Feline coronavirus: Insights into viral pathogenesis based on the spike protein structure and function

Virology

Volumn 517, Issue , 2018, Pages 108-121

  Jaimes, Javier A ^a   Whittaker, Gary R ^b  

^a Program on Infrastructure Policy   (United States)

^b NONE   (United States)

Author keywords

Cleavage activation; Coronavirus; Feline coronavirus; Feline infectious peritonitis; Pathogenesis; Serotype; Spike protein; Spike structure; Tropism

Indexed keywords

VIRUS SPIKE PROTEIN; CORONAVIRUS SPIKE GLYCOPROTEIN; S PROTEIN, FELINE INFECTIOUS PERITONITIS VIRUS (FIPV);

ARTICLE; BIOCHEMICAL ANALYSIS; FELINE CORONAVIRUS; HUMAN; HUMAN CORONAVIRUS NL63; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN STRUCTURE; SPECIES COMPARISON; TAXONOMY; VIRAL GENETICS; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS MORPHOLOGY; VIRUS PATHOGENESIS; VIRUS REPLICATION; ANIMAL; CAT; CHEMISTRY; FELINE INFECTIOUS PERITONITIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; VIROLOGY;

ANIMALS; CATS; CORONAVIRUS, FELINE; FELINE INFECTIOUS PERITONITIS; GENE EXPRESSION REGULATION, VIRAL; SPIKE GLYCOPROTEIN, CORONAVIRUS; VIRUS REPLICATION;

EID: 85040117030     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2017.12.027     Document Type: Article

References (114)

