Heparan sulfate proteoglycan binding by herpes simplex virus type 1 glycoproteins B and C, which differ in their contributions to virus attachment, penetration, and cell-to-cell spread

Journal of Virology

Volumn 72, Issue 7, 1998, Pages 6119-6130

  Laquerre, Sylvie ^a   Argnani, Rafaela ^b   Anderson, Dina B ^a   Zucchini, Silvia ^b   Manservigi, Roberto ^b   Glorioso, Joseph C ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FERRARA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN B; PROTEIN C; PROTEOHEPARAN SULFATE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE MUTATION; HERPES SIMPLEX VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; VIRUS ADSORPTION; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS TRANSMISSION;

EID: 0031746910     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.7.6119-6130.1998     Document Type: Article

References (68)

1. Allen, G. P., and L. D. Coogle. 1988. Characterization of an equine herpesvirus type 1 gene encoding a glycoprotein (gp13) with homology to herpes simplex virus glycoprotein C. J. Virol. 62:2850-2858.
2. Baines, J. D., and B. Roizman. 1993. The UL10 gene of herpes simplex virus 1 encodes a novel glycoprotein, gM, which is present in the virion and in the plasma membrane of infected cells. J. Virol. 67:1441-1452.
3. Banfield, B. W., Y. Leduc, L. Esford, K. Schubert, and F. Tufaro. 1995. Sequential isolation of proteoglycan synthesis mutants by using herpes simplex virus as a selective agent: evidence for a proteoglycan-independent virus entry pathway. J. Virol. 69:3290-3298.
4. Bergström, T., E. Trybala, and D. Spillmann. 1997. Heparan sulfate and viral tropism. Nat. Med. 3:1177.
5. Cai, W., 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.
6. Cai, W., S. Person, S. C. Warner, J. Zhou, and N. A. DeLuca. 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.
7. Campadelli-Fiume, G., D. Stirpe, A. Boscaro, E. Avitabile, L. Foá-Tomasi, D. Barker, and B. Roizman. 1990. Glycoprotein C-dependent attachment of herpes simplex virus to susceptible cells leading to productive infection. Virology 178:213-222.
8. Cardin, A. D., and H. J. R. Weintraub. 1989. Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9:21-32.
9. Compton, T., D. M. Nowlin, and N. R. Cooper. 1993. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology 193:834-841.
10. Desai, P., F. L. Homa, S. Person, and J. C. Glorioso. 1994. A genetic selection method for the transfer of HSV-1 glycoprotein B mutations from plasmid to the viral genome: preliminary characterization of transdominance and entry kinetics of mutant viruses. Virology 204:312-322.
11. Desai, P. J., P. A. Schaffer, and A. C. Minson. 1988. Excretion of non-infectious virus particles lacking glycoprotein H by a temperature-sensitive mutant of herpes simplex virus type 1: evidence that gH is essential for virion infectivity. J. Gen. Virol. 69:1147-1156.
12. 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 cell-to-cell spread in vivo and across junctions of cultured cells. J. Virol. 68:834-845.
13. Dolter, K. E., W. F. Goins, M. Levine, and J. C. Glorioso. 1992. Genetic analysis of type-specific antigenic determinants of herpes simplex virus glycoprotein C. J. Virol. 66:4864-4873.
14. Feyzi, E., E. Trybala, T. Bergström, U. Lindani, and D. Spillmann. 1997. Structural requirement of heparan sulfate for interaction with herpes simplex virus type 1 glycoprotein C. J. Biol. Chem. 272:24850-24857.
15. Fitzpatrick, D. R., L. A. Babiuk, and T. J. Zamb. 1989. Nucleotide sequence of bovine herpesvirus type 1 glycoprotein gIII, a structural model of gIII as a new member of the immunoglobulin superfamily, and implications for the homologous glycoproteins of other herpesviruses. Virology 173:46-57.
16. Fuller, A. O., and W.-C. Lee. 1992. Herpes simplex virus type 1 entry through a cascade of virus-cell interactions requires different roles of gD and gH in penetration. J. Virol. 66:5002-5012.
17. Gallagher, J. T., M. Lyon, and W. P. Steward. 1986. Structure and function of heparan sulfate proteoglycans. Biochem. J. 236:313-325.
18. Gerber, S. I., B. J. Belval, and B. C. Herold. 1995. Differences in the role of glycoprotein C of HSV-1 and HSV-2 in viral binding may contribute to serotype differences in cell tropism. Virology 214:29-39.
19. 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.
20. Handler, G. C., R. J. Eisenberg, and G. H. Cohen. 1996. Oligomeric structure of glycoproteins in herpes simplex virus type 1. J. Virol. 70:6067-6075.
