A heptad repeat in herpes simplex virus 1 gH, Located downstream of the α-helix with attributes of a fusion peptide, is critical for virus entry and fusion

Journal of Virology

Volumn 79, Issue 11, 2005, Pages 7042-7049

  Gianni, Tatiana ^a   Menotti, Laura ^a   Campadelli Fiume, Gabriella ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; VIRUS FUSION PROTEIN;

ALPHA HELIX; ANIMAL CELL; ARTICLE; CELL FUSION; CELL MEMBRANE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; HERPES SIMPLEX VIRUS 1; HYDROPHOBICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RECEPTOR BINDING; VIRUS CELL INTERACTION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; CRICETINAE; DNA, VIRAL; GENETIC COMPLEMENTATION TEST; HERPESVIRUS 1, HUMAN; MEMBRANE FUSION; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; VIRAL ENVELOPE PROTEINS; VIRULENCE;

HERPES; HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 2; SUID HERPESVIRUS 1;

EID: 18744389465     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.11.7042-7049.2005     Document Type: Article

References (52)

1. Avitabile, E., G. Lombardi, and G. Campadelli-Fiume. 2003. Herpes simplex virus glycoprotein K, but not its syncytial allele, inhibits cell-cell fusion mediated by the four fusogenic glycoproteins, gD, gB, gH, and gL. J. Virol. 77:6836-6844.
2. Avitabile, E., G. Lombardi, T. Gianni, M. Capri, and G. Campadelli-Fiume. 2004. Coexpression of UL20p and gK inhibits cell-cell fusion mediated by herpes simplex virus glycoproteins gD, gH-gL, and wild-type gB or an endocytosis-defective gB mutant and downmodulates their cell surface expression. J. Virol. 78:8015-8025.
3. Babic, N., B. G. Klupp, B. Makoschey, A. Karger, A. Flamand, and T. C. Mettenleiter. 1996. Glycoprotein gH of pseudorabies virus is essential for penetration and propagation in cell culture and in the nervous system of mice. J. Gen. Virol. 77:2277-2285.
4. Brunetti, C. R., R. L. Burke, B. Hoflack, T. Ludwig, K. S. Dingwell, and D. C. Johnson. 1995. Role of mannose-6-phosphate receptors in herpes simplex virus entry into cells and cell-to-cell transmission. J. Virol. 69:3517-3528.
5. Bullough, P. A., F. M. Hughson, J. J. Skehel, and D. C. Wiley. 1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37-43.
6. Bullough, P. A., F. M. Hughson, A. C. Treharne, R. W. Ruigrok, J. J. Skehel, and D. C. Wiley. 1994. Crystals of a fragment of influenza haemagglutinin in the low pH induced conformation. J. Mol. Biol. 236:1262-1265.
7. Cai, W. H., B. Gu, and S. Person. 1988. Role of glycoprotein B of herpes simplex virus type 1 in viral entry and cell fusion. J. Virol. 62:2596-2604. Erratum, 62:4438.
8. Cairns, T. M., R. S. Milne, M. Ponce-de-Leon, D. K. Tobin, G. H. Cohen, and R. J. Eisenberg. 2003. Structure-function analysis of herpes simplex virus type 1 gD and gH-gL: clues from gDgH chimeras. J. Virol. 77:6731-6742.
9. Campadelli-Fiume, G., F. Cocchi, L. Menotti, and M. Lopez. 2000. The novel receptors that mediate the entry of herpes simplex viruses and animal alphaherpesviruses into cells. Rev. Med. Virol. 10:305-319.
10. 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.
11. Cocchi, F., L. Menotti, P. Mirandola, M. Lopez, and G. Campadelli-Fiume. 1998. The ectodomain of a novel member of the immunoglobulin superfamily related to the poliovirus receptor has the attributes of a bona fide receptor for herpes simplex viruses 1 and 2 in human cells. J. Virol. 72:9992-10002.
12. Cole, N. L., and C. Grose. 2003. Membrane fusion mediated by herpesvirus glycoproteins: the paradigm of varicella-zoster virus. Rev. Med. Virol. 13: 207-222.
13. 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.