1. An, D.J., Jeoung, H.Y., Jeong, W., Park, J.Y., Lee, M.H., Park, B.K., Prevalence of Korean cats with natural feline coronavirus infections. Virol. J., 8, 2011, 455.
2. Armstrong, J., Niemann, H., Smeekens, S., Rottier, P., Warren, G., Sequence and topology of a model intracellular membrane protein, E1 glycoprotein, from a coronavirus. Nature 308 (1984), 751–752.
3. Balint, A., Farsang, A., Zadori, Z., Hornyak, A., Dencso, L., Almazan, F., Enjuanes, L., Belak, S., Molecular characterization of feline infectious peritonitis virus strain DF-2 and studies of the role of ORF3abc in viral cell tropism. J. Virol. 86 (2012), 6258–6267.
4. Barcena, M., Oostergetel, G.T., Bartelink, W., Faas, F.G., Verkleij, A., Rottier, P.J., Koster, A.J., Bosch, B.J., Cryo-electron tomography of mouse hepatitis virus: insights into the structure of the coronavirion. Proc. Natl. Acad. Sci. USA 106 (2009), 582–587.
5. Barker, E.N., Stranieri, A., Helps, C.R., Porter, E.L., Davidson, A.D., Day, M.J., Knowles, T., Kipar, A., Tasker, S., Limitations of using feline coronavirus spike protein gene mutations to diagnose feline infectious peritonitis. Vet. Res., 48, 2017, 60.
6. Belouzard, S., Chu, V.C., Whittaker, G.R., Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites. Proc. Natl. Acad. Sci. USA 106 (2009), 5871–5876.
7. Belouzard, S., Millet, J.K., Licitra, B.N., Whittaker, G.R., Mechanisms of coronavirus cell entry mediated by the viral spike protein. Viruses 4 (2012), 1011–1033.
8. Benetka, V., Kubber-Heiss, A., Kolodziejek, J., Nowotny, N., Hofmann-Parisot, M., Mostl, K., Prevalence of feline coronavirus types I and II in cats with histopathologically verified feline infectious peritonitis. Vet. Microbiol. 99 (2004), 31–42.
9. Black, J.W., Recovery and in vitro cultivation of a coronavirus from laboratory-induced cases of feline infectious peritonitis (FIP). Vet. Med. Small Anim. Clin.: VM SAC 75 (1980), 811–814.
10. 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 (2003), 8801–8811.
11. Brierley, I., Digard, P., Inglis, S.C., Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell 57 (1989), 537–547.
12. Brown, M.A., Troyer, J.L., Pecon-Slattery, J., Roelke, M.E., O'Brien, S.J., Genetics and pathogenesis of feline infectious peritonitis virus. Emerg. Infect. Dis. 15 (2009), 1445–1452.
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., de Haan, C.A., Coronavirus cell entry occurs through the endo-/lysosomal pathway in a proteolysis-dependent manner. PLoS Pathog., 10, 2014, e1004502.
14. Cham, T.-C., Chang, Y.-C., Tsai, P.-S., Wu, C.-H., Chen, H.-W., Jeng, C.-R., Pang, V.F., Chang, H.-W., Determination of the cell tropism of serotype 1 feline infectious peritonitis virus using the spike affinity histochemistry in paraffin-embedded tissues. Microbiol. Immunol. 61 (2017), 318–327.
15. 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:Pt 12 (1990), 3075–3080.
16. Chang, C.K., Sue, S.C., Yu, T.H., Hsieh, C.M., Tsai, C.K., Chiang, Y.C., Lee, S.J., Hsiao, H.H., Wu, W.J., Chang, W.L., Lin, C.H., Huang, T.H., Modular organization of SARS coronavirus nucleocapsid protein. J. Biomed. Sci. 13 (2006), 59–72.
17. Chang, H.W., de Groot, R.J., Egberink, H.F., Rottier, P.J., Feline infectious peritonitis: insights into feline coronavirus pathobiogenesis and epidemiology based on genetic analysis of the viral 3c gene. J. Gen. Virol. 91 (2010), 415–420.
18. Chang, H.W., Egberink, H.F., Halpin, R., Spiro, D.J., Rottier, P.J., Spike protein fusion peptide and feline coronavirus virulence. Emerg. Infect. Dis. 18 (2012), 1089–1095.
19. Chang, H.W., Egberink, H.F., Rottier, P.J., Sequence analysis of feline coronaviruses and the circulating virulent/avirulent theory. Emerg. Infect. Dis. 17 (2011), 744–746.
