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

Virology

Volumn 324, Issue 2, 2004, Pages 373-386

  Paredes, Angel M ^a   Ferreira, Davis ^b   Horton, Michelle ^b   Saad, Ali ^a   Tsuruta, Hiro ^c   Johnston, Robert ^d   Klimstra, William ^d   Ryman, Kate ^d   Hernandez, Raquel ^b   Chiu, Wah ^a   Brown, Dennis T ^b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Electron cryo microscopy; Infection; Membrane fusion; pH conditions; Sindbis virus; Structure

Indexed keywords

VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL FUSION; CELL INTERACTION; CELL MEMBRANE; CELL SURFACE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CORRELATION ANALYSIS; CRYOELECTRON MICROSCOPY; HAMSTER; KIDNEY CELL; MEMBRANE FUSION; NONHUMAN; PH; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; RHINOVIRUS; SINDBIS VIRUS; VIRUS ENVELOPE; VIRUS MORPHOLOGY;

ANIMALS; CELL FUSION; CELL LINE; CRICETINAE; CRYOELECTRON MICROSCOPY; HYDROGEN-ION CONCENTRATION; MEMBRANE FUSION; MICROSCOPY, ELECTRON; PROTEIN CONFORMATION; SINDBIS VIRUS; VIRAL ENVELOPE PROTEINS; VIRION; VIRUS REPLICATION;

SINDBIS VIRUS;

EID: 2942733550     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virol.2004.03.046     Document Type: Article

References (59)

