Stable association of herpes simplex virus with target membranes is triggered by low pH in the presence of the gD receptor, HVEM

Journal of Virology

Volumn 80, Issue 8, 2006, Pages 3773-3780

  Whitbeck, J Charles ^a   Zuo, Yi ^a   Milne, Richard S B ^a   Cohen, Gary H ^a   Eisenberg, Roselyn J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN; LIPOSOME; NECTIN 1; NECTIN 2; PROTEIN HVEM; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG; VIRUS RECEPTOR;

ACIDITY; ANIMAL CELL; ARTICLE; CHO CELL; HERPES SIMPLEX VIRUS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; VIRION; VIRUS ACTIVATION; VIRUS CELL INTERACTION; VIRUS DNA CELL DNA INTERACTION; VIRUS INACTIVATION;

ANIMALS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; CHO CELLS; CRICETINAE; HYDROGEN-ION CONCENTRATION; LIPOSOMES; RECEPTORS, TUMOR NECROSIS FACTOR; RECEPTORS, TUMOR NECROSIS FACTOR, MEMBER 14; RECEPTORS, VIRUS; SIMPLEXVIRUS; VERO CELLS; VIRION;

SIMPLEXVIRUS;

EID: 33645791673     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.8.3773-3780.2006     Document Type: Article

References (43)

