Cell-to-cell spread of wild-type herpes simplex virus type 1, but not of syncytial strains, is mediated by the immunoglobulin-like receptors that mediate virion entry, Nectin1 (PRR1/HveC/HIgR) and Nectin2 (PRR2/HveB)

Journal of Virology

Volumn 74, Issue 8, 2000, Pages 3909-3917

  Cocchi, Francesca ^a   Menotti, Laura ^a   Dubreuil, Patrice ^b   Lopez, Marc ^b   Campadelli Fiume, Gabriella ^a,c  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b INSERM   (France)

^c Sezione di Microbiologia e Virologia   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; HERPES SIMPLEX VIRUS 1; NONHUMAN; PRIORITY JOURNAL; STRAIN DIFFERENCE; VIRION; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS INFECTIVITY;

ANTIBODIES, MONOCLONAL; CELL ADHESION; CELL ADHESION MOLECULES; CELL FUSION; CELL LINE; GIANT CELLS; HERPESVIRUS 1, HUMAN; HUMANS; MUTATION; PLAQUE ASSAY; RECEPTORS, VIRUS; VIRAL ENVELOPE PROTEINS; VIRION;

EID: 0034109367     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.8.3909-3917.2000     Document Type: Article

References (55)

1. Baines, J. D., and B. Roizman. 1993. The UL10 gene of herpes simplex virus 1 encodes a novel viral glycoprotein, gM. which is present in the virion and in the plasma membrane of infected cells. J. Virol. 67:1441-1452.
2. Balan, P., N. Davis-Poynter, H. Atkinson, H. Browne, and T. Minson. 1994. An analysis of the in vitro and in vivo phenotypes of mutants of herpes simplex virus type 1 lacking glycoprotein gG, gE, gI or the putative gJ. J. Gen. Virol. 75:1245-1258.
3. Cai, W. Z., S. Person, S. C. Warner, J. H. Zhou, and N. A. De Luca. 1987. Linker-insertion nonsense and restriction-site deletion mutations of the gB glycoprotein gene of herpes simplex virus type 1. J. Virol. 61:714-721.
4. Campadelli-Fiume, G., S. Qi, E. Avitabile, L. Foà-Tomasi, R. Brandimarti, and B. Roizman. 1990. Glycoprotein D of herpes simplex virus encodes a domain which precludes penetration of cells expressing the glycoprotein by superinfecting herpes simplex virus. J. Virol. 64:6070-6079.
5. Card, J. P., and L. W. Enquist. 1995. Neurovirulence of pseudorabies virus. Crit. Rev. Neurobiol. 9:137-162.
6. Cocchi, F., M. Lopez, L. Menotti, M. Aoubala, P. Dubreuil, and G. Campadelli-Fiume. 1998. The V domain of herpesvirus lg-like receptor (HIgR) contains a major functional region in herpes simplex virus-1 entry into cells and interacts physically with the viral glycoprotein D. Proc. Natl. Acad. Sci. USA 95:15700-15705.
7. 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.
8. Dingwell, K. S., C. R. Brunetti, R. L. Hendricks, Q. Tang, M. Tang, A. J. Rainbow, and D. C. Johnson. 1994. Herpes simplex virus glycoproteins E and I facilitate spread in vivo and across junctions of cultured cells. J. Virol. 68: 834-845.
9. Dingwell, K. S., L. C. Doering, and D. C. Johnson. 1995. Glycoproteins E and I facilitate neuron-to-neuron spread of herpes simplex virus. J. Virol. 69: 7087-7098.
10. Dingwell, K. S., and D. C. Johnson. 1998. The herpes simplex virus gE-gI complex facilitates cell-to-cell spread and binds to components of cell junctions. J. Virol. 72:8933-8942.
11. Eberlé, F., P. Dubreuil, M. G. Mattei, E. Devilard, and M. Lopez. 1995. The human PRR2 gene, related to the human poliovirus receptor gene (PVR), is the true homolog of the murine MPH gene. Gene 159:267-272.
12. Ejercito, P. M., E. D. Kieff, and B. Roizman. 1968. Characterization of herpes simplex virus strains differing in their effects on social behaviour of infected cells. J. Gen. Virol. 2:357-364.
13. Foà-Tomasi, L., E. Avitabile, and G. Campadelli-Fiume. 1995. Selection of a monoclonal antibody specific for variant B human herpesvirus 6-infected mononuclear cells. J. Virol. Methods 51:289-296.
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. 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.
16. Gompels, U., and A. Minson. 1986. The properties and sequence of glycoprotein H of herpes simplex virus type 1. Virology 153:230-247.
