Mutations in the cytoplasmic tail of herpes simplex virus 1 gH reduce the fusogenicity of gB in transfected cells

Journal of Virology

Volumn 87, Issue 18, 2013, Pages 10139-10147

  Silverman, Jessica L ^a   Heldwein, Ekaterina E ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANCHORED PROTEIN; HERPES SIMPLEX VIRUS 1 GB PROTEIN; HERPES SIMPLEX VIRUS 1 GD PROTEIN; HERPES SIMPLEX VIRUS 1 GH PROTEIN; HERPES SIMPLEX VIRUS 1 GL PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ALLELE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; COMPLEX FORMATION; CONTROLLED STUDY; CYTODOMAIN; CYTOPLASMIC TAIL; FEMALE; GENE ACTIVATION; GENETIC TRANSFECTION; HERPES SIMPLEX VIRUS 1; IN VITRO STUDY; MEMBRANE FUSION; MEMBRANE FUSOGENICITY; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SUPPRESSOR GENE; SYN GENE; SYNCYTIUM; VIRUS CELL INTERACTION; VIRUS GENE;

GIANT CELLS; HERPESVIRUS 1, HUMAN; HUMANS; MUTANT PROTEINS; MUTATION; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EID: 84883309288     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01760-13     Document Type: Article

References (48)

