Alphavirus entry and membrane fusion

Viruses

Volumn 2, Issue 4, 2010, Pages 796-825

  Kielian, Margaret ^a   Chanel Vos, Chantal ^b   Liao, Maofu ^c  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alphavirus; Class II fusion protein; Endocytosis; Membrane fusion; Virus entry

Indexed keywords

CHOLESTEROL; GLYCOPROTEIN E1; GLYCOPROTEIN E2; MEMBRANE FUSION PROTEIN; MEMBRANE PROTEIN; PROTEIN P62; SPHINGOLIPID; VIRUS PROTEIN; VIRUS RNA;

CELL PH; CONFORMATIONAL TRANSITION; ENDOCYTOSIS; ENDOSOME; LIPID METABOLISM; MEMBRANE FUSION; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN TARGETING; RECEPTOR BINDING; REVIEW; SEMLIKI FOREST ALPHAVIRUS; SIGNAL TRANSDUCTION; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS MORPHOLOGY; VIRUS VIRULENCE;

ALPHAVIRUS; ANIMALIA;

EID: 78049487538     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v2040796     Document Type: Review

References (171)

1. Marsh, M.; Helenius, A. Virus entry: open sesame. Cell 2006, 124, 729-740.
2. Gruenberg, J. Viruses and endosome membrane dynamics. Curr. Opin. Cell Biol. 2009, 21, 582-588.
3. Sieczkarski, S.B.; Whittaker, G.R. Viral entry. Curr. Topics Microbiol. Immunol. 2005, 285, 1-23.
4. Harrison, S.C. Viral membrane fusion. Nat. Struct. Mol. Biol. 2008, 15, 690-698.
5. White, J.M.; Delos, S.E.; Brecher, M.; Schornberg, K. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 2008, 43, 189-219.
6. Strauss, J.H.; Strauss, E.G. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 1994, 58, 491-562.
7. Kuhn, R.J. Togaviridae: The Viruses and Their Replication. In Fields Virology; Knipe, D.M., Ed.; Lippincott, Williams and Wilkins: Philadelphia, PA, USA, 2007; Vol. 1, pp. 1001-1022.
8. Mancini, E.J.; Clarke, M.; Gowen, B.E.; Rutten, T.; Fuller, S.D. Cryo-electron microscopy reveals the functional organization of an enveloped virus, Semliki forest virus. Mol. Cell 2000, 5, 255-266.
9. Zhang, W.; Mukhopadhyay, S.; Pletnev, S.V.; Baker, T.S.; Kuhn, R.J.; Rossmann, M.G. Placement of the structural proteins in sindbis virus. J. Virol. 2002, 76, 11645-11658.
10. Roussel, A.; Lescar, J.; Vaney, M.-C.; Wengler, G.; Wengler, G.; Rey, F.A. Structure and interactions at the viral surface of the envelope protein E1 of Semliki Forest virus. Structure 2006, 14, 75-86.
11. Mukhopadhyay, S.; Zhang, W.; Gabler, S.; Chipman, P.R.; Strauss, E.G.; Strauss, J.H.; Baker, T.S.; Kuhn, R.J.; Rossmann, M.G. Mapping the structure and function of the E1 and E2 glycoproteins in alphaviruses. Structure 2006, 14, 63-73.
12. Lescar, J.; Roussel, A.; Wien, M.W.; Navaza, J.; Fuller, S.D.; Wengler, G.; Rey, F.A. The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 2001, 105, 137-148.
13. Gibbons, D.L.; Vaney, M.-C.; Roussel, A.; Vigouroux, A.; Reilly, B.; Lepault, J.; Kielian, M.; Rey, F.A. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 2004, 427, 320-325.
14. Rey, F.A.; Heinz, F.X.; Mandl, C.; Kunz, C.; Harrison, S.C. The envelope glycoprotein from tick-borne encephalitis virus at 2A resolution. Nature 1995, 375, 291-298.
15. Modis, Y.; Ogata, S.; Clements, D.; Harrison, S.C. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. USA 2003, 100, 6986-6991.
16. Modis, Y.; Ogata, S.; Clements, D.; Harrison, S.C. Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J. Virol. 2005, 79, 1223-1231.
17. Zhang, Y.; Zhang, W.; Ogata, S.; Clements, D.; Strauss, J.H.; Baker, T.S.; Kuhn, R.J.; Rossmann, M.G. Conformational changes of the flavivirus E glycoprotein. Structure (Camb) 2004, 12, 1607-1618.
18. Nybakken, G.E.; Nelson, C.A.; Chen, B.R.; Diamond, M.S.; Fremont, D.H. Crystal structure of the West Nile virus envelope glycoprotein. J. Virol. 2006, 80, 11467-11474.
19. Kanai, R.; Kar, K.; Anthony, K.; Gould, L.H.; Ledizet, M.; Fikrig, E.; Marasco, W.A.; Koski, R.A.; Modis, Y. Crystal structure of west nile virus envelope glycoprotein reveals viral surface epitopes. J. Virol. 2006, 80, 11000-11008.
