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Chapter 11 : Nidovirus Entry into Cells

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Abstract:

This chapter presents an overview of cell entry by nidoviruses, and focuses on the functioning of the coronavirus fusion protein, in particular, on its proteolytic cleavage activation and on its conformation rearrangements in the process of membrane fusion. The actual fusion reaction is primed by interaction with the target cell where any of a number of triggers-receptor binding, proteolytic cleavage, or acidic pH-can spark off a cascade of conformational changes by which the metastable trimer eventually ends up in a trimer-of-hairpins conformation that is characterized by two main features: a six-helix bundle structure formed by the antiparallel association of the HR1 and HR2 domains, and the juxtaposed fusion peptides and transmembrane domains anchored together in the fused lipid bilayer. With regard to the intermediate conformational states, experimental support has only been obtained for the occurrence of a prehairpin intermediate in which the fusion peptides, originally hidden away in the native trimeric structure, have become exposed, pointing away from the viral membrane and into the target membrane. The authors describe how coronavirus membrane fusion fits in this picture by discussing the triggers, the key structural elements in the spike protein, its conformational states, and the actual fusion process. Membrane fusion is currently viewed as a process with defined events: merging first of the apposing leaflets (lipid stalk formation or hemifusion) and then of the distal leaflets (fusion pore formation), followed by fusion pore enlargement.

Citation: Bosch B, Rottier P. 2008. Nidovirus Entry into Cells, p 157-178. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch11

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Porcine reproductive and respiratory syndrome virus
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Figures

Image of Figure 1.
Figure 1.

(Top) schematic diagram of the SARS-CoV spike protein (drawn to scale). The position of the signal sequence (SS), receptor-binding domain (RBD), putative fusion peptides (FP’ and FP), heptad repeat domains (HR1 and HR2), and trans-membrane domain (TM) are indicated, as well as the potential N glycosylation sites. (Lower part) Schematic diagram of the spike proteins of representatives of the three coronavirus groups 1, 2, and 3 (G1 to G3): FIPV (G1), MHV and SARS-CoV (G2a and G2b, respectively), and IBV (G3). Bars are drawn to scale and aligned at the S1-S2 domain junction. The cysteine residues in the S2 ectodomain are indicated by vertical gray lines. Most of these cysteines are strictly conserved among all coronavirus spike proteins, as indicated by the connecting dashed lines.

Citation: Bosch B, Rottier P. 2008. Nidovirus Entry into Cells, p 157-178. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch11
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Image of Figure 2.
Figure 2.

Schematic diagrams (left) and drawings of the postfusion core structures (right) of the fusion proteins of SARS-CoV, influenza virus, HIV-1, parainfluenza virus 5 (PIV5; formerly known as SV5), and Ebola virus. The fusion peptide is indicated by a black bar. The HR1 and HR2 regions are depicted by dark and light gray shaded bars, respectively. The positions of the furin cleavage sites are indicated by open arrowheads, and the position of the putative cathepsin L cleavage site is indicated by a filled arrowhead. The fusion proteins are C-terminally anchored in the viral membrane (gray bar). The ribbon diagrams of the postfusion core structures (PDB codes: 1WYV [ ], 1QU1 [ ], 1AIK [ ], 1SVF [ ], and 2EBO [ ], respectively) were generated using RIBBONS ( ). The interior HR1 coiled coil is depicted in black, and the HR2 polypeptide is indicated in gray. “N” and “C” indicate the N and C termini of one HR1 and HR2 peptide in each case, respectively. Their positions correspond to the approximate locations of the membrane-interacting segments of the protein, i.e., the N-terminal fusion peptide and the C-terminal transmembrane domain. aa, amino acids.

Citation: Bosch B, Rottier P. 2008. Nidovirus Entry into Cells, p 157-178. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch11
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Image of Figure 3.
Figure 3.

Schematic diagram of the two coronavirus spike protein activation pathways. Proteolytic cleavage of spikes occurs in the exocytic route by furin(-like) proteases or in the endocytic (entry) route by cathepsin proteases, as indicated by the scissors in the left and right panels, respectively.

Citation: Bosch B, Rottier P. 2008. Nidovirus Entry into Cells, p 157-178. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch11
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Image of Figure 4.
Figure 4.

(A) Sequence alignment of the putative fusion peptides of coronavirus, WBV, and torovirus spike proteins. The sequences encompassing the putative fusion peptides of the coronaviruses HCoV-NL63 (AAS89767), HCoV-229E (VGIHHC), FIPV (strain 79-1146; VGIH79), HCoV-OC43 (CAA83661), MHV-A59 (P11224), SARS-CoV (strain TOR2; P59594), and IBV (strain Beaudette; P11223), the unclassified WBV (strain DF24/00; YP_803215), equine torovirus (EToV; strain P138/72; P23052), and bovine torovirus (BToV; strain B145; CAE01339) were manually aligned at the first heptad repeat of the HR1 region, of which the hydrophobic “a” and “d” residues are boxed. The start of the HR1 domain is just after a conserved arginine marked by an asterisk. The predicted fusion peptide sequences are underlined. The helix-breaking glycines and prolines within the putative fusion peptides are indicated by dark gray shading. (B) Sequence alignment of the (putative) fusion peptides of the human parainfluenza virus type 3 (HPIV-3; genus strain NIH 47885; P06828) with that of the HCoV-229E. Identical residues are indicated by asterisks. Similar and strongly similar residues are indicated by periods and colons, respectively.

Citation: Bosch B, Rottier P. 2008. Nidovirus Entry into Cells, p 157-178. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch11
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Image of Figure 5.
Figure 5.

Alignment of the spike protein endodomains of the group 1 (G1) coronaviruses HCoV-NL63, HCoV-229E, and FIPV; of the group 2 (G2) coronaviruses HCoV-OC43, MHV-A59, and SARS-CoV; and of the group 3 (G3) coronavirus IBV-Beaudette. Indicated are the pretransmembrane region (PTM), the transmembrane region (TM; as predicted by the TMHMM program [ ] for SARS-CoV spike protein), and the cysteine-rich region (boxed). The charged residues first encountered downstream of the predicted TM are in bold. Identical residues are indicated by asterisks, and strongly similar residues are indicated by periods. Residue numbers are indicated on either side of each sequence.

Citation: Bosch B, Rottier P. 2008. Nidovirus Entry into Cells, p 157-178. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch11
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Image of Figure 6.
Figure 6.