21. Handler, G. C., G. H. Cohen, and R. J. Eisenberg. 1996. Oligomeric structure of glycoproteins in herpes simplex virus type 1. J. Virol. 70:6076-6082.
22. Haywood, A. M. 1994. Virus receptors: binding, adhesion strengthening, and changes in viral structure. J. Virol. 68:1-5.
23. Herold, B. C., S. I. Gerber, B. J. Belval, A. M. Siston, and N. Shulman. 1996. Differences in the susceptibility of herpes simplex virus types 1 and 2 to modified heparin compounds suggest serotype differences in viral entry. J. Virol. 70:3461-3469.
24. Herold, B. C., S. I. Gerber, T. Polonsky, B. J. Belval, P. N. Shaklee, and K. Holme. 1995. Identification of structural features of heparin required for inhibition of herpes simplex virus type 1 binding. Virology 206:1108-1116.
25. Herold, B. C., R. J. Visalli, N. Sumarski, C. R. Brandt, and P. G. Spear. 1994. Glycoprotein C-independent binding of herpes simplex virus to cells requires cell surface heparan sulfate and glycoprotein B. J. Gen. Virol. 75:1211-1222.
26. Herold, B. C., D. WuDunn, N. Soltys, and P. G. Spear. 1991. Glycoprotein C of herpes simplex virus type 1 plays a principal role in the adsorption of virus to cells and in infectivity. J. Virol. 65:1090-1098.
27. Herold, B. C., S. I. Gerber, B. J. Belval, A. M. Siston, and N. Scrulman. 1996. Differences in the susceptibility of herpes simplex virus types 1 and 2 to modified heparin compounds suggest serotype differences in viral entry. J. Virol. 70:3461-3469.
28. Highlander, S. L., W. F. Goins, S. Person, T. C. Holland, M. Levine, and J. C. Glorioso. 1991. Oligomer formation of the gB glycoprotein of herpes simplex virus type 1. J. Virol. 50:805-812.
29. 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.
30. Holland, T. C., F. L. Homa, S. D. Marlin, M. Levine, and J. C. Glorioso. 1984. Herpes simplex virus type 1 glycoprotein C-negative mutants exhibit multiple phenotypes, including secretion of truncated glycoproteins. J. Virol. 52:566-574.
31. Homa, F. L., D. J. M. Purifoy, J. C. Glorioso, and M. Levine. 1986. Molecular basis of the glycoprotein C-negative phenotypes of herpes simplex virus type 1 mutants selected with a virus-neutralizing monoclonal antibody. J. Virol. 58:281-289.
32. 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 glycoprotein, gL, forms a complex with glycoprotein H (gH) and affects normal folding and surface expression of gH. J. Virol. 66:2240-2250.
33. Hutchinson, L., K. Goldsmith, D. Snoddy, H. Ghosh. F. L. Graham, and D. C. Johnson. 1992. Identification and characterization of a novel herpes simplex virus glycoprotein, gK, involved in cell fusion. J. Virol. 66:5603-5609.
34. Hutchinson, L., and D. C. Johnson. 1995. Herpes simplex virus glycoprotein K promotes egress of virus particles. J. Virol. 69:5401-5413.
35. Johnson, D. C., and M. W. Ligas. 1988. Herpes simplex viruses lacking glycoprotein D are unable to inhibit viral penetration: quantitative evidence for virus-specific cell surface receptors. J. Virol. 62:4605-4612.
36. Johnson, D. C., M. R. McDermott, C. Chrisp, and J. C. Glorioso. 1986. Pathogenicity in mice of herpes simplex virus type 2 mutants unable to express glycoprotein C. J. Virol. 58:36-42.
37. Karger, A., and T. C. Mettenleiter. 1993. Glycoproteins gill and gp50 play dominant roles in the biphasic attachment of pseudorabies virus. Virology 194:654-664.
38. 34a. Karger, A., A. Saalmüller, F. Tufaro, B. W. Banfield, and T. C. Mettenleiter. 1995. Cell surface proteoglycans are not essential for infection by pseudorabies virus. J. Virol. 69:3482-3489.
39. Kjellén, L., and U. Lindahl. 1991. Proteoglycans: structures and interactions. Annu. Rev. Biochem. 60:443-475.
40. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
41. Langeland, N., H. Holmsen, J. R. Lillebaug, and L. Haarr. 1987. Evidence that neomycin inhibits binding of herpes simplex virus type 1 to the cellular receptor. J. Virol. 61:3388-3393.
42. Langeland, N., L. J. Moore, H. Holmsen, and L. Haarr. 1988. Interaction of polylysine with the cellular receptor for herpes simplex virus type 1. J. Gen. Virol. 69:1137-1145.
43. Liang, X., L. A. Babiuk, S. van Drunen Littel-van den Hurk, D. R. Fitzpatrick, and T. J. Lamb. 1991. Bovine herpesvirus 1 attachment to permissive cells is mediated by its major glycoproteins gI, gIII, and gIV. J. Virol. 65:1124-1132.
44. Liang, X., L. A. Babiuk, and T. J. Zamb. 1993. Mapping of heparin-binding structures of bovine herpesvirus 1 and pseudorabies virus gIII glycoproteins. Virology 194:233-243.
