Binding-site interactions between epstein-barr virus fusion proteins gp42 and gH/gL reveal a peptide that inhibits both epithelial and B-cell membrane fusion

Journal of Virology

Volumn 81, Issue 17, 2007, Pages 9216-9229

  Kirschner, Austin N ^a   Lowrey, Amanda S ^b   Longnecker, Richard ^b   Jardetzky, Theodore S ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; MEMBRANE PROTEIN; PROTEIN GB; PROTEIN GH; PROTEIN GL; PROTEIN GP42; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; B LYMPHOCYTE; BINDING COMPETITION; BINDING SITE; CELL FUSION; COMPLEX FORMATION; CONTROLLED STUDY; DELETION MUTANT; EPITHELIUM CELL; EPSTEIN BARR VIRUS; HERPES VIRUS; HUMAN; HUMAN CELL; MEMBRANE FUSION; MUTAGENESIS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; VIRUS CELL INTERACTION;

ANIMALS; ANTIVIRAL AGENTS; B-LYMPHOCYTES; BINDING SITES; CELL LINE; EPITHELIAL CELLS; GENETIC COMPLEMENTATION TEST; GLYCOPROTEINS; HERPESVIRUS 4, HUMAN; HUMANS; INSECTS; MEMBRANE GLYCOPROTEINS; MOLECULAR CHAPERONES; PEPTIDES; POINT MUTATION; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION; VIRAL FUSION PROTEINS; VIRAL PROTEINS; VIRUS INTERNALIZATION;

HUMAN HERPESVIRUS 4;

EID: 34548162579     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00575-07     Document Type: Article

References (60)

