The many mechanisms of viral membrane fusion proteins

Current Topics in Microbiology and Immunology

Volumn 285, Issue , 2004, Pages 25-66

  Earp, L J ^a   Delos, S E ^b   Park, H E ^a   White, J M ^b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Anti fusion antivirals; Class I fusion protein; Class II fusion protein; Conformational changes; HIV Env; Influenza HA; Low pH activation; Membrane dynamics; Membrane fusion protein; Receptor activation

Indexed keywords

ENVELOPE PROTEIN; FUSION PEPTIDE; GLYCOPROTEIN GP 120; INFLUENZA VIRUS HEMAGGLUTININ; LIPID; MEMBRANE PROTEIN; PEPTIDE; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; CELL MEMBRANE; CONFORMATIONAL TRANSITION; CYTOPLASM; DISEASE CLASSIFICATION; DNA HELIX; LIPID BILAYER; MEMBRANE FLUIDITY; MEMBRANE FUSION; MOLECULAR DYNAMICS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STRUCTURE; REVIEW; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; VIRUS ACTIVATION; VIRUS ADSORPTION; VIRUS ENVELOPE; VIRUS FUSION; VIRUS GENOME; VIRUS INFECTION; VIRUS REPLICATION;

INFLUENZA VIRUS;

EID: 5644229850     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/3-540-26764-6_2     Document Type: Review

References (218)

1. Abrahamyan LG, Markosyan RM, Moore JP, Cohen FS, and Melikyan GB (2003) Human immunodeficiency virus type 1 Env with an intersubunit disulfide bond engages coreceptors but requires bond reduction after engagement to induce fusion. J Virol 77:5829-36
2. Aguilar HC, Anderson WF, and Cannon PM (2003) Cytoplasmic tail of moloney murine leukemia virus envelope protein influences the conformation of the extracellular domain: implications for the mechanism of action of the R peptide. J Virol 77:1281-1291
3. Ahn A, Gibbons DL, and Kielian M (2002) The fusion peptide of Semliki Forest virus associates with sterol-rich membrane domains. J Virol 76:3267-75
4. Ahn A, Klimjack MR, Chatterjee PK, and Kielian M (1999) An epitope of the Semliki Forest virus fusion protein exposed during virus-membrane fusion. J Virol 73:10029-39
5. Allison SL, Schalich J, Stiasny K, Mandl CW, Kunz C, and Heinz FX (1995) Oligomeric rearrangement of tick-borne encephalitis virus envelope proteins induced by an acidic pH. J Virol 69:695-700
6. Allison SL, Stiasny K, Stadler K, Mandl CW, and Heinz FX (1999) Mapping of functional elements in the stem-anchor region of tick-borne encephalitis virus envelope protein E. J Virol 73:5605-12
7. Allison SL, Schalich J, Stiasny K, Mandl CW, and Heinz FX (2001) Mutational evidence for an internal fusion peptide in flavivirus envelope protein E. J Virol 75:4268-75
8. Armstrong RT, Kushnir AS, and White JM (2000) The transmembrane domain of influenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transition. J Cell Biol 151:425-38
9. Bagai S and Lamb RA (1995) Quantitative measurement of paramyxovirus fusion: differences in requirements of glycoproteins between simian virus 5 and human parainfluenza virus 3 or Newcastle disease virus. J Virol 69:6712-9
10. Baker KA, Dutch RE, Lamb RA, and Jardetzky TS (1999) Structural basis for paramyxovirus-mediated membrane fusion. Mol Cell 3:309-19
11. Barbey-Martin C, Gigant B, Bizebard T, Calder LJ, Wharton SA, Skehel JJ, and Knossow M (2002) An antibody that prevents the hemagglutinin low pH fusogenic transition. Virology 294:70-4
12. Barbouche R, Miquelis R, Jones IM, and Fenouillet E (2003) Protein-disulfide isomerase-mediated reduction of two disulfide bonds of HIV envelope glycoprotein 120 occurs post-CXCR4 binding and is required for fusion. J Biol Chem 278:3131-3136
13. Barnett AL, and Cunningham JM (2001) Receptor binding transforms the surface subunit of the mammalian C-type retrovirus envelope protein from an inhibitor to an activator effusion. J Virol 75:9096-105
14. Begona Ruiz-Arguello M, Gonzalez-Reyes L, Calder LJ, Palomo C, Martin D, Saiz MJ, Garcia-Barreno B, Skehel JJ, and Melero JA (2002) Effect of proteolytic processing at two distinct sites on shape and aggregation of an anchorless fusion protein of human respiratory syncytial virus and fate of the intervening segment. Virology 298:317-26
15. Blumenthal R, Sarkar DP, Durell S, Howard DE, and Morris SJ (1996) Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events. J Cell Biol 135:63-71
16. Bobkova M, Stitz J, Engelstadter M, Cichutek K, and Buchholz CJ (2002) Identification of R-peptides in envelope proteins of C-type retroviruses. J Gen Virol 83:2241-6
17. Bodian DL, Yamasaki RB, Buswell RL, Stearns JF, White JM, and Kuntz ID (1993) Inhibition of the fusion-inducing conformational change of influenza hemagglutinin by benzoquinones and hydroquinones. Biochemistry 32:2967-78
18. Borrego-Diaz E, Peeples ME, Markosyan RM, Melikyan GB, and Cohen FS (2003) Completion of trimeric hairpin formation of influenza virus hemagglutinin promotes fusion pore opening and enlargement. Virology 316:234-44
19. Bosch BJ, Zee R van der, Haan CA de, and Rottier PJ (2003) The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J Virol 77:8801-11
20. Bossart KN, Wang LF, Flora MN, Chua KB, Lam SK, Eaton BT, and Broder CC (2002) Membrane fusion tropism and heterotypic functional activities of the nipah virus and hendra virus envelope glycoproteins. J Virol 76:11186-11198
21. Bressanelli S, Stiasny K, Allison SL, Stura EA, Duquerroy S, Lescar J, Heinz FX, and Ray FA (2004) Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J 23:728-38
