Identification of an N-terminal trimeric coiled-coil core within arenavirus glycoprotein 2 permits assignment to class I viral fusion proteins

Journal of Virology

Volumn 80, Issue 12, 2006, Pages 5897-5907

  Eschli, Bruno ^a   Quirin, Katharina ^b   Wepf, Alexander ^a   Weber, Jacqueline ^a   Zinkernagel, Rolf ^a   Hengartner, Hans ^a  

^a INSTITUTE OF EXPERIMENTAL IMMUNOLOGY   (Switzerland)

^b ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; FIBRITIN; GLYCOPROTEIN 1; GLYCOPROTEIN 2; PROTEIN PRECURSOR; PROTEIN SUBUNIT; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN; VIRUS GLYCOPROTEIN;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARENAVIRUS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CROSS LINKING; ELECTRON MICROSCOPY; GEL FILTRATION CHROMATOGRAPHY; HUMAN; HUMAN CELL; LIGHT SCATTERING; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN SYNTHESIS; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; VIRUS PARTICLE;

DIMERIZATION; DISULFIDES; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMBRANE GLYCOPROTEINS; MOLECULAR WEIGHT; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; VIRAL FUSION PROTEINS;

ARENAVIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS;

EID: 33744935523     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00008-06     Document Type: Article

References (56)