20. Kielian, M.; Rey, F.A. Virus membrane fusion proteins: more than one way to make a hairpin. Nat.Rev.Micro. 2006, 4, 67-76.
21. Sanchez-San Martin, C.; Liu, C.Y.; Kielian, M. Dealing with low pH: entry and exit of alphaviruses and flaviviruses. Trends in Microbiol. 2009, 17, 514-521.
22. Kielian, M. Membrane fusion and the alphavirus life cycle. Adv.Virus Res. 1995, 45, 113-151.
23. Kielian, M.; Helenius, A. Entry of Alphaviruses. In The Togaviridae and Flaviviridae; Schlesinger, S., Schlesinger, M.J. Eds.; Plenum Press: New York, NY, USA, 1986; pp. 91-119.
24. La Linn, M.; Eble, J.A.; Lubken, C.; Slade, R.W.; Heino, J.; Davies, J.; Suhrbier, A. An arthritogenic alphavirus uses the alpha1beta1 integrin collagen receptor. Virol. 2005, 336, 229-239.
25. Klimstra, W.B.; Nangle, E.M.; Smith, M.S.; Yurochko, A.D.; Ryman, K.D. DC-SIGN and L-SIGN can act as attachment receptors for alphaviruses and distinguish between mosquito cell- and mammalian cell-derived viruses. J. Virol. 2003, 77, 12022-12032.
26. Klimstra, W.B.; Ryman, K.D.; Johnston, R.E. Adaptation of sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J. Virol. 1998, 72, 7357-7366.
27. Byrnes, A.P.; Griffin, D.E. Binding of Sindbis virus to cell surface heparan sulfate. J. Virol. 1998, 72, 7349-7356.
28. Jan, J.T.; Byrnes, A.P.; Griffin, D.E. Characterization of a Chinese hamster ovary cell line developed by retroviral insertional mutagenesis that is resistant to Sindbis virus infection. J. Virol. 1999, 73, 4919-4924.
29. Heil, M.L.; Albee, A.; Strauss, J.H.; Kuhn, R.J. An amino acid substitution in the coding region of the E2 glycoprotein adapts Ross River virus to utilize heparan sulfate as an attachment moiety. J. Virol. 2001, 75, 6303-6309.
30. Zhang, W.; Heil, M.; Kuhn, R.J.; Baker, T.S. Heparin binding sites on Ross River virus revealed by electron cryo-microscopy. Virol. 2005, 332, 511-518.
31. Byrnes, A.P.; Griffin, D.E. Large-plaque mutants of sindbis virus show reduced binding to heparan sulfate, heightened viremia, and slower clearance from the circulation. J. Virol. 2000, 74, 644-651.
32. Bernard, K.A.; Klimstra, W.B.; Johnston, R.E. Mutations in the E2 glycoprotein of Venezuelan equine encephalitis virus confer heparan sulfate interaction, low morbidity, and rapid clearance from blood of mice. Virol. 2000, 276, 93-103.
33. Wang, E.; Brault, A.C.; Powers, A.M.; Kang, W.; Weaver, S.C. Glycosaminoglycan binding properties of natural venezuelan equine encephalitis virus isolates. J. Virol. 2003, 77, 1204-1210.
34. Klimstra, W.B.; Heidner, H.W.; Johnston, R.E. The furin protease cleavage recognition sequence of sindbis virus PE2 can mediate virion attachment to cell surface heparan sulfate. J. Virol. 1999, 73, 6299-6306.
35. Smit, J.M.; Klimstra, W.B.; Ryman, K.D.; Bittman, R.; Johnston, R.E.; Wilschut, J. PE2 cleavage mutants of Sindbis virus: correlation between viral infectivity and pH-dependent membrane fusion activation of the spike heterodimer. J. Virol. 2001, 75, 11196-11204.
36. Zhang, X.; Fugere, M.; Day, R.; Kielian, M. Furin processing and proteolytic activation of Semliki Forest virus. J. Virol. 2003, 77, 2981-2989.
37. Feinberg, H.; Mitchell, D.A.; Drickamer, K.; Weis, W.I. Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR. Science 2001, 294, 2163-2166.
38. Hsieh, P.; Robbins, P.W. Regulation of asparagine-linked oligosaccharide processing. J. Biol. Chem. 1984, 259, 2375-2382.
39. Helenius, A.; Kartenbeck, J.; Simons, K.; Fries, E. On the entry of Semliki Forest virus into BHK-21 cells. J. Cell Biol. 1980, 84, 404-420.
40. Smith, A.E.; Helenius, A. How viruses enter animal cells. Science 2004, 304, 237-242.
41. Garoff, H.; Wilschut, J.; Liljeström, P.; Wahlberg, J.M.; Bron, R.; Suomalainen, M.; Smyth, J.; Salminen, A.; Barth, B.U.; Zhao, H. Assembly and entry mechanisms of Semliki Forest virus. Arch.Virol. 1994, 9, 329-338.
