprotein. J. Virol. 79:12 (2005), 7629–7640, 10.1128/JVI.79.12.7629-7640.2005.
82. Nomura, R., Kiyota, A., Suzaki, E., Kataoka, K., Ohe, Y., Miyamoto, K., et al. Human coronavirus 229E binds to CD13 in rafts and enters the cell through caveolae. J. Virol. 78:16 (2004), 8701–8708, 10.1128/JVI.78.16.8701-8708.2004 78/16/8701 [pii].
83. Ou, X., Zheng, W., Shan, Y., Mu, Z., Dominguez, S.R., Holmes, K.V., Qian, Z., Identification of the fusion peptide-containing region in betacoronavirus spike glycoproteins. J. Virol. 90:12 (2016), 5586–5600, 10.1128/JVI.00015-16 JVI.00015–16.
84. Pedersen, N.C., An update on feline infectious peritonitis: virology and immunopathogenesis. Vet. J. 201:2 (2014), 123–132, 10.1016/j.tvjl.2014.04.017.
85. Peng, G., Sun, D., Rajashankar, K.R., Qian, Z., Holmes, K.V., Li, F., Crystal structure of mouse coronavirus receptor-binding domain complexed with its murine receptor. Proc. Natl. Acad. Sci. U.S.A. 108:26 (2011), 10696–10701, 10.1073/pnas.1104306108.
86. Peng, G., Xu, L., Lin, Y.L., Chen, L., Pasquarella, J.R., Holmes, K.V., Li, F., Crystal structure of bovine coronavirus spike protein lectin domain. J. Biol. Chem. 287:50 (2012), 41931–41938, 10.1074/jbc.M112.418210.
87. Phillips, J.J., Weiss, S.R., MHV neuropathogenesis: the study of chimeric S genes and mutations in the hypervariable region. Adv. Exp. Med. Biol. 494 (2001), 115–119 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11774454.
88. Promkuntod, N., van Eijndhoven, R., de Vrieze, G., Gröne, A., Verheije, M., Mapping of the receptor-binding domain and amino acids critical for attachment in the spike protein of avian coronavirus infectious bronchitis virus. Virology 448 (2014), 26–32, 10.1016/j.virol.2013.09.018.
89. Qu, X.X., Hao, P., Song, X.J., Jiang, S.M., Liu, Y.X., Wang, P.G., et al. 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. 280:33 (2005), 29588–29595, 10.1074/jbc.M500662200.
90. Racaniello, V.R., Skalka, A.M., Flint, J., Rall, G.F., Principles of Virology, Bundle. 2015, American Society of Microbiology, Washington, DC, 10.1128/9781555819521.
91. Raj, V.S., Mou, H., Smits, S.L., Dekkers, D.H.W., Müller, M.A., Dijkman, R., et al. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495 (2013), 251–254, 10.1038/nature12005.
92. Raj, V.S., Smits, S.L., Provacia, L.B., van den Brand, J.M.A., Wiersma, L., Ouwendijk, W.J.D., et al. Adenosine deaminase acts as a natural antagonist for dipeptidyl peptidase 4-mediated entry of the Middle East respiratory syndrome coronavirus. J. Virol. 88:3 (2014), 1834–1838, 10.1128/JVI.02935-13.
93. Reguera, J., Santiago, C., Mudgal, G., Ordoño, D., Enjuanes, L., Casasnovas, J.M., Structural bases of coronavirus attachment to host aminopeptidase N and its inhibition by neutralizing antibodies. PLoS Pathog., 8(8), 2012, e1002859, 10.1371/journal.ppat.1002859.
94. Ren, W., Qu, X., Li, W., Han, Z., Yu, M., Zhou, P., et al. Difference in receptor usage between severe acute respiratory syndrome (SARS) coronavirus and SARS-like coronavirus of bat origin. J. Virol. 82:4 (2008), 1899–1907, 10.1128/JVI.01085-07.
95. Reusken, C.B., Haagmans, B.L., Müller, M.A., Gutierrez, C., Godeke, G.-J., Meyer, B., et al. Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study. Lancet Infect. Dis. 13:10 (2013), 859–866, 10.1016/S1473-3099(13)70164-6.
96. Roberts, A., Deming, D., Paddock, C.D., Cheng, A., Yount, B., Vogel, L., et al. A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog., 3(1), 2007, e5, 10.1371/journal.ppat.0030005.
97. Robertson, A.L., Headey, S.J., Ng, N.M., Wijeyewickrema, L.C., Scanlon, M.J., Pike, R.N., Bottomley, S.P., Protein unfolding is essential for cleavage within the α-helix of a model protein substrate by the serine protease, thrombin. Biochimie 122 (2016), 227–234, 10.1016/j.biochi.2015.09.021.
98. Rottier, P.J.M., Nakamura, K., Schellen, P., Volders, H., Haijema, B.J., Acquisition of macrophage tropism during the pathogenesis of feline infectious peritonitis is determined by mutations in the feline coronavirus spike protein. J. Virol. 79:22 (2005), 14122–14130, 10.1128/JVI.79.22.14122-14130.2005.