Model for coronavirus spike-mediated membrane fusion. (I) Spike in its native, prefusion state interacts with a receptor. Subsequently, dissociation of S1 and S2 is triggered by a cellular factor or condition (receptor binding, proteolytic cleavage, low pH) (II). This, in turn, primes the S2 protein to refold, to expose its fusion peptide, and to insert it into the target cell membrane, resulting in a state defined as the prefusion intermediate (II). Upon continued refolding, the HR2 region zippers alongside the HR1 trimeric coiled coil (III), thereby colocalizing the fusion peptide inserted in the target cell membrane and the transmembrane domain anchored in the viral membrane, and driving the juxtaposition of both membranes. This step can be blocked by heptad repeat corresponding peptides. Completion of the zippering process results in the formation of the HR1-HR2 six-helix bundle and leads to the creation of a hemifusion stalk and eventually to a fusion pore (IV and V), by processes that are presumably mediated by the membrane-interacting domains (e.g., fusion peptide, transmembrane domain, and cytoplasmic tail).

Citation: Bosch B, Rottier P. 2008. Nidovirus Entry into Cells, p 157-178. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch11
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References

/content/book/10.1128/9781555815790.ch11
1. Appleyard, G., and, M. Tisdale. 1985. Inhibition of the growth of human coronavirus 229E by leupeptin. J. Gen. Virol. 66 (Pt. 2):363366.
2. Baker, K. A.,, R. E. Dutch,, R. A. Lamb, and, T. S. Jardetzky. 1999. Structural basis for paramyxovirus-mediated membrane fusion. Mol. Cell 3:309319.
3. Barrett, A. J. 1986. The cystatins: a diverse superfamily of cysteine peptidase inhibitors. Biomed. Biochim. Acta 45:13631374.
4. Beniac, D. R.,, A. Andonov,, E. Grudeski, and, T. F. Booth. 2006. Architecture of the SARS coronavirus prefusion spike. Nat. Struct. Mol. Biol. 13:751752.
5. Bisht, H.,, A. Roberts,, L. Vogel,, A. Bukreyev,, P. L. Collins,, B. R. Murphy,, K. Subbarao, and, B. Moss. 2004. Severe acute respiratory syndrome coronavirus spike protein expressed by attenuated vaccinia virus protectively immunizes mice. Proc. Natl. Acad. Sci. USA 101:66416646.
6. Blau, D. M., and, K. V. Holmes. 2001. Human coronavirus HCoV-229E enters susceptible cells via the endocytic pathway. Adv. Exp. Med. Biol. 494:193198.
7. Bos, E. C.,, L. Heijnen,, W. Luytjes, and, W. J. Spaan. 1995. Mutational analysis of the murine coronavirus spike protein: effect on cell-to-cell fusion. Virology 214:453463.
8. Bos, E. C.,, W. Luytjes, and, W. J. Spaan. 1997. The function of the spike protein of mouse hepatitis virus strain A59 can be studied on virus-like particles: cleavage is not required for infectivity. J. Virol. 71:94279433.
9. Bosch, B. J.,, C. A. de Haan,, S. L. Smits, and, P. J. Rottier. 2005. Spike protein assembly into the coronavirion: exploring the limits of its sequence requirements. Virology 334:306318.
10. Bosch, B. J.,, B. E. Martina,, R. Van Der Zee,, J. Lepault,, B. J. Haijema,, C. Versluis,, A. J. Heck,, R. De Groot,, A. D. Osterhaus, and, P. J. Rottier. 2004. Severe acute respiratory syndrome coronavirus (SARS-CoV) infection inhibition using spike protein heptad repeat-derived peptides. Proc. Natl. Acad. Sci. USA 101:84558460.
11. Bosch, B. J.,, R. van der Zee,, C. A. de Haan, and, P. J. Rottier. 2003. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J. Virol. 77:88018811.
12. Bukreyev, A.,, E. W. Lamirande,, U. J. Buchholz,, L. N. Vogel,, W. R. Elkins,, M. St. Claire,, B. R. Murphy,, K. Subbarao, and, P. L. Collins. 2004. Mucosal immunisation of African green monkeys (Cercopithecus aethiops) with an attenuated parainfluenza virus expressing the SARS coronavirus spike protein for the prevention of SARS. Lancet 363:21222127.
13. Bullough, P. A.,, F. M. Hughson,, J. J. Skehel, and, D. C. Wiley. 1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:3743.
14. Carson, M. 1997. Ribbons. Methods Enzymol. 277:493505.
15. Cavanagh, D. 1995. The Coronavirus Surface Glycoprotein. Plenum Press, New York, NY.
16. Cavanagh, D.,, P. J. Davis,, D. J. Pappin,, M. M. Binns,, M. E. Boursnell, and, T. D. Brown. 1986. Coronavirus IBV: partial amino terminal sequencing of spike polypeptide S2 identifies the sequence Arg-Arg-Phe-Arg-Arg at the cleavage site of the spike precursor propolypeptide of IBV strains Beaudette and M41. Virus Res. 4:133143.
17. Chambers, P.,, C. R. Pringle, and, A. J. Easton. 1990. Heptad repeat sequences are located adjacent to hydrophobic regions in several types of virus fusion glycoproteins. J. Gen. Virol. V71(Pt. 12):30753080.
18. Chan, D. C.,, D. Fass,, J. M. Berger, and, P. S. Kim. 1997. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89:263273.
19. Chan, W. E.,, C. K. Chuang,, S. H. Yeh,, M. S. Chang, and, S. S. Chen. 2006. Functional characterization of heptad repeat 1 and 2 mutants of the spike protein of severe acute respiratory syndrome coronavirus. J. Virol. 80:32253237.
20. Chandran, K.,, N. J. Sullivan,, U. Felbor,, S. P. Whelan, and, J. M. Cunningham. 2005. Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308:16431645.
21. Chang, K. W., and, J. L. Gombold. 2001. Effects of amino acid insertions in the cysteine-rich domain of the MHV-A59 spike protein on cell fusion. Adv. Exp. Med. Biol. 494:205211.
22. Chang, K. W.,, Y. Sheng, and, J. L. Gombold. 2000. Coronavirus-induced membrane fusion requires the cysteine-rich domain in the spike protein. Virology 269:212224.
23. Chen, J.,, J. J. Skehel, and, D. C. Wiley. 1999. N- and C-terminal residues combine in the fusion-pH influenza hemagglutinin HA(2) subunit to form an N cap that terminates the triple-stranded coiled coil. Proc. Natl. Acad. Sci. USA 96:89678972.
