Dissection of the antibody response against herpes simplex virus glycoproteins in naturally infected humans

Journal of Virology

Volumn 88, Issue 21, 2014, Pages 12612-12622

  Cairns, Tina M ^a   Huang, Zhen Yu ^a   Whitbeck, J Charles ^a   de Leon, Manuel Ponce ^a   Lou, Huan ^a   Wald, Anna ^b   Krummenacher, Claude ^a   Eisenberg, Roselyn J ^a   Cohen, Gary H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GLYCOPROTEIN GB; GLYCOPROTEIN GC; GLYCOPROTEIN GD; GLYCOPROTEIN GHGL; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; GLYCOPROTEIN; NEUTRALIZING ANTIBODY; VIRAL PROTEIN; VIRUS ANTIBODY;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; HERPES SIMPLEX VIRUS; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 2; HERPES VIRUS INFECTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; NONHUMAN; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE; VIRION; VIRUS NEUTRALIZATION; VIRUS SHEDDING; WESTERN BLOTTING; ANIMAL; ANTIBODY PRODUCTION; BLOOD; HERPES SIMPLEX; IMMUNOLOGY; MOUSE; SIMPLEXVIRUS;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY FORMATION; GLYCOPROTEINS; HERPES SIMPLEX; HUMANS; IMMUNOGLOBULIN G; MICE; SIMPLEXVIRUS; VIRAL STRUCTURAL PROTEINS;

EID: 84908010593     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01930-14     Document Type: Article

References (62)

1. Bradley H, Markowitz LE, Gibson T, McQuillan GM. 2014. Seroprevalence of herpes simplex virus types 1 and 2-United States, 1999-2010. J. Infect. Dis. 209:325-333. http://dx.doi.org/10.1093/infdis/jit458.
2. Kinchington PR, Leger AJ, Guedon JM, Hendricks RL. 2012. Herpes simplex virus and varicella zoster virus, the house guests who never leave. Herpesviridae 3:5. http://dx.doi.org/10.1186/2042-4280-3-5.
3. Schiffer JT, Swan D, Al Sallaq R, Magaret A, Johnston C, Mark KE, Selke S, Ocbamichael N, Kuntz S, Zhu J, Robinson B, Huang ML, Jerome KR, Wald A, Corey L. 2013. Rapid localized spread and immunologic containment define herpes simplex virus-2 reactivation in the human genital tract. eLife 2:e00288. http://dx.doi.org/10.7554/eLife.00288.
4. Awasthi S, Balliet JW, Flynn JA, Lubinski JM, Shaw CE, Distefano DJ, Cai M, Brown M, Smith JF, Kowalski R, Swoyer R, Galli J, Copeland V, Rios S, Davidson RC, Salnikova M, Kingsley S, Bryan J, Casimiro DR, Friedman HM. 2014. Protection provided by an HSV-2 glycoprotein C and D subunit antigen vaccine against genital HSV-2 infection in HSV-1 seropositive guinea pigs. J. Virol. 88:2000-2010. http://dx.doi.org/10.1128/JVI.03163-13.
5. Awasthi S, Friedman HM. 2014. A paradigm shift: vaccine-induced antibodies as an immune correlate of protection against herpes simplex virus type 1 genital herpes. J. Infect. Dis. 209:813-815. http://dx.doi.org/10.1093/infdis/jit658.
6. Belshe RB, Heineman TC, Bernstein DI, Bellamy AR, Ewell M, van der Most R, Deal CD. 2014. Correlate of immune protection against HSV-1 genital disease in vaccinated women. J. Infect. Dis. 209:828-836. http://dx.doi.org/10.1093/infdis/jit651.
7. 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. http://dx.doi.org/10.3390/v4050800.
8. Bender FC, Samanta M, Heldwein EE, de Leon MP, Bilman E, Lou H, Whitbeck JC, Eisenberg RJ, Cohen GH. 2007. Antigenic and mutational analyses of herpes simplex virus glycoprotein B reveal four functional regions. J. Virol. 81:3827-3841. http://dx.doi.org/10.1128/JVI.02710-06.