22. Bron R, Wahlberg JM, Garoff H, and Wilschut J (1993) Membrane fusion of Semliki Forest virus in a model system: correlation between fusion kinetics and structural changes in the envelope glycoprotein. EMBO J 12:693-701
23. Brown DA and London E (2000) Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 275:17221-4
24. Bullough PA, Hughson FM, Skehel JJ, and Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37-43
25. Calder LJ, Gonzalez-Reyes L, Garcia-Barreno B, Wharton SA, Skehel JJ, Wiley DC, and Melero JA (2000) Electron microscopy of the human respiratory syncytial virus fusion protein and complexes that it forms with monoclonal antibodies. Virology 271:122-31
26. Carr CM, Chaudhry C, and Kim PS (1997) Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc Natl Acad Sci USA 94:14306-13
27. Carr CM and Kim PS (1993) A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73:823-32
28. Cathomen T, Naim HY, and Cattaneo R (1998) Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J Virol 72:1224-34
29. Chan DC, Pass D, Berger JM, and Kim PS (1997) Core structure of gp41 from the HIV envelope glycoprotein. Cell 89:263-73
30. Chan DC and Kim PS (1998) HIV entry and its inhibition. Cell 93:681-4
31. Chen J, Lee KH, Steinhauer DA, Stevens DJ, Skehel JJ, and Wiley DC (1998) Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 95:409-17
32. Chen J, Skehel JJ, and Wiley DC (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 96:8967-72
33. Chen L, German JJ, McKimm-Breschkin J, Lawrence LJ, Tulloch PA, Smith BJ, Colman PM, and Lawrence MC (2001a) The structure of the fusion glycoprotein of Newcastle disease virus suggests a novel paradigm for the molecular mechanism of membrane fusion. Structure 9:255-66
34. Chen SS, Lee SF, and Wang CT (2001b) Cellular membrane-binding ability of the C-terminal cytoplasmic domain of human immunodeficiency virus type 1 envelope transmembrane protein gp41. J Virol 75:9925-38
35. Cianci C, Yu KL, Dischino DD, Harte W, Deshpande M, Luo G, Colonno RJ, Meanwell NA, and Krystal M (1999) pH-dependent changes in photoaffinity labeling patterns of the H1 influenza virus hemagglutinin by using an inhibitor of viral fusion. J Virol 73:1785-94
36. Cleverley DZ and Lenard J (1998) The transmembrane domain in viral fusion: essential role for a conserved glycine residue in vesicular stomatitis virus G protein. Proc Natl Acad Sci USA 95:3425-30
37. Colman PM and Lawrence MC (2003) The structural biology of type I viral membrane fusion. Nat Rev Mol Cell Biol 4:309-19
38. Corver J, Ortiz A, Allison SL, Schalich J, Heinz FX, and Wilschut J (2000) Membrane fusion activity of tick-borne encephalitis virus and recombinant subviral particles in a liposomal model system. Virology 269:37-46
39. Damico RL, Crane J, and Bates P (1998) Receptor-triggered membrane association of a model retroviral glycoprotein. Proc Natl Acad Sci USA 95:2580-5
40. Danieli T, Pelletier SL, Henis YI, and White JM (1996) Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. J Cell Biol 133:559-69
41. Debnath AK, Radigan L, and Jiang S (1999) Structure-based identification of small molecule antiviral compounds targeted to the gp41 core structure of the human immunodeficiency virus type 1. J Med Chem 42:3203-9
42. Delos SE, Gilbert JM, and White JM (2000) The central proline of an internal viral fusion peptide serves two important roles. J Virol 74:1686-93
43. Delos SE and White JM (2000) Critical role for the cysteines flanking the internal fusion peptide of avian sarcoma/leukosis virus envelope glycoprotein. J Virol 74:9738-41
44. Deng R, Wang Z, Mahon PJ, Marinello M, Mirza A, and Iorio RM (1999) Mutations in the Newcastle disease virus hemagglutinin-neuraminidase protein that interfere with its ability to interact with the homologous F protein in the promotion of fusion. Virology 253:43-54
45. Dennison SM, Greenfield N, Lenard J, and Lentz BR (2002) VSV transmembrane domain (TMD) peptide promotes PEG-mediated fusion of liposomes in a conformationally sensitive fashion. Biochemistry 41:14925-14934
46. Di Simone C and Buchmeier MJ (1995) Kinetics and pH dependence of acid-induced structural changes in the lymphocytic choriomeningitis virus glycoprotein complex. Virology 209:3-9
47. Doms RW, Helenius A, and White J (1985) Membrane fusion activity of the influenza virus hemagglutinin. The low pH-induced conformational change. J Biol Chem 260:2973-81
48. Duffus WA, Levy-Mintz P, Klimjack MR, and Kielian M (1995) Mutations in the putative fusion peptide of Semliki Forest virus affect spike protein oligomerization and virus assembly. J Virol 69:2471-9
49. Durell SR, Martin I, Ruysschaert JM, Shai Y, and Blumenthal R (1997) What studies of fusion peptides tell us about viral envelope glycoprotein-mediated membrane fusion. Mol Membr Biol 14:97-112
50. Dutch RE and Lamb RA (2001) Deletion of the cytoplasmic tail of the fusion protein of the paramyxovirus simian virus 5 affects fusion pore enlargement. J Virol 75:5363-9
51. Earp LJ, Delos SE, Netter RC, Bates P, and White JM (2003) The avian retrovirus avian sarcoma/leukosis virus subtype A reaches the lipid mixing stage of fusion at neutral pH. J Virol 77:3058-3066
52. Eckert DM and Kim PS (2001) Mechanisms of viral membrane fusion and its inhibition. Annu Rev Biochem 70:777-810
53. Eckert DM, Malashkevich VN, Hong LH, Carr PA, and Kim PS (1999) Inhibiting HIV-1 entry: discovery of D-peptide inhibitors that target the gp41 coiled-coil pocket. Cell 99:103-15
