Two distinct trimeric conformations of natively membrane-anchored full-length herpes simplex virus 1 glycoprotein B

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 15, 2016, Pages 4176-4181

  Zeev Ben Mordehai, Tzviya ^a   Vasishtan, Daven ^a   Durán, Anna Hernández ^a,b   Vollmer, Benjamin ^a   White, Paul ^a   Pandurangan, Arun Prasad ^b   Siebert, C Alistair ^a   Topf, Maya ^b   Grünewald, Kay ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Class III viral fusion protein; Electron cryotomography; Membrane fusion; Prefusion conformation; Subvolume averaging

Indexed keywords

GLYCOPROTEIN B; VIRUS FUSION PROTEIN; MEMBRANE PROTEIN; VIRUS ENVELOPE PROTEIN;

ARTICLE; CONTROLLED STUDY; ELECTRON CRYOTOMOGRAPHY; ELECTRON TOMOGRAPHY; HERPES SIMPLEX VIRUS 1; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; VIRUS ENVELOPE; CHEMISTRY; CRYOELECTRON MICROSCOPY;

CRYOELECTRON MICROSCOPY; HERPESVIRUS 1, HUMAN; MEMBRANE GLYCOPROTEINS; PROTEIN CONFORMATION; VIRAL ENVELOPE PROTEINS;

EID: 84963772016     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1523234113     Document Type: Article

References (46)

