Reversible acid-induced inactivation of the membrane fusion protein of Semliki Forest virus

Journal of Virology

Volumn 79, Issue 12, 2005, Pages 7942-7948

  Waarts, Barry Lee ^a   Smit, Jolanda M ^a   Aneke, Onwuchekwa J C ^a   McInerney, Gerald M ^b   Liljeström, Peter ^b   Bittman, Robert ^c   Wilschut, Jan ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b KAROLINSKA INSTITUTE   (Sweden)

^c CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID; GLYCOPROTEIN E1; GLYCOPROTEIN E2; LIPOSOME; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN; VIRUS GLYCOPROTEIN;

ACIDITY; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN LIPID INTERACTION; PROTEIN POLYMERIZATION; SEMLIKI FOREST ALPHAVIRUS; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS NEUTRALIZATION;

ANIMALS; CELL LINE; CRICETINAE; DIMERIZATION; HYDROGEN-ION CONCENTRATION; LIPOSOMES; MEMBRANE FUSION; MEMBRANE GLYCOPROTEINS; NEUTRALIZATION TESTS; SEMLIKI FOREST VIRUS; VIRAL ENVELOPE PROTEINS; VIRAL FUSION PROTEINS;

RABBIT FIBROMA VIRUS; SEMLIKI FOREST VIRUS;

EID: 19944388914     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.12.7942-7948.2005     Document Type: Article

References (42)