1. Barbouche, R., R. Miquelis, I. M. Jones, and E. Fenouillet. 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.
2. Beyer, W. R., H. Miletic, W. Ostertag, and D. von Laer. 2001. Recombinant expression of lymphocytic choriomeningitis virus strain WE glycoproteins: a single amino acid makes the difference. J. Virol. 75:1061-1064.
3. Beyer, W. R., D. Popplau, W. Garten, D. von Laer, and O. Lenz. 2003. Endoproteolytic processing of the lymphocytic choriomeningitis virus glycoprotein by the subtilase SKI-1/S1P. J. Virol. 77:2866-2872.
4. Borrow, P., and M. B. Oldstone. 1992. Characterization of lymphocytic choriomeningitis virus-binding protein(s): a candidate cellular receptor for the virus. J. Virol. 66:7270-7281.
5. Bowen, M. D., C. J. Peters, and S. T. Nichol. 1997. Phylogenetic analysis of the Arenaviridae: patterns of virus evolution and evidence for cospeciation between arenaviruses and their rodent hosts. Mol. Phylogenet. Evol. 8:301-316.
6. Bruns, M., L. Martinez Peralta, and F. Lehmann-Grube. 1983. Lymphocytic choriomeningitis virus. III. Structural proteins of the virion. J. Gen. Virol. 64:599-611.
7. Buchmeier, M. J. 2002. Arenaviruses: protein structure and function, 1st ed., vol. 1. Springer, Berlin, Germany.
8. Buchmeier, M. J., M. D. Bowen, and C. J. Peters. 2001. Arenaviridae: the viruses and their replication, 4th ed., vol. 2. Lippincott Williams and Wilkins, Philadelphia, Pa.
9. Buchmeier, M. J., H. A. Lewicki, O. Tomori, and M. B. Oldstone. 1981. Monoclonal antibodies to lymphocytic choriomeningitis and pichinde viruses: generation, characterization, and cross-reactivity with other arenaviruses. Virology 113:73-85.
10. Buchmeier, M. J., and B. S. Parekh. 1987. Protein structure and expression among arenaviruses. Curr. Top. Microbiol. Immunol. 133:41-57.
11. Buchmeier, M. J., P. J. Southern, B. S. Parekh, M. K. Wooddell, and M. B. Oldstone. 1987. Site-specific antibodies define a cleavage site conserved among arenavirus GP-C glycoproteins. J. Virol. 61:982-985.
12. Burns, J. W., and M. J. Buchmeier. 1991. Protein-protein interactions in lymphocytic choriomeningitis virus. Virology 183:620-629.
13. Calder, L. J., L. Gonzalez-Reyes, B. Garcia-Barreno, S. A. Wharton, J. J. Skehel, D. C. Wiley, and J. A. Melero. 2000. Electron microscopy of the human respiratory syncytial virus fusion protein and complexes that it forms with monoclonal antibodies. Virology 271:122-131.
14. Cao, W., M. D. Henry, P. Borrow, H. Yamada, J. H. Elder, E. V. Ravkov, S. T. Nichol, R. W. Compans, K. P. Campbell, and M. B. Oldstone. 1998. Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282:2079-2081.
15. Chen, L., P. M. Colman, L. J. Cosgrove, M. C. Lawrence, L. J. Lawrence, P. A. Tulloch, and J. J. German. 2001. Cloning, expression, and crystallization of the fusion protein of Newcastle disease virus. Virology 290:290-299.
16. Ciurea, A., P. Klenerman, L. Hunziker, E. Horvath, B. M. Senn, A. F. Ochsenbein, H. Hengartner, and R. M. Zinkernagel. 2000. Viral persistence in vivo through selection of neutralizing antibody-escape variants. Proc. Natl. Acad. Sci. USA 97:2749-2754.
17. Colman, P. M., and M. C. Lawrence. 2003. The structural biology of type I viral membrane fusion. Nat. Rev. Mol. Cell Biol. 4:309-319.
18. Di Simone, C., and M. J. Buchmeier. 1995. Kinetics and pH dependence of acid-induced structural changes in the lymphocytic choriomeningitis virus glycoprotein complex. Virology 209:3-9.
19. Di Simone, C., M. A. Zandonatti, and M. J. Buchmeier. 1994. Acidic pH triggers LCMV membrane fusion activity and conformational change in the glycoprotein spike. Virology 198:455-465.
20. Durell, S. R., I. Martin, J. M. Ruysschaert, Y. Shai, and R. Blumenthal. 1997. What studies of fusion peptides tell us about viral envelope glycoprotein-mediated membrane fusion. Mol. Membr. Biol. 14:97-112.
21. Dutch, R. E., T. S. Jardetzky, and R. A. Lamb. 2000. Virus membrane fusion proteins: biological machines that undergo a metamorphosis. Biosci. Rep. 20:597-612.
22. Earl, P. L., R. W. Doms, and B. Moss. 1990. Oligomeric structure of the human immunodeficiency virus type 1 envelope glycoprotein. Proc. Natl. Acad. Sci. USA 87:648-652.
23. Earp, L. J., S. E. Delos, H. E. Park, and J. M. White. 2005. The many mechanisms of viral membrane fusion proteins. Curr. Top. Microbiol. Immunol. 285:25-66.
24. Eckert, D. M., and P. S. Kim. 2001. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70:777-810.
25. Eichler, R., O. Lenz, T. Strecker, M. Eickmann, H. D. Klenk, and W. Garten. 2003. Identification of Lassa virus glycoprotein signal peptide as a transacting maturation factor. EMBO Rep. 4:1084-1088.
26. Froeschke, M., M. Basler, M. Groettrup, and B. Dobberstein. 2003. Long-lived signal peptide of lymphocytic choriomeningitis virus glycoprotein pGP-C. J. Biol. Chem. 278:41914-41920.
27. Gallaher, W. R., C. DiSimone, and M. J. Buchmeier. 2001. The viral transmembrane superfamily: possible divergence of Arenavirus and Filovirus glycoproteins from a common RNA virus ancestor. BMC Microbiol. 1:1.
28. Gallina, A., T. M. Hanley, R. Mandel, M. Trahey, C. C. Broder, G. A. Viglianti, and H. J. Ryser. 2002. Inhibitors of protein-disulfide isomerase prevent cleavage of disulfide bonds in receptor-bound glycoprotein 120 and prevent HIV-1 entry. J. Biol. Chem. 277:50579-50588.