54. Edwards TG, Wyss S, Reeves JD, Zolla-Pazner S, Hoxie JA, Doms RW, and Baribaud F (2002) Truncation of the cytoplasmic domain induces exposure of conserved regions in the ectodomain of human immunodeficiency virus type 1 envelope protein. J Virol 76:2683-91
55. Einfeld DA and Hunter E (1994) Expression of the TM protein of Rous sarcoma virus in the absence of SU shows that this domain is capable of oligomerization and intracellular transport. J Virol 68:2513-20
56. Fackler OT and Peterlin BM (2000) Endocytic entry of HIV-1. Curr Biol 10:1005-8
57. Feng Y, Broder CC, Kennedy PE, and Berger EA (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872-7
58. Fenouillet E, Barbouche R, Courageot J, and Miquelis R (2001) The catalytic activity of protein disulfide isomerase is involved in human immunodeficiency virus envelope-mediated membrane fusion after CD4 cell binding. J Infect Dis 183:744-52
59. Ferlenghi I, Clarke M, Ruttan T, Allison SL, Schalich J, Heinz FX, Harrison SC, Rey F, and Fuller SD (2001) Molecular organization of a recombinant subviral particle from tick-borne encephalitis virus. MoI Cell 7:593-602
60. Ferrer M, Kapoor TM, Strassmaier T, Weissenhorn W, Skehel JJ, Oprian D, Schreiber SL, Wiley DC, and Harrison SC (1999) Selection of gp41-mediated HIV-1 cell entry inhibitors from biased combinatorial libraries of non-natural binding elements. Nat Struct Biol 6:953-60
61. Fischer C, Schroth-Diez B, Herrmann A, Garten W, and Klenk HD (1998) Acylation of the influenza hemagglutinin modulates fusion activity. Virology 248:284-94
62. Fredericksen BL and Whitt MA (1995) Vesicular stomatitis virus glycoprotein mutations that affect membrane fusion activity and abolish virus infectivity. J Virol 69:1435-43
63. Freed EO, Delwart EL, Buchschacher GLJ, and Panganiban AT (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: 70-4
64. Freed EO and Martin MA (1996) Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J Virol 70:341-51
65. Frey S, Marsh M, Gunther S, Pelchen-Matthews A, Stephens P, Ortlepp S, and Stegmann T (1995) Temperature dependence of cell-cell fusion induced by the envelope glycoprotein of human immunodeficiency virus type 1. J Virol 69:1462-72
66. Fujii G, Horvath S, Woodward S, Eiserling F, and Eisenberg D (1992) A molecular model for membrane fusion based on solution studies of an amphiphilic peptide from HIV gp41. Protein Sci 1:1454-64
67. Furuta RA, Wild CT, Weng Y, and Weiss CD (1998) Capture of an early fusion-active conformation of HIV-1 gp41. Nat Struct Biol 5:276-9
68. Gallina A, Hanley TM, Mandel R, Trahey M, Broder CC, Viglianti GA, and Ryser HJ (2002) Inhibitors of protein-disulfide isomerase prevent cleavage of disulfide bonds in receptor-bound glycoprotein 120 and prevent HIV-1 entry. J Biol Chem 277:50579-88
69. Gaudin Y, de Kinkelin P, and Benmansour A (1999a) Mutations in the glycoprotein of viral haemorrhagic septicaemia virus that affect virulence for fish and the pH threshold for membrane fusion. J Gen Virol 80:1221-9
70. Gaudin Y, Tuffereau C, Durrer P, Brunner J, Flamand A, and Ruigrok R (1999b) Rabies virus-induced membrane fusion. Mol Membr Biol 16:21-31
71. Gawrisch K, Han KH, Yang JS, Bergelson LD, and Ferretti JA (1993) Interaction of peptide fragment 828-848 of the envelope glycoprotein of human immunodeficiency virus type I with lipid bilayers. Biochemistry 32:3112-8
72. Gething MJ, Doms RW, York D, and White J (1986) Studies on the mechanism of membrane fusion: site-specific mutagenesis of the hemagglutinin of influenza virus. J Cell Biol 102:11-23
73. Gibbons DL, Vaney MC, Roussel A, Vigoureux A, Reilly B, Lepault J, Kielian M, and Rey FA (2004) Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 427:320-25
74. Gilbert JM, Mason D, and White JM (1990) Fusion of Rous sarcoma virus with host cells does not require exposure to low pH. J Virol 64:5106-13
75. Godley L, Pfeifer J, Steinhauer D, Ely B, Shaw G, Kaufmann R, Suchanek E, Pabo C, Skehel JJ, and Wiley DC (1992) Introduction of intersubunit disulfide bonds in the membrane-distal region of the influenza hemagglutinin abolishes membrane fusion activity. Cell 68:635-45
76. Golding H, Zaitseva M, de Rosny E, King LR, Manischewitz J, Sidorov I, Gorny MK, Zolla-Pazner S, Dimitrov DS, and Weiss C (2002) Dissection of human immunodeficiency virus type 1 entry with neutralizing antibodies to gp41 fusion intermediates. J Virol 76:6780-90
77. Gollins SW and Porterfield JS (1986) A new mechanism for the neutralization of enveloped viruses by antiviral antibody. Nature 321:244-6
78. Gonzalez-Reyes L, Ruiz-Arguello MB, Garcia-Barreno B, Calder L, Lopez JA, Albar JP, Skehel JJ, Wiley DC, and Melero JA (2001) Cleavage of the human respiratory syncytial virus fusion protein at two distinct sites is required for activation of membrane fusion. Proc Natl Acad Sci USA 98:9859-64
79. Gruenke JA, Armstrong RT, Newcomb WW, Brown JC, and White JM (2002) New insights into the spring-loaded conformational change of influenza hemagglutinin. J Virol 76:4456-66
80. Gunther-Ausborn S, Schoen P, Bartoldus I, Wilschut J, and Stegmann T (2000) Role of hemagglutinin surface density in the initial stages of influenza virus fusion: lack of evidence for cooperativity. J Virol 74:2714-20
81. Haffar OK, Dowbenko DJ, and Berman PW (1991) The cytoplasmic tail of HIV-1 gp160 contains regions that associate with cellular membranes. Virology 180:439-41