42. Sieczkarski, S.B.; Whittaker, G.R. Dissecting virus entry via endocytosis. J. Gen. Virol. 2002, 83, 1535-1545.
43. Marsh, M.; Helenius, A. Adsorptive endocytosis of Semliki Forest virus. J. Mol. Biol. 1980, 142, 439-454.
44. Helenius, A.; Marsh, M.; White, J. Inhibition of Semliki Forest virus penetration by lysosomotropic weak bases. J. Gen. Virol. 1982, 58, 47-61.
45. DeTulleo, L.; Kirchhausen, T. The clathrin endocytic pathway in viral infection. EMBO J. 1998, 17, 4585-4593.
46. Earp, L.J.; Delos, S.E.; Netter, R.C.; Bates, P.; White, J.M. The avian retrovirus avian sarcoma/leukosis virus subtype A reaches the lipid mixing stage of fusion at neutral pH. J. Virol. 2003, 77, 3058-3066.
47. Sieczkarski, S.B.; Whittaker, G.R. Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J. Virol. 2002, 76, 10455-10464.
48. Sieczkarski, S.B.; Whittaker, G.R. Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic 2003, 4, 333-343.
49. Glomb-Reinmund, S.; Kielian, M. The role of low pH and disulfide shuffling in the entry and fusion of Semliki Forest virus and Sindbis virus. Virol. 1998, 248, 372-381.
50. Marsh, M.; Wellsteed, J.; Kern, H.; Harms, E.; Helenius, A. Monensin inhibits Semliki Forest virus penetration into culture cells. Proc. Natl. Acad. Sci. USA 1982, 79, 5297-5301.
51. Kielian, M.C.; Marsh, M.; Helenius, A. Kinetics of endosome acidification detected by mutant and wild-type Semliki Forest virus. EMBO J. 1986, 5, 3103-3109.
52. Irurzun, A.; Nieva, J.L.; Carrasco, L. Entry of Semliki Forest virus into cells: Effects of concanamycin A and nigericin on viral membrane fusion and infection. Virol. 1997, 227, 488-492.
53. Sharkey, C.M.; North, C.L.; Kuhn, R.J.; Sanders, D.A. Ross River virus glycoprotein-pseudotyped retroviruses and stable cell lines for their production. J. Virol. 2001, 75, 2653-2659.
54. White, J.; Matlin, K.; Helenius, A. Cell fusion by Semliki Forest, influenza and Vesicular Stomatitis viruses. J. Cell Biol. 1981, 89, 674-679.
55. Omar, A.; Flaviano, A.; Kohler, U.; Koblet, H. Fusion of Semliki Forest virus infected Aedes albopictus cells at low pH is a fusion from within. Arch. Virol. 1986, 89, 145-159.
56. Lanzrein, M.; Käsermann, N.; Weingart, R.; Kempf, C. Early events of Semliki Forest Virus-induced cell-cell fusion. Virol. 1993, 196, 541-547.
57. Zaitseva, E.; Mittal, A.; Griffin, D.E.; Chernomordik, L.V. Class II fusion protein of alphaviruses drives membrane fusion through the same pathway as class I proteins. J. Cell Biol. 2005, 169, 167-177.
58. Bron, R.; Wahlberg, J.M.; Garoff, H.; Wilschut, J. Membrane fusion of Semliki Forest virus in a model system: Correlation between fusion kinetics and structural changes in the envelope glycoprotein. EMBO J. 1993, 12, 693-701.
59. Smit, J.M.; Bittman, R.; Wilschut, J. Low-pH-dependent fusion of sindbis virus with receptor-free cholesterol- and sphingolipid-containing liposomes. J. Virol. 1999, 73, 8476-8484.
60. White, J.; Helenius, A. pH-dependent fusion between the Semliki Forest virus membrane and liposomes. Proc. Natl. Acad. Sci. USA 1980, 77, 3273-3277.
61. Samsonov, A.V.; Chatterjee, P.K.; Razinkov, V.I.; Eng, C.H.; Kielian, M.; Cohen, F.S. Effects of membrane potential and sphingolipid structures on fusion of Semliki Forest virus. J. Virol. 2002, 76, 12691-12702.
62. Kielian, M.; Klimjack, M.R.; Ghosh, S.; Duffus, W.A. Mechanisms of mutations inhibiting fusion and infection by Semliki Forest virus. J. Cell Biol. 1996, 134, 863-872.
63. Chanel-Vos, C.; Kielian, M. A conserved histidine in the ij loop of the Semliki Forest virus E1 protein plays an important role in membrane fusion. J. Virol. 2004, 78, 13543-13552.
64. Liu, C.Y.; Kielian, M. E1 mutants identify a critical region in the trimer interface of the Semliki Forest virus fusion protein. J. Virol. 2009, 83, 11298-11306.
65. Liao, M.; Kielian, M. Domain III from class II fusion proteins functions as a dominant-negative inhibitor of virus-membrane fusion. J. Cell Biol. 2005, 171, 111-120.