20. Corapi, W.V., Olsen, C.W., Scott, F.W., Monoclonal antibody analysis of neutralization and antibody-dependent enhancement of feline infectious peritonitis virus. J. Virol. 66 (1992), 6695–6705.
21. Corse, E., Machamer, C.E., The cytoplasmic tail of infectious Bronchitis Virus E protein directs golgi targeting. J. Virol. 76 (2002), 1273–1284.
22. de Haan, C.A., Haijema, B.J., Schellen, P., Wichgers Schreur, P., te Lintelo, E., Vennema, H., Rottier, P.J., Cleavage of group 1 coronavirus spike proteins: how furin cleavage is traded off against heparan sulfate binding upon cell culture adaptation. J. Virol. 82 (2008), 6078–6083.
23. Dedeurwaerder, A., Desmarets, L.M., Olyslaegers, D.A., Vermeulen, B.L., Dewerchin, H.L., Nauwynck, H.J., The role of accessory proteins in the replication of feline infectious peritonitis virus in peripheral blood monocytes. Vet. Microbiol. 162 (2013), 447–455.
24. Dedeurwaerder, A., Olyslaegers, D.A., Desmarets, L.M., Roukaerts, I.D., Theuns, S., Nauwynck, H.J., ORF7-encoded accessory protein 7a of feline infectious peritonitis virus as a counteragent against IFN-alpha-induced antiviral response. J. Gen. Virol. 95 (2014), 393–402.
25. DeDiego, M.L., Alvarez, E., Almazan, F., Rejas, M.T., Lamirande, E., Roberts, A., Shieh, W.J., Zaki, S.R., Subbarao, K., Enjuanes, L., A severe acute respiratory syndrome coronavirus that lacks the E gene is attenuated in vitro and in vivo. J. Virol. 81 (2007), 1701–1713.
26. Dye, C., Siddell, S.G., Genomic RNA sequence of Feline coronavirus strain FIPV WSU-79/1146. J. Gen. Virol. 86 (2005), 2249–2253.
27. Dye, C., Temperton, N., Siddell, S.G., Type I feline coronavirus spike glycoprotein fails to recognize aminopeptidase N as a functional receptor on feline cell lines. J. Gen. Virol. 88 (2007), 1753–1760.
28. Enjuanes, L., Almazan, F., Sola, I., Zuniga, S., Biochemical aspects of coronavirus replication and virus-host interaction. Annu. Rev. Microbiol. 60 (2006), 211–230.
29. Fehr, A.R., Perlman, S., Coronaviruses: an overview of their replication and pathogenesis. Methods Mol. Biol. 1282 (2015), 1–23.
30. Foley, J.E., Poland, A., Carlson, J., Pedersen, N.C., Risk factors for feline infectious peritonitis among cats in multiple-cat environments with endemic feline enteric coronavirus. J. Am. Vet. Med. Assoc. 210 (1997), 1313–1318.
31. Gui, M., Song, W., Zhou, H., Xu, J., Chen, S., Xiang, Y., Wang, X., Cryo-electron microscopy structures of the SARS-CoV spike glycoprotein reveal a prerequisite conformational state for receptor binding. Cell Res. 27 (2017), 119–129.
32. Gunn-Moore, D.A., Gruffydd-Jones, T.J., Harbour, D.A., Detection of feline coronaviruses by culture and reverse transcriptase-polymerase chain reaction of blood samples from healthy cats and cats with clinical feline infectious peritonitis. Vet. Microbiol. 62 (1998), 193–205.
33. Haijema, B.J., Volders, H., Rottier, P.J., Live, attenuated coronavirus vaccines through the directed deletion of group-specific genes provide protection against feline infectious peritonitis. J. Virol. 78 (2004), 3863–3871.
34. Harrison, S.C., Principles of virus structure. Knipe, D.M., Howley, P.M., (eds.) Fields Virology, 6th ed., 2013, Lippincot Williams & Wilkins, Philadelphia, PA, 52–86.
35. Herrewegh, A.A., Vennema, H., Horzinek, M.C., Rottier, P.J., de Groot, R.J., The molecular genetics of feline coronaviruses: comparative sequence analysis of the ORF7a/7b transcription unit of different biotypes. Virology 212 (1995), 622–631.
36. Herrewegh, A.A.P.M., Smeenk, I., Horzinek, M.C., Rottier, P.J.M., de Groot, R.J., feline coronavirus type II strains 79-1683 and 79-1146 originate from a double recombination between feline coronavirus type I and canine coronavirus. J. Virol. 72 (1998), 4508–4514.
37. Hohdatsu, T., Izumiya, Y., Yokoyama, Y., Kida, K., Koyama, H., Differences in virus receptor for type I and type II feline infectious peritonitis virus. Arch. Virol. 143 (1998), 839–850.