1. Balachandran, N., D. E. Oba, and L. M. Hutt-Fletcher. 1987. Antigenic cross-reactions among herpes simplex virus types 1 and 2, Epstein-Barr virus, and cytomegalovirus. J. Virol. 61:1125-1135.
2. Borza, C. M., and L. Hutt-Fletcher. 2002. Alternate Replication in B cells and epithelial cells switches tropism of Epstein-Barr virus. Nat. Med. 8:594-599.
3. Borza, C. M., A. J. Morgan, S. M. Turk, and L. M. Hutt-Fletcher. 2004. Use of gHgL for attachment of Epstein-Barr virus to epithelial cells compromises infection. J. Virol. 78:5007-5014.
4. Burkitt, D. 1962. A tumour syndrome affecting children in tropical Africa. Postgrad. Med. J. 38:71-79.
5. Carfi, A., H. Gong, H. Lou, S. H. Willis, G. H. Cohen, R. J. Eisenberg, and D. C. Wiley. 2002. Crystallization and preliminary diffraction studies of the ectodomain of the envelope glycoprotein D from herpes simplex virus 1 alone and in complex with the ectodomain of the human receptor HveA. Acta Crystallogr. D 58:836-838.
6. Cocchi, F., D. Fusco, L. Menotti, T. Gianni, R. J. Eisenberg, G. H. Cohen, and G. Campadelli-Fiume. 2004. The soluble ectodomain of herpes simplex virus gD contains a membrane-proximal pro-fusion domain and suffices to mediate virus entry. Proc. Natl. Acad. Sci. USA 101:7445-7450.
7. Diakidi-Kosta, A., G. Michailidou, G. Kontogounis, A. Sivropoulou, and M. Arsenakis. 2003. A single amino acid substitution in the cytoplasmic tail of the glycoprotein B of herpes simplex virus 1 affects both syncytium formation and binding to intracellular heparan sulfate. Virus Res. 93:99-108.
8. Epstein, M. A., B. G. Achong, and Y. M. Barr. 1964. Virus particles in cultured lymphoblasts from Burkitt's lymphoma. Lancet 15:702-703.
9. Fusco, D., C. Forghieri, and G. Campadelli-Fiume. 2005. The pro-fusion domain of herpes simplex virus glycoprotein D (gD) interacts with the gD N terminus and is displaced by soluble forms of viral receptors. Proc. Natl. Acad. Sci. USA 102:9323-9328.
10. Haan, K. M., W. W. Kwok, R. Longnecker, and P. Speck. 2000. Epstein-Barr virus entry utilizing HLA-DP or HLA-DQ as a coreceptor. J. Virol. 74:2451-2454.
11. Haan, K. M., S. K. Lee, and R. Longnecker. 2001. Different functional domains in the cytoplasmic tail of glycoprotein B are involved in Epstein-Barr virus-induced membrane fusion. Virology 290:106-114.
12. Haan, K. M., and R. Longnecker. 2000. Coreceptor restriction within the HLA-DQ locus for Epstein-Barr virus infection. Proc. Natl. Acad. Sci. USA 97:9252-9257.
13. Haddad, R. S., and L. M. Hutt-Fletcher. 1989. Depletion of glycoprotein gp85 from virosomes made with Epstein-Barr virus proteins abolishes their ability to fuse with virus receptor-bearing cells. J. Virol. 63:4998-5005.
14. Heldwein, E. E., H. Lou, F. C. Bender, G. H. Cohen, R. J. Eisenberg, and S. C. Harrison. 2006. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313:217-220.
15. Henle, G., W. Henle, and V. Diehl. 1968. Relation of Burkitt's tumor-associated herpes-type virus to infectious mononucleosis. Proc. Natl. Acad. Sci. USA 59:94-101.
16. Henle, W., and G. Henle. 1970. Evidence for a relation of Epstein-Barr virus to Burkitt's lymphoma and nasopharyngeal carcinoma. Bibl. Haematol. 1970:706-713.
17. Henle, W., and G. Henle. 1977. Evidence for an etiologic relation of the Epstein-Barr virus to human malignancies. Laryngoscope 87:467-473.
18. Henle, W., and G. Henle. 1969. The relation between the Epstein-Barr virus and infectious mononucleosis, Burkitt's lymphoma and cancer of the post-nasal space. East Afr. Med. J. 46:402-406.
19. Hutt-Fletcher, L. M., and C. M. Lake. 2001. Two Epstein-Barr virus glycoprotein complexes. Curr. Top. Microbiol. Immunol. 258:51-64.
20. Hutt-Fletcher, L. M., and S. M. Turk. 2001. Virus isolation. Methods Mol. Biol. 174:119-123.
21. Jardetzky, T. S., and R. A. Lamb. 2004. Virology: a class act. Nature 427:307-308.