66. Conner, S.D.; Schmid, S.L. Regulated portals of entry into the cell. Nature 2003, 422, 37-44.
67. Doxsey, S.J.; Brodsky, F.M.; Blank, G.S.; Helenius, A. Inhibition of endocytosis by anti-clathrin antibodies. Cell 1987, 50, 453-463.
68. Schmid, S.L.; Fuchs, R.; Kielian, M.; Helenius, A.; Mellman, I. Acidification of endosome subpopulations in wild-type Chinese hamster ovary cells and temperature-sensitive acidification-defective mutants. J. Cell Biol. 1989, 108, 1291-1300.
69. Marsh, M.; Bolzau, E.; Helenius, A. Penetration of Semliki Forest virus from acidic prelysomal vacuoles. Cell 1983, 32, 931-940.
70. Colpitts, T.M.; Moore, A.C.; Kolokoltsov, A.A.; Davey, R.A. Venezuelan equine encephalitis virus infection of mosquito cells requires acidification as well as mosquito homologs of the endocytic proteins Rab5 and Rab7. Virol. 2007, 369, 78-91.
71. Mellman, I.; Fuchs, R.; Helenius, A. Acidification of the endocytic and exocytic pathways. Annu. Rev. Biochem. 1986, 55, 663-700.
72. Marsh, M.; Bron, R. SFV infection in CHO cells: Cell-type specific restrictions to productive virus entry at the cell surface. J. Cell Sci. 1997, 110, 95-103.
73. Fan, D.P.; Sefton, B.N. The entry into host cells of Sindbis virus, Vesicular Stomatitis virus and Sendai virus. Cell 1978, 15, 985-992.
74. Glomb-Reinmund, S.; Kielian, M. Fus-1, a pH-shift mutant of Semliki Forest virus, acts by altering spike subunit interactions via a mutation in the E2 subunit. J. Virol. 1998, 72, 4281-4287.
75. Abell, B.A.; Brown, D.T. Sindbis virus membrane fusion is mediated by reduction of glycoprotein disulfide bridges at the cell surface. J. Virol. 1993, 67, 5496-5501.
76. Flynn, D.C.; Meyer, W.J.; Mackenzie, J.M.; Johnston, R.E. A conformational change in Sindbis virus glycoproteins E1 and E2 is detected at the plasma membrane as a consequence of early virus-cell interaction. J. Virol. 1990, 64, 3643-3653.
77. Kielian, M.; Chatterjee, P.K.; Gibbons, D.L.; Lu, Y.E. Specific roles for lipids in virus fusion and exit: Examples from the alphaviruses. In Subcellular Biochemistry Vol. 34. Fusion of Biological Membranes and Related Problems; Hilderson, H., Fuller, S., Eds.; Plenum Publishers, New York, NY, USA, 2000; pp. 409-455.
78. Umashankar, M.; Sanchez San Martin, C.; Liao, M.; Reilly, B.; Guo, A.; Taylor, G.; Kielian, M. Differential Cholesterol Binding by Class II Fusion Proteins Determines Membrane Fusion Properties. J. Virol. 2008, 82, 9245-9253.
79. Mooney, J.J.; Dalrymple, J.M.; Alving, C.R.; Russell, P.K. Interaction of Sindbis virus with liposomal model membranes. J. Virol. 1975, 15, 225-231.
80. Kielian, M.C.; Helenius, A. The role of cholesterol in the fusion of Semliki Forest virus with membranes. J. Virol. 1984, 52, 281-283.
81. Dawidowicz, E.A. Dynamics of membrane lipid metabolism and turnover. Annu. Rev. Biochem. 1987, 56, 43-61.
82. Nes, W.R.; McKean, M.L. Occurence, Physiology, and Ecology of Sterols. In Biochemistry of Steroids and Other Isopentenoids; University Park Press, Baltimore, MD, USA, 1977; pp. 411-533.
83. Silberkang, M.; Havel, C.M.; Friend, D.S.; McCarthy, B.J.; Watson, J.A. Isoprene synthesis in isolated embryonic Drosophila cells. I. Sterol-deficient eukaryotic cells. J. Biol. Chem. 1983, 258, 8303-8311.
84. Phalen, T.; Kielian, M. Cholesterol is required for infection by Semliki Forest virus. J. Cell Biol. 1991, 112, 615-623.
85. Marquardt, M.T.; Phalen, T.; Kielian, M. Cholesterol is required in the exit pathway of Semliki Forest virus. J. Cell Biol. 1993, 123, 57-65.
86. Vashishtha, M.; Phalen, T.; Marquardt, M.T.; Ryu, J.S.; Ng, A.C.; Kielian, M. A single point mutation controls the cholesterol dependence of Semliki Forest virus entry and exit. J. Cell Biol. 1998, 140, 91-99.
87. Lu, Y.E.; Cassese, T.; Kielian, M. The cholesterol requirement for Sindbis virus entry and exit and characterization of a spike protein region involved in cholesterol dependence. J. Virol. 1999, 73, 4272-4278.
88. Lu, Y.E.; Kielian, M. Semliki Forest virus budding: Assay, mechanisms and cholesterol requirement. J. Virol. 2000, 74, 7708-7719.