38. Hohdatsu, T., Okada, S., Ishizuka, Y., Yamada, H., Koyama, H., The prevalence of types I and II feline coronavirus infections in cats. J. Vet. Med. Sci. 54 (1992), 557–562.
39. Hohdatsu, T., Yamato, H., Ohkawa, T., Kaneko, M., Motokawa, K., Kusuhara, H., Kaneshima, T., Arai, S., Koyama, H., Vaccine efficacy of a cell lysate with recombinant baculovirus-expressed feline infectious peritonitis (FIP) virus nucleocapsid protein against progression of FIP. Vet. Microbiol. 97 (2003), 31–44.
40. Holzworth, J., Some important disorders of cats. Cornell Vet. 53 (1963), 157–160.
41. Hurst, K.R., Koetzner, C.A., Masters, P.S., Identification of in vivo-interacting domains of the murine coronavirus nucleocapsid protein. J. Virol. 83 (2009), 7221–7234.
42. Hurst, K.R., Koetzner, C.A., Masters, P.S., Characterization of a critical interaction between the coronavirus nucleocapsid protein and nonstructural protein 3 of the viral replicase-transcriptase complex. J. Virol. 87 (2013), 9159–9172.
43. Jackwood, M.W., Review of infectious bronchitis virus around the world. Avian Dis. 56 (2012), 634–641.
44. Kennedy, M., Boedeker, N., Gibbs, P., Kania, S., Deletions in the 7a ORF of feline coronavirus associated with an epidemic of feline infectious peritonitis. Vet. Microbiol 81 (2001), 227–234.
45. Kennedy, M.A., Abd-Eldaim, M., Zika, S.E., Mankin, J.M., Kania, S.A., Evaluation of antibodies against feline coronavirus 7b protein for diagnosis of feline infectious peritonitis in cats. Am. J. Vet. Res. 69 (2008), 1179–1182.
46. Kipar, A., Kohler, K., Leukert, W., Reinacher, M., A comparison of lymphatic tissues from cats with spontaneous feline infectious peritonitis (FIP), cats with FIP virus infection but no FIP, and cats with no infection. J. Comp. Pathol. 125 (2001), 182–191.
47. Kipar, A., Meli, M.L., Feline infectious peritonitis: still an enigma?. Vet. Pathol. 51 (2014), 505–526.
48. Kipar, A., Meli, M.L., Baptiste, K.E., Bowker, L.J., Lutz, H., Sites of feline coronavirus persistence in healthy cats. J. Gen. Virol. 91 (2010), 1698–1707.
49. 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., Ward, A.B., Pre-fusion structure of a human coronavirus spike protein. Nature 531 (2016), 118–121.
50. Krijnse-Locker, J., Ericsson, M., Rottier, P.J., Griffiths, G., Characterization of the budding compartment of mouse hepatitis virus: evidence that transport from the RER to the Golgi complex requires only one vesicular transport step. J. Cell Biol. 124 (1994), 55–70.
51. Kubo, H., Yamada, Y.K., 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. 68 (1994), 5403–5410.
52. Lai, A.L., Millet, J.K., Daniel, S., Freed, J.H., Whittaker, G.R., The SARS-CoV fusion peptide forms an extended bipartite fusion platform that perturbs membrane order in a calcium-dependent manner. J. Mol. Biol., 2017.
53. Lai, M.M., Coronavirus: organization, replication and expression of genome. Annu. Rev. Microbiol. 44 (1990), 303–333.
54. 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 (2015), 1358–1368.
55. Li, F., Evidence for a common evolutionary origin of coronavirus spike protein receptor-binding subunits. J. Virol. 86 (2012), 2856–2858.
56. Li, F., Structure, function, and evolution of coronavirus spike proteins. Annu. Rev. Virol. 3 (2016), 237–261.
57. 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., Bosch, B.J., Identification of sialic acid-binding function for the middle east respiratory syndrome coronavirus spike glycoprotein. Proc. Natl. Acad. Sci. USA, 2017.
58. 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 (2013), 1066–1073.
59. Licitra, B.N., Sams, K.L., Lee, D.W., Whittaker, G.R., 2014. Feline Coronaviruses Associated with Feline Infectious Peritonitis Have Modifications to Spike Protein Activation Sites at Two Discrete Positions, arXiv. Cornell University Library, p. 5.
