Anti-glycoprotein D Antibodies That Permit Adsorption but Block Infection by Herpes Simplex Virus 1 Prevent Virion-cell Fusion at the Cell Surface

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1987 Aug 1

PMID 3037552

Citations 132

Authors

A O Fuller

P G Spear

Affiliations

Soon will be listed here.

Abstract

Certain monoclonal antibodies specific for glycoprotein D of herpes simplex virus have potent neutralizing activity but fail to block attachment of virus to cells. Here we have investigated the fate of neutralized and infectious virus after attachment to primate cells. Infectious virions fused with the cell surface such that naked nucleocapsids were detectable in the cytoplasm near or just under the plasma membrane. Neutralized virions did not fuse with the cell. They remained attached to the cell surface and could be rendered infectious by treatment with polyethylene glycol. We conclude that some anti-glycoprotein D neutralizing antibodies can inhibit the penetration of herpes simplex virus by blocking fusion of the virion envelope with the plasma membrane. These results identify a pathway of entry that initiates successful herpes simplex virus infection and a step in this pathway that is highly sensitive to neutralizing antibodies. A role for glycoprotein D in virion-cell fusion is indicated.

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References

Morgan C, Rose H, Mednis B . Electron microscopy of herpes simplex virus. I. Entry. J Virol. 1968; 2(5):507-16. PMC: 375640. DOI: 10.1128/JVI.2.5.507-516.1968. View

Minson A, Hodgman T, Digard P, Hancock D, Bell S, Buckmaster E . An analysis of the biological properties of monoclonal antibodies against glycoprotein D of herpes simplex virus and identification of amino acid substitutions that confer resistance to neutralization. J Gen Virol. 1986; 67 ( Pt 6):1001-13. DOI: 10.1099/0022-1317-67-6-1001. View

Dales S, SILVERBERG H . Viropexis of herpes simplex virus by HeLa cells. Virology. 1969; 37(3):475-80. DOI: 10.1016/0042-6822(69)90232-3. View

Smith J, de Harven E . Herpes simplex virus and human cytomegalovirus replication in WI-38 cells. II. An ultrastructural study of viral penetration. J Virol. 1974; 14(4):945-56. PMC: 355602. DOI: 10.1128/JVI.14.4.945-956.1974. View

Cassai E, Sarmiento M, Spear P . Comparison of the virion proteins specified by herpes simplex virus types 1 and 2. J Virol. 1975; 16(5):1327-31. PMC: 355731. DOI: 10.1128/JVI.16.5.1327-1331.1975. View

Anderson R, Brown M, Goldstein J . Role of the coated endocytic vesicle in the uptake of receptor-bound low density lipoprotein in human fibroblasts. Cell. 1977; 10(3):351-64. DOI: 10.1016/0092-8674(77)90022-8. View

Manservigi R, Spear P, Buchan A . Cell fusion induced by herpes simplex virus is promoted and suppressed by different viral glycoproteins. Proc Natl Acad Sci U S A. 1977; 74(9):3913-7. PMC: 431783. DOI: 10.1073/pnas.74.9.3913. View

Sarmiento M, Haffey M, Spear P . Membrane proteins specified by herpes simplex viruses. III. Role of glycoprotein VP7(B2) in virion infectivity. J Virol. 1979; 29(3):1149-58. PMC: 353275. DOI: 10.1128/JVI.29.3.1149-1158.1979. View

Gollins S, PORTERFIELD J . A new mechanism for the neutralization of enveloped viruses by antiviral antibody. Nature. 1986; 321(6067):244-6. DOI: 10.1038/321244a0. View

10.

Gompels U, Minson A . The properties and sequence of glycoprotein H of herpes simplex virus type 1. Virology. 1986; 153(2):230-47. DOI: 10.1016/0042-6822(86)90026-7. View

11.

Claesson-Welsh L, Spear P . Oligomerization of herpes simplex virus glycoprotein B. J Virol. 1986; 60(2):803-6. PMC: 288962. DOI: 10.1128/JVI.60.2.803-806.1986. View

12.

Jennings S, Lippe P, Pauza K, Spear P, Pereira L, Tevethia S . Kinetics of expression of herpes simplex virus type 1-specific glycoprotein species on the surfaces of infected murine, simian, and human cells: flow cytometric analysis. J Virol. 1987; 61(1):104-12. PMC: 255213. DOI: 10.1128/JVI.61.1.104-112.1987. View

13.

Stannard L, Fuller A, Spear P . Herpes simplex virus glycoproteins associated with different morphological entities projecting from the virion envelope. J Gen Virol. 1987; 68 ( Pt 3):715-25. DOI: 10.1099/0022-1317-68-3-715. View

14.

HOLMES I, Watson D . AN ELECTRON MICROSCOPE STUDY OF THE ATTACHMENT AND PENETRATION OF HERPES VIRUS IN BHK21 CELLS. Virology. 1963; 21:112-23. DOI: 10.1016/0042-6822(63)90309-x. View

15.

Epstein M, Hummeler K, Berkaloff A . THE ENTRY AND DISTRIBUTION OF HERPES VIRUS AND COLLOIDAL GOLD IN HELA CELLS AFTER CONTACT IN SUSPENSION. J Exp Med. 1964; 119:291-302. PMC: 2137830. DOI: 10.1084/jem.119.2.291. View

16.

Baucke R, Spear P . Membrane proteins specified by herpes simplex viruses. V. Identification of an Fc-binding glycoprotein. J Virol. 1979; 32(3):779-89. PMC: 525925. DOI: 10.1128/JVI.32.3.779-789.1979. View

17.

Para M, Baucke R, Spear P . Immunoglobulin G(Fc)-binding receptors on virions of herpes simplex virus type 1 and transfer of these receptors to the cell surface by infection. J Virol. 1980; 34(2):512-20. PMC: 288731. DOI: 10.1128/JVI.34.2.512-520.1980. View

18.

Deluca N, Bzik D, Person S, SNIPES W . Early events in herpes simplex virus type 1 infection: photosensitivity of fluorescein isothiocyanate-treated virions. Proc Natl Acad Sci U S A. 1981; 78(2):912-6. PMC: 319914. DOI: 10.1073/pnas.78.2.912. View

19.

Little S, Jofre J, Courtney R, Schaffer P . A virion-associated glycoprotein essential for infectivity of herpes simplex virus type 1. Virology. 1981; 115(1):149-60. DOI: 10.1016/0042-6822(81)90097-0. View

20.

Noble A, Lee G, SPRAGUE R, Parish M, Spear P . Anti-gD monoclonal antibodies inhibit cell fusion induced by herpes simplex virus type 1. Virology. 1983; 129(1):218-24. DOI: 10.1016/0042-6822(83)90409-9. View