82. Han X, Bushweller JH, Cafiso DS, and Tamm LK (2001) Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat Struct Biol 8:715-20
83. He Y, Vassell R, Zaitseva M, Nguyen N, Yang Z, Weng Y, and Weiss C (2003) Peptides trap the human immunodeficiency virus type 1 envelope glycoprotein fusion intermediate at two sites. J Virol 77:1666-1671
84. Heinz FX and Allison SL (2001) The machinery for flavivirus fusion with host cell membranes. Curr Opin Microbiol 4:450-5
85. Helenius A (1995) Alphavirus and flavivirus glycoproteins: structures and functions Cell 81:651-3
86. Hernandez LD, Hoffman LR, Wolfsberg TG, and White JM (1996) Virus-cell and cell-cell fusion. Annu Rev Cell Dev Biol 12:627-61
87. Hernandez LD, Peters RJ, Delos SE, Young JA, Agard DA, and White JM (1997) Activation of a retroviral membrane fusion protein: soluble receptor-induced liposome binding of the ALSV envelope glycoprotein. J Cell Biol 139:1455-64
88. Hernandez LD and White JM (1998) Mutational analysis of the candidate internal fusion peptide of the avian leukosis and sarcoma virus subgroup A envelope glycoprotein. J Virol 72:3259-67
89. Hoffman LR, Kuntz ID, and White JM (1997) Structure-based identification of an inducer of the low-pH conformational change in the influenza virus hemagglutinin: irreversible inhibition of infectivity. J Virol 71:8808-20
90. Hunter E (1997) Viral entry and receptors. In J. M. Coffin (ed.), Retroviruses. Cold Spring Harbor Laboratory Press, Plainview, NY, p. 71-121
91. Irurzun A, Nieva JL, and Carrasco L (1997) Entry of Semliki forest virus into cells: effects of concanamycin A and nigericin on viral membrane fusion and infection. Virology 227:488-92
92. Ito H, Watanabe S, Sanchez A, Whitt MA, and Kawaoka Y (1999) Mutational analysis of the putative fusion domain of Ebola virus glycoprotein. J Virol 73:8907-12
93. Jahn R, Lang T, and Sudhof TC (2003) Membrane fusion. Cell 112:519-533
94. Januszeski MM, Cannon PM, Chen D, Rozenberg Y, and Andersen WF (1997) Functional analysis of the cytoplasmic tail of Moloney murine leukemia virus envelope protein. J Virol 71:3613-9
95. Jeffers SA, Sanders DA, and Sanchez A (2002) Covalent modifications of the ebola virus glycoprotein. J Virol 76:12463-72
96. Jiang S, Zhao Q, and Debnath AK (2002) Peptide and non-peptide HIV fusion inhibitors. Curr Pharm Des 8:563-80
97. Joshi SB, Dutch RE, and Lamb RA (1998) A core trimer of the paramyxovirus fusion protein: parallels to influenza virus hemagglutinin and HIV-1 gp41. Virology 248:20-34
98. Kamath S and Wong TC (2002) Membrane structure of the human immunodeficiency virus gp41 fusion domain by molecular dynamics simulation. Biophys J 83: 135-43
99. Kanaseki T, Kawasaki K, Murata M, Ikeuchi Y, and Ohnishi S (1997) Structural features of membrane fusion between influenza virus and liposome as revealed by quick-freezing electron microscopy. J Cell Biol 137:1041-56
100. Kemble GW, Bodian DL, Rose J, Wilson IA, and White JM (1992) Intermonomer disulfide bonds impair the fusion activity of influenza virus hemagglutinin. J Virol 66:4940-50
101. Kemble GW, Danieli T, and White JM (1994) Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76:383-91
102. Kielian M (1995) Membrane fusion and the alphavirus life cycle. Adv Virus Res 45:113-51
103. Kielian M, Klimjack MR, Ghosh S, and Duffus WA (1996) Mechanisms of mutations inhibiting fusion and infection by Semliki Forest virus. J Cell Biol 134:863-72
104. Kielian M, Chatterjee PK, Gibbons DL, and Lu YE (2000) Specific roles for lipids in virus fusion and exit. Examples from the alphaviruses. Subcell Biochem 34:409-55
105. Kilby JM, Hopkins S, Venetta TM, DiMassimo B, Cloud GA, Lee JY, Alldredge L, Hunter E, Lambert D, Bolognesi D, Matthews T, Johnson MR, Nowak MA, Shaw GM, and Saag MS (1998) Potent suppression of HIV-1 replication in humans by T-20, a peptide inhibitor of gp41-mediated virus entry. Nat Med 4:1302-7
106. Kim FJ, Manel N, Boublik Y, Battini JL, and Sitbon M (2003) Human T-cell leukemia virus type 1 envelope-mediated syncytium formation can be activated in resistant mammalian cell lines by a carboxy-terminal truncation of the envelope cytoplasmic domain. J Virol 77:963-969
107. Kliger Y, Aharoni A, Rapaport D, Jones P, Blumenthal R, and Shai Y (1997) Fusion peptides derived from the HIV type 1 glycoprotein 41 associate within phospholipid membranes and inhibit cell-cell fusion. Structure-function study. J Biol Chem 272:13496-505
108. Kliger Y, Gallo SA, Peisajovich SG, Munoz-Barroso I, Avkin S, Blumenthal R, and Shai Y (2001) Mode of action of an antiviral peptide from HIV-1. Inhibition at a post-lipid mixing stage. J Biol Chem 276:1391-7
109. Kliger Y and Shai Y (1997) A leucine zipper-like sequence from the cytoplasmic tail of the HIV-1 envelope glycoprotein binds and perturbs lipid bilayers. Biochemistry 36:5157-69
110. Korte T, Ludwig K, Booy FP, Blumenthal R, and Herrmann A (1999) Conformational intermediates and fusion activity of influenza virus hemagglutinin. J Virol 73: 4567-74
111. Kozak SL, Heard JM, and Rabat D (2002) Segregation of CD4 and CXCR4 into distinct lipid microdomains in T lymphocytes suggests a mechanism for membrane destabilization by human immunodeficiency virus. J Virol 76:1802-15
112. Kozerski C, Ponimaskin E, Schroth-Diez B, Schmidt MF, and Herrmann A (2000) Modification of the cytoplasmic domain of influenza virus hemagglutinin affects enlargement of the fusion pore. J Virol 74:7529-37
