Cellular entry of the porcine epidemic diarrhea virus

Virus Research

Volumn 226, Issue , 2016, Pages 117-127

  Li, Wentao ^a   van Kuppeveld, Frank J M ^a   He, Qigai ^b   Rottier, Peter J M ^a   Bosch, Berend Jan ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Coronavirus; Membrane fusion; PED; PEDV; Porcine epidemic diarrhea virus; Proteolytic activation; Receptor interaction; Sialic acid; Sialic acid binding; Spike; Virus; Virus entry; Virus tropism

Indexed keywords

CORONAVIRUS SPIKE GLYCOPROTEIN; MICROSOMAL AMINOPEPTIDASE; SIALIC ACID; TRYPTASE; N ACETYLNEURAMINIC ACID; PROTEIN BINDING; VIRUS RECEPTOR;

DIARRHEA; DISEASE SEVERITY; IN VITRO STUDY; INTESTINE VILLUS ATROPHY; MALABSORPTION; MEMBRANE FUSION; NONHUMAN; PORCINE EPIDEMIC DIARRHEA VIRUS; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DEGRADATION; PROTEIN DOMAIN; REVIEW; SMALL INTESTINE MUCOSA; TARGET CELL; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS REPLICATION; ANIMAL; CHEMISTRY; CORONAVIRUS INFECTION; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PIG; STRUCTURE ACTIVITY RELATION; SWINE DISEASE; ULTRASTRUCTURE; VETERINARY; VIROLOGY;

ANIMALS; CORONAVIRUS INFECTIONS; N-ACETYLNEURAMINIC ACID; PORCINE EPIDEMIC DIARRHEA VIRUS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEOLYSIS; RECEPTORS, VIRUS; SPIKE GLYCOPROTEIN, CORONAVIRUS; STRUCTURE-ACTIVITY RELATIONSHIP; SWINE; SWINE DISEASES; VIRUS ATTACHMENT;

EID: 84978468847     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2016.05.031     Document Type: Review

References (85)

