The membrane-proximal region (MPR) of herpes simplex virus GB regulates association of the fusion loops with lipid membranes

mBio

Volumn 3, Issue 6, 2012, Pages

  Shelly, Spencer S ^a   Cairns, Tina M ^a   Whitbeck, J Charles ^a   Lou, Huan ^a   Krummenacher, Claude ^a   Cohen, Gary H ^a   Eisenberg, Roselyn J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN B; LIPOSOME;

ANIMAL CELL; ARTICLE; BACULOVIRUS; CELL SURFACE; CONTROLLED STUDY; CRYSTAL STRUCTURE; FEMALE; FUSION LOOP; GENE DELETION; HERPES SIMPLEX VIRUS 1; HERPES VIRUS INFECTION; LIPID MEMBRANE; MEMBRANE PROXIMAL REGION; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; VIRION; VIRUS CELL INTERACTION; VIRUS ENVELOPE;

SIMPLEXVIRUS;

EID: 84872166777     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00429-12     Document Type: Article

References (64)

1. Browne H, Bruun B, Minson T. 2001. Plasma membrane requirements for cell fusion induced by herpes simplex virus type 1 glycoproteins gB, gD, gH and gL. J. Gen. Virol. 82:1419-1422.
2. 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.
3. Pertel PE. 2002. Human herpesvirus 8 glycoprotein B (gB), gH, and gL can mediate cell fusion. J. Virol. 76:4390-4400.
4. Eisenberg RJ, et al. 2012. Herpes virus fusion and entry: a story with many characters. Viruses 4:800-832.
5. Connolly SA, Jackson JO, Jardetzky TS, Longnecker R. 2011. Fusing structure and function: a structural view of the herpesvirus entry machinery. Nat. Rev. Microbiol. 9:369-381.
6. Kinzler ER, Compton T. 2005. Characterization of human cytomegalovirus glycoprotein-induced cell-cell fusion. J. Virol. 79:7827-7837.
7. 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.
8. Heldwein EE, et al. 2006. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313:217-220.
9. Roche S, Bressanelli S, Rey FA, Gaudin Y. 2006. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313:187-191.
10. Kadlec J, Loureiro S, Abrescia NG, Stuart DI, Jones IM. 2008. The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat. Struct. Mol. Biol. 15:1024-1030.
11. Backovic M, Longnecker R, Jardetzky TS. 2009. Structure of a trimeric variant of the Epstein-Barr virus glycoprotein B. Proc. Natl. Acad. Sci. U.S.A. 106:2880-2885.
12. Kielian M, Rey FA. 2006. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4:67-76.
13. Lamb RA, Paterson RG, Jardetzky TS. 2006. Paramyxovirus membrane fusion: lessons from the F andHNatomic structures. Virology 344:30-37.
14. Steven AC, Spear PG. 2006. Viral glycoproteins and an evolutionary conundrum. Science 313:177-178.
15. 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.
16. Hannah BP, et al. 2009. Herpes simplex virus glycoprotein B associates with target membranes via its fusion loops. J. Virol. 83:6825-6836.
17. Roche S, Rey FA, Gaudin Y, Bressanelli S. 2007. Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science 315: 843-848.
18. Pellett PE, Kousoulas KG, Pereira L, Roizman B. 1985. Anatomy of the herpes simplex virus 1 strain F glycoprotein B gene: primary sequence and predicted protein structure of the wild type and of monoclonal antibodyresistant mutants. J. Virol. 53:243-253.
19. Bzik DJ, Fox BA, DeLuca NA, Person S. 1984. Nucleotide sequence specifying the glycoprotein gene, gB, of herpes simplex virus type 1. Virology 133:301-314.
20. Rasile L, Ghosh K, Raviprakash K, Ghosh HP. 1993. Effects of deletions in the carboxy-terminal hydrophobic region of herpes simplex virus glycoprotein gB on intracellular transport and membrane anchoring. J. Virol. 67:4856-4866.