9. Whitbeck JC, Muggeridge MI, Rux AH, Hou W, Krummenacher C, Lou H, van Geelen A, Eisenberg RJ, Cohen GH. 1999. The major neutralizing antigenic site on herpes simplex virus glycoprotein D overlaps a receptorbinding domain. J. Virol. 73:9879-9890.
10. Cairns TM, Shaner MS, Zuo Y, De-Leon M, Baribaud I, Eisenberg RJ, Cohen GH, Whitbeck JC. 2006. Epitope mapping of herpes simplex virus type 2 gH/gL defines distinct antigenic sites, including some associated with biological function. J. Virol. 80:2596-2608. http://dx.doi.org/10.1128/JVI.80.6.2596-2608.2006.
11. Peng T, De-Leon M, Jiang H, Dubin G, Lubinski JM, Eisenberg RJ, Cohen GH. 1998. The gH-gL complex of herpes simplex virus (HSV) stimulates neutralizing antibody and protects mice against HSV type 1 challenge. J. Virol. 72:65-72.
12. Nicola AV, Ponce de Leon M, Xu R, Hou W, Whitbeck JC, Krummenacher C, Montgomery RI, Spear PG, Eisenberg RJ, Cohen GH. 1998. Monoclonal antibodies to distinct sites on herpes simplex virus (HSV) glycoprotein D block HSV binding to HVEM. J. Virol. 72:3595-3601.
13. Fries LF, Friedman HM, Cohen GH, Eisenberg RJ, Hammer CH, Frank MM. 1986. Glycoprotein C of herpes simplex virus 1 is an inhibitor of the complement cascade. J. Immunol. 137:1636-1641.
14. Friedman HM, Wang L, Fishman NO, Lambris JD, Eisenberg RJ, Cohen GH, Lubinski J. 1996. Immune evasion properties of herpes simplex virus type 1 glycoprotein gC. J. Virol. 70:4253-4260.
15. Lubinski JM, Wang L, Soulika AM, Burger R, Wetsel RA, Colten H, Cohen GH, Eisenberg RJ, Lambris JD, Friedman HM. 1998. Herpes simplex virus type 1 glycoprotein gC mediates immune evasion in vivo. J. Virol. 72:8257-8263.
16. Lazear E, Whitbeck JC, De-Leon M, Cairns TM, Willis SH, Zuo Y, Krummenacher C, Cohen GH, Eisenberg RJ. 2012. Antibody-induced conformational changes in herpes simplex virus glycoprotein gD reveal new targets for virus neutralization. J. Virol. 86:1563-1576. http://dx.doi.org/10.1128/JVI.06480-11.
17. Muggeridge MI, Isola VJ, Byrn RA, Tucker TJ, Minson AC, Glorioso JC, Cohen GH, Eisenberg RJ. 1988. Antigenic analysis of a major neutralization site of herpes simpelx virus glycoprotein D using deletion mutants and monoclonal antibody-resistant mutants. J. Virol. 62:3274-3280.
18. Muggeridge MI, Wu T-T, Johnson DC, Glorioso JC, Eisenberg RJ, Cohen GH. 1990. Antigenic and functional analysis of a neutralization site of HSV-1 glycoprotein D. Virology 174:375-387. http://dx.doi.org/10.1016/0042-6822(90)90091-5.
19. Cairns TM, Fontana J, Huang ZY, Whitbeck JC, Atanasiu D, Rao S, Shelly SS, Lou H, Ponce de Leon M, Steven AC, Eisenberg RJ, Cohen GH. 2014. Mechanism of neutralization of herpes simplex virus by antibodies directed at the fusion domain of glycoprotein B. J. Virol. 88:2677-2689 http://dx.doi.org/10.1128/JVI.03200-13.
20. 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. http://dx.doi.org /10.1128/JVI.02687-09.
21. 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. http://dx.doi.org/10.1038/nsmb.1837.
22. Krummenacher C, Nicola AV, Whitbeck JC, Lou H, Hou W, Lambris JD, Geraghty RJ, Spear PG, Cohen GH, Eisenberg RJ. 1998. Herpes simplex virus glycoprotein D can bind to poliovirus receptor-related protein 1 or herpesvirus entry mediator, two structurally unrelated mediators of virus entry. J. Virol. 72:7064-7074.
