Mapping the structure and function of the E1 and E2 glycoproteins in alphaviruses

Structure

Volumn 14, Issue 1, 2006, Pages 63-73

  Mukhopadhyay, Suchetana ^a,c   Zhang, Wei ^a   Gabler, Stefan ^a   Chipman, Paul R ^a   Strauss, Ellen G ^b   Strauss, James H ^b   Baker, Timothy S ^a,d   Kuhn, Richard J ^a   Rossmann, Michael G ^a  

^a PURDUE UNIVERSITY   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c INDIANA UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; GLYCOPROTEIN E1; GLYCOPROTEIN E2; HETERODIMER; MONOMER; NUCLEOCAPSID PROTEIN; VIRUS FUSION PROTEIN;

ALPHA VIRUS; ARTICLE; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SINDBIS VIRUS;

CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; MEMBRANE GLYCOPROTEINS; NUCLEOCAPSID PROTEINS; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; SINDBIS VIRUS; VIRAL ENVELOPE PROTEINS; VIRAL FUSION PROTEINS;

ALPHAVIRUS; SINDBIS VIRUS;

EID: 33644815756     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2005.07.025     Document Type: Article

References (52)

1. T.S. Baker, N.H. Olson, and S.D. Fuller Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs Microbiol. Mol. Biol. Rev. 63 1999 862 922
2. B.U. Barth, M. Suomalainen, P. Liljestrom, and H. Garoff Alphavirus assembly and entry: role of the cytoplasmic tail of the E1 spike subunit J. Virol. 66 1992 7560 7564
3. S. Bressanelli, K. Stiasny, S.L. Allison, E.A. Stura, S. Duquerroy, J. Lescar, F.X. Heinz, and F.A. Rey Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation EMBO J. 23 2004 728 738
4. D.L.D. Caspar, and A. Klug Physical principles in the construction of regular viruses Cold Spring Harb. Symp. Quant. Biol. 27 1962 1 24
5. R.H. Cheng, R.J. Kuhn, N.H. Olson, M.G. Rossmann, H.K. Choi, T.J. Smith, and T.S. Baker Nucleocapsid and glycoprotein organization in an enveloped virus Cell 80 1995 621 630
6. H.K. Choi, L. Tong, W. Minor, P. Dumas, U. Boege, M.G. Rossmann, and G. Wengler Structure of Sindbis virus core protein reveals a chymotrypsin-like serine proteinase and the organization of the virion Nature 354 1991 37 43
7. W.D. Crill, and J.T. Roehrig Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to Vero cells J. Virol. 75 2001 7769 7773
8. N.L. Davis, D.F. Pence, W.J. Meyer, A.L. Schmaljohn, and R.E. Johnston Alternative forms of a strain-specific neutralizing antigenic site on the Sindbis virus E2 glycoprotein Virology 161 1987 101 108
9. T. Dokland, M. Walsh, J.M. Mackenzie, A.A. Khromykh, K.H. Ee, and S. Wang West nile virus core protein; tetramer structure and ribbon formation Structure 12 2004 1157 1163
10. T.E. Ellenberger, C.J. Brandl, K. Struhl, and S.C. Harrison The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted α helices: crystal structure of the protein-DNA complex Cell 71 1992 1223 1237
11. K. Gaedigk-Nitschko, and M.J. Schlesinger The Sindbis virus 6K protein can be detected in virions and is acylated with fatty acids Virology 175 1990 274 281
12. D.L. Gibbons, I. Erk, B. Reilly, J. Navaza, M. Kielian, F.A. Rey, and J. Lepault Visualization of the target-membrane-inserted fusion protein of Semliki Forest virus by combined electron microscopy and crystallography Cell 114 2003 573 583
13. D.L. Gibbons, M.C. Vaney, A. Roussel, A. Vigouroux, B. Reilly, J. Lepault, M. Kielian, and F.A. Rey Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus Nature 427 2004 320 325
14. M.L. Heil, A. Albee, J.H. Strauss, and R.J. Kuhn 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. 75 2001 6303 6309
