The Epstein-Barr virus (EBV) glycoprotein B cytoplasmic C-terminal tail domain regulates the energy requirement for EBV-induced membrane fusion

Journal of Virology

Volumn 88, Issue 20, 2014, Pages 11686-11695

  Chen, Jia ^a   Zhang, Xianming ^b   Jardetzky, Theodore S ^c   Longnecker, Richard ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; DOUBLE STRANDED DNA; GLYCOPROTEIN B; HYBRID PROTEIN; OLIGONUCLEOTIDE; EPSTEIN-BARR VIRUS GLYCOPROTEIN GP110; VIRUS PROTEIN;

ARTICLE; B LYMPHOCYTE; CARBOXY TERMINAL SEQUENCE; CHO CELL LINE; CONTROLLED STUDY; CYTOPLASM; DNA VIRUS; EPITHELIUM CELL; EPSTEIN BARR VIRUS; HERPES VIRUS; HOST CELL; MEMBRANE FUSION; MUTANT; NONHUMAN; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RECEPTOR BINDING; STRUCTURAL HOMOLOGY; SYNCYTIUM; TEMPERATURE; VIRUS ENTRY; WILD TYPE; ANIMAL; CHEMISTRY; CRICETULUS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; HAMSTER; MUTATION; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HERPESVIRUS 4, HUMAN; MEMBRANE FUSION; MUTATION; TEMPERATURE; VIRAL PROTEINS;

EID: 84907911669     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01349-14     Document Type: Article

References (52)