1. Barnard, R. J. O., S. Narayan, G. Dornadula, M. D. Miller, and J. A. T. Young. 2004. Low pH is required for avian sarcoma and leukosis virus Env-dependent viral penetration into the cytosol and not for viral uncoating. J. Virol. 78:10433-10441.
2. Bender, F. C., J. C. Whitbeck, H. Lou, G. H. Cohen, and R. J. Eisenberg. 2005. Herpes simplex virus glycoprotein B binds to cell surfaces independently of heparan sulfate and blocks virus entry. J. Virol. 79:11588-11597.
3. Bron, R., J. M. Wahlberg, H. Garoff, and J. Wilschut. 1993. Membrane fusion of Semliki Forest virus in a model system: correlation between fusion kinetics and structural changes in the envelope glycoprotein. EMBO J. 12:693-701.
4. Bullough, P. A., F. M. Hughson, J. K. Skehel, and D. C. Wiley. 2002. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37-43.
5. Cohen, G. H., V. J. Isola, J. Kuhns, P. W. Berman, and R. J. Eisenberg. 1986. Localization of discontinuous epitopes of herpes simplex virus glycoprotein D: use of a nondenaturing ("native" gel) system of polyacrylamide gel electrophoresis coupled with Western blotting. J. Virol. 60:157-166.
6. Damico, R., and P. Bates. 2000. Soluble receptor-induced retroviral infection of receptor-deficient cells. J. Virol. 74:6469-6475.
7. Earp, L. J., L. D. Hernandez, S. E. Delos, and J. M. White. 2003. Receptor-activated binding of viral fusion proteins to target membranes. Methods Enzymol. 372:428-440.
8. Earp, L. J., S. E. Delos, R. C. Netter, P. Bates, and J. M. White. 2003. The avian retrovirus avian sarcoma/leukosis virus subtype A reaches the lipid mixing stage of fusion at neutral pH. J. Virol. 77:3058-3066.
9. Eisenberg, R. J., M. Ponce de Leon, H. M. Friedman, L. F. Fries, M. M. Frank, J. C. Hastings, and G. H. Cohen. 1987. Complement component C3b binds directly to purified glycoprotein C of herpes simplex virus types 1 and 2. Microb. Pathog. 3:423-435.
10. Fass, D. 2003. Conformational changes in enveloped virus surface proteins during cell entry. Adv. Protein Chem. 64:325-362.
11. Forestell, S. P., J. S. Dando, E. Bohnlein, and R. J. Rigg. 1996. Improved detection of replication-competent retrovirus. J. Virol. Methods 60:171-178.
12. Gaudin, Y., R. W. Ruigrok, M. Knossow, and A. Flamand. 1993. Low-pH conformational changes of rabies virus glycoprotein and their role in membrane fusion. J. Virol. 67:1365-1372.
13. 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.
14. Grgacic, E. V. L., and H. Schaller. 2000. A metastable form of the large envelope protein of duck hepatitis B virus: low-pH release results in a transition to a hydrophobic, potentially fusogenic conformation. J. Virol. 74:5116-5122.
15. Gruenberg, J. 2001. The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell Biol. 2:721-730.
16. Handler, C. G., R. J. Eisenberg, and G. H. Cohen. 1996. Oligomeric structure of glycoproteins in herpes simplex virus type 1. J. Virol. 70:6067-6070.
17. Isola, V. J., R. J. Eisenberg, G. R. Siebert, C. J. Heilman, W. C. Wilcox, and G. H. Cohen. 1989. Fine mapping of antigenic site II of herpes simplex virus glycoprotein D. J. Virol. 63:2325-2334.
18. 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.
19. Kwon, H, Q. Bai, H.-J. Baek, K. Felmet, E. A. Burton, W. F. Goins, J. B. Cohen, and J. C. Glorioso. 2006. Soluble V domain of nectin-1/HveC enables entry of herpes simplex virus type 1 (HSV-1) into HSV-resistant cells by binding to viral glycoprotein D. J. Virol. 80:138-148.
20. Maeda, T., and S. Ohnishi. 1980. Activation of influenza virus by acidic media causes hemolysis and fusion of erythrocytes. FEBS Lett. 122:283-287.
21. Maeda, T., K. Kawasaki, and S. Ohnishi. 1981. Interaction of influenza virus hemagglutinin with target membrane lipids is a key step in virus-induced hemolysis and fusion at pH 5.2. Proc. Natl. Acad. Sci. USA 78:4133-4137.
22. Milne, R. S., A. V. Nicola, J. C. Whitbeck, R. J. Eisenberg, and G. H. Cohen. 2005. Glycoprotein D receptor-dependent, low-pH-independent endocytic entry of herpes simplex virus type 1. J. Virol. 79:6655-6663.
23. Mothes, W., A. L. Boerger, S. Narayan, J. M. Cunningham, and J. A. Young. 2000. Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. Cell 103:679-689.
24. Nicola, A. V., M. Ponce de Leon, R. Xu, W. Hou, J. C. Whitbeck, C. Krummenacher, R. I. Montgomery, P. G. Spear, R. J. Eisenberg, and G. H. Cohen. 1998. Monoclonal antibodies to distinct sites on herpes simplex virus (HSV) glycoprotein D block HSV binding to HVEM. J. Virol. 72:3595-3601.
25. Nicola, A. V., A. M. McEvoy, and S. E. Straus. 2003. Roles for endocytosis and low pH in herpes simplex viras entry into HeLa and Chinese hamster ovary cells. J. Virol. 77:5324-5332.
26. Nicola, A. V., and S. E. Straus. 2004. Cellular and viral requirements for rapid endocytic entry of herpes simplex virus. J. Virol. 78:7508-7517.
27. Nicola, A. V., J. Hou, E. O. Major, and S. E. Straus. 2005. Herpes simplex viras type 1 enters human epidermal keratinocytes, but not neurons, via a pH-dependent endocytic pathway. J. Virol. 79:7609-7616.
28. Sato, S. B., K. Kawasaki, and S. Ohnishi. 1983. Hemolytic activity of influenza virus hemagglutinin glycoproteins activated in mildly acidic environments. Proc. Natl. Acad. Sci. USA 80:3153-3157.
29. Smit, J. M., B. L. Waarts, R. Bittman, and J. Wilschut. 2003. Liposomes as target membranes in the study of virus receptor interaction and membrane fusion. Methods Enzymol. 372:374-392.
30. Smith, A. E., and A. Helenius. 2004. How viruses enter animal cells. Science 304:237-242.
31. Smith, J. G., W. Mothes, S. C. Blacklow, and J. M. Cunningham. 2004. The mature avian leukosis virus subgroup A envelope glycoprotein is metastable, and refolding induced by the synergistic effects of receptor binding and low pH is coupled to infection. J. Virol. 78:1403-1410.
32. Spear, P. G., and R. Longnecker. 2003. Herpesvirus entry: an update. J. Virol. 77:10179-10185.
33. Spear, P. G. 2004. Herpes simplex virus: receptors and ligands for cell entry. Cell. Microbiol. 6:401-410.
34. Stegmann, T., F. P. Booy, and J. Wilschut. 1987. Effects of low pH on influenza virus. Activation and inactivation of the membrane fusion capacity of the hemagglutinin. J. Biol. Chem. 262:17744-17749.
35. Stiasny, K., S. L. Allison, J. Schalich, and F. X. Heinz. 2002. Membrane interactions of the tick-borne encephalitis virus fusion protein E at low pH. J. Virol. 76:3784-3790.
36. Tal-Singer, R., C. Peng, M. Ponce de Leon, W. R. Ahrams, B. W. Banfield, F. Tufaro, G. H. Cohen, and R. J. Eisenberg. 1995. Interaction of herpes simplex viras glycoprotein gC with mammalian cell surface molecules. J. Virol. 69:4471-4483.
37. Tamm, L. K. 2003. Hypothesis: spring-loaded boomerang mechanism of influenza hemagglutinin-mediated membrane fusion. Biochim. Biophys. Acta 1614:14-23.
38. 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.
39. Whitbeck, J. C., C. Peng, H. Lou, R. Xu, S. H. Willis, M. Ponce de Leon, T. Peng, A. V. Nicola, R. I. Montgomery, M. S. Warner, A. M. Soulika, L. A. Spruce, W. T. Moore, J. D. Lambris, P. G. Spear, G. H. Cohen, and R. J. Eisenberg. 1997. Glycoprotein D of herpes simplex virus (HSV) binds directly to HVEM, a member of the tumor necrosis factor receptor superfamily and a mediator of HSV entry. J. Virol. 71:6083-6093.
40. White, J., J. Kartenheck, and A. Helenius. 1982. Membrane fusion activity of influenza virus. EMBO J. 1:217-222.
41. Wittels, M., and P. G. Spear. 1991. Penetration of cells by herpes simplex virus does not require a low pH-dependent endocytic pathway. Virus Res. 18:271-290.
42. Yamada, S., and S. Ohnishi. 1986. Vesicular stomatitis virus binds and fuses with phospholipid domain in target cell membranes. Biochemistry 25:3703-3708.
43. Zelus, B. D., J. H. Schickli, D. M. Blau, S. R. Weiss, and K. V. Holmes. 2003. Conformational changes in the spike glycoprotein of murine coronavirus are induced at 37°C either by soluble murine CEACAM1 receptors or by pH 8. J. Virol. 77:830-840.