Identification and characterization of the putative fusion peptide of the severe acute respiratory syndrome-associated coronavirus spike protein

Journal of Virology

Volumn 79, Issue 11, 2005, Pages 7195-7206

  Sainz Jr , Bruno ^a   Rausch, Joshua M ^a   Gallaher, William R ^b   Garry, Robert F ^a   Wimley, William C ^a  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; GLYCINE; PHENYLALANINE; PROLINE; VIRUS FUSION PROTEIN; VIRUS SPIKE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE PERMEABILITY; HYDROPHOBICITY; LIPID VESICLE; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; SARS CORONAVIRUS; VIRUS CELL INTERACTION;

AMINO ACID SEQUENCE; CIRCULAR DICHROISM; LIPOSOMES; MEMBRANE FUSION; MEMBRANE GLYCOPROTEINS; MEMBRANE LIPIDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; SARS VIRUS; VIRAL ENVELOPE PROTEINS; VIRAL FUSION PROTEINS;

CORONAVIRIDAE; CORONAVIRUS; SARS COV;

EID: 18744404801     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.11.7195-7206.2005     Document Type: Article

References (100)

1. Agirre, A., C. Flach, F. M. Goni, R. Mendelsohn, J. M. Valpuesta, F. Wu, and J. L. Nieva. 2000. Interactions of the HIV-1 fusion peptide with large unilamellar vesicles and monolayers. A cryo-TEM and spectroscopic study. Biochim. Biophys. Acta 1467:153-164.
2. Bergeron, E., M. J. Vincent, L. Wickham, J. Hamelin, A. Basak, S. T. Nichol, M. Chretien, and N. G. Seidah. 2005. Implication of proprotein convertases in the processing and spread of severe acute respiratory syndrome coronavirus. Biochem. Biophys. Res. Commun. 326:554-563.
3. Blumenthal, R., M. J. Clague, S. R. Durell, and R. M. Epand. 2003. Membrane fusion. Chem. Rev. 103:53-69.
4. 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 214:453-463.
5. 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. 71:9427-9433.
6. 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 101:8455-8460.
7. 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. 77:8801-8811.
8. Bosch, M. L., P. L. Earl, K. Fargnoli, S. Picciafuoco, F. Giombini, F. Wong-Staal, and G. Franchini. 1989. Identification of the fusion peptide of primate immunodeficiency viruses. Science 244:694-697.
9. Bresnahan, P. A., R. Leduc, L. Thomas, J. Thorner, H. L. Gibson, A. J. Brake, P. J. Barr, and G. Thomas. 1990. Human fur gene encodes a yeast KEX2-like endoprotease that cleaves pro-beta-NGF in vivo. J. Cell Biol. 111:2851-2859.
10. Caffrey, M., M. Cai, J. Kaufman, S. J. Stahl, P. T. Wingfield, D. G. Covell, A. M. Gronenborn, and G. M. Clore. 1998. Three-dimensional solution structure of the 44 kDa ectodomain of SIV gp41. EMBO J. 17:4572-4584.
11. Carr, C. M., and P. S. Kim. 1993. A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73:823-832.
12. Cavanagh, D., and P. J. Davis. 1986. Coronavirus IBV: removal of spike glycopolypeptide S1 by urea abolishes infectivity and haemagglutination but not attachment to cells. J. Gen. Virol. 67:1443-1448.
13. Chan, D. C., D. Fass, J. M. Berger, and P. S. Kim. 1997. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89:263-273.
14. Chang, D. K., S. F. Cheng, and W. J. Chien. 1997. The amino-terminal fusion domain peptide of human immunodeficiency virus type 1 gp41 inserts into the sodium dodecyl sulfate micelle primarily as a helix with a conserved glycine at the micelle-water interface. J. Virol. 71:6593-6602.
15. Chang, D. K., S. F. Cheng, and V. D. Trivedi. 1999. Biophysical characterization of the structure of the amino-terminal region of gp41 of HIV-1. Implications on viral fusion mechanism. J. Biol. Chem. 274:5299-5309.