1. Heldwein EE, Krummenacher C. 2008. Entry of herpesviruses into mammalian cells. Cell. Mol. Life Sci. 65:1653-1668.
2. Cai WH, Gu B, Person S. 1988. Role of glycoprotein B of herpes simplex virus type 1 in viral entry and cell fusion. J. Virol. 62:2596-2604.
3. Forrester A, Farrell H, Wilkinson G, Kaye J, Davis-Poynter N, Minson T. 1992. Construction and properties of a mutant of herpes simplex virus type 1 with glycoproteinHcoding sequences deleted. J. Virol. 66:341-348.
4. Ligas MW, Johnson DC. 1988. A herpes simplex virus mutant in which glycoprotein D sequences are replaced by b-galactosidase sequences binds to but is unable to penetrate into cells. J. Virol. 62:1486-1494.
5. Muggeridge MI. 2000. Characterization of cell-cell fusion mediated by herpes simplex virus 2 glycoproteins gB, gD, gH and gL in transfected cells. J. Gen. Virol. 81:2017-2027.
6. Turner A, Bruun B, Minson T, Browne H. 1998. Glycoproteins gB, gD, and gHgL of herpes simplex virus type 1 are necessary and sufficient to mediate membrane fusion in a Cos cell transfection system. J. Virol. 72: 873-875.
7. Dingwell KS, Brunetti CR, Hendricks RL, Tang Q, Tang M, Rainbow AJ, Johnson DC. 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.
8. Uchida H, Chan J, Shrivastava I, Reinhart B, Grandi P, Glorioso JC, Cohen JB. 2013. Novel mutations in gB and gH circumvent the requirement for known gD receptors in herpes simplex virus 1 entry and cell-tocell spread. J. Virol. 87:1430-1442.
9. Eisenberg RJ, Atanasiu D, Cairns TM, Gallagher JR, Krummenacher C, Cohen GH. 2012. Herpes virus fusion and entry: a story with many characters. Viruses 4:800-832.
10. Krummenacher C, Supekar VM, Whitbeck JC, Lazear E, Connolly SA, Eisenberg RJ, Cohen GH, Wiley DC, Carfi A. 2005. Structure of unliganded HSV gD reveals a mechanism for receptor-mediated activation of virus entry. EMBO J. 24:4144-4153.
11. Atanasiu D, Saw WT, Cohen GH, Eisenberg RJ. 2010. Cascade of events governing cell-cell fusion induced by herpes simplex virus glycoproteins gD, gH/gL, and gB. J. Virol. 84:12292-12299.
12. Hannah BP, Heldwein EE, Bender FC, Cohen GH, Eisenberg RJ. 2007. Mutational evidence of internal fusion loops in herpes simplex virus glycoprotein B. J. Virol. 81:4858-4865.
13. Heldwein EE, Lou H, Bender FC, Cohen GH, Eisenberg RJ, Harrison SC. 2006. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313:217-220.
14. Atanasiu D, Whitbeck JC, Cairns TM, Reilly B, Cohen GH, Eisenberg RJ. 2007. Bimolecular complementation reveals that glycoproteins gB and gH/gL of herpes simplex virus interact with each other during cell fusion. Proc. Natl. Acad. Sci. U. S. A. 104:18718-18723.
15. Atanasiu D, Whitbeck JC, de Leon MP, Lou H, Hannah BP, Cohen GH, Eisenberg RJ. 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.
16. Vanarsdall AL, Ryckman BJ, Chase MC, Johnson DC. 2008. Human cytomegalovirus glycoproteins gB and gH/gL mediate epithelial cell-cell fusion when expressed either in cis or in trans. J. Virol. 82:11837-11850.
17. Ejercito PM, Kieff ED, Roizman B. 1968. Characterization of herpes simplex virus strains differing in their effects on social behaviour of infected cells. J. Gen. Virol. 2:357-364.
18. Bzik DJ, Fox BA, DeLuca NA, Person S. 1984. Nucleotide sequence of a region of the herpes simplex virus type 1 gB glycoprotein gene: mutations affecting rate of virus entry and cell fusion. Virology 137:185-190.
19. Weise K, Kaerner HC, Glorioso J, Schroder CH. 1987. Replacement of glycoprotein B gene sequences in herpes simplex virus type 1 strain ANG by corresponding sequences of the strain KOS causes changes of plaque morphology and neuropathogenicity. J. Gen. Virol. 68:1909-1919.
20. Baghian A, Huang L, Newman S, Jayachandra S, Kousoulas KG. 1993. Truncation of the carboxy-terminal 28 amino acids of glycoprotein B specified by herpes simplex virus type 1 mutant amb1511-7 causes extensive cell fusion. J. Virol. 67:2396-2401.
21. Diakidi-Kosta A, Michailidou G, Kontogounis G, Sivropoulou A, Arsenakis M. 2003. A single amino acid substitution in the cytoplasmic tail of the glycoprotein B of herpes simplex virus 1 affects both syncytium formation and binding to intracellular heparan sulfate. Virus Res. 93:99-108.
22. Engel JP, Boyer EP, Goodman JL. 1993. Two novel single amino acid syncytial mutations in the carboxy terminus of glycoprotein B of herpes simplex virus type 1 confer a unique pathogenic phenotype. Virology 192: 112-120.
23. Foster TP, Melancon JM, Kousoulas KG. 2001. An alpha-helical domain within the carboxyl terminus of herpes simplex virus type 1 (HSV-1) glycoprotein B (gB) is associated with cell fusion and resistance to heparin inhibition of cell fusion. Virology 287:18-29.
24. Gage PJ, Levine M, Glorioso JC. 1993. Syncytium-inducing mutations localize to two discrete regions within the cytoplasmic domain of herpes simplex virus type 1 glycoprotein B. J. Virol. 67:2191-2201.