1. Baggen, J., Thibaut, H.J., Staring, J., Jae, L.T., Liu, Y., Guo, H., Slager, J.J., de Bruin, J.W., van Vliet, A.L., Blomen, V.A., Overduin, P., Sheng, J., de Haan Xander, C.A., de Vries, E., Meijer, A., Rossmann, M.G., Brummelkamp, T.R., van Kuppeveld, F.J., Enterovirus D68 receptor requirements unveiled by haploid genetics. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), 1399–1404.
2. 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. U. S. A. 106 (2009), 5871–5876.
3. 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.
4. 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.
5. Chang, S., Bae, J., Kang, T., Kim, J., Chung, G., Lim, C., Laude, H., Yang, M., Jang, Y., Identification of the epitope region capable of inducing neutralizing antibodies against the porcine epidemic diarrhea virus. Mol. Cells 14 (2002), 295–299.
6. Corman, V.M., Baldwin, H.J., Tateno, A.F., Zerbinati, R.M., Annan, A., Owusu, M., Nkrumah, E.E., Maganga, G.D., Oppong, S., Adu-Sarkodie, Y., Vallo, P., da Silva Filho, L.V., Leroy, E.M., Thiel, V., van der Hoek, L., Poon, L.L., Tschapka, M., Drosten, C., Drexler, J.F., Evidence for an ancestral association of human Coronavirus 229E with bats. J. Virol. 89 (2015), 11858–11870.
7. Cox, E., Pensaert, M.B., Callebaut, P., Vandeun, K., Intestinal replication of a porcine respiratory Coronavirus closely related antigenically to the enteric transmissible gastroenteritis virus. Vet. Microbiol. 23 (1990), 237–243.
8. Cruz, D.J.M., Kim, C., Shin, H., Phage-displayed peptides having antigenic similarities with porcine epidemic diarrhea virus (PEDV) neutralizing epitopes. Virology 354 (2006), 28–34.
9. Dastjerdi, A., Carr, J., Ellis, R.J., Steinbach, F., Williamson, S., Porcine epidemic diarrhea virus among farmed pigs, Ukraine. Emerg. Infect. Dis. 21 (2015), 2235–2237.
10. Debouck, P., Pensaert, M., Coussement, W., The pathogenesis of an enteric infection in pigs, experimentally induced by the coronavirus-like agent, CV 777. Vet. Microbiol. 6 (1981), 157–165.
11. Delmas, B., Gelfi, J., L'Haridon, R., Sjöström, H., Laude, H., 1992. Aminopeptidase N is a major receptor for the enteropathogenic coronavirus TGEV.
12. Deng, F., Ye, G., Liu, Q., Navid, M.T., Zhong, X., Li, Y., Wan, C., Xiao, S., He, Q., Fu, Z.F., Identification and comparison of receptor binding characteristics of the spike protein of two porcine epidemic diarrhea virus strains. Viruses, 8, 2016, 55.
13. Dermody, T.S., Nibert, M.L., Bassel-Duby, R., Fields, B.N., A sigma 1 region important for hemagglutination by serotype 3 reovirus strains. J. Virol. 64 (1990), 5173–5176.
14. Desmarets, L., Theuns, S., Olyslaegers, D., Dedeurwaerder, A., Vermeulen, B.L., Roukaerts, I., Nauwynck, H.J., Establishment of feline intestinal epithelial cell cultures for the propagation and study of feline enteric coronaviruses. Vet. Res., 44, 2013, 10.1186.
15. Drexler, J.F., Corman, V.M., Drosten, C., Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS. Antiviral Res. 101 (2014), 45–56.
16. Ducatelle, R., Coussement, W., Pensaert, M., Debouck, P., Hoorens, J., In vivo morphogenesis of a new porcine enteric coronavirus, CV 777. Arch. Virol. 68 (1981), 35–44.
17. Ducatelle, R., Coussement, W., Debouck, P., Hoorens, J., Pathology of experimental CV777 coronavirus enteritis in piglets: II. Electron microscopic study. Vet. Pathol. 19 (1982), 57–66.
18. Eckert, D.M., Kim, P.S., Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70 (2001), 777–810.
19. Esper, F., Ou, Z., Huang, Y.T., Human coronaviruses are uncommon in patients with gastrointestinal illness. J. Clin. Virol. 48 (2010), 131–133.
20. Farsani, S.M.J., Dijkman, R., Jebbink, M.F., Goossens, H., Ieven, M., Deijs, M., Molenkamp, R., van der Hoek, L., The first complete genome sequences of clinical isolates of human coronavirus 229E. Virus Genes 45 (2012), 433–439.
21. Gallagher, T., Perlman, S., Public health: broad reception for coronavirus. Nature 495 (2013), 176–177.
22. Godet, M., Grosclaude, J., Delmas, B., Laude, H., Major receptor-binding and neutralization determinants are located within the same domain of the transmissible gastroenteritis virus (Coronavirus) spike protein. J. Virol. 68 (1994), 8008–8016.