16. Chen, P. S., T. Y. Toribara, and H. Warner. 1956. Microdetermination of phosphorus. Anal. Chem. 28:1756-1758.
17. Davies, S. M., S. M. Kelly, N. C. Price, and J. P. Bradshaw. 1998. Structural plasticity of the feline leukaemia virus fusion peptide: a circular dichroism study. FEBS Lett. 425:415-418.
18. 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. 78:6048-6054.
19. Delos, S. E., J. M. Gilbert, and J. M. White. 2000. The central proline of an internal viral fusion peptide serves two important roles. J. Virol. 74:1686-1693.
20. Drosten, C., S. Gunther, W. Preiser, S. van der Werf, H. R. Brodt, S. Becker, H. Rabenau, M. Panning, L. Kolesnikova, R. A. Fouchier, A. Berger, A. M. Burguiere, J. Cinatl, M. Eickmann, N. Escriou, K. Grywna, S. Kramme, J. C. Manuguerra, S. Muller, V. Rickerts, M. Sturmer, S. Vieth, H. D. Klenk, A. D. Osterhaus, H. Schmitz, and H. W. Doerr. 2003. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348:1967-1976.
21. Durell, S. R., I. Martin, J. M. Ruysschaert, Y. Shai, and R. Blumenthal. 1997. What studies of fusion peptides tell us about viral envelope glycoprotein-mediated membrane fusion. Mol. Membr. Biol. 14:97-112.
22. Fiske, C. H., and Y. Subbarow. 1925. The colorimetric determination of phosphorus. J. Biol. Chem. 66:375-400.
23. Freed, E. O., E. L. Delwart, G. L. Buchschacher, Jr., and A. T. Panganiban. 1992. A mutation in the human immunodeficiency virus type 1 transmembrane glycoprotein gp41 dominantly interferes with fusion and infectivity. Proc. Natl. Acad. Sci. USA 89:70-74.
24. Freed, E. O., D. J. Myers, and R. Risser. 1990. Characterization of the fusion domain of the human immunodeficiency virus type 1 envelope glycoprotein gp41. Proc. Natl. Acad. Sci. USA 87:4650-4654.
25. Gallagher, T. M., and M. J. Buchmeier. 2001. Coronavirus spike proteins in viral entry and pathogenesis. Virology 279:371-374.
26. Gallaher, W. R. 1987. Detection of a fusion peptide sequence in the transmembrane protein of human immunodeficiency virus. Cell 50:327-328.
27. Gallaher, W. R. 1996. Similar structural models of the transmembrane proteins of Ebola and avian sarcoma viruses. Cell 85:477-478.
28. Gallaher, W. R., J. M. Ball, R. F. Garry, M. C. Griffin, and R. C. Montelaro. 1989. A general model for the transmembrane proteins of HIV and other retroviruses. AIDS Res. Hum. Retrovir. 5:431-440.
29. Gallaher, W. R., and R. F. Garry. 2003. Model of the pre-insertion region of the spike (S2) fusion glycoprotein of the human SARS coronavirus: implications for antiviral therapeutics. [Online.] http://www.virology.net/ Articles/sars/s2model.html.
30. Gallaher, W. R., J. P. Segrest, and E. Hunter. 1992. Are fusion peptides really "sided" insertional helices? Cell 70:531-532.
31. Garry, R. F., and S. Dash. 2003. Proteomics computational analyses suggest that hepatitis C virus E1 and pestivirus E2 envelope glycoproteins are truncated class II fusion proteins. Virology 307:255-265.
32. Gething, M. J., R. W. Doms, D. York, and J. White. 1986. Studies on the mechanism of membrane fusion: site-specific mutagenesis of the hemagglutinin of influenza virus. J. Cell Biol. 102:11-23.