22. Jones, N. A., and R. J. Geraghty. 2004. Fusion activity of lipid-anchored envelope glycoproteins of herpes simplex virus type 1. Virology 324:213-228.
23. Kirschner, A. N., J. Omerovic, B. Popov, R. Longnecker, and T. S. Jardetzky. 2006. Soluble Epstein-Barr virus glycoproteins gH, gL, and gp42 form a 1:1:1 stable complex that acts like soluble gp42 in B-cell fusion but not in epithelial cell fusion. J. Virol. 80:9444-9454.
24. Krummenacher, C., V. M. Supekar, J. C. Whitbeck, E. Lazear, S. A. Connolly, R J. Eisenberg, G. H. Cohen, D. C. Wiley, and A. Carfi. 2005. Structure of unliganded HSV gD reveals a mechanism for receptor-mediated activation of virus entry. EMBO J. 24:4144-4153.
25. Li, Q., C. Buranathai, C. Grose, and L. M. Hutt-Fletcher. 1997. Chaperone functions common to nonhomologous Epstein-Barr virus gL and varicella-zoster virus gL proteins. J. Virol. 71:1667-1670.
26. Li, Q., M. K. Spriggs, S. Kovats, S. M. Turk, M. R. Comeau, B. Nepom, and L. M. Hutt-Fletcher. 1997. Epstein-Barr virus uses HLA class II as a cofactor for infection of B lymphocytes. J. Virol. 71:4657-4662.
27. Li, Q., S. M. Turk, and L. M. Hutt-Fletcher. 1995. The Epstein-Barr virus (EBV) BZLF2 gene product associates with the gH and gL homologs of EBV and carries an epitope critical to infection of B cells but not of epithelial cells. J. Virol. 69:3987-3994.
28. McShane, M. P., and R. Longnecker. 2004. Cell-surface expression of a mutated Epstein-Barr virus glycoprotein B allows fusion independent of other viral proteins. Proc. Natl. Acad. Sci. USA 101:17474-17479.
29. McShane, M. P., M. M. Mullen, K. M. Haan, T. S. Jardetzky, and R. Longnecker. 2003. Mutational analysis of the HLA class II interaction with Epstein-Barr virus glycoprotein 42. J. Virol. 77:7655-7662.
30. Miller, N., and L. M. Hutt-Fletcher. 1988. A monoclonal antibody to glycoprotein gp85 inhibits fusion but not attachment of Epstein-Barr virus. J. Virol. 62:2366-2372.
31. Molesworth, S. J., C. M. Lake, C. M. Borza, S. M. Turk, and L. M. Hutt-Fletcher. 2000. Epstein-Barr virus gH is essential for penetration of B cells but also plays a role in attachment of virus to epithelial cells. J. Virol. 74:6324-6332.
32. Mullen, M. M., K. M. Haan, R. Longnecker, and T. S. Jardetzky. 2002. Structure of the Epstein-Barr virus gp42 protein bound to the MHC class II receptor HLA-DR1. Mol. Cell 9:375-385.
33. Oda, T., S. Imai, S. Chiba, and K. Takada. 2000. Epstein-Barr virus lacking glycoprotein gp85 cannot infect B cells and epithelial cells. Virology 276:52-58.
34. Okuma, K. M., S. Nakamura, S. Nakano, Y. Niho, and Y. Matsuura. 1999. Host range of human T-cell leukemia virus type I analyzed by a cell fusion-dependent reporter gene activation assay. Virology 254:235-244.
35. Omerovic, J., L. Lev, and R. Longnecker. 2005. The amino terminus of Epstein-Barr virus glycoprotein gH is important for fusion with epithelial and B cells. J. Virol. 79:12408-12415.
36. Omerovic, J., and R. Longnecker. 1 May 2007, posting date. Functional homology of gHs and gLs from EBV-related γ-herpesviruses for EBV-induced membrane fusion. Virology 365:157-165. [Epub ahead of print.]
37. Perez-Romero, P., A. Perez, A. Capul, R. Montgomery, and A. O. Fuller. 2005. Herpes simplex virus entry mediator associates in infected cells in a complex with viral proteins gD and at least gH. J. Virol. 79:4540-4544.
38. Ressing, M. E., D. van Leeuwen, F. A. Verreck, S. Keating, R. Gomez, K. L. Franken, T. H. Ottenhoff, M. Spriggs, T. N. Schumacher, L. M. Hutt-Fletcher, M. Rowe, and E. J. Wiertz. 2005. Epstein-Barr virus gp42 is post-translationally modified to produce soluble gp42 that mediates HLA class II immune evasion. J. Virol. 79:841-852.
39. Rey, F. A. 2006. Molecular gymnastics at the herpesvirus surface. EMBO Rep. 7:1000-1005.
40. Rickinson, A. B., and E. Kieff. 1996. Epstein-Barr virus, p. 2397-2446. In B. N. Fields, D. M. Knipe, P. M. Howley, R. M. Chanock, J. L. Melnick, T. P. Monath, B. Roizman, and S. E. Straus (ed.), Virology, 3rd ed. Raven Press, Ltd., New York, NY.
