Low-pH-dependent changes in the conformation and oligomeric state of the prefusion form of herpes simplex virus glycoprotein B are separable from fusion activity

Journal of Virology

Volumn 85, Issue 19, 2011, Pages 9964-9973

  Dollery, Stephen J ^a   Wright, Catherine C ^b   Johnson, David C ^b   Nicola, Anthony V ^a,c  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN B; HERPESVIRUS ENTRY MEDIATOR LIGAND; HYBRID PROTEIN; NECTIN 1; OLIGOMER; TRYPTOPHAN;

ACIDITY; AMINO ACID SEQUENCE; ANTIGENICITY; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOPLASM; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE SPECTROSCOPY; GENE MUTATION; HERPES SIMPLEX VIRUS; HYDROPHOBICITY; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RECEPTOR BINDING; VIRION; VIRUS ENTRY;

ANIMALS; CERCOPITHECUS AETHIOPS; HERPESVIRUS 1, HUMAN; HYDROGEN-ION CONCENTRATION; MUTANT PROTEINS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SPECTROMETRY, FLUORESCENCE; VERO CELLS; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

HERPESVIRIDAE; SIMPLEXVIRUS;

EID: 80053964873     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05291-11     Document Type: Article

References (68)

1. Arii, J., et al. 2010. Non-muscle myosin IIA is a functional entry receptor for herpes simplex virus-1. Nature 467:859-862.
2. Arii, J., et al. 2009. Entry of herpes simplex virus 1 and other alphaherpesviruses via the paired immunoglobulin-like type 2 receptor alpha. J. Virol. 83:4520-4527.
3. Atanasiu, D., W. T. Saw, G. H. Cohen, and R. J. Eisenberg. 2010. Cascade of events governing cell-cell fusion induced by herpes simplex virus glycoproteins gD, gH/gL, and gB. J. Virol. 84:12292-12299.
4. Atanasiu, D., et al. 2010. Bimolecular complementation defines functional regions of herpes simplex virus gB that are involved with gH/gL as a necessary step leading to cell fusion. J. Virol. 84:3825-3834.
5. Avitabile, E., C. Forghieri, and G. Campadelli-Fiume. 2009. Cross talk among the glycoproteins involved in herpes simplex virus entry and fusion: the interaction between gB and gH/gL does not necessarily require gD. J. Virol. 83:10752-10760.
6. Batterson, W., D. Furlong, and B. Roizman. 1983. Molecular genetics of herpes simplex virus. VIII. Further characterization of a temperature-sensitive mutant defective in release of viral DNA and in other stages of the viral reproductive cycle. J. Virol. 45:397-407.
7. Beechem, J. M., and L. Brand. 1985. Time-resolved fluorescence of proteins. Annu. Rev. Biochem. 54:43-71.
8. Bender, F. C., et al. 2007. Antigenic and mutational analyses of herpes simplex virus glycoprotein B reveal four functional regions. J. Virol. 81:3827- 3841.
9. 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.
10. Bender, F. C., et al. 2003. Specific association of glycoprotein B with lipid rafts during herpes simplex virus entry. J. Virol. 77:9542-9552.
11. Bordier, C. 1981. Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256:1604-1607.
12. Campadelli-Fiume, G., et al. 2007. The multipartite system that mediates entry of herpes simplex virus into the cell. Rev. Med. Virol. 17:313-326.
13. Carfi, A., et al. 2001. Herpes simplex virus glycoprotein D bound to the human receptor HveA. Mol. Cell 8:169-179.
14. Chowdary, T. K., et al. 2010. Crystal structure of the conserved herpesvirus fusion regulator complex gH-gL. Nat. Struct. Mol. Biol. 17:882-888.
15. 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.
16. Copeland, A. M., W. W. Newcomb, and J. C. Brown. 2009. Herpes simplex virus replication: roles of viral proteins and nucleoporins in capsid-nucleus attachment. J. Virol. 83:1660-1668.
17. Delboy, M. G., and A. V. Nicola. 2011. A pre-immediate early role for tegument ICP0 in the proteasome-dependent entry of herpes simplex virus. J. Virol. 85:5910-5918.
18. Delboy, M. G., J. L. Patterson, A. M. Hollander, and A. V. Nicola. 2006. Nectin-2-mediated entry of a syncytial strain of herpes simplex virus via pH-independent fusion with the plasma membrane of Chinese hamster ovary cells. Virol. J. 3:105.
19. Delboy, M. G., D. G. Roller, and A. V. Nicola. 2008. Cellular proteasome activity facilitates herpes simplex virus entry at a postpenetration step. J. Virol. 82:3381-3390.