23. Grasland, B., Bigault, L., Bernard, C., Quenault, H., Toulouse, O., Fablet, C., Rose, N., Touzain, F., Blanchard, Y., 2015. Complete genome sequence of a porcine epidemic diarrhea s gene indel strain isolated in france in december 2014. Genome Announc 3, 10.1128/genomeA. 00535-15.
24. Guo, D., Zhu, Q., Zhang, H., Sun, D., Proteomic analysis of membrane proteins of vero cells: exploration of potential proteins responsible for virus entry. DNA Cell Biol. 33 (2014), 20–28.
25. Hanke, D., Jenckel, M., Petrov, A., Ritzmann, M., Stadler, J., Akimkin, V., Blome, S., Pohlmann, A., Schirrmeier, H., Beer, M., Hoeper, D., Comparison of porcine epidemic diarrhea viruses from Germany and the United States, 2014. Emerg. Infect. Dis. 21 (2015), 493–496.
26. Heald-Sargent, T., Gallagher, T., Ready, set, fuse! The coronavirus spike protein and acquisition of fusion competence. Viruses 4 (2012), 557–580.
27. Hofmann, M., Wyler, R., Propagation of the virus of porcine epidemic diarrhea in cell culture. J. Clin. Microbiol. 26 (1988), 2235–2239.
28. Hofmann, H., Pyrc, K., van der Hoek, L., Geier, M., Berkhout, B., Pohlmann, S., Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 7988–7993.
29. Hou, X.L., Yu, L.Y., Liu, J., Development and evaluation of enzyme-linked immunosorbent assay based on recombinant nucleocapsid protein for detection of porcine epidemic diarrhea (PEDV) antibodies. Vet. Microbiol. 123 (2007), 86–92.
30. Jung, K., Hu, H., Eyerly, B., Lu, Z., Chepngeno, J., Saif, L.J., Pathogenicity of 2 porcine deltacoronavirus strains in gnotobiotic pigs. Emerg. Infect. Dis. 21 (2015), 650–654.
31. Krempl, C., Herrler, G., Sialic acid binding activity of transmissible gastroenteritis coronavirus affects sedimentation behavior of virions and solubilized glycoproteins. J. Virol. 75 (2001), 844–849.
32. Krempl, C., Schultze, B., Laude, H., Herrler, G., Point mutations in the S protein connect the sialic acid binding activity with the enteropathogenicity of transmissible gastroenteritis coronavirus. J. Virol. 71 (1997), 3285–3287.
33. Lee, D.K., Park, C.K., Kim, S.H., Lee, C., Heterogeneity in spike protein genes of porcine epidemic diarrhea viruses isolated in Korea. Virus Res. 149 (2010), 175–182.
34. Li, B., Ge, J., Li, Y., Porcine aminopeptidase N is a functional receptor for the PEDV coronavirus. Virology 365 (2007), 166–172.
35. Li, W., Li, H., Liu, Y., Pan, Y., Deng, F., Song, Y., Tang, X., He, Q., New variants of porcine epidemic diarrhea virus, China, 2011. Emerg. Infect. Dis. 18 (2012), 1350–1353.
36. Li, C., Li, Z., Zou, Y., Wicht, O., van Kuppeveld, F.J.M., Rottier, P.J.M., Bosch, B.J., Manipulation of the porcine epidemic diarrhea virus genome using targeted RNA recombination. PLoS One, 8, 2013, e69997.
37. Li, W., Wicht, O., van Kuppeveld, F.J.M., He, Q., Rottier, P.J.M., Bosch, B., 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 (2015), 8077–8081.
38. Lin, C.M., Annamalai, T., Liu, X., Gao, X., Lu, Z., El-Tholoth, M., Hu, H., Saif, L.J., Wang, Q., Experimental infection of a US spike-insertion deletion porcine epidemic diarrhea virus in conventional nursing piglets and cross-protection to the original US PEDV infection. Vet. Res., 46, 2015 (134-015-0278-9).
39. Liu, C., Tang, J., Ma, Y., Liang, X., Yang, Y., Peng, G., Qi, Q., Jiang, S., Li, J., Du, L., Li, F., Receptor usage and cell entry of porcine epidemic diarrhea coronavirus. J. Virol. 89 (2015), 6121–6125.
40. Martelli, R., Lavazza, A., Nigrelli, A.D., Merialm, G., Alborali, L.G., Pensaert, M.B., Epidemic of diarrhoea caused by porcine epidemic diarrhoea virus in Italy. Vet. Rec. 162 (2008), 307–310.
41. Masuda, T., Murakami, S., Takahashi, O., Miyazaki, A., Ohashi, S., Yamasato, H., Suzuki, T., New porcine epidemic diarrhoea virus variant with a large deletion in the spike gene identified in domestic pigs. Arch. Virol. 160 (2015), 2565–2568.
42. Meng, F., Suo, S., Zarlenga, D.S., Cong, Y., Ma, X., Zhao, Q., Ren, X., A phage-displayed peptide recognizing porcine aminopeptidase N is a potent small molecule inhibitor of PEDV entry. Virology 456 (2014), 20–27.
43. Mesquita, J.R., Hakze-van der Honing, R., Almeida, A., Lourenco, M., van der Poel, W.H., Nascimento, M.S., Outbreak of porcine epidemic diarrhea virus in Portugal, 2015. Transbound Emerg. Dis. 62 (2015), 586–588.