89. Hafer, A.; Whittlesey, R.; Brown, D.T.; Hernandez, R. Differential incorporation of cholesterol by Sindbis virus grown in mammalian or insect cells. J. Virol. 2009, 83, 9113-9121.
90. Bowers, D.F.; Abell, B.A.; Brown, D.T. Replication and tissue tropism of the alphavirus Sindbis in the mosquito Aedes albopictus. Virol. 1995, 212, 1-12.
91. Scott, T.W.; Weaver, S.C. Eastern equine encephalomyelitis virus: Epidemiology and evolution of mosquito transmission. Adv. Virus Res. 1989, 37, 277-328.
92. Marquardt, M.T.; Kielian, M. Cholesterol-depleted cells that are relatively permissive for Semliki Forest virus infection. Virol. 1996, 224, 198-205.
93. Nieva, J.L.; Bron, R.; Corver, J.; Wilschut, J. Membrane fusion of Semliki Forest virus requires sphingolipids in the target membrane. EMBO J. 1994, 13, 2797-2804.
94. Wilschut, J.; Corver, J.; Nieva, J.L.; Bron, R.; Moesby, L.; Reddy, K.C.; Bittman, R. Fusion of Semliki Forest virus with cholesterol-containing liposomes at low pH: A specific requirement for sphingolipids. Mol. Membrane Biol. 1995, 12, 143-149.
95. Brown, D.A.; London, E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 2000, 275, 17221-17224.
96. Waarts, B.L.; Bittman, R.; Wilschut, J. Sphingolipid and cholesterol dependence of alphavirus membrane fusion. Lack of correlation with lipid raft formation in target liposomes. J. Biol. Chem. 2002, 277, 38141-38147.
97. Meyer, W.J.; Johnston, R.E. Structural rearrangement of infecting Sindbis virions at the cell surface: Mapping of newly accessible epitopes. J. Virol. 1993, 67, 5117-5125.
98. Meyer, W.J.; Gidwitz, S.; Ayers, V.K.; Schoepp, R.J.; Johnston, R.E. Conformational alteration of Sindbis virion glycoproteins induced by heat, reducing agents, or low pH. J. Virol. 1992, 66, 3504-3513.
99. Wahlberg, J.M.; Boere, W.A.M.; Garoff, H. The heterodimeric association between the membrane proteins of Semliki Forest virus changes its sensitivity to low pH during virus maturation. J. Virol. 1989, 63, 4991-4997.
100. Wahlberg, J.M.; Garoff, H. 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. 1992, 116, 339-348.
101. Justman, J.; Klimjack, M.R.; Kielian, M. Role of spike protein conformational changes in fusion of Semliki Forest virus. J. Virol. 1993, 67, 7597-7607.
102. Hammar, L.; Markarian, S.; Haag, L.; Lankinen, H.; Salmi, A.; Cheng, H.R. Prefusion rearrangements resulting in fusion peptide exposure in Semliki forest virus. J. Biol. Chem. 2003, 278, 7189-7198.
103. Gibbons, D.L.; Ahn, A.; Liao, M.; Hammar, L.; Cheng, R.H.; Kielian, M. Multistep regulation of membrane insertion of the fusion peptide of Semliki Forest virus. J. Virol. 2004, 78, 3312-3318.
104. Wahlberg, J.M.; Bron, R.; Wilschut, J.; Garoff, H. Membrane fusion of Semliki Forest virus involves homotrimers of the fusion protein. J. Virol. 1992, 66, 7309-7318.
105. Kielian, M.; Helenius, A. pH-induced alterations in the fusogenic spike protein of Semliki Forest Virus. J. Cell Biol. 1985, 101, 2284-2291.
106. Shome, S.G.; Kielian, M. Differential roles of two conserved glycine residues in the fusion peptide of Semliki Forest virus. Virol. 2001, 279, 146-160.
107. Salminen, A.; Wahlberg, J.M.; Lobigs, M.; Liljeström, P.; Garoff, H. Membrane fusion process of Semliki Forest virus II: Cleavage- dependent reorganization of the spike protein complex controls virus entry. J. Cell Biol. 1992, 116, 349-357.
108. 2+ ions. Virol. 1997, 238, 14-21.
109. Kielian, M.; Jungerwirth, S.; Sayad, K.U.; DeCandido, S. Biosynthesis, maturation, and acid-activation of the Semliki Forest virus fusion protein. J. Virol. 1990, 64, 4614-4624.
110. Ahn, A.; Klimjack, M.R.; Chatterjee, P.K.; Kielian, M. An epitope of the Semliki Forest virus fusion protein exposed during virus-membrane fusion. J. Virol. 1999, 73, 10029-10039.
111. Phinney, B.S.; Blackburn, K.; Brown, D.T. The surface conformation of sindbis virus glycoproteins E1 and E2 at neutral and low pH, as determined by mass spectrometry-based mapping. J. Virol. 2000, 74, 5667-5678.