17. Gruenheid, S., L. Gatzke, H. Meadows, and F. Tufaro. 1993. Herpes simplex virus infection and propagation in a mouse L cell mutant lacking heparan sulfate proteoglycans. J. Virol. 67:93-100.
18. Haanes, E. J., C. M. Nelson, C. L. Soule, and J. L. Goodman. 1994. The UL45 gene product is required for herpes simplex virus type 1 glycoprotein-B-induced cell fusion. J. Virol. 68:5825-5834.
19. Highlander, S. L., S. L. Sutherland, P. J. Gage, D. C. Johnson, M. Levine, and J. C. Glorioso. 1987. Neutralizing monoclonal antibodies specific for herpes simplex virus glycoprotein D inhibit virus penetration. J. Virol. 61: 3356-3364.
20. Hoggan, M. D., and B. Roizman. 1959. The isolation and properties of a variant of herpes simplex producing multinucleated giant cells in monolayer cultures in the presence of antibody. Am. J. Hyg. 70:208-219.
21. Huang, T., and G. Campadelli-Fiume. 1996. Anti-idiotypic antibodies mimicking glycoprotein D of herpes simplex virus identify a cellular protein required for virus spread from cell to cell and viral induced polykaryocytosis. Proc. Natl. Acad. Sci. USA 93:1836-1840.
22. Johnson, D. C., R. L. Burke, and T. Gregory. 1990. Soluble forms of herpes simplex virus glycoprotein D bind to a limited number of cell surface receptors and inhibit virus entry into cells. J. Virol. 64:2569-2576.
23. Johnson, D. C., M. C. Frame, M. W. Ligas, A. M. Cross, and N. D. Stow. 1988. Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI. J. Virol. 62:1347-1354.
24. 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.
25. Krummenacher, C., A. H. Rux, J. C. Whitbeck, M. Ponce-de-Leon, H. Lou, I. Baribaud, W. Hou, C. Zou, R. J. Geraghty, P. G. Spear, R. J. Eisenberg, and G. H. Cohen. 1999. The first immunoglobulin-like domain of HveC is sufficient to bind herpes simplex virus gD with full affinity, while the third domain is involved in oligomerization of HveC. J. Virol. 73:8127-8137.
26. Ligas, M. W., and D. C. Johnson. 1988. A herpes simplex virus mutant in which glycoprotein D sequences are replaced by β-galactosidase sequences binds to but is unable to penetrate into cells. J. Virol. 62:1486-1494.
27. Lopez, M., M. Aoubala, F. Jordier, D. Isnardon, S. Gomez, and P. Dubreuil. 1998. The human poliovirus receptor related 2 protein is a new hematopoietic/endothelial homophilic adhesion molecule. Blood 92:4602-4611.
28. Lopez, M., F. Cocchi, L. Menotti, E. Avitabile, P. Dubreuil, and G. Campadelli-Fiume. 2000. Nectin2α (PRR2α or HveB) and nectin2δ are low-efficiency mediators for entry of herpes simplex virus mutants carrying the Leu25Pro substitution in glycoprotein D. J. Virol. 74:1267-1274.
29. Lopez, M., F. Eberlé, M. G. Mattei, J. Gabert, F. Birg, F. Bardin, C. Maroc, and P. Dubreuil. 1995. Complementary DNA characterization and chromosomal localization of a human gene related to the poliovirus receptor-encoding gene. Gene 155:261-265.
30. Lopez, M., F. Jordier, F. Bardin, L. Coulombel, C. Chabannon, and P. Dubreuil. 1997. Identification of a new class of IgG superfamily antigens expressed in hemopoiesis, p. 1081-1083. In T. Kishimoto, H. Kikutani, A. von der Borne, D. Y. Mason, M. Miyasaka, A. Moretta, K. Okumura, S. Shaw, T. A. Springer, K. Sugumura, and H. Zola (ed.), Leukocyte typing VI: white cell differentiation antigens. Garland Publishing, Inc., New York, N. Y.
31. MacLean, C. A., L. M. Robertson, and F. E. Jamieson. 1993. Characterization of the UL10 gene product of herpes simples virus type 1 and investigation of its role in vivo. J. Gen. Virol. 74:975-983.
32. Mendelsohn, C. L., E. Wimmer, and V. R. Racaniello. 1989. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56:855-865.
33. Miyahara, M., H. Nakanishi, K. Takahashi, K. Satoh-Horikawa, K. Tachibana, and Y. Takai. 2000. Interaction of nectin with afadin is necessary for its clustering at cell-cell contact sites but not for its cis dimerization or trans interaction. J. Biol. Chem. 275:613-618.
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. Navarro, D., P. Paz, and L. Pereira. 1992. Domains of herpes simplex virus glycoprotein B that function in virus penetration, cell-to-cell spread, and cell fusion. Virology 186:99-112.
