A site of varicella-zoster virus vulnerability identified by structural studies of neutralizing antibodies bound to the glycoprotein complex gHgL

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

Volumn 112, Issue 19, 2015, Pages 6056-6061

  Xing, Yi ^a   Oliver, Stefan L ^b   Nguyen, TuongVi ^a   Ciferri, Claudio ^a,f   Nandi, Avishek ^a   Hickman, Julie ^a   Giovani, Cinzia ^c   Yang, Edward ^b   Palladino, Giuseppe ^d   Grose, Charles ^e   Uematsu, Yasushi ^c   Lilja, Anders E ^a,g   Arvin, Ann M ^b   Carfí, Andrea ^a  

^a GLAXOSMITHKLINE   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c GSK   (Italy)

^d Novartis Vaccines ^*  (United States)

^e UNIVERSITY OF IOWA CHILDREN S HOSPITAL   (United States)

^f GENENTECH INC   (United States)

^g HOOKIPA BIOTECH AG   (Austria)

Author keywords

Crystal structures; Electron microscopy; GHgL; Neutralizing antibodies; VZV

Indexed keywords

CHEMOKINE; EPITOPE; HUMAN MONOCLONAL ANTIBODY; IMMUNOGLOBULIN G RC; IMMUNOGLOBULIN G24; IMMUNOGLOBULIN G94; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS GLYCOPROTEIN GHGL; GLYCOPROTEIN; GLYCOPROTEIN GHGL, VARICELLA-ZOSTER VIRUS; IMMUNOGLOBULIN FRAGMENT; MONOCLONAL ANTIBODY; PROTEIN BINDING; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

ALPHA HELIX; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN ANTIBODY COMPLEX; ANTIGEN BINDING; ANTIGENICITY; ARTICLE; BETA SHEET; BINDING AFFINITY; BINDING SITE; CELL FUSION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CROSS LINKING; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; DISULFIDE BOND; ENZYME INHIBITION; EPITOPE MAPPING; HERPES SIMPLEX VIRUS 2; HERPESVIRIDAE; HYDROGEN BOND; HYDROPHOBICITY; IN VIVO STUDY; MEMBRANE FUSION; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN TARGETING; SOMATIC MUTATION; SURFACE AREA; SURFACE PLASMON RESONANCE; VARICELLA ZOSTER VIRUS; VIRAL PHENOMENA AND FUNCTIONS; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS NEUTRALIZATION; VIRUS VULNERABILITY; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; IMMUNOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SERODIAGNOSIS; X RAY CRYSTALLOGRAPHY;

ALPHAHERPESVIRINAE; HERPESVIRIDAE; HUMAN HERPESVIRUS 3;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CRYSTALLOGRAPHY, X-RAY; EPITOPES; GLYCOPROTEINS; HERPESVIRUS 3, HUMAN; HUMANS; IMMUNOGLOBULIN FRAGMENTS; MICE; MODELS, MOLECULAR; NEUTRALIZATION TESTS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SURFACE PLASMON RESONANCE; VIRAL ENVELOPE PROTEINS;

EID: 84929191590     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1501176112     Document Type: Article

References (38)