29. Glushakova, S. E., I. S. Lukashevich, and L. A. Baratova. 1990. Prediction of arenavirus fusion peptides on the basis of computer analysis of envelope protein sequences. FEBS Lett. 269:145-147.
30. Glushakova, S. E., V. G. Omelyanenko, I. S. Lukashevitch, A. A. Bogdanov, Jr., A. B. Moshnikova, A. T. Kozytch, and V. P. Torchilin. 1992. The fusion of artificial lipid membranes induced by the synthetic arenavirus 'fusion peptide'. Biochim. Biophys. Acta 1110:202-208.
31. Heinz, F. X., and S. L. Allison. 2001. The machinery for flavivirus fusion with host cell membranes. Curr. Opin. Microbiol. 4:450-455.
32. Imperiali, M., C. Thoma, E. Pavoni, A. Brancaccio, N. Callewaert, and A. Oxenius. 2005. O mannosylation of alpha-dystroglycan is essential for lymphocytic choriomeningitis virus receptor function. J. Virol. 79:14297-14308.
33. Jardetzky, T. S., and R. A. Lamb. 2004. Virology: a class act. Nature 427:307-308.
34. Jones, D. T. 1999. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292:195-202.
35. Kielian, M., and F. A. Key. 2006. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4:67-76.
36. Kunz, S., J. M. Rojek, M. Kanagawa, C. F. Spiropoulou, R. Barresi, K. P. Campbell, and M. B. A. Oldstone. 2005. Posttranslational modification of α-dystroglycan, the cellular receptor for arenaviruses, by the glycosyltransferase LARGE is critical for virus binding. J. Virol. 79:14282-14296.
37. Kunz, S., N. Sevilla, D. B. McGavern, K. P. Campbell, and M. B. Oldstone. 2001. Molecular analysis of the interaction of LCMV with its cellular receptor [alpha]-dystroglycan. J. Cell Biol. 155:301-310.
38. Lenz, O., J. ter Meulen, H. D. Klenk, N. G. Seidah, and W. Garten. 2001. The Lassa virus glycoprotein precursor GP-C is proteolytically processed by subtilase SKI-1/SIP. Proc. Natl. Acad. Sci. USA 98:12701-12705.
39. Letarov, A. V., Y. Y. Lender, S. P. Boudko, and V. V. Mesyanzhinov. 1999. The carboxy-terminal domain initiates trimerization of bacteriophage T4 fibritin. Biochemistry (Moscow) 64:817-823.
40. Meyer, B. J., J. C. De La Torre, and P. J. Southern. 2002. Arenaviruses: genomic RNAs, transcription, and replication, 1st ed., vol. 1. Springer, Berlin, Germany.
41. Neuman, B. W., B. D. Adair, J. W. Burns, R. A. Milligan, M. J. Buchmeier, and M. Yeager. 2005. Complementarity in the supramolecular design of arenaviruses and retroviruses revealed by electron cryomicroscopy and image analysis. J. Virol. 79:3822-3830.
42. Parekh, B. S., and M. J. Buchmeier. 1986. Proteins of lymphocytic choriomeningitis virus: antigenic topography of the viral glycoproteins. Virology 153:168-178.
43. Ruigrok, R. W., A. Aitken, L. J. Calder, S. R. Martin, J. J. Skehel, S. A. Wharton, W. Weis, and D. C. Wiley. 1988. Studies on the structure of the influenza virus haemagglutinin at the pH of membrane fusion. J. Gen. Virol. 69:2785-2795.
44. Ryser, H. J., E. M. Levy, R. Mandel, and G. J. DiSciullo. 1994. Inhibition of human immunodeficiency virus infection by agents that interfere with thioldisulfide interchange upon virus-receptor interaction. Proc. Natl. Acad. Sci. USA 91:4559-4563.
45. Schawaller, M., G. E. Smith, J. J. Skehel, and D. C. Wiley. 1989. Studies with crosslinking reagents on the oligomeric structure of the env glycoprotein of HIV. Virology 172:367-369.
46. Schibli, D. J., and W. Weissenhorn. 2004. Class I and class II viral fusion protein structures reveal similar principles in membrane fusion. Mol. Membr. Biol. 21:361-371.
47. Seiler, P., U. Kalinke, T. Rulicke, E. M. Bucher, C. Bose, R. M. Zinkernagel, and H. Hengartner. 1998. Enhanced virus clearance by early inducible lymphocytic choriomeningitis virus-neutralizing antibodies in immunoglobulin-transgenic mice. J. Virol. 72:2253-2258.
48. Singh, M., B. Berger, and P. S. Kim. 1999. LearnCoil-VMF: computational evidence for coiled-coil-like motifs in many viral membrane-fusion proteins. J. Mol. Biol. 290:1031-1041.
49. Sissoeff, L., M. Mousli, P. England, and C. Tuffereau. 2005. Stable trimerization of recombinant rabies virus glycoprotein ectodomain is required for interaction with the p75NTR receptor. J. Gen. Virol. 86:2543-2552.
50. 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.
51. Spiropoulou, C. F., S. Kunz, P. E. Rollin, K. P. Campbell, and M. B. Oldstone. 2002. New World arenavirus clade C, but not clade A and B viruses, utilizes α-dystroglycan as its major receptor. J. Virol. 76:5140-5146.
52. Stevens, J., A. L. Corper, C. F. Basler, J. K. Taubenberger, P. Palese, and I. A. Wilson. 2004. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303:1866-1870.
53. Wallin, M., M. Ekstrom, and H. Garoff. 2004. Isomerization of the intersubunit disulphide-bond in Env controls retrovirus fusion. EMBO J. 23:54-65.
54. Weber, E. L., and M. J. Buchmeier. 1988. Fine mapping of a peptide sequence containing an antigenic site conserved among arenaviruses. Virology 164:30-38.
55. Wright, K. E., R. C. Spiro, J. W. Burns, and M. J. Buchmeier. 1990. Posttranslational processing of the glycoproteins of lymphocytic choriomeningitis virus. Virology 177:175-183.
56. Yang, X., J. Lee, E. M. Mahony, P. D. Kwong, R. Wyatt, and J. Sodroski. 2002. Highly stable trimers formed by human immunodeficiency virus type 1 envelope glycoproteins fused with the trimeric motif of T4 bacteriophage fibritin. J. Virol. 76:4634-4642.