14. Forrester, A., H. Farrell, G. Wilkinson, J. Kaye, N. Davis Poynter, and T. Minson. 1992. Construction and properties of a mutant of herpes simplex virus type 1 with glycoprotein H coding sequences deleted. J. Virol. 66:341-348.
15. Galdiero, M., A. Whiteley, B. Bruun, S. Bell, T. Minson, and H. Browne. 1997. Site-directed and linker insertion mutagenesis of herpes simplex virus type 1 glycoprotein H. J. Virol. 71:2163-2170.
16. Geraghty, R. J., C. Krummenacher, G. H. Cohen, R. J. Eisenberg, and P. G. Spear. 1998. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280:1618-1620.
17. Gianni, T., P. L. Martelli, R. Casadio, and G. Campadelli-Fiume. 2005. The ectodomain of herpes simplex virus glycoprotein H contains a membrane α-helix with attributes of an internal fusion peptide, positionally conserved in the Herpesviridae family. J. Virol. 79:2931-2940.
18. Gompels, U., and A. Minson. 1986. The properties and sequence of glycoprotein H of herpes simplex virus type 1. Virology 153:230-247.
19. Greenberg, M., N. Cammack, M. Salgo, and L. Smiley. 2004. HIV fusion and its inhibition in antiretroviral therapy. Rev. Med. Virol. 14:321-337.
20. 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.
21. Huber, M. T., and T. Compton. 1998. The human cytomegalovirus UL74 gene encodes the third component of the glycoprotein H-glycoprotein L-containing envelope complex. J. Virol. 72:8191-8197.
22. Hutchinson, L., H. Browne, V. Wargent, N. Davis-Poynter, S. Primorac, K. Goldsmith, A. C. Minson, and D. C. Johnson. 1992. A novel herpes simplex virus glycoprotein, gL, forms a complex with glycoprotein H (gH) and affects normal folding and surface expression of gH. J. Virol. 66:2240-2250.
23. Jahn, R., T. Lang, and T. C. Sudhof. 2003. Membrane fusion. Cell 112:519-533.
24. Jardetzky, T. S., and R. A. Lamb. 2004. Virology: a class act. Nature 427: 307-308.
25. Kieff, E. D., S. L. Bachenheimer, and B. Roizman. 1971. Size, composition, and structure of the deoxyribonucleic acid of herpes simplex virus subtypes 1 and 2. J. Virol. 8:125-132.
26. Krummenacher, C., A. V. Nicola, J. C. Whitbeck, H. Lou, W. Hou, J. D. Lambris, R. J. Geraghty, P. G. Spear, G. H. Cohen, and R. J. Eisenberg. 1998. Herpes simplex virus glycoprotein D can bind to poliovirus receptor-related protein 1 or herpesvirus entry mediator, two structurally unrelated mediators of virus entry. J. Virol. 72:7064-7074.
27. Ligas, M. W., and D. C. Johnson. 1988. A herpes simplex virus mutant in which glycoprotein D sequences are replaced by beta-galactosidase sequences binds to but is unable to penetrate into cells. J. Virol. 62:1486-1494.
28. Lopper, M., and T. Compton. 2004. Coiled-coil domains in glycoproteins B and H are involved in human cytomegalovirus membrane fusion. J. Virol. 78:8333-8341.
29. Lupas, A. 1997. Predicting coiled-coil regions in proteins. Curr. Opin. Struct. Biol. 7:388-393.
30. Lupas, A., M. Van Dyke, and J. Stock. 1991. Predicting coiled coils from protein sequences. Science 252:1162-1164.
31. Menotti, L., R. Casadio, C. Bertucci, M. Lopez, and G. Campadelli-Fiume. 2002. Substitution in the murine nectin1 receptor of a single conserved amino acid at a position distal from the herpes simplex virus gD binding site confers high affinity binding to gD. J. Virol. 76:5463-5471.
32. Menotti, L., F. Cocchi, and G. Campadelli-Fiume. 2002. Critical residues in the CC′ ridge of the human nectin1 receptor V domain enable herpes simplex virus entry into the cell and act synergistically with the downstream region. Virology 301:6-12.