113. Kozlov MM and Chernomordik LV (2002) The protein coat in membrane fusion: lessons from fission. Traffic 3:256-67
114. Kozlovsky Y and Kozlov MM (2002) Stalk model of membrane fusion: solution of energy crisis. Biophys J 82:882-95
115. Kuhn RJ, Zhang W, Rossmann MG, Pletnev SV, Corver J, Lenches E, Jones CT, Mukhopadhyay S, Chipman PR, Strauss EG, Baker TS, and Strauss JH (2002) Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108:717-25
116. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, and Hendrickson W (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648-59
117. Lamb RA (1993) Paramyxovirus fusion: a hypothesis for changes. Virology 197:1-11
118. Lambert DM, Barney S, Lambert AL, Guthrie K, Medinas R, Davis DE, Bucy T, Erickson J, Merutka G, and Petteway SRJ (1996) Peptides from conserved regions of paramyxovirus fusion (F) proteins are potent inhibitors of viral fusion. Proc Natl Acad Sci USA 93:2186-91
119. Lavillette D, Boson B, Russell SJ, and Cosset FL (2001) Activation of membrane fusion by murine leukemia viruses is controlled in cis or in trans by interactions between the receptor-binding domain and a conserved disulfide loop of the carboxy terminus of the surface glycoprotein. J Virol 75:3685-95
120. Lavillette D, Maurice M, Roche C, Russell SJ, Sitbon M, and Cosset FL (1998) A proline-rich motif downstream of the receptor binding domain modulates conformation and fusogenicity of murine retroviral envelopes. J Virol 72:9955-65
121. Lescar J, Roussel A, Wien MW, Navaza J, Fuller SD, Wengler G, and Rey FA (2001) The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105:137-48
122. Li M, Yang C, and Compans RW (2001) Mutations in the cytoplasmic tail of murine leukemia virus envelope protein suppress fusion inhibition by R peptide. J Virol 75:2337-44
123. Li Y, Drone C, Sat E, and Ghosh HP (1993) Mutation analysis of the vesicular stomatitis virus glycoprotein G for membrane fusion domains. J Virol 67:4070-7
124. Li Y, Han X, and Tamm LK (2003) Thermodynamics of fusion peptide-membrane interactions. Biochemistry 42:7245-51
125. Lu M, Blacklow SC, and Kim PS (1995) A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat Struct Biol 2:1075-82
126. Luciw PA, Shaw KE, Shacklett BL, and Marthas ML (1998) Importance of the intracytoplasmic domain of the simian immunodeficiency virus (SIV) envelope glycoprotein for pathogenesis. Virology 252:9-16
127. Markosyan RM, Cohen FS, and Melikyan GB (2003) HIV-1 envelope proteins complete their folding into six-helix bundles immediately after fusion pore formation. Mol Biol Cell 14:926-38
128. Markovic I, Leikina E, Zhukovsky M, Zimmerberg J, and Chernomordik LV (2001) Synchronized activation and refolding of influenza hemagglutinin in multimeric fusion machines. J Cell Biol 155:833-44
129. Markovic I, Pulyaeva H, Sokoloff A, and Chernomordik LV (1998) Membrane fusion mediated by baculovirus gp64 involves assembly of stable gp64 trimers into multiprotein aggregates. J Cell Biol 143:1155-66
130. Martin I and Ruysschaert JM (2000) Common properties of fusion peptides from diverse systems. Biosci Rep 20:483-500
131. Martin II, Ruysschaert J, and Epand RM (1999) Role of the N-terminal peptides of viral envelope proteins in membrane fusion. Adv Drug Deliv Rev 38:233-255
132. Matsuyama S, Delos SE, and White JM (2004) Sequential roles of receptor binding and low pH in forming prehairpin and hairpin conformations of an avian retroviral envelope glycoprotein. J Virol (in press)
133. McClure MO, Sommerfell MA, Marsh M, and Weiss RA (1990) The pH independence of mammalian retrovirus infection. J Gen Virol 71:767-73
134. McGinnes LW, Gravel K, and Morrison TG (2002) Newcastle disease virus HN protein alters the conformation of the F protein at cell surfaces. J Virol 76:12622-33
135. Melikyan GB, Brener SA, Ok DC, and Cohen FS (1997a) Inner but not outer membrane leaflets control the transition from glycosylphosphatidylinositol- anchored influenza hemagglutinin-induced hemifusion to full fusion. J Cell Biol 136:995-1005
136. Melikyan GB, Jin H, Lamb RA, and Cohen FS (1997b) The role of the cytoplasmic tail region of influenza virus hemagglutinin in formation and growth of fusion pores. Virology 235:118-28
137. Melikyan GB, Markosyan RM, Hemmati H, Delmedico MK, Lambert DM, and Cohen FS (2000a) Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion. J Cell Biol 151:413-23
138. Melikyan GB, Markosyan RM, Roth MG, and Cohen FS (2000b) A point mutation in the transmembrane domain of the hemagglutinin of influenza virus stabilizes a hemifusion intermediate that can transit to fusion. Mol Biol Cell 11:3765-75
139. Modis Y, Ogata S, Clements D, and Harrison SC (2004) Structure of the dengue virus envelope protein after membrane fusion. Nature 427:313-9
140. Mothes W, Boerger AL, Narayan S, Cunningham JM, and Young JA (2000) Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. Cell 103:679-89
141. Munoz-Barroso I, Durell S, Sakaguchi K, Appella E, and Blumenthal R (1998) Dilation of the human immunodeficiency virus-1 envelope glycoprotein fusion pore revealed by the inhibitory action of a synthetic peptide from gp41. J Cell Biol 140:315-23
142. Munoz-Barroso I, Salzwedel K, Hunter E, and Blumenthal R (1999) Role of the membrane-proximal domain in the initial stages of human immunodeficiency virus type 1 envelope glycoprotein-mediated membrane fusion. J Virol 73:6089-92