60. Look, A.T., Ashmun, R.A., Shapiro, L.H., Peiper, S.C., Human myeloid plasma membrane glycoprotein CD13 (gp150) is identical to aminopeptidase N. J. Clin. Investig. 83 (1989), 1299–1307.
61. Madu, I.G., Chu, V.C., Lee, H., Regan, A.D., Bauman, B.E., Whittaker, G.R., Heparan sulfate is a selective attachment factor for the avian coronavirus infectious bronchitis virus beaudette. Avian Dis. 51 (2007), 45–51.
62. Madu, I.G., Roth, S.L., Belouzard, S., Whittaker, G.R., Characterization of a highly conserved domain within the severe acute respiratory syndrome coronavirus spike protein S2 domain with characteristics of a viral fusion peptide. J. Virol. 83 (2009), 7411–7421.
63. Masters, P.S., Perlman, S., Coronaviridae. Knipe, D.M., Howley, P.M., (eds.) Fields Virology, 6th ed., 2013, Lippincot Williams & Wilkins, Philadelphia, PA, 825–858.
64. McKeirnan, A.J., Evermann, J.F., Davis, E.V., Ott, R.L., Comparative properties of feline coronaviruses in vitro. Can. J. Vet. Res. = Rev. Can. De. Rech. Vet. 51 (1987), 212–216.
65. Meli, M., Kipar, A., Muller, C., Jenal, K., Gonczi, E., Borel, N., Gunn-Moore, D., Chalmers, S., Lin, F., Reinacher, M., Lutz, H., High viral loads despite absence of clinical and pathological findings in cats experimentally infected with feline coronavirus (FCoV) type I and in naturally FCoV-infected cats. J. Feline Med. Surg. 6 (2004), 69–81.
66. Millet, J.K., Whittaker, G.R., Host cell entry of Middle East respiratory syndrome coronavirus after two-step, furin-mediated activation of the spike protein. Proc. Natl. Acad. Sci. USA 111 (2014), 15214–15219.
67. Millet, J.K., Whittaker, G.R., Host cell proteases: critical determinants of coronavirus tropism and pathogenesis. Virus Res. 202 (2015), 120–134.
68. Neuman, B.W., Kiss, G., Kunding, A.H., Bhella, D., Baksh, M.F., Connelly, S., Droese, B., Klaus, J.P., Makino, S., Sawicki, S.G., Siddell, S.G., Stamou, D.G., Wilson, I.A., Kuhn, P., Buchmeier, M.J., A structural analysis of M protein in coronavirus assembly and morphology. J. Struct. Biol. 174 (2011), 11–22.
69. Nieto-Torres, J.L., DeDiego, M.L., Verdia-Baguena, C., Jimenez-Guardeno, J.M., Regla-Nava, J.A., Fernandez-Delgado, R., Castano-Rodriguez, C., Alcaraz, A., Torres, J., Aguilella, V.M., Enjuanes, L., Severe acute respiratory syndrome coronavirus envelope protein ion channel activity promotes virus fitness and pathogenesis. PLoS Pathog., 10, 2014, e1004077.
70. Olsen, C.W., A review of feline infectious peritonitis virus: molecular biology, immunopathogenesis, clinical aspects, and vaccination. Vet. Microbiol. 36 (1993), 1–37.
71. Pedersen, N.C., Morphologic and physical characteristics of feline infectious peritonitis virus and its growth in autochthonous peritoneal cell cultures. Am. J. Vet. Res. 37 (1976), 567–572.
72. Pedersen, N.C., A review of feline infectious peritonitis virus infection: 1963–2008. J. Feline Med. Surg. 11 (2009), 225–258.
73. Pedersen, N.C., Black, J.W., Boyle, J.F., Evermann, J.F., McKeirnan, A.J., Ott, R.L., Pathogenic differences between various feline coronavirus isolates. Adv. Exp. Med. Biol. 173 (1984), 365–380.
74. Pedersen, N.C., Boyle, J.F., Floyd, K., Infection studies in kittens, using feline infectious peritonitis virus propagated in cell culture. Am. J. Vet. Res. 42 (1981), 363–367.
75. Pedersen, N.C., Boyle, J.F., Floyd, K., Fudge, A., Barker, J., An enteric coronavirus infection of cats and its relationship to feline infectious peritonitis. Am. J. Vet. Res. 42 (1981), 368–377.
76. Pedersen, N.C., Liu, H., Dodd, K.A., Pesavento, P.A., Significance of coronavirus mutants in feces and diseased tissues of cats suffering from feline infectious peritonitis. Viruses 1 (2009), 166–184.