20. Dollery, S. J., M. G. Delboy, and A. V. Nicola. 2010. Low pH-induced conformational change in herpes simplex virus glycoprotein B. J. Virol. 84:3759-3766.
21. Eisenberg, R. J., et al. 1985. Localization of epitopes of herpes simplex virus type 1 glycoprotein D. J. Virol. 53:634-644.
22. Eisenberg, R. J., et al. 1994. Structure and function of glycoprotein D of herpes simplex virus, p. 43-65. In Y. Becker and G. Darai (ed.), Frontiers in virology, vol. 3. Springer-Verlag, Heidelberg, Germany.
23. Finnen, R. L., et al. 2006. Postentry events are responsible for restriction of productive varicella-zoster virus infection in Chinese hamster ovary cells. J. Virol. 80:10325-10334.
24. Forrester, A., et al. 1992. Construction and properties of a mutant of herpes simplex virus type 1 with glycoprotein H coding sequences deleted. J. Virol. 66:341-348.
25. Friedman, H. M., G. H. Cohen, R. J. Eisenberg, C. A. Seidel, and D. B. Cines. 1984. Glycoprotein C of herpes simplex virus 1 acts as a receptor for the C3b complement component on infected cells. Nature 309:633-635.
26. Fusco, D., C. Forghieri, and G. Campadelli-Fiume. 2005. The pro-fusion domain of herpes simplex virus glycoprotein D (gD) interacts with the gD N terminus and is displaced by soluble forms of viral receptors. Proc. Natl. Acad. Sci. U. S. A. 102:9323-9328.
27. Gaudin, Y. 2000. Reversibility in fusion protein conformational changes. The intriguing case of rhabdovirus-induced membrane fusion. Subcell. Biochem. 34:379-408.
28. Gianni, T., M. Amasio, and G. Campadelli-Fiume. 2009. Herpes simplex virus gD forms distinct complexes with fusion executors gB and gH/gL in part through the C-terminal profusion domain. J. Biol. Chem. 284:17370-17382.
29. Gianni, T., V. Gatta, and G. Campadelli-Fiume. 2010 V 3-integrin routes herpes simplex virus to an entry pathway dependent on cholesterol-rich lipid rafts and dynamin2. Proc. Natl. Acad. Sci. U. S. A. 107:22260-22265.
30. Gillet, L., S. Colaco, and P. G. Stevenson. 2008. Glycoprotein B switches conformation during murid herpesvirus 4 entry. J. Gen. Virol. 89:1352-1363.
31. Hannah, B. P., et al. 2009. Herpes simplex virus glycoprotein B associates with target membranes via its fusion loops. J. Virol. 83:6825-6836.
32. Hannah, B. P., E. E. Heldwein, F. C. Bender, G. H. Cohen, and R. J. Eisenberg. 2007. Mutational evidence of internal fusion loops in herpes simplex virus glycoprotein B. J. Virol. 81:4858-4865.
33. Heldwein, E. E., et al. 2006. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313:217-220.
34. 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.
35. Krummenacher, C., A. Carfi, R. J. Eisenberg, and G. H. Cohen. 2007. Herpesvirus entry into cells: the enigma variations. In S. Poehlmann and G. Simmons (ed.), Viral entry into host cells. Landes Bioscience, Austin, TX.
36. Krummenacher, C., et al. 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.
37. Krummenacher, C., et al. 2005. Structure of unliganded HSV gD reveals a mechanism for receptor-mediated activation of virus entry. EMBO J. 24: 4144-4153.
38. Luxton, G. W., et al. 2005. Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc. Natl. Acad. Sci. U. S. A. 102:5832-5837.
39. 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.
40. Nicola, A. V., J. Hou, E. O. Major, and S. E. Straus. 2005. Herpes simplex virus type 1 enters human epidermal keratinocytes, but not neurons, via a pH-dependent endocytic pathway. J. Virol. 79:7609-7616.
41. Nicola, A. V., A. M. McEvoy, and S. E. Straus. 2003. Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells. J. Virol. 77:5324-5332.
42. Nicola, A. V., et al. 1998. Monoclonal antibodies to distinct sites on herpes simplex virus (HSV) glycoprotein D block HSV binding to HVEM. J. Virol. 72:3595-3601.
43. 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.
44. 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.
45. Pereira, L., D. V. Dondero, D. Gallo, V. Devlin, and J. D. Woodie. 1982. Serological analysis of herpes simplex virus types 1 and 2 with monoclonal antibodies. Infect. Immun. 35:363-367.