24. Chu, V. C.,, L. J. McElroy,, V. Chu,, B. E. Bauman, and, G. R. Whittaker. 2006. The avian coronavirus infectious bronchitis virus undergoes direct low-pH-dependent fusion activation during entry into host cells. J. Virol. 80:31803188.
25. Collins, A. R., and, A. Grubb. 1991. Inhibitory effects of recombinant human cystatin C on human coronaviruses. Antimicrob. Agents Chemother. 35:24442446.
26. Collins, A. R., and, A. Grubb. 1998. Cystatin D, a natural salivary cysteine protease inhibitor, inhibits coronavirus replication at its physiologic concentration. Oral Microbiol. Immunol. 13:5961.
27. Cowley, J. A., and, P. J. Walker. 2002. The complete genome sequence of gill-associated virus of Penaeus monodon prawns indicates a gene organisation unique among nidoviruses. Arch. Virol. 147:19771987.
28. Cyr-Coats, K. S.,, H. R. Payne, and, J. Storz. 1988. The influence of the host cell and trypsin treatment on bovine corona-virus infectivity. Zentbl. Vetmed. Reihe B 35:752759.
29. Davies, H. A., and, M. R. Macnaughton. 1979. Comparison of the morphology of three coronaviruses. Arch.Virol. 59:2533.
30. de Groot, R. J.,, W. Luytjes,, M. C. Horzinek,, B. A. van der Zeijst,, W. J. Spaan, and, J. A. Lenstra. 1987. Evidence for a coiled-coil structure in the spike proteins of coronaviruses. J. Mol. Biol. 196:963966.
31. de Groot, R. J.,, J. Maduro,, J. A. Lenstra,, M. C. Horzinek,, B. A. van der Zeijst, and, W. J. Spaan. 1987. cDNA cloning and sequence analysis of the gene encoding the peplomer protein of feline infectious peritonitis virus. J. Gen. Virol. 68(Pt. 10):26392346.
32. de Groot, R. J.,, R. J. ter Haar,, M. C. Horzinek, and, B. A. van der Zeijst. 1987. Intracellular RNAs of the feline infectious peritonitis coronavirus strain 79–1146. J. Gen. Virol. 68(Pt. 4):9951002.
33. de Haan, C. A., and, P. J. Rottier. 2005. Molecular interactions in the assembly of coronaviruses. Adv. Virus. Res. 64:165230.
34. de Haan, C. A.,, K. Stadler,, G. J. Godeke,, B. J. Bosch, and, P. J. Rottier. 2004. Cleavage inhibition of the murine coronavirus spike protein by a furin-like enzyme affects cell-cell but not virus-cell fusion. J. Virol. 78:60486054.
35. de Haan, C. A.,, E. Te Lintelo,, Z. Li,, M. Raaben,, T. Wurdinger,, B. J. Bosch, and, P. J. Rottier. 2006. Cooperative involvement of the s1 and s2 subunits of the murine coronavirus spike protein in receptor binding and extended host range. J. Virol. 80:1090910918.
36. Delmas, B., and, H. Laude. 1990. Assembly of coronavirus spike protein into trimers and its role in epitope expression. J. Virol. 64:53675375.
37. Delputte, P. L.,, S. Costers, and, H. J. Nauwynck. 2005. Analysis of porcine reproductive and respiratory syndrome virus attachment and internalization: distinctive roles for heparan sulphate and sialoadhesin. J. Gen. Virol. 86:14411445.
38. Delputte, P. L.,, N. Vanderheijden,, H. J. Nauwynck, and, M. B. Pensaert. 2002. Involvement of the matrix protein in attachment of porcine reproductive and respiratory syndrome virus to a heparinlike receptor on porcine alveolar macrophages. J. Virol. 76:43124320.
39. Dimitrov, D. S. 2004. Virus entry: molecular mechanisms and biomedical applications. Nat. Rev. Microbiol. 2:109122.
40. Duquerroy, S.,, A. Vigouroux,, P. J. Rottier,, F. A. Rey, and, B. J. Bosch. 2005. Central ions and lateral asparagine/glutamine zippers stabilize the post-fusion hairpin conformation of the SARS coronavirus spike glycoprotein. Virology 335:276285.
41. Earp, L. J.,, S. E. Delos,, H. E. Park, and, J. M. White. 2005. The many mechanisms of viral membrane fusion proteins. Curr. Top. Microbiol. Immunol. 285:2566.
42. Eckert, D. M., and, P. S. Kim. 2001. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70:777810.
43. Egberink, H. F.,, J. Ederveen,, P. Callebaut, and, M. C. Horzinek. 1988. Characterization of the structural proteins of porcine epizootic diarrhea virus, strain CV777. Am. J. Vet. Res. 49:13201324.
44. Epand, R. M. 2003. Fusion peptides and the mechanism of viral fusion. Biochim. Biophys. Acta 1614:116121.
45. Follis, K. E.,, J. York, and, J. H. Nunberg. 2005. Serine-scanning mutagenesis studies of the C-terminal heptad repeats in the SARS coronavirus S glycoprotein highlight the important role of the short helical region. Virology 341:122129.
46. Follis, K. E.,, J. York, and, J. H. Nunberg. 2006. Furin cleavage of the SARS coronavirus spike glycoprotein enhances cell-cell fusion but does not affect virion entry. Virology 350:358369.
47. Frana, M. F.,, J. N. Behnke,, L. S. Sturman, and, K. V. Holmes. 1985. Proteolytic cleavage of the E2 glycoprotein of murine coronavirus: host-dependent differences in proteolytic cleavage and cell fusion. J. Virol. 56:912920.
48. Gallagher, T. M. 1997. A role for naturally occurring variation of the murine coronavirus spike protein in stabilizing association with the cellular receptor. J. Virol. 71:31293137.
49. Gallagher, T. M., and, M. J. Buchmeier. 2001. Coronavirus spike proteins in viral entry and pathogenesis. Virology 279:371374.
50. Gallagher, T. M.,, M. J. Buchmeier, and, S. Perlman. 1992. Cell receptor-independent infection by a neurotropic murine coronavirus. Virology 191:517522.
51. Gallagher, T. M.,, C. Escarmis, and, M. J. Buchmeier. 1991. Alteration of the pH dependence of coronavirus-induced cell fusion: effect of mutations in the spike glycoprotein. J. Virol. 65:19161928.
52. Garwes, D. J., and, D. H. Pocock. 1975. The polypeptide structure of transmissible gastroenteritis virus. J. Gen. Virol. 29:2534.
53. Giroglou, T.,, J. Cinatl, Jr.,, H. Rabenau,, C. Drosten,, H. Schwalbe,, H. W. Doerr, and, D. von Laer. 2004. Retroviral vectors pseudotyped with severe acute respiratory syndrome coronavirus S protein. J. Virol. 78:90079015.