33. Goldsmith, C. S., K. M. Tatti, T. G. Ksiazek, P. E. Rollin, J. A. Comer, W. W. Lee, P. A. Rota, B. Bankamp, W. J. Bellini, and S. R. Zaki. 2004. Ultrastructural characterization of SARS coronavirus. Emerg. Infect. Dis. 10:320-326.
34. Gomara, M. J., P. Mora, I. Mingarro, and J. L. Nieva. 2004. Roles of a conserved proline in the internal fusion peptide of Ebola glycoprotein. FEBS Lett. 569:261-266.
35. 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. 67:4504-4512.
36. 35a. 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. 79:1743-1752.
37. Harter, C., P. James, T. Bachi, G. Semenza, and J. Brunner. 1989. Hydrophobic binding of the ectodomain of influenza hemagglutinin to membranes occurs through the "fusion peptide". J. Biol. Chem. 264:6459-6464.
38. Hernandez, L. D., L. R. Hotfman, T. G. Wolfsberg, and J. M. White. 1996. Virus-cell and cell-cell fusion. Annu. Rev. Cell Dev. Biol. 12:627-661.
39. Hernandez, L. D., and J. M. White. 1998. Mutational analysis of the candidate internal fusion peptide of the avian leukosis and sarcoma virus subgroup A envelope glycoprotein. J. Virol. 72:3259-3267.
40. Hingley, S. T., I. Leparc-Goffart, and S. R. Weiss. 1998. The spike protein of murine coronavirus mouse hepatitis virus strain A59 is not cleaved in primary glial cells and primary hepatocytes. J. Virol. 72:1606-1609.
41. Hoffman, K., and W. Stoffel. 1993. TMbase - a database of membrane-spanning segments. Biol. Chem. Hoppe-Seyler 374:166-170.
42. Horvath, C. M., and R. A. Lamb. 1992. Studies on the fusion peptide of a paramyxovirus fusion glycoprotein: roles of conserved residues in cell fusion. J. Virol. 66:2443-2455.
43. Hunter, E., E. Hill, M. Hardwick, A. Bhown, D. E. Schwartz, and R. Tizard. 1983. Complete sequence of the Rous sarcoma virus env gene: identification of structural and functional regions of its product. J. Virol. 46:920-936.
44. Ito, H., S. Watanabe, A. Sanchez, M. A. Whitt, and Y. Kawaoka. 1999. Mutational analysis of the putative fusion domain of Ebola virus glycoprotein. J. Virol. 73:8907-8912.
45. Jeffers, S. A., S. M. Tusell, L. Gillim-Ross, E. M. Hemmila, J. E. Achenbach, G. J. Babcock, W. D. Thomas, Jr., L. B. Thackray, M. D. Young, R. J. Mason, D. M. Ambrosino, D. E. Wentworth, J. C. Demartini, and K. V. Holmes. 2004, CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA 101:15748-15753.
46. Ksiazek, T. G., D. Erdman, C. S. Goldsmith, S. R. Zaki, T. Peret, S. Emery, S. Tong, C. Urbani, J. A. Comer, W. Lim, P. E. Rollin, S. F. Dowell, A. E. Ling, C. D. Humphrey, W. J. Shieh, J. Guarner, C. D. Paddock, P. Rota, B. Fields, J. DeRisi, J. Y. Yang, N. Cox, J. M. Hughes, J. W. LeDuc, W. J. Bellini, and L. J. Anderson. 2003. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348:1953-1966.
47. Lear, J. D., and W. F. DeGrado. 1987. Membrane binding and conformational properties of peptides representing the NH2 terminus of influenza HA-2. J. Biol. Chem. 262:6500-6505.
48. Lee, H. J., C. K. Shieh, A. E. Gorbalenya, E. V. Koonin, N. La Monica, J. Tuler, A. Bagdzhadzhyan, and M. M. Lai. 1991. The complete sequence (22 kilobases) of murine coronavirus gene 1 encoding the putative proteases and RNA polymerase. Virology 180:567-582.