23. Tronstein E, Johnston C, Huang ML, Selke S, Magaret A, Warren T, Corey L, Wald A. 2011. Genital shedding of herpes simplex virus among symptomatic and asymptomatic persons with HSV-2 infection. JAMA 305:1441-1449. http://dx.doi.org/10.1001/jama.2011.420.
24. Sisk WP, Bradley JD, Leipold RJ, Stoltzfus AM, Ponce de Leon M, Hilf M, Peng C, Cohen GH, Eisenberg RJ. 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.
25. Nicola AV, Willis SH, Naidoo NN, Eisenberg RJ, Cohen GH. 1996. Structure-function analysis of soluble forms of herpes simplex virus glycoprotein D. J. Virol. 70:3815-3822.
26. Krummenacher C, Rux AH, Whitbeck JC, De-Leon M, Lou H, Baribaud I, Hou W, Zou C, Geraghty RJ, Spear PG, Eisenberg RJ, Cohen GH. 1999. The first immunoglobulin-like domain of HveC is sufficient to bind herpes simplex virus gD with full affinity, while the third domain is involved in oligomerization of HveC. J. Virol. 73:8127-8137.
27. Tal-Singer R, Peng C, Ponce De Leon M, Abrams WR, Banfield BW, Tufaro F, Cohen GH, Eisenberg RJ. 1995. Interaction of herpes simplex virus glycoprotein gC with mammalian cell surface molecules. J. Virol. 69:4471-4483.
28. Hannah BP, Cairns TM, Bender FC, Whitbeck JC, Lou H, Eisenberg RJ, Cohen GH. 2009. Herpes simplex virus glycoprotein B associates with target membranes via its fusion loops. J. Virol. 83:6825-6836. http://dx.doi.org/10.1128/JVI.00301-09.
29. Bender FC, Whitbeck JC, Ponce de Leon M, Lou H, Eisenberg RJ, Cohen GH. 2003. Specific association of glycoprotein B with lipid rafts during herpes simplex virus entry. J. Virol. 77:9542-9552. http://dx.doi.org/10.1128/JVI.77.17.9542-9552.2003.
30. Shelly SS, Cairns TM, Whitbeck JC, Lou H, Krummenacher C, Cohen GH, Eisenberg RJ. 2012. The membrane-proximal region (MPR) of herpes simplex virus gB regulates association of the fusion loops with lipid membranes. mBio 3(6):e00429-12. http://dx.doi.org /10.1128/mBio.00429-12.
31. Cairns TM, Whitbeck JC, Lou H, Heldwein EE, Chowdary TK, Eisenberg RJ, Cohen GH. 2011. Capturing the herpes simplex virus core fusion complex (gB-gH/gL) in an acidic environment. J. Virol. 85:6175-6184. http://dx.doi.org/10.1128/JVI.00119-11.
32. Cohen GH, Isola VJ, Kuhns J, Berman PW, Eisenberg RJ. 1986. Localization 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.
33. 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. http: //dx.doi.org/10.1128/JVI.79.18.11588-11597.2005.
34. Navarro D, Paz P, Pereira L. 1992. Domains of herpes simplex virus I glycoprotein B that function in virus penetration, cell-to-cell spread, and cell fusion. Virology 186:99-112. http://dx.doi.org/10.1016/0042-6822(92)90064-V.
35. Pereira L, Ali M, Kousoulas K, Huo B, Banks T. 1989. Domain structure of herpes simplex virus 1 glycoprotein B: neutralizing epitopes map in regions of continuous and discontinuous residues. Virology 172:11-24. http://dx.doi.org/10.1016/0042-6822(89)90102-5.
36. Cairns TM, Fontana J, Huang ZY, Whitbeck JC, Atanasiu D, Rao S, Shelly SS, Lou H, de Leon MP, Steven AC, Eisenberg RJ, Cohen GH. 2014 Mechanism of neutralization of HSV by antibodies directed at the fusion domain of glycoprotein B. J. Virol. 88:2677-2689. http://dx.doi.org /10.1128/JVI.03200-13.