54. Gombold, J. L.,, S. T. Hingley, and, S. R. Weiss. 1993. Fusion-defective mutants of mouse hepatitis virus A59 contain a mutation in the spike protein cleavage signal. J. Virol. 67:45044512.
55. Gombold, J. L.,, S. T. Hingley, and, S. R. Weiss. 1993. Identification of peplomer cleavage site mutations arising during persistence of MHV-A59. Adv. Exp. Med. Biol. 342:157163.
56. Granzow, H.,, F. Weiland,, D. Fichtner,, H. Schutze,, A. Karger,, E. Mundt,, B. Dresenkamp,, P. Martin, and, T. C. Mettenleiter. 2001. Identification and ultrastructural characterization of a novel virus from fish. J. Gen. Virol. 82:28492859.
57. Guillén, J.,, A. J. Pérez-Berná,, M. R. Moreno, and, J. Villalaín. 2005. Identification of the membrane-active regions of the severe acute respiratory syndrome coronavirus spike membrane glycoprotein using a 16/18-mer peptide scan: implications for the viral fusion mechanism. J. Virol. 79:17431752.
58. Hakansson-McReynolds, S.,, S. Jiang,, L. Rong, and, M. Caffrey. 2006. Solution structure of the severe acute respiratory syndrome-coronavirus heptad repeat 2 domain in the prefusion state. J. Biol. Chem. 281:1196511971.
59. Hansen, G. H.,, B. Delmas,, L. Besnardeau,, L. K. Vogel,, H. Laude,, H. Sjostrom, and, O. Noren. 1998. The coronavirus transmissible gastroenteritis virus causes infection after receptor-mediated endocytosis and acid-dependent fusion with an intracellular compartment. J. Virol. 72:527534.
60. Hernandez, L. D.,, L. R. Hoffman,, T. G. Wolfsberg, and, J. M. White. 1996. Virus-cell and cell-cell fusion. Annu. Rev. Cell Dev. Biol. 12:627661.
61. Hingley, S. T.,, I. Leparc-Goffart, and, S. R. Weiss. 1998. The mouse hepatitis virus A59 spike protein is not cleaved in primary hepatocyte and glial cell cultures. Adv. Exp. Med. Biol. 440:529535.
62. Hirano, N.,, K. Fujiwara,, S. Hino, and, M. Matumoto. 1974. Replication and plaque formation of mouse hepatitis virus (MHV-2) in mouse cell line DBT culture. Arch. Gesamte. Virusforsch. 44:298302.
63. Hofmann, H.,, K. Hattermann,, A. Marzi,, T. Gramberg,, M. Geier,, M. Krumbiegel,, S. Kuate,, K. Uberla,, M. Niedrig, and, S. Pohlmann. 2004. 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. 78:61346142.
64. Hofmann, H.,, G. Simmons,, A. J. Rennekamp,, C. Chaipan,, T. Gramberg,, E. Heck,, M. Geier,, A. Wegele,, A. Marzi,, P. Bates, and, S. Pohlmann. 2006. Highly conserved regions within the spike proteins of human coronaviruses 229E and NL63 determine recognition of their respective cellular receptors. J. Virol. 80:86398652.
65. Hofmann, M., and, R. Wyler. 1988. Propagation of the virus of porcine epidemic diarrhea in cell culture. J. Clin. Microbiol. 26:22352239.
66. Holmes, K. V., and, S. R. Compton. 1995. Coronavirus Receptors. Plenum Press, New York, NY.
67. Homma, M. 1971. Trypsin action on the growth of Sendai virus in tissue culture cells. I. Restoration of the infectivity for L cells by direct action of trypsin on L cell-borne Sendai virus. J. Virol. 8:619629.
68. Honey, K., and, A. Y. Rudensky. 2003. Lysosomal cysteine proteases regulate antigen presentation. Nat. Rev. Immunol. 3:472482.
69. Horzinek, M. C.,, J. Ederveen,, B. Kaeffer,, D. de Boer, and, M. Weiss. 1986. The peplomers of Berne virus. J. Gen. Virol. 67(Pt. 11):24752483.
70. Horzinek, M. C.,, M. Weiss, and, J. Ederveen. 1984. Berne virus is not ‘coronavirus-like.’ J. Gen. Virol. 65(Pt. 3):645649.
71. Huang, I. C.,, B. J. Bosch,, F. Li,, W. Li,, K. H. Lee,, S. Ghiran,, N. Vasilieva,, T. S. Dermody,, S. C. Harrison,, P. R. Dormitzer,, M. Farzan,, P. J. Rottier, and, H. Choe. 2006. SARS coronavirus, but not human coronavirus NL63, utilizes cathepsin L to infect ACE2-expressing cells. J. Biol. Chem. 281:31983203.
72. Hyllseth, B. 1973. Structural proteins of equine arteritis virus. Arch. Gesamte Virusforsch. 40:177188.
73. Jitrapakdee, S.,, S. Unajak,, N. Sittidilokratna,, R. A. Hodgson,, J. A. Cowley,, P. J. Walker,, S. Panyim, and, V. Boonsaeng. 2003. Identification and analysis of gp116 and gp64 structural glycoproteins of yellow head nidovirus of Penaeus monodon shrimp. J. Gen. Virol. 84:863873.
74. Keck, J. G.,, L. H. Soe,, S. Makino,, S. A. Stohlman, and, M. M. Lai. 1988. RNA recombination of murine coronaviruses: recombination between fusion-positive mouse hepatitis virus A59 and fusion-negative mouse hepatitis virus 2. J. Virol. 62:19891998.
75. Keng, C. T.,, A. Zhang,, S. Shen,, K. M. Lip,, B. C. Fielding,, T. H. Tan,, C. F. Chou,, C. B. Loh,, S. Wang,, J. Fu,, X. Yang,, S. G. Lim,, W. Hong, and, Y. J. Tan. 2005. Amino acids 1055 to 1192 in the S2 region of severe acute respiratory syndrome coronavirus S protein induce neutralizing antibodies: implications for the development of vaccines and antiviral agents. J. Virol. 79:32893296.
76. Keyaerts, E.,, L. Vijgen,, P. Maes,, J. Neyts, and, M. Van Ranst. 2004. In vitro inhibition of severe acute respiratory syndrome coronavirus by chloroquine. Biochem. Biophys. Res. Commun. 323:264268.
77. Kido, H.,, Y. Yokogoshi,, K. Sakai,, M. Tashiro,, Y. Kishino,, A. Fukutomi, and, N. Katunuma. 1992. Isolation and characterization of a novel trypsin-like protease found in rat bronchiolar epithelial Clara cells. A possible activator of the viral fusion glycoprotein. J. Biol. Chem. 267:1357313579.
78. Kielian, M., and, F. A. Rey. 2006. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4:6776.
79. Klenk, H. D., and, W. Garten. 1994. Host cell proteases controlling virus pathogenicity. Trends Microbiol. 2:3943.
80. Kooi, C.,, M. Cervin, and, R. Anderson. 1991. Differentiation of acid-pH-dependent and -nondependent entry pathways for mouse hepatitis virus. Virology 180:108119.