49. Li, W., M. J. Moore, N. Vasilieva, J. Sui, S. K. Wong, M. A. Berne, M. Somasundaran, J. L. Sullivan, K. Luzuriaga, T. C. Greenough, H. Choe, and M. Farzan. 2003, Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450-454.
50. Liu, S., G. Xiao, Y. Chen, Y. He, J. Niu, C. R. Escalante, H. Xiong, J. Farmar, A. K. Debnath, P. Tien, S. Jiang, C. S. Goldsmith, K. M. Tatti, T. G. Ksiazek, P. E. Rollin, J. A. Comer, W. W. Lee, P. A. Rota, B. Bankamp, W. J. Bellini, and S. R. Zaki. 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 363:938-947.
51. Luo, Z., and S. R. Weiss. 1998. Roles in cell-to-cell fusion of two conserved hydrophobic regions in the murine coronavirus spike protein. Virology 244: 483-494.
52. Luo, Z. L., and S. R. Weiss. 1998. Mutational analysis of fusion peptide-like regions in the mouse hepatitis virus strain A59 spike protein. Adv. Exp. Med. Biol. 440:17-23.
53. 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 161:479-487.
54. Malashkevich, V. N., D. C. Chan, C. T. Chutkowski, and P. S. Kim. 1998. Crystal structure of the simian immunodeficiency virus (SIV) gp41 core: conserved helical interactions underlie the broad inhibitory activity of gp41 peptides. Proc. Natl. Acad. Sci. USA 95:9134-9139.
55. Mayer, L. D., M. J. Hope, and P. R. Cullis. 1986. Vesicles of variable sizes produced by a rapid extrusion procedure. Biochim. Biophys. Acta 858:161-168.
56. Molloy, S. S., P. A. Bresnahan, S. H. Leppla, K. R. Kumpel, 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. 267:16396-16402.
57. Nayar, R., M. J. Hope, and P. R. Cullis. 1989. Generation of large unilamellar vesicles from long-chain saturated phosphatidylcholines by extrusion technique. Biochim. Biophys. Acta 986:200-206.
58. Nichols, J. W., and R. E. Pagano. 1982. Use of resonance energy transfer to study the kinetics of amphiphile transfer between vesicles. Biochemistry 21:1720-1726.
59. Nieva, J. L., and A. Agirre. 2003. Are fusion peptides a good model to study viral cell fusion? Biochim. Biophys. Acta 1614:104-115.
60. Nieva, J. L., S. Nir, A. Muga, F. M. Goni, and J. Wilschut. 1994. Interaction of the HIV-1 fusion peptide with phospholipid vesicles: different structural requirements for fusion and leakage. Biochemistry 33:3201-3209.
61. Peiris, J. S., S. T. Lai, L. L. Poon, Y. Guan, L. Y. Yam, W. Lim, J. Nicholls, W. K. Yee, W. W. Yan, M. T. Cheung, V. C. Cheng, K. H. Chan, D. N. Tsang, R. W. Yung, T. K. Ng, and K. Y. Yuen. 2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319-1325.
62. Peisajovich, S. G., and Y. Shai. 2003. Viral fusion proteins: multiple regions contribute to membrane fusion. Biochim. Biophys. Acta 1614:122-129.
63. Pereira, F. B., F. M. Goni, A. Muga, and J. L. Nieva. 1997. Permeabilization and fusion of uncharged lipid vesicles induced by the HIV-1 fusion peptide adopting an extended conformation: dose and sequence effects. Biophys. J. 73:1977-1986.
64. Pereira, F. B., J. M. Valpuesta, G. Basanez, F. M. Goni, and J. L. Nieva. 1999. Interbilayer lipid mixing induced by the human immunodeficiency virus type-1 fusion peptide on large unilamellar vesicles: the nature of the nonlamellar intermediates. Chem. Phys. Lipids 103:11-20.