1. Longnecker R, Kieff E, Cohen JI. 2013. Chapter 61. Epstein-Barr virus, p 1898-1959. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (ed), Fields virology, 6th ed, vol 2. Lippincott, Williams & Wilkins, Philadelphia, PA.
2. Kirschner AN, Omerovic J, Popov B, Longnecker R, Jardetzky TS. 2006. Soluble Epstein-Barr virus glycoproteins gH, gL, and gp42 form a 1:1:1 stable complex that acts like soluble gp42 in B-cell fusion but not in epithelial cell fusion. J. Virol. 80:9444-9454. http://dx.doi.org/10.1128/JVI.00572-06.
3. Mullen MM, Haan KM, Longnecker R, Jardetzky TS. 2002. Structure of the Epstein-Barr virus gp42 protein bound to the MHC class II receptor HLA-DR1. Mol. Cell 9:375-385. http://dx.doi.org/10.1016 /S1097-2765(02)00465-3.
4. Borza CM, Hutt-Fletcher LM. 2002. Alternate replication in B cells and epithelial cells switches tropism of Epstein-Barr virus. Nat. Med. 8:594-599. http://dx.doi.org/10.1038/nm0602-594.
5. Wang X, Kenyon WJ, Li Q, Mullberg J, Hutt-Fletcher LM. 1998. Epstein-Barr virus uses different complexes of glycoproteins gH and gL to infect B lymphocytes and epithelial cells. J. Virol. 72:5552-5558.
6. 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. http://dx.doi.org/10.1038 /nrmicro2548.
7. Wang X, Hutt-Fletcher LM. 1998. Epstein-Barr virus lacking glycoprotein gp42 can bind to B cells but is not able to infect. J. Virol. 72:158-163.
8. Chesnokova LS, Nishimura SL, Hutt-Fletcher LM. 2009. Fusion of epithelial cells by Epstein-Barr virus proteins is triggered by binding of viral glycoproteins gHgL to integrins αvβ6 or αvβ8. Proc. Natl. Acad. Sci. U. S. A. 106:20464-20469. http://dx.doi.org/10.1073/pnas.0907508106.
9. Li Q, Turk SM, Hutt-Fletcher LM. 1995. The Epstein-Barr virus (EBV) BZLF2 gene product associates with the gH and gL homologs of EBV and carries an epitope critical to infection of B cells but not of epithelial cells. J. Virol. 69:3987-3994.
10. Li Q, Buranathai C, Grose C, Hutt-Fletcher LM. 1997. Chaperone functions common to nonhomologous Epstein-Barr virus gL and varicella-zoster virus gL proteins. J. Virol. 71:1667-1670.
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. http://dx.doi.org/10.1073/pnas.0810530106.
12. 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. http://dx.doi.org/10.1007/s00018-008-7534-3.
13. 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. http://dx.doi.org/10.1126/science.1127683.
14. 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. http://dx.doi.org /10.1038/nsmb.1484.
15. 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. http://dx.doi.org/10.1126/science.1126548.
16. Plate AE, Reimer JJ, Jardetzky TS, Longnecker R. 2011. Mapping regions of Epstein-Barr virus (EBV) glycoprotein B (gB) important for fusion function with gH/gL. Virology 413:26-38. http://dx.doi.org/10.1016/j.virol.2010.12.006.
17. Chen J, Jardetzky TS, Longnecker R. 2013. The large groove found in the gH/gL structure is an important functional domain for Epstein-Barr virus fusion. J. Virol. 87:3620-3627. http://dx.doi.org/10.1128/JVI.03245-12.
18. Wu L, Borza CM, Hutt-Fletcher LM. 2005. Mutations of Epstein-Barr virus gH that are differentially able to support fusion with B cells or epithelial cells. J. Virol. 79:10923-10930. http://dx.doi.org/10.1128/JVI.79.17.10923-10930.2005.
19. Wu L, Hutt-Fletcher LM. 2007. Point mutations in EBV gH that abrogate or differentially affect B cell and epithelial cell fusion. Virology 363:148-155. http://dx.doi.org/10.1016/j.virol.2007.01.025.
20. Pellett PE, Biggin MD, Barrell B, Roizman B. 1985. Epstein-Barr virus genome may encode a protein showing significant amino acid and predicted secondary structure homology with glycoprotein B of herpes simplex virus 1. J. Virol. 56:807-813.
21. Maurer UE, Sodeik B, Grunewald K. 2008. Native 3D intermediates of membrane fusion in herpes simplex virus 1 entry. Proc. Natl. Acad. Sci. U. S. A. 105:10559-10564. http://dx.doi.org/10.1073/pnas.0801674105.
22. Garcia NJ, Chen J, Longnecker R. 2013. Modulation of Epstein-Barr virus glycoprotein B (gB) fusion activity by the gB cytoplasmic tail domain. mBio 4(1):e00571-12. http://dx.doi.org/10.1128/mBio.00571-12.
23. Omerović J, Lev L, Longnecker R. 2005. The amino terminus of Epstein-Barr virus glycoprotein gH is important for fusion with epithelial and B cells. J. Virol. 79:12408-12415. http://dx.doi.org/10.1128 /JVI.79.19.12408-12415.2005.
24. Silva AL, Omerović J, Jardetzky TS, Longnecker R. 2004. Mutational analyses of Epstein-Barr virus glycoprotein 42 reveal functional domains not involved in receptor binding but required for membrane fusion. J. Virol. 78:5946-5956. http://dx.doi.org/10.1128/JVI.78.11.5946-5956.2004.
25. Chen J, Rowe CL, Jardetzky TS, Longnecker R. 2012. The KGD motif of Epstein-Barr virus gH/gL is bifunctional, orchestrating infection of B cells and epithelial cells. mBio 3(1):e00290-11. http://dx.doi.org/10.1128/mBio.00290-11.
26. Silverman JL, Heldwein EE. 2013. Mutations in the cytoplasmic tail of herpes simplex virus 1 gH reduce the fusogenicity of gB in transfected cells. J. Virol. 87:10139-10147. http://dx.doi.org/10.1128/JVI.01760-13.