112. Klimjack, M.R.; Jeffrey, S.; Kielian, M. Membrane and protein interactions of a soluble form of the Semliki Forest virus fusion protein. J. Virol. 1994, 68, 6940-6946.
113. Wengler, G.; Wengler, G.; Rey, F.A. The isolation of the ectodomain of the alphavirus E1 protein as a soluble hemagglutinin and its crystallization. Virol. 1999, 257, 472-482.
114. Lu, Y.E.; Eng, C.H.; Shome, S.G.; Kielian, M. In vivo generation and characterization of a soluble form of the Semliki forest virus fusion protein. J. Virol. 2001, 75, 8329-8339.
115. Zhao, H.; Garoff, H. Role of cell surface spikes in alphavirus budding. J. Virol. 1992, 66, 7089-7095.
116. Sanchez-San Martin, C.; Sosa, H.; Kielian, M. A stable prefusion intermediate of the alphavirus fusion protein reveals critical features of class II membrane fusion. Cell Host Microbe 2008, 4, 600-608.
117. Gibbons, D.L.; Erk, I.; Reilly, B.; Navaza, J.; Kielian, M.; Rey, F.A.; Lepault, J. Visualization of the target-membrane-inserted fusion protein of Semliki Forest virus by combined electron microscopy and crystallography. Cell 2003, 114, 573-583.
118. Gibbons, D.L.; Reilly, B.; Ahn, A.; Vaney, M.-C.; Vigouroux, A.; Rey, F.A.; Kielian, M. Purification and crystallization reveal two types of interactions of the fusion protein homotrimer of Semliki Forest virus. J. Virol. 2004, 787, 3514-3523.
119. Modis, Y.; Ogata, S.; Clements, D.; Harrison, S.C. Structure of the dengue virus envelope protein after membrane fusion. Nature 2004, 427, 313-319.
120. Bressanelli, S.; Stiasny, K.; Allison, S.L.; Stura, E.A.; Duquerroy, S.; Lescar, J.; Heinz, F.X.; Rey, F.A. Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J. 2004, 23, 728-738.
121. Gibbons, D.L.; Kielian, M. Molecular dissection of the Semliki Forest virus homotrimer reveals two functionally distinct regions of the fusion protein. J. Virol. 2002, 76, 1194-1205.
122. Markosyan, R.M.; Kielian, M.; Cohen, F.S. Fusion induced by a class II viral fusion protein, semliki forest virus E1, is dependent on the voltage of the target cell. J. Virol. 2007, 81, 11218-11225.
123. Wengler, G.; Koschinski, A.; Repp, H. During entry of alphaviruses, the E1 glycoprotein molecules probably form two separate populations that generate either a fusion pore or ion-permeable pores. J. Gen. Virol. 2004, 85, 1695-1701.
124. Lanzrein, M.; Weingart, R.; Kempf, C. pH-dependent pore formation in Semliki forest virus-infected Aedes albopictus cells. Virol. 1993, 193, 296-302.
125. Nyfeler, S.; Senn, K.; Kempf, C. Expression of Semliki Forest virus E1 protein in Escherichia coli. Low pH-induced pore formation. J. Biol. Chem. 2001, 276, 15453-15457.
126. Wengler, G.; Koschinski, A.; Dreyer, F. Entry of alphaviruses at the plasma membrane converts the viral surface proteins into an ion-permeable pore that can be detected by electrophysiological analyses of whole-cell membrane currents. J. Gen. Virol. 2003, 84, 173-181.
127. Koschinski, A.; Wengler, G.; Repp, H. Rare earth ions block the ion pores generated by the class II fusion proteins of alphaviruses and allow analysis of the biological functions of these pores. J. Gen. Virol. 2005, 86, 3311-3320.
128. Smit, J.M.; Li, G.; Schoen, P.; Corver, J.; Bittman, R.; Lin, K.C.; Wilschut, J. Fusion of alphaviruses with liposomes is a non-leaky process. FEBS Lett 2002, 521, 62-66.
129. Gaedigk-Nitschko, K.; Schlesinger, M.J. The Sindbis virus 6K protein can be detected in virions and is acylated with fatty acids. Virol. 1990, 175, 274-281.
130. Firth, A.E.; Chung, B.Y.; Fleeton, M.N.; Atkins, J.F. Discovery of frameshifting in Alphavirus 6K resolves a 20-year enigma. Virol. J. 2008, 5, 108.
131. Liljeström, P.; Lusa, S.; Huylebroeck, D.; Garoff, H. In vitro mutagenesis of a full-length cDNA clone of Semliki Forest virus: the small 6,000-molecular-weight membrane protein modulates virus release. J. Virol. 1991, 65, 4107-4113.
132. McInerney, G.M.; Smit, J.M.; Liljestrom, P.; Wilschut, J. Semliki Forest virus produced in the absence of the 6K protein has an altered spike structure as revealed by decreased membrane fusion capacity. Virol. 2004, 325, 200-206.