33. Milne, R. S., S. L. Hanna, A. H. Rux, S. H. Willis, G. H. Cohen, and R. J. Eisenberg. 2003. Function of herpes simplex virus type 1 gD mutants with different receptor-binding affinities in virus entry and fusion. J. Virol. 77: 8962-8972.
34. Montgomery, R. I., M. S. Warner, B. J. Lum, and P. G. Spear. 1996. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87:427-436.
35. Mori, Y., X. Yang, P. Akkapaiboon, T. Okuno, and K. Yamanishi. 2003. Human herpesvirus 6 variant A glycoprotein H-glycoprotein L-glycoprotein Q complex associates with human CD46. J. Virol. 77:4992-4999.
36. Morrison, T. G. 2003. Structure and function of a paramyxovirus fusion protein. Biochim. Biophys. Acta 1614:73-84.
37. Okazaki, K., and H. Kida. 2004. A synthetic peptide from a heptad repeat region of herpesvirus glycoprotein B inhibits virus replication. J. Gen. Virol. 85:2131-2137.
38. Okuma, K., M. 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.
39. Peng, T., M. Ponce de Leon, M. J. Novotny, H. Jiang, J. D. Lambris, G. Dubin, P. G. Spear, G. H. Cohen, and R. J. Eisenberg. 1998. Structural and antigenic analysis of a truncated form of the herpes simplex virus glycoprotein gH-gL complex. J. Virol. 72:6092-6103.
40. Peng, T., M. Ponce-de-Leon, H. Jiang, G. Dubin, J. M. Lubinski, R. J. Eisenberg, and G. H. Cohen. 1998. The gH-gL complex of herpes simplex virus (HSV) stimulates neutralizing antibody and protects mice against HSV type 1 challenge. J. Virol. 72:65-72.
41. Pertel, P. E., A. Fridberg, M. L. Parish, and P. G. Spear. 2001. Cell fusion induced by herpes simplex virus glycoproteins gB, gD, and gH-gL requires a gD receptor but not necessarily heparan sulfate. Virology 279:313-324.
42. Rizo, J., and T. C. Sudhof. 2002. Snares and Munc18 in synaptic vesicle fusion. Nat. Rev. Neurosci. 3:641-653.
43. Roop, C., L. Hutchinson, and D. C. Johnson. 1993. A mutant herpes simplex virus type 1 unable to express glycoprotein L cannot enter cells, and its particles lack glycoprotein H. J. Virol. 67:2285-2297.
44. Rovero, S., A. Amici, E. D. Carlo, R. Bei, P. Nanni, E. Quaglino, P. Porcedda, K. Boggio, A. Smorlesi, P. L. Lollini, L. Landuzzi, M. P. Colombo, M. Giovarelli, P. Musiani, and G. Forni. 2000. DNA vaccination against rat her-2/Neu p185 more effectively inhibits carcinogenesis than transplantable carcinomas in transgenic BALB/c mice. J. Immunol. 165:5133-5142.
45. Showalter, S. D., M. Zweig, and B. Hampar. 1981. Monoclonal antibodies to herpes simplex virus type 1 proteins, including the immediate-early protein ICP 4. Infect. Immun. 34:684-692.
46. Skehel, J. J., and D. C. Wiley. 1998. Coiled coils in both intracellular vesicle and viral membrane fusion. Cell 95:871-874.
47. Spear, P. G., and R. Longnecker. 2003. Herpesvirus entry: an update. J. Virol. 77:10179-10185.
48. Turner, A., B. Bruun, T. Minson, and H. Browne. 1998. Glycoproteins gB, gD, and gHgL of herpes simplex virus type 1 are necessary and sufficient to mediate membrane fusion in a Cos cell transfection system. J. Virol. 72:873-875.
49. 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.
50. Watanabe, S., A. Takada, T. Watanabe, H. Ito, H. Kida, and Y. Kawaoka. 2000. Functional importance of the coiled-coil of the Ebola virus glycoprotein. J. Virol. 74:10194-10201.
51. Westra, D. F., H. B. Kuiperij, G. W. Welling, A. J. Scheffer, T. H. The, and S. Welling-Wester. 1999. Domains of glycoprotein H of herpes simplex virus type 1 involved in complex formation with glycoprotein L. Virology 261:96-105.
52. Zago, A., C. R. Jogger, and P. G. Spear. 2004. Use of herpes simplex virus and pseudorabies virus chimeric glycoprotein D molecules to identify regions critical for membrane fusion. Proc. Natl. Acad. Sci. USA 101:17498-17503.