41. Silva, A. L., J. Omerovic, T. S. Jardetzky, and R. Longnecker. 2004. Mutational analyses of Epstein-Barr virus glycoprotein 42 reveal functional domains not involved in receptor binding but required for membrane fusion. J. Virol. 78:5946-5956.
42. Sodora, D. L., G. H. Cohen, M. I. Muggeridge, and R. J. Eisenberg. 1991. Absence of asparagine-linked oligosaccharides from glycoprotein D of herpes simplex virus type 1 results in a structurally altered but biologically active protein. J. Virol. 65:4424-4431.
43. Spear, P. G., and R. Longnecker. 2003. Herpesvirus entry: an update. J. Virol. 77:10179-10185.
44. Spear, P. G., S. Manoj, M. Yoon, C. R. Jogger, A. Zago, and D. Myscofski. 2006. Different receptors binding to distinct interfaces on herpes simplex virus gD can trigger events leading to cell fusion and viral entry. Virology 344:17-24.
45. Speck, P., K. M. Haan, and R. Longnecker. 2000. Epstein-Barr virus entry into cells. Virology 277:1-5.
46. Spriggs, M. K., R. J. Armitage, M. R. Comeau, L. Strockbine, T. Farrah, B. Macduff, D. Ulrich, M. R. Alderson, J. Mullberg, and J. I. Cohen. 1996. The extracellular domain of the Epstein-Barr virus BZLF2 protein binds the HLA-DR beta chain and inhibits antigen presentation. J. Virol. 70:5557-5563.
47. Steven, A. C., and P. G. Spear. 2006. Biochemistry. Viral glycoproteins and an evolutionary conundrum. Science 313:177-178.
48. Strnad, B. C., T. Schuster, R. Klein, R. F. Hopkins III, T. Witmer, R. H. Neubauer, and H. Rabin. 1982. Production and characterization of monoclonal antibodies against the Epstein-Barr virus membrane antigen. J. Virol. 41:258-264.
49. Subramanian, R. P., and R. J. Geraghty. 2007. Herpes simplex virus type 1 mediates fusion through a hemifusion intermediate by sequential activity of glycoproteins D, H, L, and B. Proc. Natl. Acad. Sci. USA 104:2903-2908.
50. Takada, K. 2001. Role of Epstein-Barr virus in Burkitt's lymphoma. Curr. Top. Microbiol. Immunol. 258:141-151.
51. Takada, K., K. Horinouchi, Y. Ono, T. Aya, T. Osato, M. Takahashi, and S. Hayasaka. 1991. An Epstein-Barr virus-producer line Akata: establishment of the cell line and analysis of viral DNA. Virus Genes 5:147-156.
52. Urquiza, M., J. Suarez, R. Lopez, E. Vega, H. Patino, J. Garcia, M. A. Patarroyo, F. Guzman, and M. E. Patarroyo. 2004. Identifying gp85-regions involved in Epstein-Barr virus binding to B-lymphocytes. Biochem. Biophys. Res. Commun. 319:221-229.
53. Volpi, A. 2004. Epstein-Barr virus and human herpesvirus type 8 infections of the central nervous system. Herpes 11(Suppl. 2):120A-127A.
54. Wang, X., and L. M. Hutt-Fletcher. 1998. Epstein-Barr virus lacking glycoprotein gp42 can bind to B cells but is not able to infect. J. Virol. 72:158-163.
55. Wang, X., W. J. Kenyon, Q. Li, J. Mullberg, and L. M. Hutt-Fletcher. 1998. Epstein-Barr virus uses different complexes of glycoproteins gH and gL to infect B lymphocytes and epithelial cells. J. Virol. 72:5552-5558.
56. Wei, W. I., and J. S. Sham. 2005. Nasopharyngeal carcinoma. Lancet 365:2041-2054.
57. Whetter, L. E., S. P. Day, E. A. Brown, O. Elroy-Stein, and S. M. Lemon. 1994. Analysis of hepatitis A virus translation in a T7 polymerase-expressing cell line. Arch. Virol. Suppl. 9:291-298.
58. Wu, L., C. M. Borza, and L. M. Hutt-Fletcher. 2005. Mutations of Epstein-Barr virus gH that are differentially able to support fusion with B cells or epithelial cells. J. Virol. 79:10923-10930.
59. Wu, L., and L. M. Hutt-Fletcher. 2007. Point mutations in EBV gH that abrogate or differentially affect B cell and epithelial cell fusion. Virology.
60. Yaswen, L. R., E. B. Stephens, L. C. Davenport, and L. M. Hutt-Fletcher. 1993. Epstein-Barr virus glycoprotein gp85 associates with the BKRF2 gene product and is incompletely processed as a recombinant protein. Virology 195:387-396.