77. Pedersen, N.C., Liu, H., Scarlett, J., Leutenegger, C.M., Golovko, L., Kennedy, H., Kamal, F.M., Feline infectious peritonitis: role of the feline coronavirus 3c gene in intestinal tropism and pathogenicity based upon isolates from resident and adopted shelter cats. Virus Res. 165 (2012), 17–28.
78. Pedersen, N.C., Sato, R., Foley, J.E., Poland, A.M., Common virus infections in cats, before and after being placed in shelters, with emphasis on feline enteric coronavirus. J. Feline Med. Surg. 6 (2004), 83–88.
79. Pedersen, N.C., Ward, J., Mengeling, W.L., Antigenic relationship of the feline infectious peritonitis virus to coronaviruses of other species. Arch. Virol. 58 (1978), 45–53.
80. Pervushin, K., Tan, E., Parthasarathy, K., Lin, X., Jiang, F.L., Yu, D., Vararattanavech, A., Soong, T.W., Liu, D.X., Torres, J., Structure and inhibition of the SARS coronavirus envelope protein ion channel. PLoS Pathog., 5, 2009, e1000511.
81. Poland, A.M., Vennema, H., Foley, J.E., Pedersen, N.C., Two related strains of feline infectious peritonitis virus isolated from immunocompromised cats infected with a feline enteric coronavirus. J. Clin. Microbiol. 34 (1996), 3180–3184.
82. Porter, E., Tasker, S., Day, M.J., Harley, R., Kipar, A., Siddell, S.G., Helps, C.R., Amino acid changes in the spike protein of feline coronavirus correlate with systemic spread of virus from the intestine and not with feline infectious peritonitis. Vet. Res., 45, 2014, 49.
83. Promkuntod, N., van Eijndhoven, R.E., de Vrieze, G., Grone, A., Verheije, M.H., 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.
84. Regan, A.D., Shraybman, R., Cohen, R.D., Whittaker, G.R., Differential role for low pH and cathepsin-mediated cleavage of the viral spike protein during entry of serotype II feline coronaviruses. Vet. Microbiol. 132 (2008), 235–248.
85. Regan, A.D., Whittaker, G.R., Utilization of DC-SIGN for entry of feline coronaviruses into host cells. J. Virol. 82 (2008), 11992–11996.
86. 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 alpha-helix of a model protein substrate by the serine protease, thrombin. Biochimie 122 (2016), 227–234.
87. Rossen, J.W., Kouame, J., Goedheer, A.J., Vennema, H., Rottier, P.J., Feline and canine coronaviruses are released from the basolateral side of polarized epithelial LLC-PK1 cells expressing the recombinant feline aminopeptidase-N cDNA. Arch. Virol. 146 (2001), 791–799.
88. Shang, J., Zheng, Y., Yang, Y., Liu, C., Geng, Q., Tai, W., Du, L., Zhou, Y., Zhang, W., Li, F., Cryo-EM structure of porcine delta coronavirus spike protein in the pre-fusion state. J. Virol., 2017.
89. Shiba, N., Maeda, K., Kato, H., Mochizuki, M., Iwata, H., Differentiation of feline coronavirus type I and II infections by virus neutralization test. Vet. Microbiol. 124 (2007), 348–352.
90. Sturman, L.S., Holmes, K.V., Behnke, J., Isolation of coronavirus envelope glycoproteins and interaction with the viral nucleocapsid. J. Virol. 33 (1980), 449–462.
91. Takano, T., Katada, Y., Moritoh, S., Ogasawara, M., Satoh, K., Satoh, R., Tanabe, M., Hohdatsu, T., Analysis of the mechanism of antibody-dependent enhancement of feline infectious peritonitis virus infection: aminopeptidase N is not important and a process of acidification of the endosome is necessary. J. Gen. Virol. 89 (2008), 1025–1029.
92. Takano, T., Kawakami, C., Yamada, S., Satoh, R., Hohdatsu, T., Antibody-dependent enhancement occurs upon re-infection with the identical serotype virus in feline infectious peritonitis virus infection. J. Vet. Med. Sci. 70 (2008), 1315–1321.
93. Tekes, G., Hofmann-Lehmann, R., Bank-Wolf, B., Maier, R., Thiel, H.J., Thiel, V., Chimeric feline coronaviruses that encode type II spike protein on type I genetic background display accelerated viral growth and altered receptor usage. J. Virol. 84 (2010), 1326–1333.