21. Salzwedel K, West JT, Hunter E. 1999. A conserved tryptophan-rich motif in the membrane-proximal region of the human immunodeficiency virus type 1 gp41 ectodomain is important for Env-mediated fusion and virus infectivity. J. Virol. 73:2469-2480.
22. Tong S, et al. 2001. Three membrane-proximal amino acids in the human parainfluenza type 2 (HPIV 2) F protein are critical for fusogenic activity. Virology 280:52-61.
23. Zhou J, Dutch RE, Lamb RA. 1997. Proper spacing between heptad repeat B and the transmembrane domain boundary of the paramyxovirus SV5 F protein is critical for biological activity. Virology 239:327-339.
24. Jeetendra E, et al. 2003. The membrane-proximal region of vesicular stomatitis virus glycoprotein G ectodomain is critical for fusion and virus infectivity. J. Virol. 77:12807-12818.
25. Li Z, Blissard GW. 2009. The pretransmembrane domain of the Autographa californica multicapsid nucleopolyhedrovirus gp64 protein is critical for membrane fusion and virus infectivity. J. Virol. 83:10993-11004.
26. Suárez T, Gallaher WR, Agirre A, Goñi FM, Nieva JL. 2000. Membrane interface-interacting sequences within the ectodomain of the human immunodeficiency virus type 1 envelope glycoprotein: putative role during viral fusion. J. Virol. 74:8038-8047.
27. Killian JA, von Heijne G. 2000. How proteins adapt to a membrane-water interface. Trends Biochem. Sci. 25:429-434.
28. Jeetendra E, Robison CS, Albritton LM, Whitt MA. 2002. The membrane-proximal domain of vesicular stomatitis virus G protein functions as a membrane fusion potentiator and can induce hemifusion. J. Virol. 76:12300-12311.
29. Modis Y, Ogata S, Clements D, Harrison SC. 2004. Structure of the dengue virus envelope protein after membrane fusion. Nature 427: 313-319.
30. Rey FA, Heinz FX, Mandl C, Kunz C, Harrison SC. 1995. The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375:291-298.
31. Roche S, Albertini AA, Lepault J, Bressanelli S, Gaudin Y. 2008. Structures of vesicular stomatitis virus glycoprotein: membrane fusion revisited. Cell. Mol. Life Sci. 65:1716-1728.
32. 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.
33. Wanas E, Efler S, Ghosh K, Ghosh HP. 1999. Mutations in the conserved carboxy-terminal hydrophobic region of glycoprotein gB affect infectivity of herpes simplex virus. J. Gen. Virol. 80:3189-3198.
34. Zheng Z, Maidji E, Tugizov S, Pereira L. 1996. Mutations in the carboxyl-terminal hydrophobic sequence of human cytomegalovirus glycoprotein B alter transport and protein chaperone binding. J. Virol. 70: 8029-8040.
35. Gibbons DL, et al. 2004. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 427: 320-325.
36. Roussel A, et al. 2006. Structure and interactions at the viral surface of the envelope protein E1 of Semliki Forest virus. Structure 14:75-86.
37. Zhang Y, et al. 2004. Conformational changes of the flavivirus E glycoprotein. Structure 12:1607-1618.
38. Cairns TM, et al. 2011. Capturing the herpes simplex virus core fusion complex (gB-gH/gL) in an acidic environment. J. Virol. 85:6175-6184.
39. Besenicar M, Macek P, Lakey JH, Anderluh G. 2006. Surface plasmon resonance in protein-membrane interactions. Chem. Phys. Lipids 141: 169-178.
40. General Electric Company. May 2007. Biacore X100 handbook, edition AC. GE Healthcare Bio-Sciences AB, Uppsala, Sweden.
41. Silverman JL, Sharma S, Cairns TM, Heldwein EE. 2010. Fusiondeficient insertion mutants of herpes simplex virus type 1 glycoprotein B adopt the trimeric postfusion conformation. J. Virol. 84:2001-2012.
42. White JM, Delos SE, Brecher M, Schornberg K. 2008. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 43:189-219.