81. Kowalchyk, K., and, P. G. Plagemann. 1985. Cell surface receptors for lactate dehydrogenase-elevating virus on subpopulation of macrophages. Virus Res. 2:211229.
82. Kreutz, L. C., and, M. R. Ackermann. 1996. Porcine reproductive and respiratory syndrome virus enters cells through a low pH-dependent endocytic pathway. Virus Res. 42:137147.
83. Krueger, D. K.,, S. M. Kelly,, D. N. Lewicki,, R. Ruffolo, and, T. M. Gallagher. 2001. Variations in disparate regions of the murine coronavirus spike protein impact the initiation of membrane fusion. J. Virol. 75:27922802.
84. Krzystyniak, K., and, J. M. Dupuy. 1984. Entry of mouse hepatitis virus 3 into cells. J. Gen. Virol. 65(Pt. 1):227231.
85. Lai, S. C.,, P. C. Chong,, C. T. Yeh,, L. S. Liu,, J. T. Jan,, H. Y. Chi,, H. W. Liu,, A. Chen, and, Y. C. Wang. 2005. Characterization of neutralizing monoclonal antibodies recognizing a 15-residues epitope on the spike protein HR2 region of severe acute respiratory syndrome coronavirus (SARS-CoV). J. Biomed. Sci. 12:711727.
86. Lamb, R. A.,, R. G. Paterson, and, T. S. Jardetzky. 2006. Paramyxovirus membrane fusion: lessons from the F and HN atomic structures. Virology 344:3037.
87. Laude, H.,, D. Rasschaert,, B. Delmas,, M. Godet,, J. Gelfi, and, B. Charley. 1990. Molecular biology of transmissible gastroenteritis virus. Vet. Microbiol. 23:147154.
88. Lewicki, D. N., and, T. M. Gallagher. 2002. Quaternary structure of coronavirus spikes in complex with carcinoembryonic antigen-related cell adhesion molecule cellular receptors. J. Biol. Chem. 277:1972719734.
89. Li, D., and, D. Cavanagh. 1992. Coronavirus IBV-induced membrane fusion occurs at near-neutral pH. Arch. Virol. 122:307316.
90. Li, F.,, M. Berardi,, W. Li,, M. Farzan,, P. R. Dormitzer, and, S. C. Harrison. 2006. Conformational states of the severe acute respiratory syndrome coronavirus spike protein ectodomain. J. Virol. 80:67946800.
91. Lip, K. M.,, S. Shen,, X. Yang,, C. T. Keng,, A. Zhang,, H. L. Oh,, Z. H. Li,, L. A. Hwang,, C. F. Chou,, B. C. Fielding,, T. H. Tan,, J. Mayrhofer,, F. G. Falkner,, J. Fu,, S. G. Lim,, W. Hong, and, Y. J. Tan. 2006. Monoclonal antibodies targeting the HR2 domain and the region immediately upstream of the HR2 of the S protein neutralize in vitro infection of severe acute respiratory syndrome coronavirus. J. Virol. 80:941950.
92. Liu, S.,, G. Xiao,, Y. Chen,, Y. He,, J. Niu,, C. R. Escalante,, H. Xiong,, J. Farmar,, A. K. Debnath,, P. Tien, and, S. Jiang. 2004. Interaction between heptad repeat 1 and 2 regions in spike protein of SARS-associated coronavirus: implications for virus fusogenic mechanism and identification of fusion inhibitors. Lancet 363:938947.
93. Lontok, E.,, E. Corse, and, C. E. Machamer. 2004. Intracellular targeting signals contribute to localization of coronavirus spike proteins near the virus assembly site. J. Virol. 78:59135922.
94. Luo, Z.,, A. M. Matthews, and, S. R. Weiss. 1999. Amino acid substitutions within the leucine zipper domain of the murine coronavirus spike protein cause defects in oligomerization and the ability to induce cell-to-cell fusion. J. Virol. 73:81528159.
95. Luytjes, W.,, L. S. Sturman,, P. J. Bredenbeek,, J. Charite,, B. A. van der Zeijst,, M. C. Horzinek, and, W. J. Spaan. 1987. Primary structure of the glycoprotein E2 of coronavirus MHV-A59 and identification of the trypsin cleavage site. Virology 161:479487.
96. Malashkevich, V. N.,, B. J. Schneider,, M. L. McNally,, M. A. Milhollen,, J. X. Pang, and, P. S. Kim. 1999. Core structure of the envelope glycoprotein GP2 from Ebola virus at 1.9-A resolution. Proc. Natl. Acad. Sci. USA 96:26622667.
97. Marsh, M., and, A. Helenius. 2006. Virus entry: open sesame. Cell 124:729740.
98. Matsuyama, S.,, S. E. Delos, and, J. M. White. 2004. Sequential roles of receptor binding and low pH in forming prehairpin and hairpin conformations of a retroviral envelope glycoprotein. J. Virol. 78:82018209.
99. Matsuyama, S., and, F. Taguchi. 2002. Communication between S1N330 and a region in S2 of murine coronavirus spike protein is important for virus entry into cells expressing CEACAM1b receptor. Virology 295:160171.
100. Matsuyama, S., and, F. Taguchi. 2002. Receptor-induced conformational changes of murine coronavirus spike protein. J. Virol. 76:1181911826.
101. Matsuyama, S.,, M. Ujike,, S. Morikawa,, M. Tashiro, and, F. Taguchi. 2005. Protease-mediated enhancement of severe acute respiratory syndrome coronavirus infection. Proc. Natl. Acad. Sci. USA 102:1254312547.
102. Mizzen, L.,, A. Hilton,, S. Cheley, and, R. Anderson. 1985. Attenuation of murine coronavirus infection by ammonium chloride. Virology 142:378388.
103. Moller, S.,, M. D. Croning, and, R. Apweiler. 2001. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17:646653.
104. Molloy, S. S.,, P. A. Bresnahan,, S. H. Leppla,, K. R. Klimpel, and, G. Thomas. 1992. Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J. Biol. Chem. 267:1639616402.
105. Morrison, T. G. 2003. Structure and function of a paramyxovirus fusion protein. Biochim. Biophys. Acta. 1614:7384.
106. Mothes, W.,, A. L. Boerger,, S. Narayan,, J. M. Cunningham, and, J. A. Young. 2000. Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. Cell 103:679689.
107. Nash, T. C., and, M. J. Buchmeier. 1997. Entry of mouse hepatitis virus into cells by endosomal and nonendosomal pathways. Virology 233:18.
108. Nauwynck, H. J.,, X. Duan,, H. W. Favoreel,, P. Van Oostveldt, and, M. B. Pensaert. 1999. Entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages via receptor-mediated endocytosis. J. Gen. Virol. 80(Pt. 2):297305.
109. Neuman, B. W.,, B. D. Adair,, C. Yoshioka,, J. D. Quispe,, G. Orca,, P. Kuhn,, R. A. Milligan,, M. Yeager, and, M. J. Buchmeier. 2006. Supramolecular architecture of severe acute respiratory syndrome coronavirus revealed by electron cryomicroscopy. J. Virol. 80:79187928.