94. 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 (1996), 8669–8674.
95. Van Hamme, E., Desmarets, L., Dewerchin, H.L., Nauwynck, H.J., Intriguing interplay between feline infectious peritonitis virus and its receptors during entry in primary feline monocytes. Virus Res. 160 (2011), 32–39.
96. Vennema, H., Poland, A., Foley, J., Pedersen, N.C., Feline infectious peritonitis viruses arise by mutation from endemic feline enteric coronaviruses. Virology 243 (1998), 150–157.
97. 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. USA 85 (1988), 4526–4529.
98. Walls, A.C., Tortorici, M.A., Bosch, B.J., Frenz, B., Rottier, P.J., DiMaio, F., Rey, F.A., Veesler, D., Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature 531 (2016), 114–117.
99. Walls, A.C., Tortorici, M.A., Frenz, B., Snijder, J., Li, W., Rey, F.A., DiMaio, F., Bosch, B.J., Veesler, D., Glycan shield and epitope masking of a coronavirus spike protein observed by cryo-electron microscopy. Nat. Struct. Mol. Biol. 23 (2016), 899–905.
100. Ward, J.M., Morphogenesis of a virus in cats with experimental feline infectious peritonitis. Virology 41 (1970), 191–194.
101. Ward, J.M., Munn, R.J., Gribble, D.H., Dungworth, D.L., An observation of feline infectious peritonitis. Vet. Rec. 83 (1968), 416–417.
102. Wesseling, J.G., Vennema, H., Godeke, G.J., Horzinek, M.C., Rottier, P.J., Nucleotide sequence and expression of the spike (S) gene of canine coronavirus and comparison with the S proteins of feline and porcine coronaviruses. J. Gen. Virol. 75:Pt 7 (1994), 1789–1794.
103. White, J.M., Delos, S.E., Brecher, M., Schornberg, K., Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 43 (2008), 189–219.
104. White, J.M., Whittaker, G.R., Fusion of enveloped viruses in endosomes. Traffic 17 (2016), 593–614.
105. Whittaker, G.R., André N., Millet, J.K., Improving virus taxonomy by re-contextualizing sequence-based classification with biologically-relevant data: the case of the Alphacoronavirus 1 species. mSphere 3 (2018), e00463–00417.
106. Wickramasinghe, I.N., van Beurden, S.J., Weerts, E.A., Verheije, M.H., The avian coronavirus spike protein. Virus Res. 194 (2014), 37–48.
107. Winter, C., Schwegmann-Wessels, C., Cavanagh, D., Neumann, U., Herrler, G., Sialic acid is a receptor determinant for infection of cells by avian Infectious bronchitis virus. J. Gen. Virol. 87 (2006), 1209–1216.
108. Wolfe, L.G., Griesemer, R.A., Feline infectious peritonitis. Pathol. Vet. 3 (1966), 255–270.
109. Woo, P.C., Lau, S.K., Lam, C.S., Lau, C.C., Tsang, A.K., Lau, J.H., Bai, R., Teng, J.L., Tsang, C.C., Wang, M., Zheng, B.J., Chan, K.H., Yuen, K.Y., 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 (2012), 3995–4008.
110. Wurzer, W.J., Obojes, K., Vlasak, R., The sialate-4-O-acetylesterases of coronaviruses related to mouse hepatitis virus: a proposal to reorganize group 2 Coronaviridae. J. Gen. Virol. 83 (2002), 395–402.
111. Xiong, X., Tortorici, M.A., Snijder, J., Yoshioka, C., Walls, A.C., Li, W., McGuire, A.T., Rey, F.A., Bosch, B.J., Veesler, D., Glycan shield and fusion activation of a deltacoronavirus spike glycoprotein fine-tuned for enteric infections. J. Virol., 2017.
112. Yuan, Y., Cao, D., Zhang, Y., Ma, J., Qi, J., Wang, Q., Lu, G., Wu, Y., Yan, J., Shi, Y., Zhang, X., Gao, G.F., Cryo-EM structures of MERS-CoV and SARS-CoV spike glycoproteins reveal the dynamic receptor binding domains. Nat. Commun., 8, 2017, 15092.
113. Zhang, Y., Buckles, E., Whittaker, G.R., Expression of the C-type lectins DC-SIGN or L-SIGN alters host cell susceptibility for the avian coronavirus, infectious bronchitis virus. Vet. Microbiol. 157 (2012), 285–293.
114. Zook, B.C., King, N.W., Robison, R.L., McCombs, H.L., Ultrastructural evidence for the viral etiology of feline infectious peritonitis. Pathol. Vet. 5 (1968), 91–95.