43. Hearty S, Conroy PJ, Ayyar BV, Byrne B, O'Kennedy R. 2010. Surface plasmon resonance for vaccine design and efficacy studies: recent applications and future trends. Expert Rev. Vaccines 9:645-664.
44. Anderluh G, Besenicar M, Kladnik A, Lakey JH, Macek P. 2005. Properties of nonfused liposomes immobilized on an L1 Biacore chip and their permeabilization by a eukaryotic pore-forming toxin. Anal. Biochem. 344: 43-52.
45. Zhou J, Blissard GW. 2008. Identification of a GP64 subdomain involved in receptor binding by budded virions of the baculovirus Autographica californica multicapsid nucleopolyhedrovirus. J. Virol. 82:4449-4460.
46. Li Z, Blissard GW. 2011. Autographa californica multiple nucleopolyhedrovirus gp64 protein: roles of histidine residues in triggering membrane fusion and fusion pore expansion. J. Virol. 85:12492-12504.
47. Stampfer SD, Lou H, Cohen GH, Eisenberg RJ, Heldwein EE. 2010. Structural basis of local, pH-dependent conformational changes in glycoprotein B from herpes simplex virus type 1. J. Virol. 84:12924-12933.
48. Fuller AO, Spear PG. 1987. Anti-glycoprotein D antibodies that permit adsorption but block infection by herpes simplex virus 1 prevent virioncell fusion at the cell surface. Proc. Natl. Acad. Sci. U. S. A. 84:5454-5458.
49. Nicola AV, McEvoy AM, Straus SE. 2003. Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells. J. Virol. 77:5324-5332.
50. Wittels M, Spear PG. 1991. Penetration of cells by herpes simplex virus does not require a low pH-dependent endocytic pathway. Virus Res. 18: 271-290.
51. Milne RS, Nicola AV, Whitbeck JC, Eisenberg RJ, Cohen GH. 2005. Glycoprotein D receptor-dependent, low-pH-independent endocytic entry of herpes simplex virus type 1. J. Virol. 79:6655-6663.
52. 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.
53. Silverman JL, et al. 2012. Membrane requirement for the folding of the HSV-1 gB cytodomain suggests a unique mechanism of fusion regulation. J. Virol. 86:8171-8184.
54. Handler CG, Eisenberg RJ, Cohen GH. 1996. Oligomeric structure of glycoproteins in herpes simplex virus type 1. J. Virol. 70:6067-6070.
55. Bender FC, et al. 2007. Antigenic and mutational analyses of herpes simplex virus glycoprotein B reveal four functional regions. J. Virol. 81: 3827-3841.
56. Cairns TM, et al. 2007. N-terminal mutants of herpes simplex virus type 2 gH are transported without gL but require gL for function. J. Virol. 81:5102-5111.
57. 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.
58. Bender FC, et al. 2003. Specific association of glycoprotein B with lipid rafts during herpes simplex virus entry. J. Virol. 77:9542-9552.
59. Sisk WP, et al. 1994. High-level expression and purification of secreted forms of herpes simplex virus type 1 glycoprotein gD synthesized by baculovirus-infected insect cells. J. Virol. 68:766-775.
60. Rux AH, et al. 1998. Functional region IV of glycoprotein D from herpes simplex virus modulates glycoprotein binding to the herpesvirus entry mediator. J. Virol. 72:7091-7098.
61. Cohen GH, Isola VJ, Kuhns J, Berman PW, Eisenberg RJ. 1986. Local- ization 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.
62. Lazear E, et al. 2008. Engineered disulfide bonds in herpes simplex virus type 1 gD separate receptor binding from fusion initiation and viral entry. J. Virol. 82:700-709.
63. Doms RW, Helenius A, White J. 1985. Membrane fusion activity of the influenza virus hemagglutinin. The low pH-induced conformational change. J. Biol. Chem. 260:2973-2981.
64. Kielian M, Klimjack MR, Ghosh S, Duffus WA. 1996. Mechanisms of mutations inhibiting fusion and infection by Semliki Forest virus. J. Cell Biol. 134:863-872.