110. Neumann, G.,, H. Feldmann,, S. Watanabe,, I. Lukashevich, and, Y. Kawaoka. 2002. Reverse genetics demonstrates that proteolytic processing of the Ebola virus glycoprotein is not essential for replication in cell culture. J. Virol. 76:406410.
111. Niemann, H., and, H. D. Klenk. 1981. Coronavirus glyco-protein E1, a new type of viral glycoprotein. J. Mol. Biol. 153:9931010.
112. Nomura, R.,, A. Kiyota,, E. Suzaki,, K. Kataoka,, Y. Ohe,, K. Miyamoto,, T. Senda, and, T. Fujimoto. 2004. Human coronavirus 229E binds to CD13 in rafts and enters the cell through caveolae. J. Virol. 78:87018708.
113. Opstelten, D. J.,, P. de Groote,, M. C. Horzinek,, H. Vennema, and, P. J. Rottier. 1993. Disulfide bonds in folding and transport of mouse hepatitis coronavirus glycoproteins. J. Virol. 67:73947401.
114. Pager, C. T.,, W. W. Craft, Jr.,, J. Patch, and, R. E. Dutch. 2006. A mature and fusogenic form of the Nipah virus fusion protein requires proteolytic processing by cathepsin L. Virology 346:251257.
115. Pager, C. T., and, R. E. Dutch. 2005. Cathepsin L is involved in proteolytic processing of the Hendra virus fusion protein. J. Virol. 79:1271412720.
116. Park, H. E.,, J. A. Gruenke, and, J. M. White. 2003. Leash in the groove mechanism of membrane fusion. Nat. Struct. Biol. 10:10481053.
117. Payne, H. R., and, J. Storz. 1988. Analysis of cell fusion induced by bovine coronavirus infection. Arch. Virol. 103:2733.
118. Payne, H. R.,, J. Storz, and, W. G. Henk. 1990. Initial events in bovine coronavirus infection: analysis through immunogold probes and lysosomotropic inhibitors. Arch. Virol. 114:175189.
119. Persson, B., and, P. Argos. 1997. Prediction of membrane protein topology utilizing multiple sequence alignments. J. Protein Chem. 16:453457.
120. Petit, C. M.,, J. M. Melancon,, V. N. Chouljenko,, R. Colgrove,, M. Farzan,, D. M. Knipe, and, K. G. Kousoulas. 2005. Genetic analysis of the SARS-coronavirus spike glycoprotein functional domains involved in cell-surface expression and cell-to-cell fusion. Virology 341:215230.
121. Pratelli, A.,, V. Martella,, N. Decaro,, A. Tinelli,, M. Camero,, F. Cirone,, G. Elia,, A. Cavalli,, M. Corrente,, G. Greco,, D. Buonavoglia,, M. Gentile,, M. Tempesta, and, C. Buonavoglia. 2003. Genetic diversity of a canine coronavirus detected in pups with diarrhoea in Italy. J. Virol. Methods 110:917.
122. Pyrc, K.,, B. J. Bosch,, B. Berkhout,, M. F. Jebbink,, R. Dijkman,, P. Rottier, and, L. van der Hoek. 2006. Inhibition of human coronavirus NL63 infection at early stages of the replication cycle. Antimicrob. Agents Chemother. 50:20002008.
123. Qiu, Z.,, S. T. Hingley,, G. Simmons,, C. Yu,, J. Das Sarma,, P. Bates, and, S. R. Weiss. 2006. Endosomal proteolysis by cathepsins is necessary for murine coronavirus mouse hepatitis virus type 2 spike-mediated entry. J. Virol. 80:57685776.
124. Rost, B.,, G. Yachdav, and, J. Liu. 2004. The Predict Protein server. Nucleic Acids Res. 32:W321W326.
125. Routledge, E.,, R. Stauber,, M. Pfleiderer, and, S. G. Siddell. 1991. Analysis of murine coronavirus surface glycoprotein functions by using monoclonal antibodies. J. Virol. 65:254262.
126. Sainz, B., Jr.,, E. C. Mossel,, W. R. Gallaher,, W. C. Wimley,, C. J. Peters,, R. B. Wilson, and, R. F. Garry. 2006. Inhibition of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) infectivity by peptides analogous to the viral spike protein. Virus Res. 120:146155.
127. Sainz, B., Jr.,, J. M. Rausch,, W. R. Gallaher,, R. F. Garry, and, W. C. Wimley. 2005. The aromatic domain of the coronavirus class I viral fusion protein induces membrane permeabilization: putative role during viral entry. Biochemistry 44:947958.
128. Sainz, B., Jr.,, J. M. Rausch,, W. R. Gallaher,, R. F. Garry, and, W. C. Wimley. 2005. Identification and characterization of the putative fusion peptide of the severe acute respiratory syndrome-associated coronavirus spike protein. J. Virol. 79:71957206.
129. Sawicki, S. G. 1987. Characterization of a small plaque mutant of the A59 strain of mouse hepatitis virus defective in cell fusion. Adv. Exp. Med. Biol. 218:169174.
130. Scheid, A., and, P. W. Choppin. 1974. Identification of biological activities of paramyxovirus glycoproteins. Activation of cell fusion, hemolysis, and infectivity of proteolytic cleavage of an inactive precursor protein of Sendai virus. Virology 57:475490.
131. Schibli, D. J., and, W. Weissenhorn. 2004. Class I and class II viral fusion protein structures reveal similar principles in membrane fusion. Mol. Membr. Biol. 21:361371.
132. Schmidt, I.,, M. Skinner, and, S. Siddell. 1987. Nucleotide sequence of the gene encoding the surface projection glyco-protein of coronavirus MHV-JHM. J. Gen. Virol. 68(Pt. 1):4756.
133. Schmidt, M. F. 1982. Acylation of viral spike glycoproteins: a feature of enveloped RNA viruses. Virology 116:327338.
134. Schornberg, K.,, S. Matsuyama,, K. Kabsch,, S. Delos,, A. Bouton, and, J. White. 2006. Role of endosomal cathepsins in entry mediated by the Ebola virus glycoprotein. J. Virol. 80: 41744178.
135. Schroth-Diez, B.,, K. Ludwig,, B. Baljinnyam,, C. Kozerski,, Q. Huang, and, A. Herrmann. 2000. The role of the transmembrane and of the intraviral domain of glycoproteins in membrane fusion of enveloped viruses. Biosci. Rep. 20:571595.
136. Schütze, H.,, R. Ulferts,, B. Schelle,, S. Bayer,, H. Granzow,, B. Hoffmann,, T. C. Mettenleiter, and, J. Ziebuhr. 2006. Characterization of White bream virus reveals a novel genetic cluster of nidoviruses. J. Virol. 80:1159811609.