1. Abell B.A., Brown D.T. Sindbis virus membrane fusion is mediated by reduction of glycoprotein disulfide bridges at the cell surface. J. Virol. 67(9):1993;5496-5501
2. Anthony R.P., Brown D.T. Protein-protein interactions in an alphavirus membrane. J. Virol. 65(3):1991;1187-1194
3. Anthony R.P., Paredes A.M., Brown D.T. Disulfide bonds are essential for the stability of the Sindbis virus envelope. Virology. 190(1):1992;330-336
4. Belnap D.M., Filman D.J., Trus B.L., Cheng N., Booy F.P., Conway J.F., Curry S., Hiremath C.N., Tsang S.K., Steven A.C., Hogle J.M. Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J. Virol. 74(3):2000;1342-1354
5. Brown D.T., Edwards J. Structural changes in alphaviruses accompanying the process of membrane penetration. Semin. Virol. 3:1992;519-527
6. 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. 69(4):1995;2471-2479
7. Duzgunes N., Pedroso de Lima M.C., Stamatatos L., Flasher D., Alford D., Friend D.S., Nir S. Fusion activity and inactivation of influenza virus: kinetics of low pH-induced fusion with cultured cells. J. Gen. Virol. 73(Pt 1):1992;27-37
8. Edwards J., Brown D.T. Sindbis virus-mediated cell fusion from without is a two-step event. J. Gen. Virol. 67(Pt 2):1986;377-380
9. Edwards J., Mann E., Brown D.T. Conformational changes in Sindbis virus envelope proteins accompanying exposure to low pH. J. Virol. 45(3):1983;1090-1097
10. Fan D.P., Sefton B.M. The entry into host cells of Sindbis virus, vesicular stomatitis virus and Sendai virus. Cell. 15(3):1978;985-992
11. Feener E.P., Shen W., Ryser H.H.-J. Cleavage of disulfide bonds in endocytosed macromolecules: a processing not associated with lysosomes or endosomes. J. Biol. Chem. 265:1990;18780-18785
12. Ferlenghi I., Gowen B., de Haas F., Mancini E.J., Garoff H., Sjoberg M., Fuller S.D. The first step: activation of the Semliki Forest virus spike protein precursor causes a localized conformational change in the trimeric spike [In Process Citation]. J. Mol. Biol. 283(1):1998;71-81
13. Flynn D.C., Meyer W.J., Mackenzie J.M. Jr., 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. 64(8):1990;3643-3653
14. Fuller S. Low pH induces swiveling of the glycoprotein heterodimers in the Semliki Forest virus spike complex. Cell. 81:1995;715-725
15. 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. 74(17):2000;7772-7780
16. 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. 427(6972):2004;320-325
17. Giranda V.L., Heinz B.A., Oliveira M.A., Minor I., Kim K.H., Kolatkar P.R., Rossmann M.G., Rueckert R.R. Acid-induced structural changes in human rhinovirus 14: possible role in uncoating. Proc. Natl. Acad. Sci. U.S.A. 89(21):1992;10213-10217
18. 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. Virology. 248(2):1998;372-381
19. Haag L., Garoff H., Xing L., Hammar L., Kan S.T., Cheng R.H. Acid-induced movements in the glycoprotein shell of an alphavirus turn the spikes into membrane fusion mode. EMBO J. 21(17):2002;4402-4410
20. Hase T., Summers P.L., Cohen W.H. A comparative study of entry modes into C6/36 cells by Semliki Forest and Japanese encephalitis viruses. Arch. Virol. 108(1-2):1989;101-114
21. Hase T., Summers P.L., Eckels K.H. Flavivirus entry into cultured mosquito cells and human peripheral blood monocytes. Arch. Virol. 104(1-2):1989;129-143
22. Haywood A.M., Boyer B.P. Fusion of influenza virus membranes with liposomes at pH 7.5. Proc. Natl. Acad. Sci. 82:1985;4611-4615
23. Hewat E.A., Neumann E., Blaas D. The concerted conformational changes during human rhinovirus 2 uncoating. Mol. Cell. 10(2):2002;317-326
24. Jardetzky T.S., Lamb R.A. Virology: a class act. Nature. 427(6972):2004;307-308
25. Kielian M. Membrane fusion and the alphavirus life cycle. Adv. Virus Res. 45:1995;113-151
26. Kielian M. Structural surprises from the Flaviviruses and alphaviruses. Mol. Cell. 9(3):2002;454-456
27. Kielian M., Jungerwirth S. Mechanisms of enveloped virus entry into cells. Mol. Biol. Med. 7(1):1990;17-31
28. Kielian M., Klimjack M.R., Ghosh S., Duffus W.A. Mechanisms of mutations inhibiting fusion and infection by Semliki Forest virus. J. Cell Biol. 134(4):1996;863-872
29. 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. 72(9):1998;7357-7366
30. 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. 77(22):2003;12022-12032
31. Koschinski A., Wengler G., Repp H. The membrane proteins of Flaviviruses form ion-permeable pores in the target membrane after fusion: identification of the pores and analysis of their possible role in virus infection. J. Gen. Virol. 84(Pt 7):2003;1711-1721