99. Saeki, K., Ohtsuka, N., Taguchi, F., Identification of spike protein residues of murine coronavirus responsible for receptor-binding activity by use of soluble receptor-resistant mutants. J. Virol. 71:12 (1997), 9024–9031 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/9371559.
100. Schickli, J.H., Zelus, B.D., Wentworth, D.E., Sawicki, S.G., Holmes, K.V., The murine coronavirus mouse hepatitis virus strain A59 from persistently infected murine cells exhibits an extended host range. J. Virol. 71:12 (1997), 9499–9507 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/9371612.
101. Schultze, B., Gross, H.-J., Brossmer, R., Herrler, G., The S protein of bovine coronavirus is a hemagglutinin recognizing 9-0-acetylated sialic acid as a receptor determinant. J. Virol. 65:11 (1991), 6232–6237.
102. Schultze, B., Krempl, C., Ballesteros, M.L., Shaw, L., Schauer, R., Enjuanes, L., Herrler, G., Transmissible gastroenteritis coronavirus, but not the related porcine respiratory coronavirus, has a sialic acid (N-glycolylneuraminic acid) binding activity. J. Virol. 70:8 (1996), 5634–5637 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/8764078.
103. Schwegmann-Wessels, C., Zimmer, G., Schroder, B., Breves, G., Herrler, G., Binding of transmissible gastroenteritis coronavirus to brush border membrane sialoglycoproteins. J. Virol. 77:21 (2003), 11846–11848, 10.1128/JVI.77.21.11846.
104. Simmons, G., Gosalia, D.N., Rennekamp, A.J., Reeves, J.D., Diamond, S.L., Bates, P., Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc. Natl. Acad. Sci. U.S.A. 102:33 (2005), 11876–11881.
105. Song, H.-D., Tu, C.-C., Zhang, G.-W., Wang, S.-Y., Zheng, K., Lei, L.-C., et al. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc. Natl. Acad. Sci. U.S.A. 102:7 (2005), 2430–2435, 10.1073/pnas.0409608102.
106. Song, D., Moon, H., Kang, B., Porcine epidemic diarrhea: a review of current epidemiology and available vaccines. Clin. Exp. Vaccine Res. 4:2 (2015), 166–176, 10.7774/cevr.2015.4.2.166.
107. Supekar, V.M., Bruckmann, C., Ingallinella, P., Bianchi, E., Pessi, A., Carfí, A., Structure of a proteolytically resistant core from the severe acute respiratory syndrome coronavirus S2 fusion protein. Proc. Natl. Acad. Sci. U.S.A. 101:52 (2004), 17958–17963, 10.1073/pnas.0406128102.
108. Taguchi, F., Matsuyama, S., Soluble receptor potentiates receptor-independent infection by murine coronavirus. J. Virol. 76:3 (2002), 950–958 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11773370.
109. Terada, Y., Shiozaki, Y., Shimoda, H., Mahmoud, H.Y.A.H., Noguchi, K., Nagao, Y., et al. Feline infectious peritonitis virus with a large deletion in the 5′-terminal region of the spike gene retains its virulence for cats. J. Gen. Virol. 93:Pt. 9 (2012), 1930–1934, 10.1099/vir.0.043992-0.
110. Terada, Y., Matsui, N., Noguchi, K., Kuwata, R., Shimoda, H., Soma, T., et al. Emergence of pathogenic coronaviruses in cats by homologous recombination between feline and canine coronaviruses. PLoS One, 9(9), 2014, e106534, 10.1371/journal.pone.0106534.
111. Tresnan, D.B., Holmes, K.V., Feline aminopeptidase N is a receptor for all group I coronaviruses. Adv. Exp. Med. Biol. 440 (1998), 69–75 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/9782266.
112. Tresnan, D.B., Levis, R., Holmes, K.V., Feline aminopeptidase N serves as a receptor for feline, canine, porcine, and human coronaviruses in serogroup I. J. Virol. 70:12 (1996), 8669–8674 Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=190961&tool=pmcentrez&rendertype=abstract.
113. Tsai, J.C., De Groot, L., Pinon, J.D., Iacono, K.T., Phillips, J.J., Seo, S.H., et al. Amino acid substitutions within the heptad repeat domain 1 of murine coronavirus spike protein restrict viral antigen spread in the central nervous system. Virology 312:2 (2003), 369–380, 10.1016/S0042-6822(03)00248-4.
114. Tu, C., Crameri, G., Kong, X., Chen, J., Sun, Y., Yu, M., et al. Antibodies to SARS coronavirus in civets. Emerg. Infect. Dis. 10:12 (2004), 2244–2248, 10.3201/eid1012.040520.
115. Tusell, S.M., Schittone, S.A., Holmes, K.V., Mutational analysis of aminopeptidase N, a receptor for several group 1 coronaviruses, identifies key determinants of viral host range. J. Virol. 81:3 (2007), 1261–1273, 10.1128/JVI.01510-06.
116. van Doremalen, N., Miazgowicz, K.L., Milne-Price, S., Bushmaker, T., Robertson, S., Scott, D., et al. Host species restriction of Middle East respiratory syndrome coronavirus through its receptor, dipeptidyl peptidase 4. J. Virol. 88:16 (2014), 9220–9232, 10.1128/JVI.00676-14.