45. Lidholt, K., J. L. Weinke, C. S. Kiser, F. N. Lugemwa, K. J. Bame, S. Cheifetz, J. Massague, U. Lindahl, and J. D. Esko. 1992. A single mutation affects both N-acetylglucosaminyltransferase and glucoronosyltransferase activities in a Chinese hamster ovary cell mutant defective in heparan sulfate biosynthesis. Proc. Natl. Acad. Sci. USA 89:2267-2271.
46. 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.
47. Little, S. P., J. T. Jofre. R. J. Courtney, and P. A. Schaffer. 1981. A virion-associated glycoprotein essential for infectivity of herpes simplex virus type 1. Virology 115:149-160.
48. Lycke, E., M. Johansson, B. Svennerholm, and U. Lindahl. 1991. Binding of herpes simplex virus to cellular heparan sulfate, an initial step in the adsorption process. J. Gen. Virol. 72:1131-1137.
49. Manservigi, R., P. G. Spear, and A. Buchan. 1977. Cell fusion induced by herpes simplex virus is promoted and suppressed by different viral glycoproteins. Proc. Natl. Acad. Sci. USA 74:3913-3917.
50. Marlin, S. D., S. L. Highlander, T. C. Holland, M. Levine, and J. C. Glorioso. 1986. Antigenic variation (mar mutations) in herpes simplex virus glycoprotein B can induce temperature-dependent alterations in gB processing and virus production. J. Virol. 59:142-153.
51. Marlin, S. D., T. C. Holland, M. Levine, and J. C. Glorioso. 1985. Epitopes of herpes simplex virus type 1 glycoprotein gC are clustered in two distinct antigenic sites. J. Virol. 53:128-136.
52. McClain, D. S., and A. O. Fuller. 1994. Cell-specific kinetics and efficiency of herpes simplex virus type 1 are determined by two distinct phases of attachment. Virology 198:690-702.
53. Mettenleiter, T. C., L. Zsak, F. Zuckermann, N. Sugg, H. Kern, and T. Ben-Porat. 1990. Interaction of glycoprotein gIII with a cellular heparinlike substance mediates adsorption of pseudorabies virus. J. Virol. 64:278-286.
54. 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.
55. Okazaki, K., T. Matsuzaki, Y. Sugahara, J. Okada, M. Hasebe, Y. Iwamura, M. Ohnishi, T. Kanno, M. Shimizu, E. Honda, and Y. Kono. 1991. BHV-1 adsorption is mediated by the interaction of glycoprotein gIII with heparinlike moiety on the cell surface. Virology 181:666-670.
56. Robbins, A. K., R. J. Watson, M. E. Whealy, W. W. Hays, and L. W. Enquist. 1986. Characterization of a pseudorabies virus glycoprotein gene with homology to herpes simplex virus type 1 and type 2 glycoprotein C. J. Virol. 58:339-347.
57. Roizman, B., and A. E. Sears. 1996. Herpes simplex viruses and their replication, p. 2231-2295. In B. N. Fields, D. M. Knipe, P. M. Howley, et al. (ed.), Fields virology, 3rd ed. Lippincot-Raven Publishers, Philadelphia, Pa.
58. 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.
59. 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.
60. Shieh, M.-T., D. WuDunn, R. I. Montgomery, J. D. Esko, and P. G. Spear. 1992. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J. Cell Biol. 116:1273-1281.
61. Spear, P. G. 1993. Entry of alphaherpesviruses into cells. Semin. Virol. 4:167-180.
62. Subramanian, G., D. S. McClain, A. Perez, and A. O. Fuller. 1994. Swine testis cells contain functional heparan sulfate but are defective in entry of herpes simplex virus. J. Virol. 68:5667-5676.
63. Tal-Singer, R., C. Peng, M. Ponce de Leon, W. R. Abrams, B. W. Banfield, F. Tufaro, G. H. Cohen, and R. J. Eisenberg. 1995. Interaction of herpes simplex virus glycoprotein gC with mammalian cell surface molecules. J. Virol. 69:4471-4483.
64. Tengelsein, L. A., N. E. Pederson, P. R. Shaver, M. W. Wathen, and F. L. Homa. 1993. Herpes simplex virus type 1 DNA cleavage and encapsidation require the product of the UL28 gene: isolation and characterization of two UL28 deletion mutants. J. Virol. 67:3470-3480.
65. Trybala, E., T. Bergström, D. Spillmann, B. Svennerholm, S. Olofsson, S. J. Flynn, and P. Ryan. 1996, Mode of interaction between pseudorabies virus and heparan sulfate/heparin. Virology 218:35-42.
66. Trybala, E., T. Bergström, B. Svennerholm, S. Jeansson, J. C. Glorioso, and S. Olofsson. 1994. Localization of the functional site on herpes simplex virus type 1 glycoprotein C involved in binding to cell surface heparan sulfate. J. Gen. Virol. 75:743-752.
67. Wickham, T. J., P. W. Roelvink, D. E. Brough, and I. Kovesdi. 1996. Adenovirus targeted to heparan containing receptors increases its gene delivery efficiency to multiple cell types. Nat. Biotechnol. 14:1570-1573.
68. WuDunn, D., and P. G. Spear. 1989. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J. Virol. 63:52-58.