46. Raghu, H., N. Sharma-Walia, M. V. Veettil, S. Sadagopan, and B. Chandran. 2009. Kaposi's sarcoma-associated herpesvirus utilizes an actin polymerization-dependent macropinocytic pathway to enter human dermal microvascular endothelial and human umbilical vein endothelial cells. J. Virol. 83: 4895-4911.
47. Roche, S., S. Bressanelli, F. A. Rey, and Y. Gaudin. 2006. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313:187-191.
48. Roche, S., F. A. Rey, Y. Gaudin, and S. Bressanelli. 2007. Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science 315:843-848.
49. Roller, D. G., S. J. Dollery, J. L. Doyle, and A. V. Nicola. 2008. Structurefunction analysis of herpes simplex virus glycoprotein B with fusion-fromwithout activity. Virology 382:207-216.
50. Ryckman, B. J., M. A. Jarvis, D. D. Drummond, J. A. Nelson, and D. C. Johnson. 2006. Human cytomegalovirus entry into epithelial and endothelial cells depends on genes UL128 to UL150 and occurs by endocytosis and low-pH fusion. J. Virol. 80:710-722.
51. Satoh, T., et al. 2008. PILRalpha is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B. Cell 132:935-944.
52. Shukla, D., and P. G. Spear. 2001. Herpesviruses and heparan sulfate: an intimate relationship in aid of viral entry. J. Clin. Invest. 108:503-510.
53. Siekavizza-Robles, C. R., S. J. Dollery, and A. V. Nicola. 2010. Reversible conformational change in herpes simplex virus glycoprotein B with fusionfrom-without activity is triggered by mildly acidic pH. Virol. J. 7:352.
54. Sodeik, B., M. W. Ebersold, and A. Helenius. 1997. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol. 136:1007-1021.
55. Spear, P. G., et al. 2006. Different receptors binding to distinct interfaces on herpes simplex virus gD can trigger events leading to cell fusion and viral entry. Virology 344:17-24.
56. Stampfer, S. D., H. Lou, G. H. Cohen, R. J. Eisenberg, and E. E. Heldwein. 2010. Structural basis of local, pH-dependent conformational changes in glycoprotein B from herpes simplex virus type 1. J. Virol. 84:12924-12933.
57. Stiles, K. M., R. S. Milne, G. H. Cohen, R. J. Eisenberg, and C. Krummenacher. 2008. The herpes simplex virus receptor nectin-1 is down-regulated after trans-interaction with glycoprotein D. Virology 373:98-111.
58. Stuve, L. L., et al. 1987. Structure and expression of the herpes simplex virus type 2 glycoprotein gB gene. J. Virol. 61:326-335.
59. Sun, X., S. Belouzard, and G. R. Whittaker. 2008. Molecular architecture of the bipartite fusion loops of vesicular stomatitis virus glycoprotein G, a class III viral fusion protein. J. Biol. Chem. 283:6418-6427.
60. Tal-Singer, R., et al. 1995. Interaction of herpes simplex virus glycoprotein gC with mammalian cell surface molecules. J. Virol. 69:4471-4483.
61. Tiwari, V., and D. Shukla. 2010. Phosphoinositide 3 kinase signalling may affect multiple steps during herpes simplex virus type-1 entry. J. Gen. Virol. 91:3002-3009.
62. Vanarsdall, A. L., B. J. Ryckman, M. C. Chase, and D. C. Johnson. 2008. Human cytomegalovirus glycoproteins gB and gH/gL mediate epithelial cellcell fusion when expressed either in cis or in trans. J. Virol. 82:11837-11850.
63. Wang, D., Q. C. Yu, J. Schroer, E. Murphy, and T. Shenk. 2007. Human cytomegalovirus uses two distinct pathways to enter retinal pigmented epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 104:20037-20042.
64. Whitbeck, J. C., et al. 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.
65. Williams, R. K., and S. E. Straus. 1997. Specificity and affinity of binding of herpes simplex virus type 2 glycoprotein B to glycosaminoglycans. J. Virol. 71:1375-1380.
66. Willis, S. H., et al. 1997. Expression and purification of secreted forms of herpes simplex virus glycoproteins from baculovirus-infected insect cells. Methods Mol. Med. 10:131-156.
67. Wright, C. C., et al. 2009. Fusion between perinuclear virions and the outer nuclear membrane requires the fusogenic activity of herpes simplex virus gB. J. Virol. 83:11847-11856.
68. Zhou, J., and G. W. Blissard. 2006. Mapping the conformational epitope of a neutralizing antibody (AcV1) directed against the AcMNPV GP64 protein. Virology 352:427-437.