15. R. Hernandez, H. Lee, C. Nelson, and D.T. Brown A single deletion in the membrane-proximal region of the Sindbis virus glycoprotein E2 endodomain blocks virus assembly J. Virol. 74 2000 4220 4228
16. R. Hernandez, D. Ferreira, C. Sinodis, K. Litton, and D.T. Brown Single amino acid insertions at the junction of the Sindbis virus E2 transmembrane domain and endodomain disrupt virus envelopment and alter infectivity J. Virol. 79 2005 7682 7697
17. Ji, Y., Marinescu, D.C., Zhang, W., and Baker, T.S. (2003). Orientation refinement of virus structures with unknown symmetry. Paper presented at: IEEE Computer Society (Los Alamitos, California).
18. R.J. Kuhn, W. Zhang, M.G. Rossmann, S.V. Pletnev, J. Corver, E. Lenches, C.T. Jones, S. Mukhopadhyay, P.R. Chipman, and E.G. Strauss Structure of dengue virus: implications for flavivirus organization, maturation, and fusion Cell 108 2002 717 725
19. S. Lee, K.E. Owen, H.K. Choi, H. Lee, G. Lu, G. Wengler, D.T. Brown, M.G. Rossmann, and R.J. Kuhn Identification of a protein binding site on the surface of the alphavirus nucleocapsid and its implication in virus assembly Structure 4 1996 531 541
20. J. Lescar, A. Roussel, M.W. Wien, J. Navaza, S.D. Fuller, G. Wengler, and F.A. Rey The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH Cell 105 2001 137 148
21. M. Liao, and M. Kielian The conserved glycine residues in the transmembrane domain of the Semliki Forest virus fusion protein are not required for assembly and fusion Virology 332 2005 430 437
22. S. Lusa, H. Garoff, and P. Liljestrom Fate of the 6K membrane protein of Semliki Forest virus during virus assembly Virology 185 1991 843 846
23. S. Lustig, A.C. Jackson, C.S. Hahn, D.E. Griffin, E.G. Strauss, and J.H. Strauss Molecular basis of Sindbis virus neurovirulence in mice J. Virol. 62 1988 2329 2336
24. L. Ma, C.T. Jones, T.D. Groesch, R.J. Kuhn, and C.B. Post Solution structure of dengue virus capsid protein reveals another fold Proc. Natl. Acad. Sci. USA 101 2004 3414 3419
25. E.J. Mancini, M. Clarke, B.E. Gowen, T. Rutten, and S.D. Fuller Cryo-electron microscopy reveals the functional organization of an enveloped virus, Semliki Forest virus Mol. Cell 5 2000 255 266
26. C.W. Mandl, S.L. Allison, H. Holzmann, T. Meixner, and F.X. Heinz Attenuation of tick-borne encephalitis virus by structure-based site-specific mutagenesis of a putative flavivirus receptor binding site J. Virol. 74 2000 9601 9609
27. W.J. Meyer, and R.E. Johnston Structural rearrangement of infecting Sindbis virions at the cell surface: mapping of newly accessible epitopes J. Virol. 67 1993 5117 5125
28. Y. Modis, S. Ogata, D. Clements, and S.C. Harrison Structure of the dengue virus envelope protein after membrane fusion Nature 427 2004 313 319
29. S. Mukhopadhyay, P.R. Chipman, E.M. Hong, R.J. Kuhn, and M.G. Rossmann In vitro-assembled alphavirus core-like particles maintain a structure similar to that of nucleocapsid cores in mature virus J. Virol. 76 2002 11128 11132
30. A.M. Paredes, D.T. Brown, R. Rothnagel, W. Chiu, R.J. Schoepp, R.E. Johnston, and B.V. Prasad Three-dimensional structure of a membrane-containing virus Proc. Natl. Acad. Sci. USA 90 1993 9095 9099
31. A.M. Paredes, H. Heidner, P. Thuman-Commike, B.V. Prasad, R.E. Johnston, and W. Chiu Structural localization of the E3 glycoprotein in attenuated Sindbis virus mutants J. Virol. 72 1998 1534 1541
32. A. Paredes, K. Alwell-Warda, S.C. Weaver, W. Chiu, and S.J. Watowich Venezuelan equine encephalomyelitis virus structure and its divergence from old world alphaviruses J. Virol. 75 2001 9532 9537