32. Lee H., Brown D.T. Mutations in an exposed domain of Sindbis virus capsid protein result in the production of noninfectious virions and morphological variants. Virology. 202:1994;390-400
33. Lee S., Owen K.E., Choi H.K., Lee H., Lu G., Wengler G., Brown D.T., Rossmann M.G., Kuhn R.J. Identification of a protein binding site on the surface of the alphavirus nucleocapsid and its implication in virus assembly. Structure. 4(5):1996;531-541
34. 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. 105(1):2001;137-148
35. Levy-Mintz P., Kielian M. Mutagenesis of the putative fusion domain of the Semliki Forest virus spike protein. J. Virol. 65(8):1991;4292-4300
36. Luukkonen A., Brummer-Korvenkontio M., Renkonen O. Lipids of cultured mosquito cells (Aedes albopictus). Comparison with cultured mammalian fibroblasts (BHK 21 cells). Biochim. Biophys. Acta. 326(2):1973;256-261
37. Meyer W.J., Johnston R.E. Structural rearrangement of infecting Sindbis virions at the cell surface: mapping of newly accessible epitopes. J. Virol. 67(9):1993;5117-5125
38. 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. 66(6):1992;3504-3513
39. Mitchell C.J., Niebylski M.L., Smith G.C., Karabatsos N., Martin D., Mutebi J.P., Craig G.B. Jr., Mahler M.J. Isolation of eastern equine encephalitis virus from Aedes albopictus in Florida. Science. 257(5069):1992;526-527
40. Modis Y., Ogata S., Clements D., Harrison S.C. Structure of the dengue virus envelope protein after membrane fusion. Nature. 427(6972):2004;313-319
41. Mulvey M., Brown D.T. Formation and rearrangement of disulfide bonds during maturation of the Sindbis virus E1 glycoprotein. J. Virol. 68(2):1994;805-812
42. Paredes A.M., Brown D.T., Rothnagel R., Chiu W., Schoepp R.J., Johnston R.E., Prasad B.V. Three-dimensional structure of a membrane-containing virus. Proc. Natl. Acad. Sci. U.S.A. 90(19):1993;9095-9099
43. Paredes A.M., Heidner H., Thuman-Commike P., Prasad B.V., Johnston R.E., Chiu W. Structural localization of the E3 glycoprotein in attenuated Sindbis virus mutants. J. Virol. 72(2):1998;1534-1541
44. Pletnev S.V., Zhang W., Mukhopadhyay S., Fisher B.R., Hernandez R., Brown D.T., Baker T.S., Rossmann M.G., Kuhn R.J. Locations of carbohydrate sites on alphavirus glycoproteins show that E1 forms an icosahedral scaffold. Cell. 105(1):2001;127-136
45. Rietveld A.G., Koorengevel M.C., de Kruijff B. Non-bilayer lipids are required for efficient protein transport across the plasma membrane of Escherichia coli. EMBO J. 14(22):1995;5506-5513
46. Saad A., Zhou Z.H., Jakana J., Chiu W., Rixon F.J. Roles of triplex and scaffolding proteins in herpes simplex virus type 1 capsid formation suggested by structures of recombinant particles. J. Virol. 73(8):1999;6821-6830
47. Saad A., Ludtke S.J., Jakana J., Rixon F.J., Tsuruta H., Chiu W. Fourier amplitude decay of electron cryomicroscopic images of single particles effects on structure determination. J. Struct. Biol. 133(1):2001;32-42
48. Sieczkarski S.B., Whittaker G.R. Dissecting virus entry via endocytosis. J. Gen. Virol. 83(Pt 7):2002;1535-1545
49. Smith J.F., Brown D.T. Envelopments of Sindbis virus: synthesis and organization of proteins in cells infected with wild type and maturation-defective mutants. J. Virol. 22(3):1977;662-678
50. Stiasny K., Allison S.L., Schalich J., Heinz F.X. Membrane interactions of the tick-borne encephalitis virus fusion protein E at low pH. J. Virol. 76(8):2002;3784-3790
51. Strauss J.H., Strauss E.G. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:1994;491-562
52. Strauss J.H., Wang K.S., Schmaljohn A.L., Kuhn R.J., Strauss E.G. Host-cell receptors for Sindbis virus. Arch. Virol., Suppl. 9:1994;473-484
53. Stubbs M.J., Miller A., Sizer P.J., Stephenson J.R., Crooks A.J. X-ray solution scattering of Sindbis virus. Changes in conformation induced at low pH. J. Mol. Biol. 221(1):1991;39-42
54. White J.M. Membrane fusion. Science. 258(5084):1992;917-924
55. White J., Kartenbeck J., Helenius A. Fusion of Semliki Forest virus with the plasma membrane can be induced by low pH. J. Cell Biol. 87:1980;264-272
56. White J., Kielian M., Helenius A. Membrane fusion proteins of enveloped animal viruses. Q. Rev. Biophys. 16(2):1983;151-195
57. 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. 76(22):2002;11645-11658
58. Zhou Z.H., Dougherty M., Jakana J., He J., Rixon F.J., Chiu W. Seeing the herpesvirus capsid at 8.5 A. Science. 288(5467):2000;877-880
59. Zhou Z.H., Baker M.L., Jiang W., Dougherty M., Jakana J., Dong G., Lu G., Chiu W. Electron cryomicroscopy and bioinformatics suggest protein fold models for rice dwarf virus. Nat. Struct. Biol. 8(10):2001;868-873