1. Arvin A, Abendroth A (2007) VZV: Immunobiology and host response. Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis, eds Arvin A, Campadelli-Fiume G, Mocarski E, et al. (Cambridge Univ Press, Cambridge, UK).
2. Zerboni L, Sen N, Oliver SL, Arvin AM (2014) Molecular mechanisms of varicella zoster virus pathogenesis. Nat Rev Microbiol 12(3):197-210.
3. Moffat J, Ku C-C, Zerboni L, Sommer M, Arvin A (2007) Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis, eds Arvin A, Campadelli-Fiume G, Mocarski E, et al. (Cambridge Univ Press, Cambridge, UK).
4. Takahashi M, et al. (1985) Clinical experience with Oka live varicella vaccine in Japan. Postgrad Med J 61(Suppl 4):61-67.
5. Holcomb K, Weinberg JM (2006) A novel vaccine (Zostavax) to prevent herpes zoster and postherpetic neuralgia. J Drugs Dermatol 5(9):863-866.
6. Leroux-Roels I, et al. (2012) A phase 1/2 clinical trial evaluating safety and immunogenicity of a varicella zoster glycoprotein e subunit vaccine candidate in young and older adults. J Infect Dis 206(8):1280-1290.
7. Centers for Disease Control and Prevention (CDC) (2013) Updated recommendations for use of VariZIG-United States, 2013. MMWR Morb Mortal Wkly Rep 62(28):574-576.
8. Peng T, et al. (1998) Structural and antigenic analysis of a truncated form of the herpes simplex virus glycoprotein gH-gL complex. J Virol 72(7):6092-6103.
9. Vleck SE, et al. (2011) Structure-function analysis of varicella-zoster virus glycoprotein H identifies domain-specific roles for fusion and skin tropism. Proc Natl Acad Sci USA 108(45):18412-18417.
10. Suenaga T, et al. (2010) Myelin-associated glycoprotein mediates membrane fusion and entry of neurotropic herpesviruses. Proc Natl Acad Sci USA 107(2):866-871.
11. Chowdary TK, et al. (2010) Crystal structure of the conserved herpesvirus fusion regulator complex gH-gL. Nat Struct Mol Biol 17(7):882-888.
12. 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.
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(5784):187-191.
14. Heldwein EE, et al. (2006) Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313(5784):217-220.
15. 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.
16. Atanasiu D, et al. (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 USA 104(47):18718-18723.
17. Avitabile E, Forghieri C, Campadelli-Fiume G (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(20):10752-10760.
18. Yang E, Arvin AM, Oliver SL (2014) The cytoplasmic domain of varicella-zoster virus glycoprotein H regulates syncytia formation and skin pathogenesis. PLoS Pathog 10(5):e1004173.
19. Oliver SL, et al. (2013) An immunoreceptor tyrosine-based inhibition motif in varicella-zoster virus glycoprotein B regulates cell fusion and skin pathogenesis. Proc Natl Acad Sci USA 110(5):1911-1916.
20. Montalvo EA, Grose C (1986) Neutralization epitope of varicella zoster virus on native viral glycoprotein gp118 (VZV glycoprotein gpIII). Virology 149(2):230-241.
21. Vleck SE, et al. (2010) Anti-glycoprotein H antibody impairs the pathogenicity of varicella-zoster virus in skin xenografts in the SCID mouse model. J Virol 84(1): 141-152.
22. Rodriguez JE, Moninger T, Grose C (1993) Entry and egress of varicella virus blocked by same anti-gH monoclonal antibody. Virology 196(2):840-844.
23. Suzuki K, Akahori Y, Asano Y, Kurosawa Y, Shiraki K (2007) Isolation of therapeutic human monoclonal antibodies for varicella-zoster virus and the effect of light chains on the neutralizing activity. J Med Virol 79(6):852-862.
24. Birlea M, et al. (2013) Human anti-varicella-zoster virus (VZV) recombinant monoclonal antibody produced after Zostavax immunization recognizes the gH/gL complex and neutralizes VZV infection. J Virol 87(1):415-421.
25. 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.
26. Malkowska M, Kokoszynska K, Dymecka M, Rychlewski L, Wyrwicz LS (2013) Alphaherpesvirinae and Gammaherpesvirinae glycoprotein L and CMV UL130 originate from chemokines. Virol J 10:1.
27. Akahori Y, et al. (2009) Characterization of neutralizing epitopes of varicella-zoster virus glycoprotein H. J Virol 83(4):2020-2024.
28. Brochet X, Lefranc MP, Giudicelli V (2008) IMGT/V-QUEST: The highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 36(Web Server issue):W503-W508.
29. Corey L, et al.; Chiron HSV Vaccine Study Group (1999) Recombinant glycoprotein vaccine for the prevention of genital HSV-2 infection: Two randomized controlled trials. JAMA 282(4):331-340.
30. Rieder F, Steininger C (2014) Cytomegalovirus vaccine: Phase II clinical trial results. Clin Microbiol Infect 20(Suppl 5):95-102.
31. Correia BE, et al. (2014) Proof of principle for epitope-focused vaccine design. Nature 507(7491):201-206.
32. Cairns TM, et al. (2006) Epitope mapping of herpes simplex virus type 2 gH/gL defines distinct antigenic sites, including some associated with biological function. J Virol 80(6):2596-2608.
33. Atanasiu D, et al. (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.
34. Gompels UA, et al. (1991) Characterization and sequence analyses of antibody-selected antigenic variants of herpes simplex virus show a conformationally complex epitope on glycoprotein H. J Virol 65(5):2393-2401.
35. Galdiero M, et al. (1997) Site-directed and linker insertion mutagenesis of herpes simplex virus type 1 glycoprotein H. J Virol 71(3):2163-2170.
36. 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(19): 12408-12415.
37. 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(7): 3620-3627.
38. Plate AE, Smajlović J, Jardetzky TS, Longnecker R (2009) Functional analysis of glycoprotein L (gL) from rhesus lymphocryptovirus in Epstein-Barr virus-mediated cell fusion indicates a direct role of gL in gB-induced membrane fusion. J Virol 83(15): 7678-7689.