44. Millet, J.K., Whittaker, G.R., Host cell proteases: critical determinants of coronavirus tropism and pathogenesis. Virus Res., 2014.
45. Mina-Osorio, P., The moonlighting enzyme CD13: old and new functions to target. Trends Mol. Med. 14 (2008), 361–371.
46. Nam, E., Lee, C., Contribution of the porcine aminopeptidase N (CD13) receptor density to porcine epidemic diarrhea virus infection. Vet. Microbiol. 144 (2010), 41–50.
47. Oh, J., Lee, K., Choi, H., Lee, C., Immunogenicity and protective efficacy of recombinant S1 domain of the porcine epidemic diarrhea virus spike protein. Arch. Virol. 159 (2014), 2977–2987.
48. Ojkic, D., Hazlett, M., Fairles, J., Marom, A., Slavic, D., Maxie, G., Alexandersen, S., Pasick, J., Alsop, J., Burlatschenko, S., The first case of porcine epidemic diarrhea in Canada. Can. Vet. J. 56 (2015), 149–152.
49. Oka, T., Saif, L.J., Marthaler, D., Esseili, M.A., Meulia, T., Lin, C., Vlasova, A.N., Jung, K., Zhang, Y., Wang, Q., Cell culture isolation and sequence analysis of genetically diverse US porcine epidemic diarrhea virus strains including a novel strain with a large deletion in the spike gene. Vet. Microbiol. 173 (2014), 258–269.
50. Park, J., Shin, H., Porcine epidemic diarrhea virus infects and replicates in porcine alveolar macrophages. Virus Res. 191 (2014), 143–152.
51. Park, J.E., Cruz, D.J., Shin, H.J., Trypsin-induced hemagglutination activity of porcine epidemic diarrhea virus. Arch. Virol. 155 (2010), 595–599.
52. Park, J., Park, E., Yu, J., Rho, J., Paudel, S., Hyun, B., Yang, D., Shin, H., Development of transgenic mouse model expressing porcine aminopeptidase N and its susceptibility to porcine epidemic diarrhea virus. Virus Res. 197 (2015), 108–115.
53. Pasick, J., Berhane, Y., Ojkic, D., Maxie, G., Embury-Hyatt, C., Swekla, K., Handel, K., Fairles, J., Alexandersen, S., Investigation into the role of potentially contaminated feed as a source of the first-Detected outbreaks of porcine epidemic diarrhea in Canada. Transbound. Emerg. Dis. 61 (2014), 397–410.
54. Pensaert, M., De Bouck, P., A new coronavirus-like particle associated with diarrhea in swine. Arch. Virol. 58 (1978), 243–247.
55. Puranaveja, S., Poollperm, P., Lertwatcharasarakul, P., Kesdaengsakonwut, S., Boonsoongnern, A., Urairong, K., Kitikoon, P., Choojai, P., Kedkovid, R., Teankum, K., Thanawongnuwech, R., Chinese-like strain of porcine epidemic diarrhea virus, Thailand. Emerg. Infect. Dis. 15 (2009), 1112–1115.
56. Raj, V.S., Mou, H., Smits, S.L., Dekkers, D.H., Müller, M.A., Dijkman, R., Muth, D., Demmers, J.A., Zaki, A., Fouchier, R.A., Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495 (2013), 251–254.
57. 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, 2012, e1002859.
58. Rydell, G.E., Nilsson, J., Rodriguez-Diaz, J., Ruvoen-Clouet, N., Svensson, L., Le Pendu, J., Larson, G., Human noroviruses recognize sialyl Lewis x neoglycoprotein. Glycobiology 19 (2009), 309–320.
59. Sanchez, C.M., Gebauer, F., Sune, C., Mendez, A., Dopazo, J., Enjuanes, L., Genetic evolution and tropism of transmissible gastroenteritis Coronaviruses. Virology 190 (1992), 92–105.
60. 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 (1996), 5634–5637.
61. Schwegmann-Weßels, C., Herrler, G., Sialic acids as receptor determinants for coronaviruses. Glycoconj. J. 23 (2006), 51–58.
62. Schwegmann-Wessels, C., Bauer, S., Winter, C., Enjuanes, L., Laude, H., Herrler, G., The sialic acid binding activity of the S protein facilitates infection by porcine transmissible gastroenteritis coronavirus. Virol. J., 8, 2011, 435.
63. Shirato, K., Maejima, M., Hirai, A., Ami, Y., Takeyama, N., Tsuchiya, K., Kusanagi, K., Nunoya, T., Taguchi, F., Enhanced cell fusion activity in porcine epidemic diarrhea virus adapted to suckling mice. Arch. Virol. 155 (2010), 1989–1995.
64. Shirato, K., Matsuyama, S., Ujike, M., Taguchi, F., Role of proteases in the release of porcine epidemic diarrhea virus from infected cells. J. Virol. 85 (2011), 7872–7880.
65. Shirato, K., Maejima, M., Matsuyama, S., Ujike, M., Miyazaki, A., Takeyama, N., Ikeda, H., Taguchi, F., Mutation in the cytoplasmic retrieval signal of porcine epidemic diarrhea virus spike (S) protein is responsible for enhanced fusion activity. Virus Res. 161 (2011), 188–193.