33. S.V. Pletnev, W. Zhang, S. Mukhopadhyay, B.R. Fisher, R. Hernandez, D.T. Brown, T.S. Baker, M.G. Rossmann, and R.J. Kuhn Locations of carbohydrate sites on alphavirus glycoproteins show that E1 forms an icosahedral scaffold Cell 105 2001 127 136
34. F.A. Rey, F.X. Heinz, C. Mandl, C. Kunz, and S.C. Harrison The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution Nature 375 1995 291 298
35. M.G. Rossmann Fitting atomic models into electron-microscopy maps Acta Crystallogr. D Biol. Crystallogr. 56 2000 1341 1349
36. M.G. Rossmann, R. Bernal, and S.V. Pletnev Combining electron microscopic with x-ray crystallographic structures J. Struct. Biol. 136 2001 190 200
37. M. Sjoberg, and H. Garoff Interactions between the transmembrane segments of the alphavirus E1 and E2 proteins play a role in virus budding and fusion J. Virol. 77 2003 3441 3450
38. U. Skoging, M. Vihinen, L. Nilsson, and P. Liljestrom Aromatic interactions define the binding of the alphavirus spike to its nucleocapsid Structure 4 1996 519 529
39. T.J. Smith, R.H. Cheng, N.H. Olson, P. Peterson, E. Chase, R.J. Kuhn, and T.S. Baker Putative receptor binding sites on alphaviruses as visualized by cryoelectron microscopy Proc. Natl. Acad. Sci. USA 92 1995 10648 10652
40. J.H. Strauss, and E.G. Strauss The alphaviruses: gene expression, replication, and evolution Microbiol. Rev. 58 1994 491 562
41. E.G. Strauss, D.S. Stec, A.L. Schmaljohn, and J.H. Strauss Identification of antigenically important domains in the glycoproteins of Sindbis virus by analysis of antibody escape variants J. Virol. 65 1991 4654 4664
42. E.G. Strauss, E.M. Lenches, and J.H. Strauss Molecular genetic evidence that the hydrophobic anchors of glycoproteins E2 and E1 interact during assembly of alphaviruses J. Virol. 76 2002 10188 10194
43. C.H. von Bonsdorff, and S.C. Harrison Sindbis virus glycoproteins form a regular icosahedral surface lattice J. Virol. 16 1975 141 145
44. C.H. von Bonsdorff, and S.C. Harrison Hexagonal glycoprotein arrays from Sindbis virus membranes J. Virol. 28 1978 578 583
45. T.A. Wilkinson, T.L. Tellinghuisen, R.J. Kuhn, and C.B. Post Association of Sindbis virus capsid protein with phospholipid membranes and the E2 glycoprotein: implications for alphavirus assembly Biochemistry 44 2005 2800 2810
46. W. Zhang, B.R. Fisher, N.H. Olson, J.H. Strauss, R.J. Kuhn, and T.S. Baker Aura virus structure suggests that the T = 4 organization is a fundamental property of viral structural proteins J. Virol. 76 2002 7239 7246
47. W. Zhang, S. Mukhopadhyay, S.V. Pletnev, T.S. Baker, R.J. Kuhn, and M.G. Rossmann Placement of the structural proteins in Sindbis virus J. Virol. 76 2002 11645 11658
48. W. Zhang, P.R. Chipman, J. Corver, P.R. Johnson, Y. Zhang, S. Mukhopadhyay, T.S. Baker, J.H. Strauss, M.G. Rossmann, and R.J. Kuhn Visualization of membrane protein domains by cryo-electron microscopy of dengue virus Nat. Struct. Biol. 10 2003 907 912
49. X. Zhang, S.B. Walker, P.R. Chipman, M.L. Nibert, and T.S. Baker Reovirus polymerase lambda 3 localized by cryo-electron microscopy of virions at a resolution of 7.6 Å Nat. Struct. Biol. 10 2003 1011 1018
50. Y. Zhang, J. Corver, P.R. Chipman, W. Zhang, S.V. Pletnev, D. Sedlak, T.S. Baker, J.H. Strauss, R.J. Kuhn, and M.G. Rossmann Structures of immature flavivirus particles EMBO J. 22 2003 2604 2613
51. Y. Zhang, W. Zhang, S. Ogata, D. Clements, J.H. Strauss, T.S. Baker, R.J. Kuhn, and M.G. Rossmann Conformational changes of the flavivirus E glycoprotein Structure 12 2004 1607 1618
52. W. Zhang, M. Heil, R.J. Kuhn, and T.S. Baker Heparin binding sites on Ross River virus revealed by electron cryo-microscopy Virology 332 2005 511 518