143. Netter RC (2002) Ph.D Dissertation. University of Pennsylvania.
144. Nir S, Duzgunes N, de Lima MC, and Hoekstra D (1990) Fusion of enveloped viruses with cells and liposomes. Activity and inactivation. Cell Biophys 17:181-201
145. Nussbaum O, Broder CC, and Berger EA (1994) Fusogenic mechanisms of enveloped-virus glycoproteins analyzed by a novel recombinant vaccinia virus-based assay quantitating cell fusion-dependent reporter gene activation. J Virol 68:5411-22
146. Ohuchi M, Ohuchi R, Sakai T, and Matsumoto A (2002) Tight binding of influenza virus hemagglutinin to its receptor interferes with fusion pore dilation. J Virol 76:1405-13
147. Owens RJ, Burke C, and Rose JK (1994) Mutations in the membrane-spanning domain of the human immunodeficiency virus envelope glycoprotein that affect fusion activity. J Virol 68:570-4
148. Park HE, Gruenke JA, and White JM (2003) Leash in the groove mechanism of membrane fusion. Nat Struct Biol 10:1048-53
149. Paterson RG, Russell CJ, and Lamb RA (2000) Fusion protein of the paramyxovirus SV5: destabilizing and stabilizing mutants effusion activation. Virology 270:17-30
150. Pelkmans L and Helenius A (2003) Insider information: what viruses tell us about endocytosis. Curr Opin Cell Biol 15:414-22
151. Percherancier Y, Lagane B, Planchenault T, Staropoli I, Altmeyer R, Virelizier JL, Arenzana-Seisdedos F, Hoessli DC, and Bachelerie F (2003) HIV-I entry into T-cells is not dependent on CD4 and CCR5 localization to sphingolipid-enriched, detergent-resistant, raft membrane domains. J Biol Chem 278:3153-3161
152. Pereira FB, Goni FM, and Nieva JL (1995) Liposome destabilization induced by the HIV-I fusion peptide effect of a single amino acid substitution. FEBS Lett 362:243-6
153. Pietschmann T, Zentgraf H, Rethwilm A, and Lindemann D (2000) An evolutionary conserved positively charged amino acid in the putative membrane-spanning domain of the foamy virus envelope protein controls fusion activity. J Virol 74:4474-82
154. Piller SC, Dubay JW, Derdeyn CA, and Hunter E (2000) Mutational analysis of conserved domains within the cytoplasmic tail of gp41 from human immunodeficiency virus type 1: effects on glycoprotein incorporation and infectivity. J Virol 74:11717-23
155. Pinter A, Kopelman R, Li Z, Kayman SC, and Sanders DA (1997) Localization of the labile disulfide bond between SU and TM of the murine leukemia virus envelope protein complex to a highly conserved CWLC motif in SU that resembles the active-site sequence of thiol-disulfide exchange enzymes. J Virol 71:8073-7
156. Popik W, Alee TM, and Au WC (2002) Human immunodeficiency virus type 1 uses lipid raft-colocalized CD4 and chemokine receptors for productive entry into CD4(+) T cells. J Virol 76:4709-22
157. Puri A, Winick J, Lowy RJ, Covell D, Eidelman O, Walter A, and Blumenthal R (1988) Activation of vesicular stomatitis virus fusion with cells by pretreatment at low pH. J Biol Chem 263:4749-53
158. Qiao H, Armstrong RT, Melikyan GB, Cohen FS, and White JM (1999) A specific point mutant at position 1 of the influenza hemagglutinin fusion peptide displays a hemifusion phenotype. Mol Biol Cell 10:2759-69
159. Qiao H, Pelletier SL, Hoffman L, Hacker J, Armstrong RT, and White JM (1998) Specific single or double proline substitutions in the "spring-loaded" coiled-coil region of the influenza hemagglutinin impair or abolish membrane fusion activity. J Cell Biol 141:1335-47
160. Ragheb JA and Anderson WF (1994) pH-independent murine leukemia virus ecotropic envelope-mediated cell fusion: implications for the role of the R peptide and p12E TM in viral entry. J Virol 68:3220-31
161. Reeves JD, Gallo SA, Ahmad N, Miamidian JL, Harvey PE, Sharron M, Pohlman S, Sfakianos JN, Derdeyn CA, Blumenthal R, Hunter E, and Doms RW (2002) Sensitivity of HIV-1 to entry inhibitors correlates with envelope/coreceptor affinity, receptor density, and fusion kinetics. Proc Natl Acad Sci USA 99:16249-54
162. Rein A, Mirro J, Haynes JG, Ernst SM, and Nagashima K (1994) Function of the cytoplasmic domain of a retroviral transmembrane protein: p15E-p2E cleavage activates the membrane fusion capability of the murine leukemia virus Env protein. J Virol 68:1773-81
163. Rey FA, Heinz FX, Mandl C, Kunz C, and Harrison SC (1995) The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375:291-8
164. Rousso I, Mixon MB, Chen BK, and Kim PS (2000) Palmitoylation of the HIV-1 envelope glycoprotein is critical for viral infectivity. Proc Natl Acad Sci USA 97:13523-5
165. Russell CJ, Jardetzky TS, and Lamb RA (2001) Membrane fusion machines of paramyxoviruses: capture of intermediates effusion. EMBO J 20:4024-34