137. Schwegmann-Wessels, C.,, M. Al-Falah,, D. Escors,, Z. Wang,, G. Zimmer,, H. Deng,, L. Enjuanes,, H. Y. Naim, and, G. Herrler. 2004. A novel sorting signal for intracellular localization is present in the S protein of a porcine coronavirus but absent from severe acute respiratory syndrome-associated coronavirus. J. Biol. Chem. 279:4366143666.
138. Simmons, G.,, D. N. Gosalia,, A. J. Rennekamp,, J. D. Reeves,, S. L. Diamond, and, P. Bates. 2005. Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc. Natl. Acad. Sci. USA 102:1187611881.
139. Simmons, G.,, J. D. Reeves,, A. J. Rennekamp,, S. M. Amberg,, A. J. Piefer, and, P. Bates. 2004. Characterization of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) spike glycoprotein-mediated viral entry. Proc. Natl. Acad. Sci. USA 101:42404245.
140. Sittidilokratna, N.,, N. Phetchampai,, V. Boonsaeng, and, P. J. Walker. 2006. Structural and antigenic analysis of the yellow head virus nucleocapsid protein p20. Virus Res. 116:2129.
141. Snijder, E. J.,, J. A. Den Boon,, W. J. Spaan,, M. Weiss, and, M. C. Horzinek. 1990. Primary structure and post-translational processing of the Berne virus peplomer protein. Virology 178:355363.
142. Song, H. C.,, M. Y. Seo,, K. Stadler,, B. J. Yoo,, Q. L. Choo,, S. R. Coates,, Y. Uematsu,, T. Harada,, C. E. Greer,, J. M. Polo,, P. Pileri,, M. Eickmann,, R. Rappuoli,, S. Abrignani,, M. Houghton, and, J. H. Han. 2004. Synthesis and characterization of a native, oligomeric form of recombinant severe acute respiratory syndrome coronavirus spike glycoprotein. J. Virol. 78:1032810335.
143. Sonnhammer, E. L.,, G. von Heijne, and, A. Krogh. 1998. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 6:175182.
144. Stauber, R.,, M. Pfleiderera, and, S. Siddell. 1993. Proteolytic cleavage of the murine coronavirus surface glycoprotein is not required for fusion activity. J. Gen. Virol. 74(Pt. 2):183191.
145. Storz, J.,, R. Rott, and, G. Kaluza. 1981. Enhancement of plaque formation and cell fusion of an enteropathogenic coronavirus by trypsin treatment. Infect. Immun. 31:12141222.
146. Sturman, L. S.,, C. S. Ricard, and, K. V. Holmes. 1985. Proteolytic cleavage of the E2 glycoprotein of murine coronavirus: activation of cell-fusing activity of virions by trypsin and separation of two different 90K cleavage fragments. J. Virol. 56:904911.
147. Sturman, L. S.,, C. S. Ricard, and, K. V. Holmes. 1990. Conformational change of the coronavirus peplomer glyco-protein at pH 8.0 and 37°C correlates with virus aggregation and virus-induced cell fusion. J. Virol. 64:30423050.
148. Supekar, V. M.,, C. Bruckmann,, P. Ingallinella,, E. Bianchi,, A. Pessi, and, A. Carfi. 2004. Structure of a proteolytically resistant core from the severe acute respiratory syndrome coronavirus S2 fusion protein. Proc. Natl. Acad. Sci. USA 101:1795817963.
149. Taguchi, F. 1993. Fusion formation by the uncleaved spike protein of murine coronavirus JHMV variant cl-2. J. Virol. 67:11951202.
150. Taguchi, F., and, S. Matsuyama. 2002. Soluble receptor potentiates receptor-independent infection by murine coronavirus. J. Virol. 76:950958.
151. Thomas, G. 2002. Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell. Biol. 3:753766.
152. Thorp, E. B.,, J. A. Boscarino,, H. L. Logan,, J. T. Goletz, and, T. M. Gallagher. 2006. Palmitoylations on murine coronavirus spike proteins are essential for virion assembly and infectivity. J. Virol. 80:12801289.
153. Tripet, B.,, M. W. Howard,, M. Jobling,, R. K. Holmes,, K. V. Holmes, and, R. S. Hodges. 2004. Structural characterization of the SARS-coronavirus spike S fusion protein core. J. Biol. Chem. 279:2083620849.
154. Tsai, J. C.,, B. D. Zelus,, K. V. Holmes, and, S. R. Weiss. 2003. The N-terminal domain of the murine coronavirus spike glycoprotein determines the CEACAM1 receptor specificity of the virus strain. J. Virol. 77:841850.
155. van Berlo, M. F.,, W. J. van den Brink,, M. C. Horzinek, and, B. A. van der Zeijst. 1987. Fatty acid acylation of viral proteins in murine hepatitis virus-infected cells. Brief report. Arch. Virol. 95:123128.
156. Vanderheijden, N.,, P. L. Delputte,, H. W. Favoreel,, J. Vandekerckhove,, J. Van Damme,, P. A. van Woensel, and, H. J. Nauwynck. 2003. Involvement of sialoadhesin in entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages. J. Virol. 77:82078215.
157. Vincent, M. J.,, E. Bergeron,, S. Benjannet,, B. R. Erickson,, P. E. Rollin,, T. G. Ksiazek,, N. G. Seidah, and, S. T. Nichol. 2005. Chloroquine is a potent inhibitor of SARS coronavirus infection and spread. Virol. J. 2:69.
158. Volchkov, V. E.,, H. Feldmann,, V. A. Volchkova, and, H. D. Klenk. 1998. Processing of the Ebola virus glycoprotein by the proprotein convertase furin. Proc. Natl. Acad. Sci. USA 95:57625767.
159. Watanabe, R.,, S. Matsuyama, and, F. Taguchi. 2006. Receptor-independent infection of murine coronavirus: analysis by spinoculation. J. Virol. 80:49014908.
160. Weismiller, D. G.,, L. S. Sturman,, M. J. Buchmeier,, J. O. Fleming, and, K. V. Holmes. 1990. Monoclonal antibodies to the peplomer glycoprotein of coronavirus mouse hepatitis virus identify two subunits and detect a conformational change in the subunit released under mild alkaline conditions. J. Virol. 64:30513055.
161. Weiss, M.,, F. Steck, and, M. C. Horzinek. 1983. Purification and partial characterization of a new enveloped RNA virus (Berne virus). J. Gen. Virol. 64(Pt. 9):18491858.
162. Wesseling, J. G.,, H. Vennema,, G. J. Godeke,, M. C. Horzinek, and, P. J. Rottier. 1994. 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):17891794.
163. White, J. M. 1990. Viral and cellular membrane fusion proteins. Annu. Rev. Physiol. 52:675697.
164. White, J. M. 1992. Membrane fusion. Science 258:917924.