133. Kim, K.H.; Strauss, E.G.; Strauss, J.H. Adaptive mutations in Sindbis virus E2 and Ross River virus E1 that allow efficient budding of chimeric viruses. J. Virol. 2000, 74, 2663-2670.
134. Berglund, P.; Sjoberg, M.; Garoff, H.; Atkins, G.J.; Sheahan, B.J.; Liljestrom, P. Semliki Forest virus expression system: production of conditionally infectious recombinant particles. Biotechnology (NY) 1993, 11, 916-920.
135. Davis, N.L.; Brown, K.W.; Greenwald, G.F.; Zajac, A.J.; Zacny, V.L.; Smith, J.F.; Johnston, R.E. Attenuated mutants of venezuelan equine encephalitis virus containing lethal mutations in the PE2 cleavage signal combined with a second-site suppressor mutation in E1. Virol. 1995, 212, 102-110.
136. Russell, D.L.; Dalrymple, J.M.; Johnston, R.E. Sindbis virus mutations which coordinately affect glycoprotein processing, penetration, and virulence in mice. J. Virol. 1989, 63, 16l9-1629.
137. Heidner, H.W.; McKnight, K.L.; Davis, N.L.; Johnston, R.E. Lethality of PE2 incorporation into Sindbis virus can be suppressed by second-site mutations in E3 and E2. J. Virol. 1994, 68, 2683-2692.
138. Ferlenghi, I.; Gowen, B.; Haas, F.D.; Mancini, E.J.; Garoff, H.; Sjoberg, M.; Fuller, S.D. The first step:maturation of the Semliki Forest virus spike occurs through a dramatic localized conformational change. J. Mol. Biol. 1998, 283, 71-81.
139. Tubulekas, I.; Liljeström, P. Suppressors of cleavage-site mutations in the p62 envelope protein of Semliki Forest virus reveal dynamics in spike structure and function. J. Virol. 1998, 72, 2825-2831.
140. Zhang, X.; Kielian, M. Mutations that promote furin-independent growth of Semliki Forest virus affect p62-E1 interactions and membrane fusion. Virol. 2004, 327, 287-296.
141. Zhang, X.; Kielian, M. An interaction site of the envelope proteins of Semliki Forest virus that is preserved after proteolytic activation. Virol. 2005, 337, 344-352.
142. Strauss, E.G.; Lenches, E.M.; Strauss, J.H. Molecular genetic evidence that the hydrophobic anchors of glycoproteins E2 and E1 interact during assembly of alphaviruses. J. Virol. 2002, 76, 10188-10194.
143. Yao, J.S.; Strauss, E.G.; Strauss, J.H. Molecular genetic study of the interaction of Sindbis virus E2 with Ross River virus E1 for virus budding. J. Virol. 1998, 72, 1418-1423.
144. Kielian, M.C.; Keränen, S.; Kääriäinen, L.; Helenius, A. Membrane fusion mutants of Semliki Forest virus. J. Cell Biol. 1984, 98, 139-145.
145. Garoff, H.; Frischauf, A.-M.; Simons, K.; Lehrach, H.; Delius, H. Nucleotide sequence of cDNA coding for Semliki Forest virus membrane glycoproteins. Nature 1980, 288, 236-241.
146. Ahn, A.; Gibbons, D.L.; Kielian, M. The fusion peptide of Semliki Forest virus associates with sterol-rich membrane domains. J. Virol. 2002, 76, 3267-3275.
147. Levy-Mintz, P.; Kielian, M. Mutagenesis of the putative fusion domain of the Semliki Forest virus spike protein. J. Virol. 1991, 65, 4292-4300.
148. Duffus, W.A.; Levy-Mintz, P.; Klimjack, M.R.; Kielian, M. Mutations in the putative fusion peptide of Semliki Forest virus affect spike protein oligomerization and virus assembly. J. Virol. 1995, 69, 2471-2479.
149. Gibbons, D.L.; Ahn, A.; Chatterjee, P.K.; Kielian, M. Formation and characterization of the trimeric form of the fusion protein of Semliki Forest virus. J. Virol. 2000, 74, 7772-7780.
150. Ruigrok, R.W.H.; Martin, S.R.; Wharton, S.A.; Skehel, J.J.; Bayley, P.M.; Wiley, D.C. Conformational changes in the hemagglutinin of influenza virus which accompany heat-induced fusion of virus with liposomes. Virol. 1986, 155, 484-497.
151. Russell, C.J.; Jardetzky, T.S.; Lamb, R.A. Membrane fusion machines of paramyxoviruses: capture of intermediates of fusion. EMBO J. 2001, 20, 4024-4034.
152. Carr, C.M.; Chaudhry, C.; Kim, P.S. Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc.Natl. Acad. Sci. USA 1997, 94, 14306-14313.
153. Stiasny, K.; Allison, S.L.; Mandl, C.W.; Heinz, F.X. Role of Metastability and Acidic pH in Membrane Fusion by Tick-Borne Encephalitis Virus. J. Virol. 2001, 75, 7392-7398.