166. Saez-Cirion A, Gomara MJ, Agirre A, and Nieva JL (2003) Pre-transmembrane sequence of Ebola glycoprotein. Interfacial hydrophobicity distribution and interaction with membranes. FEBS Lett 533:47-53
167. Saez-Cirion A, Nir S, Lorizate M, Agirre A, Cruz A, Perez-Gil J, and Nieva JL (2002) Sphingomyelin and cholesterol promote HIV-1 gp41 pretransmembrane sequence surface aggregation and membrane restructuring. J Biol Chem 277:21776-85
168. Sakai T, Ohuchi R, and Ohuchi M (2002) Fatty acids on the A/USSR/77 influenza virus hemagglutinin facilitate the transition from hemifusion to fusion pore formation. J Virol 76:4603-11
169. Salzwedel K, West JT, and Hunter E (1999) A conserved tryptophan-rich motif in the membrane-proximal region of the human immunodeficiency virus type 1 gp41 ectodomain is important for Env-mediated fusion and virus infectivity. J Virol 73:2469-80
170. Schibli DJ, Montelaro RC, and Vogel HJ (2001) The membrane-proximal tryptophan-rich region of the HIV glycoprotein, gp41, forms a well-defined helix in dodecylphosphocholine micelles. Biochemistry 40:9570-8
171. Schmid E, Zurbriggen A, Gassen U, Rima B, ter Meulen V, and Schneider-Schaulies J (2000) Antibodies to CD9, a tetraspan transmembrane protein, inhibit canine distemper virus-induced cell-cell fusion but not virus-cell fusion. J Virol 74: 7554-61
172. Schoch C and Blumenthal R (1993) Role of the fusion peptide sequence in initial stages of influenza hemagglutinin-induced cell fusion. J Biol Chem 268:9267-74
173. Schultz A and Rein A (1985) Maturation of murine leukemia virus Env proteins in the absence of other viral proteins. Virology 145:335-9
174. Seth S, Vincent A, and Compans RW (2003) Mutations in the cytoplasmic domain of a paramyxovirus fusion glycoprotein rescue syncytium formation and eliminate the hemagglutinin-neuraminidase protein requirement for membrane fusion. J Virol 77:167-78
175. Shin JS and Abraham SN (2001) Caveolae as portals of entry for microbes. Microbes Infect 3:755-61
176. Sjoberg M and Garoff H (2003) Interactions between the transmembrane segments of the alphavirus E1 and E2 proteins play a role in virus budding and fusion. J Virol 77:3441-3450
177. Skehel JJ, Cross K, Steinhauer D, and Wiley DC (2001) Influenza fusion peptides. Biochem Soc Trans 29:623-6
178. Skehel JJ and Wiley DC (2000) Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69:531-69
179. Staschke KA, Hatch SD, Tang JC, Hornback WJ, Munroe JE, Colacino JM, and Muesing MA (1998) Inhibition of influenza virus hemagglutinin-mediated membrane fusion by a compound related to podocarpic acid. Virology 248:264-274
180. Stegmann T, Bartoldus I, and Zumbrunn J (1995) Influenza hemagglutinin-mediated membrane fusion: influence of receptor binding on the lag phase preceding fusion. Biochemistry 34:1825-32
181. Stegmann T, Booy FP, and Wilschut J (1987) Effects of low pH on influenza virus. Activation and inactivation of the membrane fusion capacity of the hemagglutinin. J Biol Chem 262:17744-9
182. Stein BS, Gowda SD, Lifson JD, Penhallow RC, Bensch KG, and Engleman EG (1987) pH-independent HIV entry into CD4-positive T cells via virus envelope fusion to the plasma membrane. Cell 49:659-68
183. Stiasny K, Allison SL, Mandl CW, and Heinz FX (2001) Role of metastability and acidic pH in membrane fusion by tick-borne encephalitis virus. J Virol 75:7392-7398
184. Stiasny K, Allison SL, Marchler-Bauer A, Kunz C, and Heinz FX (1996) Structural requirements for low-pH-induced rearrangements in the envelope glycoprotein of tick-borne encephalitis virus. J Virol 70:8142-8147
185. Stiasny K, Allison SL, Schalich J, and Heinz FX (2002) Membrane interactions of the tick-borne encephalitis virus fusion protein E at low pH. J Virol 76:3784-90
186. Stone-Hulslander J and Morrison TG (1997) Detection of an interaction between the HN and F proteins in Newcastle disease virus-infected cells. J Virol 71:6287-95
187. Suarez T, Gallaher WR, Agirre A, Goni FM, and Nieva JL (2000) Membrane interface-interacting sequences within the ectodomain of the human immunodeficiency virus type 1 envelope glycoprotein: putative role during viral fusion. J Virol 74:8038-47
188. Suomalainen M (2002) Lipid rafts and assembly of enveloped viruses. Traffic 3:705-9
189. Taguchi F and Matsuyama S (2002) Soluble receptor potentiates receptor-independent infection by murine coronavirus. J Virol 76:950-8
190. Takimoto T, Taylor GL, Connaris HC, Crennell SJ, and Portner A (2002) Role of the hemagglutinin-neuraminidase protein in the mechanism of paramyxovirus-cell membrane fusion. J Virol 76:13028-33
191. Tamm LK and Han X (2000) Viral fusion peptides: a tool set to disrupt and connect biological membranes. Biosci Rep 20:501-18