66. Steinrigl, A., Fernández, S.R., Stoiber, F., Pikalo, J., Sattler, T., Schmoll, F., First detection, clinical presentation and phylogenetic characterization of Porcine epidemic diarrhea virus in Austria. BMC Vet. Res., 11, 2015, 1.
67. Stevenson, G.W., Hoang, H., Schwartz, K.J., Burrough, E.R., Sun, D., Madson, D., Cooper, V.L., Pillatzki, A., Gauger, P., Schmitt, B.J., Koster, L.G., Killian, M.L., Yoon, K.J., Emergence of Porcine epidemic diarrhea virus in the United States: clinical signs, lesions, and viral genomic sequences. J. Vet. Diagn. Invest. 25 (2013), 649–654.
68. Straw, B.E., Zimmerman, J., D'Allaire, S., Taylor, D., 2006. Diseases of swine 9 th edition. Diseases of Swine 9th Edition, 387–395.
69. Sun, D., Feng, L., Shi, H., Chen, J., Cui, X., Chen, H., Liu, S., Tong, Y., Wang, Y., Tong, G., Identification of two novel B cell epitopes on porcine epidemic diarrhea virus spike protein. Vet. Microbiol. 131 (2008), 73–81.
70. Sun, R., Cai, R., Chen, Y., Liang, P., Chen, D., Song, C., Outbreak of porcine epidemic diarrhea in suckling piglets, China. Emerg. Infect. Dis. 18 (2012), 161–163.
71. Theuns, S., Conceicao-Neto, N., Christiaens, I., Zeller, M., Desmarets, L.M., Roukaerts, I.D., Acar, D.D., Heylen, E., Matthijnssens, J., Nauwynck, H.J., 2015. Complete genome sequence of a porcine epidemic diarrhea virus from a novel outbreak in belgium, january 2015. Genome Announc 3, 10.1128/genomeA. 00506-15.
72. Vlasova, A.N., Marthaler, D., Wang, Q., Culhane, M.R., Rossow, K.D., Rovira, A., Collins, J., Saif, L.J., Distinct characteristics and complex evolution of PEDV strains, North America, may 2013–February 2014. Emerg. Infect. Dis. 20 (2014), 1620–1628.
73. Walls, A.C., Tortorici, M.A., Bosch, B., Frenz, B., Rottier, P.J., DiMaio, F., Rey, F.A., Veesler, D., Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature, 2016.
74. Wang, L., Byrum, B., Zhang, Y., New variant of porcine epidemic diarrhea virus, United States, 2014. Emerg. Infect. Dis. 20 (2014), 917–919.
75. Wang, X., Chen, J., Shi, D., Shi, H., Zhang, X., Yuan, J., Jiang, S., Feng, L., Immunogenicity and antigenic relationships among spike proteins of porcine epidemic diarrhea virus subtypes G1 and G2. Arch. Virol., 2015.
76. Wicht, O., Burkard, C., de Haan, C.A., van Kuppeveld, F.J., Rottier, P.J., Bosch, B.J., Identification and characterization of a proteolytically primed form of the murine coronavirus spike proteins after fusion with the target cell. J. Virol. 88 (2014), 4943–4952.
77. Wicht, O., Li, W., Willems, L., Meuleman, T.J., Wubbolts, R.W., van Kuppeveld, F.J., Rottier, P.J., Bosch, B.J., Proteolytic activation of the porcine epidemic diarrhea coronavirus spike fusion protein by trypsin in cell culture. J. Virol. 88 (2014), 7952–7961.
78. 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.
79. 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 (2009), 8744–8758.
80. Yeager, C.L., Ashmun, R.A., Williams, R.K., Cardellichio, C.B., Shapiro, L.H., Look, A.T., Holmes, K.V., 1992. Human aminopeptidase N is a receptor for human coronavirus 229E.
81. Zamolodchikova, T., Serine proteases of small intestine mucosa—localization, functional properties, and physiological role. Biochemistry (Moscow) 77 (2012), 820–829.
82. Zeng, S., Zhang, H., Ding, Z., Luo, R., An, K., Liu, L., Bi, J., Chen, H., Xiao, S., Fang, L., Proteome analysis of porcine epidemic diarrhea virus (PEDV)‐infected Vero cells. Proteomics 15 (2015), 1819–1828.
83. Zhang Y., Yao Y., Gao X., Wang Y., Jia X., Xiao Y., Wang T., Li X., Tian K., 2016, Development of a Neutralizing Monoclonal Antibody Against Porcine Epidemic Diarrhea Virus S1 Protein, Monoclonal Antibodies in Immunodiagnosis and Immunotherapy.
84. de Groot, R.J., Baker, S.C., Baric, R.S., Brown, C.S., Drosten, C., Enjuanes, L., Fouchier, R.A., Galiano, M., Gorbalenya, A.E., Memish, Z.A., Perlman, S., Poon, L.L., Snijder, E.J., Stephens, G.M., Woo, P.C., Zaki, A.M., Zambon, M., Ziebuhr, J., Middle east respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus study group. J. Virol. 87 (2013), 7790–7792.
85. 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.