165. Wieringa, R.,, A. A. De Vries,, S. M. Post, and, P. J. Rottier. 2003. Intra- and intermolecular disulfide bonds of the GP2b glycoprotein of equine arteritis virus: relevance for virus assembly and infectivity. J. Virol. 77:1299613004.
166. Wieringa, R.,, A. A. de Vries, and, P. J. Rottier. 2003. Formation of disulfide-linked complexes between the three minor envelope glycoproteins (GP2b, GP3, and GP4) of equine arteritis virus. J. Virol. 77:62166226.
167. Wieringa, R.,, A. A. de Vries,, J. van der Meulen,, G. J. Godeke,, J. J. Onderwater,, H. van Tol,, H. K. Koerten,, A. M. Mommaas,, E. J. Snijder, and, P. J. Rottier. 2004. Structural protein requirements in equine arteritis virus assembly. J. Virol. 78:1301913027.
168. Wilson, I. A.,, J. J. Skehel, and, D. C. Wiley. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289:366373.
169. Wimley, W. C., and, S. H. White. 1993. Membrane partitioning: distinguishing bilayer effects from the hydrophobic effect. Biochemistry 32:63076312.
170. Wissink, E. H.,, M. V. Kroese,, H. A. van Wijk,, F. A. Rijsewijk,, J. J. Meulenberg, and, P. J. Rottier. 2005. Envelope protein requirements for the assembly of infectious virions of porcine reproductive and respiratory syndrome virus. J. Virol. 79:1249512506.
171. Wolf, E.,, P. S. Kim, and, B. Berger. 1997. MultiCoil: a program for predicting two- and three-stranded coiled coils. Protein Sci. 6:11791189.
172. Wool-Lewis, R. J., and, P. Bates. 1999. Endoproteolytic processing of the Ebola virus envelope glycoprotein: cleavage is not required for function. J. Virol. 73:14191426.
173. Wurdinger, T.,, M. H. Verheije,, K. Broen,, B. J. Bosch,, B. J. Haijema,, C. A. de Haan,, V. W. van Beusechem,, W. R. Gerritsen, and, P. J. Rottier. 2005. Soluble receptor-mediated targeting of mouse hepatitis coronavirus to the human epidermal growth factor receptor. J. Virol. 79:1531415322.
174. Wurdinger, T.,, M. H. Verheije,, M. Raaben,, B. J. Bosch,, C. A. de Haan,, V. W. van Beusechem,, P. J. Rottier, and, W. R. Gerritsen. 2005. Targeting non-human coronaviruses to human cancer cells using a bispecific single-chain antibody. Gene Ther. 12:13941404.
175. Xiao, X.,, S. Chakraborti,, A. S. Dimitrov,, K. Gramatikoff, and, D. S. Dimitrov. 2003. The SARS-CoV S glycoprotein: expression and functional characterization. Biochem. Biophys. Res. Commun. 312:11591164.
176. Xu, Y.,, Y. Liu,, Z. Lou,, L. Qin,, X. Li,, Z. Bai,, H. Pang,, P. Tien,, G. F. Gao, and, Z. Rao. 2004. Structural basis for coronavirus-mediated membrane fusion. Crystal structure of mouse hepatitis virus spike protein fusion core. J. Biol. Chem. 279:3051430522.
177. Xu, Y.,, Z. Lou,, Y. Liu,, H. Pang,, P. Tien,, G. F. Gao, and, Z. Rao. 2004. Crystal structure of severe acute respiratory syndrome coronavirus spike protein fusion core. J. Biol. Chem. 279:4941449419.
178. Xu, Y.,, J. Zhu,, Y. Liu,, Z. Lou,, F. Yuan,, D. K. Cole,, L. Ni,, N. Su,, L. Qin,, X. Li,, Z. Bai,, J. I. Bell,, H. Pang,, P. Tien,, G. F. Gao, and, Z. Rao. 2004. Characterization of the heptad repeat regions, HR1 and HR2, and design of a fusion core structure model of the spike protein from severe acute respiratory syndrome (SARS) coronavirus. Biochemistry 43:1406414071.
179. Yamada, Y. K.,, K. Takimoto,, M. Yabe, and, F. Taguchi. 1998. Requirement of proteolytic cleavage of the murine coronavirus MHV-2 spike protein for fusion activity. Adv. Exp. Med. Biol. 440:8993.
180. Yan, Z.,, B. Tripet, and, R. S. Hodges. 2006. Biophysical characterization of HRC peptide analogs interaction with heptad repeat regions of the SARS-coronavirus Spike fusion protein core. J. Struct. Biol. 155:162175.
181. Yang, Z. Y.,, Y. Huang,, L. Ganesh,, K. Leung,, W. P. Kong,, O. Schwartz,, K. Subbarao, and, G. J. Nabel. 2004. pH-dependent entry of severe acute respiratory syndrome coronavirus is mediated by the spike glycoprotein and enhanced by dendritic cell transfer through DC-SIGN. J. Virol. 78:56425650.
182. Yao, Y. X.,, J. Ren,, P. Heinen,, M. Zambon, and, I. M. Jones. 2004. Cleavage and serum reactivity of the severe acute respiratory syndrome coronavirus spike protein. J. Infect. Dis. 190:9198.
183. Ye, R.,, C. Montalto-Morrison, and, P. S. Masters. 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. 78:99049917.
184. Yin, H. S.,, R. G. Paterson,, X. Wen,, R. A. Lamb, and, T. S. Jardetzky. 2005. Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc. Natl. Acad. Sci. USA 102:92889293.
185. Yin, H. S.,, X. Wen,, R. G. Paterson,, R. A. Lamb, and, T. S. Jardetzky. 2006. Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439:3844.
186. Yoshikura, H., and, S. Tejima. 1981. Role of protease in mouse hepatitis virus-induced cell fusion. Studies with a cold-sensitive mutant isolated from a persistent infection. Virology 113:503511.
187. Youn, S.,, E. W. Collisson, and, C. E. Machamer. 2005. Contribution of trafficking signals in the cytoplasmic tail of the infectious bronchitis virus spike protein to virus infection. J. Virol. 79:1320913217.
188. Yuan, K.,, L. Yi,, J. Chen,, X. Qu,, T. Qing,, X. Rao,, P. Jiang,, J. Hu,, Z. Xiong,, Y. Nie,, X. Shi,, W. Wang,, C. Ling,, X. Yin,, K. Fan,, L. Lai,, M. Ding, and, H. Deng. 2004. Suppression of SARS-CoV entry by peptides corresponding to heptad regions on spike glycoprotein. Biochem. Biophys. Res. Commun. 319:746752.
189. Zelus, B. D.,, J. H. Schickli,, D. M. Blau,, S. R. Weiss, and, K. V. Holmes. 2003. Conformational changes in the spike glycoprotein of murine coronavirus are induced at 37°C either by soluble murine CEACAM1 receptors or by pH 8. J. Virol. 77:830840.
190. Zhou, H., and, S. Perlman. 2006. Preferential infection of mature dendritic cells by mouse hepatitis virus strain JHM. J. Virol. 80:25062514.

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