192. Tamm LK, Han X, Li Y, and Lai AL (2002) Structure and function of membrane fusion peptides. Biopolymers 66:249-60
193. Taylor GM and Sanders DA (1999) The role of the membrane-spanning domain sequence in glycoprotein-mediated membrane fusion. Mol Biol Cell 10:2803-15
194. Tong S and Compans RW (2000) Oligomerization, secretion, and biological function of an anchor-free parainfluenza virus type 2 (PI2) fusion protein. Virology 270:368-76
195. Tong S, Li M, Vincent A, Compans RW, Fritsch E, Beier R, Klenk C, Ohuchi M, and Klenk HD (2002) Regulation of fusion activity by the cytoplasmic domain of a paramyxovirus F protein. Virology 301:322-333
196. Vashishtha M, Phalen T, Marquardt MT, Ryu JS, Ng AC, and Kielian M (1998) A single point mutation controls the cholesterol dependence of Semliki Forest virus entry and exit. J Cell Biol 140:91-9
197. Viard M, Parolini I, Sargiacomo M, Fecchi K, Ramoni C, Ablan S, Ruscetti FW, Wang JM, and Blumenthal R (2002) Role of cholesterol in human immunodeficiency virus type 1 envelope protein-mediated fusion with host cells. J Virol 76:11584-95
198. Waarts BL, Bittman R, and Wilschut J (2002) Sphingolipid and cholesterol dependence of alphavirus membrane fusion. Lack of correlation with lipid raft formation in target liposomes. J Biol Chem 277:38141-38147
199. Wahlberg JM, Bron R, Wilschut J, and Garoff H (1992) Membrane fusion of Semliki Forest virus involves homotrimers of the fusion protein. J Virol 66:7309-18
200. Wahlberg JM and Garoff H (1992) Membrane fusion process of Semliki Forest virus. I: Low pH-induced rearrangement in spike protein quaternary structure precedes virus penetration into cells. J Cell Biol 116:339-48
201. +-induced insertion of influenza hemagglutinin HA2 N-terminal segment into viral membrane. J Biol Chem 269:18353-8
202. Weissenhorn W, Carfi A, Lee KH, Skehel JJ, and Wiley DC (1998) Crystal structure of the Ebola virus membrane fusion subunit, GP2, from the envelope glycoprotein ectodomain. Mol Cell 2:605-16
203. Weissenhorn W, Dessen A, Calder LJ, Harrison SC, Skehel JJ, and Wiley DC (1999) Structural basis for membrane fusion by enveloped viruses. Mol Membr Biol 16:3-9
204. Weissenhorn W, Dessen A, Harrison SC, Skehel JJ, and Wiley DC (1997) Atomic structure of the ectodomain from HIV-1 gp41. Nature 387:426-30
205. West JT, Johnston PB, Dubay SR, and Hunter E (2001) Mutations within the putative membrane-spanning domain of the simian immunodeficiency virus transmembrane glycoprotein define the minimal requirements for fusion, incorporation, and infectivity. J Virol 75:9601-12
206. Wharton SA, Skehel JJ, and Wiley DC (2000) Temperature dependence of fusion by sendai virus. Virology 271:71-78
207. White J and Helenius A (1980) pH-dependent fusion between the Semliki Forest virus membrane and liposomes. Proc Natl Acad Sci USA 77:3273-7
208. White J, Kartenbeck J, and Helenius A (1980) Fusion of Semliki forest virus with the plasma membrane can be induced by low pH. J Cell Biol 87:264-72
209. White J, Kartenbeck J, and Helenius A (1982) Membrane fusion activity of influenza virus. EMBO J 1:217-22
210. White JM (1990) Viral and cellular membrane fusion proteins. Annu Rev Physiol 52:675-97
211. Wilson IA, Skehel JJ, and Wiley DC (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289:366-373
212. Xiang SH, Kwong PD, Gupta R, Rizzuto CD, Casper DJ, Wyatt R, Wang L, Hendrickson WA, Doyle ML, and Sodroski J (2002) Mutagenic stabilization and/or disruption of a CD4-bound state reveals distinct conformations of the human immunodeficiency virus type 1 gp120 envelope glycoprotein. J Virol 76:9888-9899
213. Yang C and Compans RW (1996) Analysis of the cell fusion activities of chimeric simian immunodeficiency virus-murine leukemia virus envelope proteins: inhibitory effects of the R peptide. J Virol 70:248-54
214. Yang L and Huang HW (2002) Observation of a membrane fusion intermediate structure. Science 297:1877-9
215. Yao Q, Hu X, and Compans RW (1997) Association of the parainfluenza virus fusion and hemagglutinin-neuraminidase glycoproteins on cell surfaces. J Virol 71:650-6
216. Young JK, Li D, Abramowitz MC, and Morrison TG (1999) Interaction of peptides with sequences from the Newcastle disease virus fusion protein heptad repeat regions. J Virol 73:5945-56
217. Zarkik S, Defrise-Quertain F, Porteteile D, Burny A, and Ruysschaert JM (1997) Fusion of bovine leukemia virus with target cells monitored by R18 fluorescence and PCR assays. J Virol 71:738-40
218. Zhou J, Dutch RE, and Lamb RA (1997) Proper spacing between heptad repeat B and the transmembrane domain boundary of the paramyxovirus SV5 F protein is critical for biological activity. Virology 239:327-39