25. Lin E, Spear PG. 2007. Random linker-insertion mutagenesis to identify functional domains of herpes simplex virus type 1 glycoprotein B. Proc. Natl. Acad. Sci. U. S. A. 104:13140-13145.
26. Haanes EJ, Nelson CM, Soule CL, Goodman JL. 1994. The UL45 gene product is required for herpes simplex virus type 1 glycoprotein B-induced fusion. J. Virol. 68:5825-5834.
27. Silverman JL, Greene NG, King DS, Heldwein EE. 2012. Membrane requirement for folding of the herpes simplex virus 1 gB cytodomain suggests a unique mechanism of fusion regulation. J. Virol. 86:8171-8184.
28. Harman A, Browne H, Minson T. 2002. The transmembrane domain and cytoplasmic tail of herpes simplex virus type 1 glycoprotein H play a role in membrane fusion. J. Virol. 76:10708-10716.
29. Jackson JO, Lin E, Spear PG, Longnecker R. 2010. Insertion mutations in herpes simplex virus 1 glycoprotein H reduce cell surface expression, slow the rate of cell fusion, or abrogate functions in cell fusion and viral entry. J. Virol. 84:2038-2046.
30. Browne HM, Bruun BC, Minson AC. 1996. Characterization of herpes simplex virus type 1 recombinants with mutations in the cytoplasmic tail of glycoprotein H. J. Gen. Virol. 77:2569-2573.
31. Wilson DW, Davis-Poynter N, Minson AC. 1994. Mutations in the cytoplasmic tail of herpes simplex virus glycoprotein H suppress cell fusion by a syncytial strain. J. Virol. 68:6985-6993.
32. Chowdary TK, Cairns TM, Atanasiu D, Cohen GH, Eisenberg RJ, Heldwein EE. 2010. Crystal structure of the conserved herpesvirus fusion regulator complex gH-gL. Nat. Struct. Mol. Biol. 17:882-888.
33. Pertel PE, Fridberg A, Parish ML, Spear PG. 2001. Cell fusion induced by herpes simplex virus glycoproteins gB, gD, and gH-gL requires a gD receptor but not necessarily heparan sulfate. Virology 279:313-324.
34. Chowdary TK, Heldwein EE. 2010. Syncytial phenotype of C-terminally truncated herpes simplex virus type 1 gB is associated with diminished membrane interactions. J. Virol. 84:4923-4935.
35. Krummenacher C, Baribaud I, Sanzo JF, Cohen GH, Eisenberg RJ. 2002. Effects of herpes simplex virus on structure and function of nectin-1/HveC. J. Virol. 76:2424-2433.
36. Heckman KL, Pease LR. 2007. Gene splicing and mutagenesis by PCRdriven overlap extension. Nat. Protoc. 2:924-932.
37. Connolly SA, Landsburg DJ, Carfi A, Wiley DC, Cohen GH, Eisenberg RJ. 2003. Structure-based mutagenesis of herpes simplex virus glycoproteinDdefines three critical regions at the gD-HveA/HVEM binding interface. J. Virol. 77:8127-8140.
38. Okuma K, Nakamura M, Nakano S, Niho Y, Matsuura Y. 1999. Host range of human T-cell leukemia virus type I analyzed by a cell fusiondependent reporter gene activation assay. Virology 254:235-244.
39. Krummenacher C, Baribaud F, Ponce De Leon M, Baribaud I, Whitbeck JC, Xu R, Cohen GH, Eisenberg RJ. 2004. Comparative usage of herpesvirus entry mediator A and nectin-1 by laboratory strains and clinical isolates of herpes simplex virus. Virology 322:286-299.
40. Bender FC, Whitbeck JC, Lou H, Cohen GH, Eisenberg RJ. 2005. Herpes simplex virus glycoprotein B binds to cell surfaces independently of heparan sulfate and blocks virus entry. J. Virol. 79:11588-11597.
41. Kamen DE, Gross ST, Girvin ME, Wilson DW. 2005. Structural basis for the physiological temperature dependence of the association of VP16 with the cytoplasmic tail of herpes simplex virus glycoprotein H. J. Virol. 79: 6134-6141.
42. Aguilar HC, Anderson WF, Cannon PM. 2003. Cytoplasmic tail of Moloney murine leukemia virus envelope protein influences the conformation of the extracellular domain: implications for mechanism of action of the R peptide. J. Virol. 77:1281-1291.
43. Loving R, Li K, Wallin M, Sjoberg M, Garoff H. 2008. R-Peptide cleavage potentiates fusion-controlling isomerization of the intersubunit disulfide in Moloney murine leukemia virus Env. J. Virol. 82:2594-2597.
44. Waning DL, Russell CJ, Jardetzky TS, Lamb RA. 2004. Activation of aparamyxovirus fusion protein is modulated by inside-out signaling from the cytoplasmic tail. Proc. Natl. Acad. Sci. U. S. A. 101:9217-9222.
45. Roy NH, Chan J, Lambele M, Thali M. 2013. Clustering and mobility of HIV-1 Env at viral assembly sites predict its propensity to induce cell-cell fusion. J. Virol. 87:7516-7525.
46. Balan P, Davis-Poynter N, Bell S, Atkinson H, Browne H, Minson T. 1994. An analysis of the in vitro and in vivo phenotypes of mutants of herpes simplex virus type 1 lacking glycoproteins gG, gE, gI or the putative gJ. J. Gen. Virol. 75:1245-1258.
47. Davis-Poynter N, Bell S, Minson T, Browne H. 1994. Analysis of the contribution of herpes simplex virus type 1 membrane proteins to the induction of cell-cell fusion. J. Virol. 68:7586-7590.
48. Johnson DC, Huber MT. 2002. Directed egress of animal viruses promotes cell-to-cell spread. J. Virol. 76:1-8.