65. Pritsker, M., J. Rucker, T. L. Hoffman, R. W. Doms, and Y. Shai. 1999. Effect of nonpolar substitutions of the conserved Phe11 in the fusion peptide of HIV-1 gp41 on its function, structure, and organization in membranes. Biochemistry 38:11359-11371.
66. Rafalski, M., J. D. Lear, and W. F. DeGrado. 1990. Phospholipid interactions of synthetic peptides representing the N-terminus of HIV gp41. Biochemistry 29:7917-7922.
67. Rafalski, M., A. Ortiz, A. Rockwell, L. C. van Ginkel, J. D. Lear, W. F. DeGrado, and J. Wilschut. 1991. Membrane fusion activity of the influenza virus hemagglutinin: interaction of HA2 N-terminal peptides with phospholipid vesicles. Biochemistry 30:10211-10220.
68. Rausch, J. M., and W. C. Wimley. 2001. A high-throughput screen for identifying transmembrane pore-forming peptides. Anal. Biochem. 293:258-263.
69. Rockwell, N. C., D. J. Krysan, T. Komiyama, and R. S. Fuller. 2002. Precursor processing by kex2/furin proteases. Chem. Rev. 102:4525-4548.
70. Rota, P. A., M. S. Oberste, S. S. Monroe, W. A. Nix, R. Campagnoli, J. P. Icenogle, S. Penaranda, B. Bankamp, K. Maher, M. H. Chen, S. Tong, A. Tamin, L. Lowe, M. Frace, J. L. DeRisi, Q. Chen, D. Wang, D. D. Erdman, T. C. Peret, C. Burns, T. G. Ksiazek, P. E. Rollin, A. Sanchez, S. Liffick, B. Holloway, J. Limor, K. McCaustland, M. Olsen-Rasmussen, R. Fouchier, S. Gunther, A. D. Osterhaus, C. Drosten, M. A. Pallansch, L. J. Anderson, and W. J. Bellini. 2003. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300:1394-1399.
71. Ruiz-Arguello, M. B., F. M. Goni, F. B. Pereira, and J. L. Nieva. 1998. Phosphatidylinositol-dependent membrane fusion induced by a putative fusogenic sequence of Ebola virus. J. Virol. 72:1775-1781.
72. Saez-Cirion, A., M. J. Gomara, A. Agirre, and J. L. Nieva. 2003. Pre-transmembrane sequence of Ebola glycoprotein. Interfacial hydrophobiciry distribution and interaction with membranes. FEBS Lett. 533:47-53.
73. Saez-Cirion, A., and J. L. Nieva. 2002. Conformational transitions of membrane-bound HIV-1 fusion peptide. Biochim. Biophys. Acta 1564:57-65.
74. 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 44:947-958.
75. Spaan, W., D. Cavanagh, and M. C. Horzinek. 1988. Coronaviruses: structure and genome expression. J. Gen. Virol. 69:2939-2952.
76. Stauber, R., M. Pfleiderer, and S. Siddell. 1993. Proteolytic cleavage of the murine coronavirus surface glycoprotein is not required for its fusion activity. Adv. Exp. Med. Biol. 342:165-170.
77. 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. 74:183-191.
78. Struck, D. K., D. Hoekstra, and R. E. Pagano. 1981. Use of resonance energy transfer to monitor membrane fusion. Biochemistry 20:4093-4099.
79. Suarez, T., W. R. Gallaher, A. Agirre, F. M. Goni, and J. L. Nieva. 2000. Membrane interface-interacting sequences within the ectodomain of the human immunodeficiency virus type 1 envelope glycoprotein: putative role during viral fusion. J. Virol. 74:8038-8047.
80. Suarez, T., M. J. Gomara, F. M. Goni, I. Mingarro, A. Muga, E. Perez-Paya, and J. L. Nieva. 2003. Calcium-dependent conformational changes of membrane-bound Ebola fusion peptide drive vesicle fusion. FEBS Lett. 535:23-28.