36. Nicola, A. V., S. H. Willis, N. N. Naidoo, R. J. Eisenberg, and G. H. Cohen. 1996. Structure-function analysis of soluble forms of herpes simplex virus glycoprotein D. J. Virol. 70:3815-3822.
37. Nixdorf, R., J. Schmidt, A. Karger, and T. Mettenleiter. 1999. Infection of Chinese hamster ovary cells by pseudorabies virus. J. Virol. 73:8019-8026.
38. Noble, A. G., G. T. Lee, R. Sprague, M. L. Parish, and P. G. Spear. 1983. Anti-gD monoclonal antibodies inhibit cell fusion induced by herpes simplex virus type 1. Virology 129:218-224.
39. Novotny, M. J., M. L. Parish, and P. G. Spear. 1996. Variability of herpes simplex virus 1 gL and anti-gL antibodies that inhibit cell fusion but not viral infectivity. Virology 221:1-13.
40. Peeters, B., N. De Wind, M. Hooisma, F. Wagenaar, A. Gielkens, and R. Moormann. 1992. Pseudorabies virus envelope glycoproteins gp50 and gII are essential for virus penetration, but only gII is involved in membrane fusion. J. Virol. 66:894-905.
41. Raub, I., and T. C. Mettenleiter. 1991. Pseudorabies virus glycoproteins gII and gp50 are essential for virus penetration. J. Virol. 65:5348-5356.
42. Roizman, B., and A. E. Sears. 1996. Herpes simplex viruses and their replication, p. 2231-2295. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed., vol. 2. Lippincott-Raven Publishers, Philadelphia, Pa.
43. Roller, J. R., and D. Rauch. 1998. Herpesvirus entry mediator HVEM mediates cell-cell spread in BHK(TK ) cell clones. J. Virol. 72:1411-1417.
44. 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.
45. Schmidt, J., B. G. Klupp, A. Karger, and T. C. Mettenleiter. 1997. Adaptability in herpesviruses: glycoprotein D-independent infectivity of pseudorabies virus. J. Virol. 71:17-24.
46. Shieh, M. T., and P. G. Spear. 1994. Herpesvirus-induced cell fusion that is dependent on cell surface heparan sulfate or soluble heparin. J. Virol. 68: 1224-1228.
47. Shukla, D., J. Liu, P. Blaiklock, N. W. Shworak, X. Bai, J. D. Esko, G. H. Cohen, R. J. Eisenberg, R. D. Rosenberg, and P. G. Spear. 1999. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99: 13-22.
48. Spear, P. G. 1993. Membrane fusion induced by herpes simplex virus, p. 201-232. In J. Bentz (ed.), Viral fusion mechanisms. CRC Press, Inc., Boca Raton, Fla.
49. Spear, P. G., M. T. Shieh, B. C. Herold, D. WuDunn, and T. I. Koshy. 1992. Heparan sulfate glycosaminoglycans as primary cell surface receptors for herpes simplex virus. Adv. Exp. Med. Biol. 313:341-353.
50. Takahashi, K., H. Nakanishi, M. Miyahara, K. Mandai, K. Satoh, A. Satoh, H. Nishioka, J. Aoki, A. Nomoto, A. Mizoguchi, and Y. Takai. 1999. Nectin/ PRR: an immunoglobulin-like cell adhesion molecule recruited to cadherin-based adherens junctions through interaction with afadin, a PDZ domain-containing protein. J. Cell Biol. 145:539-549.
51. Terry-Allison, T., R. I. Montgomery, J. C. Whitbeck, R. Xu, G. H. Cohen, R. J. Eisenberg, and P. G. Spear. 1998. HveA (herpesvirus entry mediator A), a coreceptor for herpes simplex virus entry, also participates in virus-induced cell fusion. J. Virol. 72:5802-5810.
52. Tirabassi, R. S., R. A. Townley, M. G. Eldridge, and L. W. Enquist. 1997. Characterization of pseudorabies virus mutants expressing carboxy-terminal truncations of gE: evidence for envelope incorporation, virulence, and neurotropism domains. J. Virol. 71:6455-6464.
53. Warner, M. S., R. J. Geraghty, W. M. Martinez, R. I. Montgomery, J. C. Whitbeck, R. Xu, R. J. Eisenberg, G. H. Cohen, and P. G. Spear. 1998. A cell surface protein with herpesvirus entry activity (HveB) confers susceptibility to infection by mutants of herpes simplex virus type 1, herpes simplex virus type 2, and pseudorabies virus. Virology 246:179-189.
54. Whealy, M. E., J. P. Card, A. K. Robbins, J. R. Dubin, H. J. Rziha, and L. W. Enquist. 1993. Specific pseudorabies virus infection of the rat visual system requires both gI and gp63 glycoproteins. J. Virol. 67:3786-3797.
55. Wildy, P., W. C. Russel, and R. W. Horne. 1960. The morphology of herpes virus. Virology 12:204-222.