27. Reimer JJ, Backovic M, Deshpande CG, Jardetzky T, Longnecker R. 2009. Analysis of Epstein-Barr virus glycoprotein B functional domains via linker insertion mutagenesis. J. Virol. 83:734-747. http://dx.doi.org /10.1128/JVI.01817-08.
28. McShane MP, Longnecker R. 2004. Cell-surface expression of a mutated Epstein-Barr virus glycoprotein B allows fusion independent of other viral proteins. Proc. Natl. Acad. Sci. U. S. A. 101:17474-17479. http://dx.doi.org/10.1073/pnas.0404535101.
29. 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. http://dx.doi.org/10.1128 /JVI.00206-10.
30. Park SJ, Seo MD, Lee SK, Lee BJ. 2008. Membrane binding properties of EBV gp110 C-terminal domain; evidences for structural transition in the membrane environment. Virology 379:181-190. http://dx.doi.org/10.1016/j.virol.2008.06.031.
31. 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. http: //dx.doi.org/10.1128/JVI.01791-09.
32. Omerović J, Longnecker R. 2007. Functional homology of gHs and gLs from EBV-related gamma-herpesviruses for EBV-induced membrane fusion. Virology 365:157-165. http://dx.doi.org/10.1016/j.virol.2007.03.054.
33. Kirschner AN, Lowrey AS, Longnecker R, Jardetzky TS. 2007. Binding-site interactions between Epstein-Barr virus fusion proteins gp42 and gH/gL reveal a peptide that inhibits both epithelial and B-cell membrane fusion. J. Virol. 81:9216-9229. http://dx.doi.org/10.1128 /JVI.00575-07.
34. Kirschner AN, Sorem J, Longnecker R, Jardetzky TS. 2009. Structure of Epstein-Barr virus glycoprotein 42 suggests a mechanism for triggering receptor-activated virus entry. Structure 17:223-233. http://dx.doi.org/10.1016/j.str.2008.12.010.
35. Shaw PL, Kirschner AN, Jardetzky TS, Longnecker R. 2010. Characteristics of Epstein-Barr virus envelope protein gp42. Virus Genes 40:307-319. http://dx.doi.org/10.1007/s11262-010-0455-x.
36. Sorem J, Jardetzky TS, Longnecker R. 2009. Cleavage and secretion of Epstein-Barr virus glycoprotein 42 promote membrane fusion with B lymphocytes. J. Virol. 83:6664-6672. http://dx.doi.org/10.1128/JVI.00195-09.
37. Paterson RG, Russell CJ, Lamb RA. 2000. Fusion protein of the paramyxovirus SV5: destabilizing and stabilizing mutants of fusion activation. Virology 270:17-30. http://dx.doi.org/10.1006/viro.2000.0267.
38. Waning DL, Russell CJ, Jardetzky TS, Lamb RA. 2004. Activation of a paramyxovirus fusion protein is modulated by inside-out signaling from the cytoplasmic tail. Proc. Natl. Acad. Sci. U. S. A. 101:9217-9222. http: //dx.doi.org/10.1073/pnas.0403339101.
39. Rowe CL, Connolly SA, Chen J, Jardetzky TS, Longnecker R. 2013. A soluble form of Epstein-Barr virus gH/gL inhibits EBV-induced membrane fusion and does not function in fusion. Virology 436:118-126. http: //dx.doi.org/10.1016/j.virol.2012.10.039.
40. Aguilar HC, Matreyek KA, Choi DY, Filone CM, Young S, Lee B. 2007. Polybasic KKR motif in the cytoplasmic tail of Nipah virus fusion protein modulates membrane fusion by inside-out signaling. J. Virol. 81:4520-4532. http://dx.doi.org/10.1128/JVI.02205-06.
41. Li Q, Spriggs MK, Kovats S, Turk SM, Comeau MR, Nepom B, Hutt-Fletcher LM. 1997. Epstein-Barr virus uses HLA class II as a cofactor for infection of B lymphocytes. J. Virol. 71:4657-4662.
42. Yin HS, Paterson RG, Wen X, Lamb RA, Jardetzky TS. 2005. Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc. Natl. Acad. Sci. U. S. A. 102:9288-9293. http://dx.doi.org/10.1073/pnas.0503989102.
43. Samal S, Khattar SK, Paldurai A, Palaniyandi S, Zhu X, Collins PL, Samal SK. 2013. Mutations in the cytoplasmic domain of the Newcastle disease virus fusion protein confer hyperfusogenic phenotypes modulating viral replication and pathogenicity. J. Virol. 87:10083-10093. http://dx.doi.org/10.1128/JVI.01446-13.
44. Zokarkar A, Lamb RA. 2012. The paramyxovirus fusion protein C-terminal region: mutagenesis indicates an indivisible protein unit. J. Virol. 86:2600-2609. http://dx.doi.org/10.1128/JVI.06546-11.
45. Sergel T, Morrison TG. 1995. Mutations in the cytoplasmic domain of the fusion glycoprotein of Newcastle disease virus depress syncytia formation. Virology 210:264-272. http://dx.doi.org/10.1006/viro.1995.1343.
46. 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. http://dx.doi.org/10.1128/JVI.00932-12.
47. 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.
48. 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.
49. Haan KM, Lee SK, Longnecker R. 2001. Different functional domains in the cytoplasmic tail of glycoprotein B are involved in Epstein-Barr virusinduced membrane fusion. Virology 290:106-114. http://dx.doi.org/10.1006/viro.2001.1141.
50. Claesson-Welsh L, Spear PG. 1986. Oligomerization of herpes simplex virus glycoprotein B. J. Virol. 60:803-806.
51. Atanasiu D, Cairns TM, Whitbeck JC, Saw WT, Rao S, Eisenberg RJ, Cohen GH. 2013. Regulation of herpes simplex virus gB-induced cell-cell fusion by mutant forms of gH/gL in the absence of gD and cellular receptors. mBio 4(2):e00046-13. http://dx.doi.org/10.1128 /mBio.00046-13.
52. 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-to-cell spread. J. Virol. 87:1430-1442. http://dx.doi.org/10.1128 /JVI.02804-12.