81. Suarez, T., S. Nir, F. M. Goni, A. Saez-Cirion, and J. L. Nieva. 2000. The pre-transmembrane region of the human immunodeficiency virus type-1 glycoprotein: a novel fusogenic sequence. FEBS Lett. 477:145-149.
82. Taguchi, F. 1993. Fusion formation by the uncleaved spike protein of murine coronavirus JHMV variant cl-2. J. Virol. 67:1195-1202.
83. Taguchi, F. 1995. The S2 subunit of the murine coronavirus spike protein is not involved in receptor binding. J. Virol. 69:7260-7263.
84. Taguchi, F., and Y. K. Shimazaki. 2000. Functional analysis of an epitope in the S2 subunit of the murine coronavirus spike protein: involvement in fusion activity. J. Gen. Virol. 81:2867-2871.
85. Tripet, B., M. W. Howard, M. Johling, 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. 279:20836-20849.
86. Wang, P., J. Chen, A. Zheng, Y. Nie, X. Shi, W. Wang, G. Wang, M. Luo, H. Liu, L. Tan, X. Song, Z. Wang, X. Yin, X. Qu, X. Wang, T. Qing, M. Ding, and H. Deng. 2004. Expression cloning of functional receptor used by SARS coronavirus. Biochem. Biophys. Res. Commun. 315:439-444.
87. Weissenhorn, W., A. Carfi, K. H. Lee, J. J. Skehel, and D. C. Wiley. 1998. Crystal structure of the Ebola virus membrane fusion subunit, GP2, from the envelope glycoprotein ectodomain. Mol. Cell 2:605-616.
88. Weissenhorn, W., A. Dessen, S. C. Harrison, J. J. Skehel, and D. C. Wiley. 1997. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387:426-430.
89. White, J., M. Kielian, and A. Helenius. 1983. Membrane fusion proteins of enveloped animal viruses. Q. Rev. Biophys. 16:151-195.
90. White, J. M. 1992. Membrane fusion. Science 258:917-924.
91. White, S. H., and W. C. Wimley. 1999. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:319-365.
92. While, S. H., W. C. Wimley, A. S. Ladokhin, and K. Hristova. 1998. Protein folding in membranes: determining energetics of peptide-bilayer interactions. Methods Enzymol. 295:62-87.
93. 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 289:366-373.
94. Wimley, W. C., K. Hristova, A. S. Ladokhin, L. Silvestro, P. H. Axelsen, and S. H. White. 1998. Folding of beta-sheet membrane proteins: a hydrophobic hexapeptide model. J. Mol. Biol. 277:1091-1110.
95. Wimley, W. C., and S. H. White. 1996. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3:842-848.
96. Wong, S. K., W. Li, M. J. Moore, H. Choe, and M. Farzan. 2004. A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2. J. Biol. Chem. 279:3197-3201.
97. Wu, X. D., B. Shang, R. F. Yang, H. Yu, Z. H. Ma, X. Shen, Y. Y. Ji, Y. Lin, Y. D. Wu, G. M. Lin, L. Tian, X. Q. Gan, S. Yang, W. H. Jiang, E. H. Dai, X. Y. Wang, H. L. Jiang, Y. H. Xie, X. L. Zhu, G. Pei, L. Li, J. R. Wu, and B. Sun. 2004. The spike protein of severe acute respiratory syndrome (SARS) is cleaved in virus infected Vero-E6 cells. Cell Res. 14:400-406.
98. 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. 279:30514-30522.
99. 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. 279:49414-49419.
100. Zhu, J., G. Xiao, Y. Xu, F. Yuan, C. Zheng, Y. Liu, H. Yan, D. K. Cole, J. I. Bell, Z. Rao, P. Tien, and G. F. Gao. 2004. Following the rule: formation of the 6-helix bundle of the fusion core from severe acute respiratory syndrome coronavirus spike protein and identification of potent peptide inhibitors. Biochem. Biophys. Res. Commun. 319:283-288.