1. Martens S, McMahon HT (2008) Mechanisms of membrane fusion: Disparate players and common principles. Nat Rev Mol Cell Biol 9(7):543-556.
2. Mercer J, Schelhaas M, Helenius A (2010) Virus entry by endocytosis. Annu Rev Biochem 79:803-833.
3. Grünewald K, et al. (2003) Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 302(5649):1396-1398.
4. Pellett P, Roizman B (2007) The family Herpesviridae: A brief introduction. Fields Virology, eds Knipe D, Howley PM (Lippincott, Williams and Wilkins, Philadelphia), 5th Ed, pp 2479-2499.
5. Loret S, Guay G, Lippé R (2008) Comprehensive characterization of extracellular herpes simplex virus type 1 virions. J Virol 82(17):8605-8618.
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(5):369-381.
7. Backovic M, et al. (2010) Structure of a core fragment of glycoprotein H from pseudorabies virus in complex with antibody. Proc Natl Acad Sci USA 107(52):22635-22640.
8. Backovic M, Longnecker R, Jardetzky TS (2009) Structure of a trimeric variant of the Epstein-Barr virus glycoprotein B. Proc Natl Acad Sci USA 106(8):2880-2885.
9. Chowdary TK, et al. (2010) Crystal structure of the conserved herpesvirus fusion regulator complex gH-gL. Nat Struct Mol Biol 17(7):882-888.
10. Heldwein EE, et al. (2006) Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313(5784):217-220.
11. Matsuura H, Kirschner AN, Longnecker R, Jardetzky TS (2010) Crystal structure of the Epstein-Barr virus (EBV) glycoprotein H/glycoprotein L (gH/gL) complex. Proc Natl Acad Sci USA 107(52):22641-22646.
12. Harrison SC (2015) Viral membrane fusion. Virology 479-480:498-507.
13. Chandramouli S, et al. (2015) Structure of HCMV glycoprotein B in the postfusion conformation bound to a neutralizing human antibody. Nat Commun 6:8176.
14. Burke HG, Heldwein EE (2015) Crystal Structure of the Human Cytomegalovirus Glycoprotein B. PLoS Pathog 11(10):e1005227.
15. Backovic M, Jardetzky TS (2009) Class III viral membrane fusion proteins. Curr Opin Struct Biol 19(2):189-196.
16. 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(10):1024-1030.
17. 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 USA 102(26):9288-9293.
18. Zeev-Ben-Mordehai T, Vasishtan D, Siebert CA, Whittle C, Grünewald K (2014) Extracellular vesicles: A platform for the structure determination of membrane proteins by Cryo-EM. Structure 22(11):1687-1692.
19. Claesson-Welsh L, Spear PG (1986) Oligomerization of herpes simplex virus glycoprotein B. J Virol 60(2):803-806.
20. Maurer UE, et al. (2013) The structure of herpesvirus fusion glycoprotein B-bilayer complex reveals the protein-membrane and lateral protein-protein interaction. Structure 21(8):1396-1405.
21. Bender FC, et al. (2007) Antigenic and mutational analyses of herpes simplex virus glycoprotein B reveal four functional regions. J Virol 81(8):3827-3841.
22. Cairns TM, et al. (2014) Mechanism of neutralization of herpes simplex virus by antibodies directed at the fusion domain of glycoprotein B. J Virol 88(5):2677-2689.
23. Baquero E, et al. (2015) Structure of the low pH conformation of Chandipura virus G reveals important features in the evolution of the vesiculovirus glycoprotein. PLoS Pathog 11(3):e1004756.
24. 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 USA 104(32):13140-13145.
25. Gallagher JR, et al. (2014) Functional fluorescent protein insertions in herpes simplex virus gB report on gB conformation before and after execution of membrane fusion. PLoS Pathog 10(9):e1004373.
26. Park HE, Gruenke JA, White JM (2003) Leash in the groove mechanism of membrane fusion. Nat Struct Biol 10(12):1048-1053.
27. Roche S, Rey FA, Gaudin Y, Bressanelli S (2007) Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science 315(5813):843-848.
28. Kielian M, Rey FA (2006) Virus membrane-fusion proteins: more than one way to make a hairpin. Nat Rev Microbiol 4(1):67-76.
29. Zeev-Ben-Mordehai T, Vasishtan D, Siebert CA, Grünewald K (2014) The full-length cell-cell fusogen EFF-1 is monomeric and upright on the membrane. Nat Commun 5:3912.
30. 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(1):313-324.
31. Mastronarde DN (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152(1):36-51.
32. Sandberg K, Mastronarde DN, Beylkin G (2003) A fast reconstruction algorithm for electron microscope tomography. J Struct Biol 144(1-2):61-72.
33. Nicastro D, et al. (2006) The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313(5789):944-948.
34. Heymann JB, Belnap DM (2007) Bsoft: Image processing and molecular modeling for electron microscopy. J Struct Biol 157(1):3-18.
35. Eswar N, et al. (2006) Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics Chapter 5: Unit 5.6.
36. Pettersen EF, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605-1612.
37. Pintilie GD, Zhang J, Goddard TD, Chiu W, Gossard DC (2010) Quantitative analysis of cryo-EM density map segmentation by watershed and scale-space filtering, and fitting of structures by alignment to regions. J Struct Biol 170(3):427-438.
38. Garzón JI, Kovacs J, Abagyan R, Chacón P (2007) ADP-EM: Fast exhaustive multiresolution docking for high-throughput coverage. Bioinformatics 23(4):427-433.
39. Kawabata T (2008) Multiple subunit fitting into a low-resolution density map of a macromolecular complex using a gaussian mixture model. Biophys J 95(10):4643-4658.
40. Lasker K, Topf M, Sali A, Wolfson HJ (2009) Inferential optimization for simultaneous fitting of multiple components into a CryoEM map of their assembly. J Mol Biol 388(1):180-194.
41. Pandurangan AP, Shakeel S, Butcher SJ, Topf M (2014) Combined approaches to flexible fitting and assessment in virus capsids undergoing conformational change. J Struct Biol 185(3):427-439.
42. Vasishtan D, Topf M (2011) Scoring functions for cryoEM density fitting. J Struct Biol 174(2):333-343.
43. Topf M, et al. (2008) Protein structure fitting and refinement guided by cryo-EM density. Structure 16(2):295-307.
44. Mackeen MM, et al. (2010) Small-molecule-based inhibition of histone demethylation in cells assessed by quantitative mass spectrometry. J Proteome Res 9(8):4082-4092.
45. Ishihama Y, et al. (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4(9):1265-1272.
46. Trudgian DC, et al. (2011) Comparative evaluation of label-free SINQ normalized spectral index quantitation in the central proteomics facilities pipeline. Proteomics 11(14):2790-2797.