117. Vijgen, L., Keyaerts, E., Lemey, P., Maes, P., Van Reeth, K., Nauwynck, H., et al. Evolutionary history of the closely related group 2 coronaviruses: porcine hemagglutinating encephalomyelitis virus, bovine coronavirus, and human coronavirus OC43. J. Virol. 80:14 (2006), 7270–7274, 10.1128/JVI.02675-05.
118. Vlasak, R., Luytjes, W., Spaan, W., Palese, P., Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses. Proc. Natl. Acad. Sci. U.S.A. 85:12 (1988), 4526–4529, 10.1073/pnas.85.12.4526.
119. Walls, A.C., Tortorici, M.A., Bosch, B.-J., Frenz, B., Rottier, P.J.M., DiMaio, F., et al. Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature 531:7592 (2016), 114–117, 10.1038/nature16988.
120. Wang, F.I., Fleming, J.O., Lai, M.M., Sequence analysis of the spike protein gene of murine coronavirus variants: study of genetic sites affecting neuropathogenicity. Virology 186:2 (1992), 742–749 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1310195.
121. Wang, H., Yang, P., Liu, K., Guo, F., Zhang, Y., Zhang, G., Jiang, C., SARS coronavirus entry into host cells through a novel clathrin- and caveolae-independent endocytic pathway. Cell Res. 18:2 (2008), 290–301, 10.1038/cr.2008.15.
122. Wang, N., Shi, X., Jiang, L., Zhang, S., Wang, D., Tong, P., et al. Structure of MERS-CoV spike receptor-binding domain complexed with human receptor DPP4. Cell Res. 23:8 (2013), 986–993, 10.1038/cr.2013.92.
123. Wang, Q., Qi, J., Yuan, Y., Xuan, Y., Han, P., Wan, Y., et al. Bat origins of MERS-CoV supported by bat coronavirus HKU4 usage of human receptor CD26. Cell Host Microbe 16:3 (2014), 328–337, 10.1016/j.chom.2014.08.009.
124. WHO | Middle East respiratory syndrome coronavirus (MERS-CoV) – Saudi Arabia, WHO. 2016.
125. Widagdo, W., Raj, V.S., Schipper, D., Kolijn, K., van Leenders, G.J.L.H., Bosch, B.J., Bensaid, A., Differential expression of the Middle East respiratory syndrome coronavirus receptor in the upper respiratory tracts of humans and dromedary camels. J. Virol. 90:9 (2016), 4838–4842, 10.1128/JVI.02994-15 Editor.
126. Woo, P.C.Y., Lau, S.K.P., Lam, C.S.F., Lau, C.C.Y., Tsang, A.K.L., Lau, J.H.N., et al. Discovery of seven novel mammalian and avian coronaviruses in the genus deltacoronavirus supports bat coronaviruses as the gene source of alphacoronavirus and betacoronavirus and avian coronaviruses as the gene source of gammacoronavirus and deltacoronavirus. J. Virol. 86:7 (2012), 3995–4008, 10.1128/JVI.06540-11.
127. Wu, K., Li, W., Peng, G., Li, F., Crystal structure of NL63 respiratory coronavirus receptor-binding domain complexed with its human receptor. Proc. Natl. Acad. Sci. U.S.A. 106:47 (2009), 19970–19974, 10.1073/pnas.0908837106.
128. Xu, Y., Lou, Z., Liu, Y., Pang, H., Tien, P., Gao, G.F., Rao, Z., Crystal structure of severe acute respiratory syndrome coronavirus spike protein fusion core. J. Biol. Chem. 279:47 (2004), 49414–49419, 10.1074/jbc.M408782200.
129. Yamada, Y., Liu, D.X., 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. 83:17 (2009), 8744–8758, 10.1128/JVI.00613-09.
130. Yamada, Y., Liu, X.B., Fang, S.G., Tay, F.P.L., Liu, D.X., Acquisition of cell-cell fusion activity by amino acid substitutions in spike protein determines the infectivity of a coronavirus in cultured cells. PLoS One, 4(7), 2009, e6130, 10.1371/journal.pone.0006130.
131. Yang, Y., Du, L., Liu, C., Wang, L., Ma, C., Tang, J., 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. U.S.A. 111:34 (2014), 12516–12521, 10.1073/pnas.1405889111.
132. Yang, Y., Liu, C., Du, L., Jiang, S., Shi, Z., Baric, R.S., Li, F., Two mutations were critical for bat-to-human transmission of Middle East respiratory syndrome coronavirus. J. Virol. 89:17 (2015), 9119–9123, 10.1128/JVI.01279-15.
133. Zelus, B.D., Schickli, J.H., Blau, D.M., Weiss, S.R., Holmes, K.V., Conformational changes in the spike glycoprotein of murine coronavirus are induced at 37 degrees C either by soluble murine CEACAM1 receptors or by pH 8. J. Virol. 77:2 (2003), 830–840, 10.1128/JVI.77.2.830-840.2003.