154. Kampmann, T.; Mueller, D.S.; Mark, A.E.; Young, P.R.; Kobe, B. The Role of Histidine Residues in Low-pH-Mediated Viral Membrane Fusion. Structure 2006, 14, 1481-1487.
155. Qin, Z.L.; Zheng, Y.; Kielian, M. Role of conserved histidine residues in the low pH-dependence of the Semliki Forest virus fusion protein. J. Virol. 2009, 83, 4670-4677.
156. Chatterjee, P.K.; Eng, C.H.; Kielian, M. Novel mutations that control the sphingolipid and cholesterol dependence of the Semliki Forest virus fusion protein. J. Virol. 2002, 76, 12712-12722.
157. Chatterjee, P.K.; Vashishtha, M.; Kielian, M. Biochemical consequences of a mutation that controls the cholesterol dependence of Semliki Forest virus fusion. J. Virol. 2000, 74, 1623-1631.
158. Schuffenecker, I.; Iteman, I.; Michault, A.; Murri, S.; Frangeul, L.; Vaney, M.C.; Lavenir, R.; Pardigon, N.; Reynes, J.M.; Pettinelli, F.; Biscornet, L.; Diancourt, L.; Michel, S.; Duquerroy, S.; Guigon, G.; Frenkiel, M.P.; Brehin, A.C.; Cubito, N.; Despres, P.; Kunst, F.; Rey, F.A.; Zeller, H.; Brisse, S. Genome Microevolution of Chikungunya Viruses Causing the Indian Ocean Outbreak. PLoS Med. 2006, 3, e263.
159. Vazeille, M.; Moutailler, S.; Coudrier, D.; Rousseaux, C.; Khun, H.; Huerre, M.; Thiria, J.; Dehecq, J.S.; Fontenille, D.; Schuffenecker, I.; Despres, P.; Failloux, A.B. Two Chikungunya Isolates from the Outbreak of La Reunion (Indian Ocean) Exhibit Different Patterns of Infection in the Mosquito, Aedes albopictus. PLoS ONE 2007, 2, e1168.
160. Tsetsarkin, K.A.; Vanlandingham, D.L.; McGee, C.E.; Higgs, S. A Single Mutation in Chikungunya Virus Affects Vector Specificity and Epidemic Potential. PLoS Pathog. 2007, 3, e201.
161. Tsetsarkin, K.A.; McGee, C.E.; Volk, S.M.; Vanlandingham, D.L.; Weaver, S.C.; Higgs, S. Epistatic roles of E2 glycoprotein mutations in adaption of chikungunya virus to Aedes albopictus and Ae. aegypti mosquitoes. PLoS One 2009, 4, e6835.
162. Chanel-Vos, C.; Kielian, M. Second-site revertants of a Semliki Forest virus fusion-block mutation reveal the dynamics of a class II membrane fusion protein. J. Virol. 2006, 80, 6115-6122.
163. Liao, M.; Kielian, M. Site-directed antibodies against the stem region reveal low pH-induced conformational changes of the Semliki Forest virus fusion protein. J. Virol. 2006, 80, 9599-9607.
164. Liao, M.; Kielian, M. Functions of the stem region of the Semliki Forest virus fusion protein during virus fusion and assembly. J. Virol. 2006, 80, 11362-11369.
165. Earp, L.J.; Delos, S.E.; Park, H.E.; White, J.M. The many mechanisms of viral membrane fusion proteins. Curr. Topics Microbiol. Immunol. 2005, 285, 25-66.
166. Barth, B.U.; Suomalainen, M.; Liljeström, P.; Garoff, H. Alphavirus assembly and entry: Role of the cytoplasmic tail of the E1 spike subunit. J. Virol. 1992, 66, 7560-7564.
167. Hernandez, R.; Sinodis, C.; Horton, M.; Ferreira, D.; Yang, C.; Brown, D.T. Deletions in the transmembrane domain of a sindbis virus glycoprotein alter virus infectivity, stability, and host range. J. Virol. 2003, 77, 12710-12719.
168. Sjoberg, M.; Garoff, H. Interactions between the transmembrane segments of the alphavirus E1 and E2 proteins play a role in virus budding and fusion. J. Virol. 2003, 77, 3441-3450.
169. Whitehurst, C.B.; Willis, J.H.; Sinodis, C.N.; Hernandez, R.; Brown, D.T. Single and multiple deletions in the transmembrane domain of the Sindbis virus E2 glycoprotein identify a region critical for normal virus growth. Virol. 2006, 347, 199-207.
170. Liao, M.; Kielian, M. The conserved glycine residues in the transmembrane domain of the Semliki Forest virus fusion protein are not required for assembly and fusion. Virol. 2005, 332, 430-437.
171. Paredes, A.M.; Ferreira, D.; Horton, M.; Saad, A.; Tsuruta, H.; Johnston, R.; Klimstra, W.; Ryman, K.; Hernandez, R.; Chiu, W.; Brown, D.T. Conformational changes in Sindbis virions resulting from exposure to low pH and interactions with cells suggest that cell penetration may occur at the cell surface in the absence of membrane fusion. Virol. 2004, 324, 373-386.