1. Ahn, A., D. L. Gibbons, and M. Kielian. 2002. The fusion peptide of Semliki Forest virus associates with sterol-rich membrane domains. J. Virol. 76: 3267-3275.
2. Bressanelli, S., K. Stiasny, S. L. Allison, E. A. Stura, S. Duquerroy, J. Lescar, F. X. Heinz, F. A. Rey. 2004. Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J. 23:728-738.
3. Bron, R., J. M. Wahlberg, H. Garoff, and J. Wilschut. 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.
4. 2+ ions. Virology 238:14-21.
5. Corver, J., L. Moesby, R. K. Erukulla, K. C. Reddy, R. Bittman, and J. Wilschut. 1995. Sphingolipid-dependent fusion of Semliki Forest virus with cholesterol-containing liposomes requires both the 3-hydroxyl group and the double bond of the sphingolipid backbone. J. Virol. 69:3220-3223.
6. Garoff, H., A. M. Frischauf, K. Simons, H. Lehrach, and H. Delius. 1980. Nucleotide sequence of cDNA coding for Semliki Forest virus membrane glycoproteins. Nature 288:236-241.
7. Gaudin, Y. 2000. Reversibility in fusion protein conformational changes. The intriguing case of rhabdovirus-induced membrane fusion. Subcell. Biochem. 34:379-408.
8. Gibbons, D. L., A. Ahn, P. K. Chatterjee, and M. Kielian. 2000. Formation and characterization of the trimeric form of the fusion protein of Semliki Forest virus. J. Virol. 74:7772-7780.
9. Gibbons, D. L., A. Ahn, M. Liao, L. Hammar, R. H. Cheng, and M. Kielian. 2004. Multistep regulation of membrane insertion of the fusion peptide of Semliki Forest virus. J. Virol. 78:3312-3318.
10. Gibbons, D. L., I. Erk, B. Reilly, J. Navaza, M. Kielian, F. A. Rey, and J. Lepault. 2003. Visualization of the target-membrane-inserted fusion protein of Semliki Forest virus by combined electron microscopy and crystallography. Cell 114:573-583.
11. Gibbons, D. L., M.-C. Vaney, A. Roussel, A. Vigouroux, B. Reilly, J. Lepault, M. Kielian, and F. A. Rey. 2004. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 427:320-325.
12. Haag, L., H. Garoff, L. Xing, L. Hammar, S.-T. Kan, and R. H. Cheng. 2002. Acid-induced movements in the glycoprotein shell of an alphavirus turn the spikes into membrane fusion mode. EMBO J. 21:4402-4410.
13. Hammar, L., S. Markarian, L. Haag, H. Lankinen, A. Salmi, R. H. Cheng. 2003. Prefusion rearrangements resulting in fusion peptide exposure in Semliki Forest virus. J. Biol. Chem. 278:7189-7198.
14. Helenius, A., J. Kartenbeck, K. Simons, and E. Fries. 1980. On the entry of Semliki forest virus into BHK-21 cells. J. Cell Biol. 84:404-420.
15. Kielian, M., P. K. Chatterjee, D. L. Gibbons, and Y. E. Lu. 2000. Specific roles for lipids in virus fusion and exit. Examples from the alphaviruses. Subcell. Biochem. 34:409-455.
16. Kielian, M., and A. Helenius. 1984. Role of cholesterol in fusion of Semliki Forest virus with membranes. J. Virol. 52:281-283.
17. Kielian, M., M. R. Klimjack, S. Ghosh, and W. A. Duffus. 1996. Mechanisms of mutations inhibiting fusion and infection by Semliki Forest virus. J. Cell Biol. 134:863-872.
18. Klimjack, M. R., S. Jeffrey, and M. Kielian. 1994. Membrane and protein interactions of a soluble form of the Semliki Forest virus fusion protein. J. Virol. 68:6940-6946.
19. Lescar, J., A. Roussel, M. W. Wien, J. Navaza, S. D. Fuller, G. Wengler, G. Wengler, and F. A. Rey. 2001. The Fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105:137-148.
20. Marsh, M., E. Bolzau, and A. Helenius. 1983. Penetration of Semliki Forest virus from acidic prelysosomal vacuoles. Cell 32:931-940.
21. McInerney, G. M., J. M. Smit, P. Liljeström, and J. Wilschut. 2004. Semliki Forest virus produced in the absence of the 6K protein has an altered spike structure as revealed by decreased membrane fusion capacity. Virology 325: 200-206.
22. Modis, Y., S. Ogata, D. Clements, and S. C. Harrison. 2003. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. USA 100:6986-6991.
23. Modis, Y., S. Ogata, D. Clements, and S. C. Harrison. 2004. Structure of the dengue virus envelope protein after membrane fusion. Nature 427:313-319.
24. Moesby, L., J. Corver, R. K. Erukulla, R. Bittman, and J. Wilschut. 1995. Sphingolipids activate membrane fusion of Semliki Forest virus in a stereoscospecific manner. Biochemistry 34:10319-10324.
25. Nieva, J. L., R. Bron, J. Corver, and J. Wilschut. 1994. Membrane fusion of Semliki Forest virus requires sphingolipids in the target membrane. EMBO J. 13:2797-2804.
26. Reed, L. J., and H. Muench. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
27. Rey, F. A., F. X. Heinz, C. Mandl, C. Kunz, and S. C. Harrison. 1995. The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution. Nature 375:291-298.
28. Roche, S., and Y. Gaudin. 2002. Characterization of the equilibrium between the native and fusion-inactive conformation of rabies virus glycoprotein indicates that the fusion complex is made of several trimers. Virology 297: 128-135.
29. Skehel, J. J., and D. C. Wiley. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531-569.
30. Smit, J. M., R. Bittman, and J. Wilschut. 1999. Low-pH-dependent fusion of Sindbis virus with receptor-free cholesterol- and sphingolipid-containing liposomes. J. Virol. 73:8476-8484.
31. Smit, J. M., L. Gang, P. Schoen, J. Corver, R. Bittman, K. C. Lin, and J. Wilschut. 2002. Fusion of alphaviruses with liposomes is a non-leaky process. FEBS Lett. 521:62-66.
32. Smit, J. M., W. B. Klimstra, K. Ryman, R. Bittman, R. E. Johnston, and J. Wilschut. 2001. PE2 cleavage mutants of Sindbis virus: correlation between viral infectivity and pH-dependent membrane fusion activation of the spike heterodimer. J. Virol. 75:11196-11204.
33. Smit, J. M., B.-L. Waarts, R. Bittman, and J. Wilschut. 2003. Liposomes as target membranes in the study of virus receptor interaction and membrane fusion. Methods Enzymol. 372:374-392.
34. Smit, J. M., B.-L. Waarts, K. Kimata, W. B. Klimstra, R. Bittman, and J. Wilschut. 2002. Adaptation of alphaviruses to heparan sulfate: interaction of Sindbis and Semliki Forest viruses with liposomes containing lipid-conjugated heparin. J. Virol. 76:10128-10137.
35. Vashishtha, M., T. Phalen, M. T. Marquardt, J. S. Ryu, A. C. Ng, and M. Kielian. 1998. A single point mutation controls the cholesterol dependence of Semliki Forest virus entry and exit. J. Cell Biol. 140:91-99.
36. Waarts, B.-L., R. Bittman, and J. Wilschut. 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.
37. Wahlberg, J. M., R. Bron, J. Wilschut, and H. Garoff. 1992. Membrane fusion of Semliki Forest virus involves homotrimers of the fusion protein. J. Virol. 66:7309-7318.
38. Wahlberg, J. M., and H. Garoff. 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. 116:339-348.
39. White, J. M., and A. Helenius. 1980. pH-dependent fusion between the Semliki Forest virus membrane and liposomes. Proc. Natl. Acad. Sci. USA 77:3273-3277.
40. Wilschut, J., J. Corver, J. L. Nieva, R. Bron, L. Moesby, K. C. Reddy, and R. Bittman. 1995. Fusion of Semliki Forest virus with cholesterol-containing liposomes at low pH: a specific requirement for sphingolipids. Mol. Membr. Biol. 12:143-149.
41. Wilson, I. A., J. J. Skehel, and D. C. Wiley. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature 289:366-373.
42. Yao, Y., K. Ghosh, R. F. Epand, R. M. Epand, and H. P. Gosh. 2003. Membrane fusion activity of vesicular stomatitis virus glycoprotein G is induced by low pH but not by heat or denaturant. Virology 310:319-332.