37. Isola VJ, Eisenberg RJ, Siebert GR, Heilman CJ, Wilcox WC, Cohen GH. 1989. Fine mapping of antigenic site II of herpes simplex virus glycoprotein D. J. Virol. 63:2325-2334.
38. Cairns TM, Landsburg DJ, Whitbeck JC, Eisenberg RJ, Cohen GH. 2005 Contribution of cysteine residues to the structure and function of herpes simplex virus gH/gL. Virology 332:550-562. http://dx.doi.org/10.1016/j.virol.2004.12.006.
39. Peng T, Ponce de Leon M, Novotny MJ, Jiang H, Lambris JD, Dubin G, Spear PG, Cohen GH, Eisenberg RJ. 1998. Structural and antigenic analysis of a truncated form of the herpes simplex virus glycoprotein gH-gL complex. J. Virol. 72:6092-6103.
40. Eisenberg RJ, Ponce de Leon M, Friedman HM, Fries LF, Frank MM, Hastings JC, Cohen GH. 1987. Complement component c3b binds directly to purified glycoprotein C of herpes simplex virus types 1 and 2. Microb. Pathog. 3:423-435. http://dx.doi.org/10.1016/0882-4010(87)90012-X.
41. Hung SL, Peng C, Kostavasili I, Friedman HM, Lambris JD, Eisenberg RJ, Cohen GH. 1994. The interaction of glycoprotein C of herpes simplex virus types 1 and 2 with the alternative complement pathway. Virology 203:299-312. http://dx.doi.org/10.1006/viro.1994.1488.
42. Krummenacher C, Baribaud I, Ponce de Leon M, Whitbeck JC, Lou H, Cohen GH, Eisenberg RJ. 2000. Localization of a binding site for herpes simplex virus glycoprotein D on herpesvirus entry mediator C by using antireceptor monoclonal antibodies. J. Virol. 74:10863-10872. http://dx.doi.org/10.1128/JVI.74.23.10863-10872.2000.
43. Rux AH, Lou H, Lambris JD, Friedman HM, Eisenberg RJ, Cohen GH. 2002 Kinetic analysis of glycoproteinCof herpes simplex virus types 1 and 2 binding to heparin, heparan sulfate, and complement component c3b. Virology 294:324-332. http://dx.doi.org/10.1006/viro.2001.1326.
44. Aldaz-Carroll L, Whitbeck JC, Ponce de Leon M, Lou H, Hirao L, Isaacs SN, Moss B, Eisenberg RJ, Cohen GH. 2005. Epitope-mapping studies define two major neutralization sites on the vaccinia virus extracellular enveloped virus glycoprotein b5r. J. Virol. 79:6260-6271. http://dx.doi.org/10.1128/JVI.79.10.6260-6271.2005.
45. Whitbeck JC, Huang ZY, Cairns TM, Gallagher JR, Lou H, De-Leon M, Belshe RB, Eisenberg RJ, Cohen GH. 2014. Repertoire of epitopes recognized by serum IgG from humans vaccinated with herpes simplex virus type 2 glycoprotein D. J. Virol. 88:7786-7795. http://dx.doi.org/10.1128/JVI.00544-14.
46. 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.
47. 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. http://dx.doi.org/10.1128/JVI.02755-06.
48. 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. http://dx.doi.org/10.1073 /pnas.0707452104.
49. 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. http://dx.doi.org/10.1128 /JVI.01700-10.
50. Sanchez-Pescador L, Pereira L, Charlebois ED, Kohl S. 1993. Antibodies to epitopes of herpes simplex virus type 1 glycoprotein B (gB) in human sera: analysis of functional gB epitopes defined by inhibition of murine monoclonal antibodies. J. Infect. Dis. 168:844-853. http://dx.doi.org/10.1093/infdis/168.4.844.
51. Eing BR, Kuhn JE, Braun RW. 1989. Neutralizing activity of antibodies against the major herpes simplex virus type 1 glycoproteins. J. Med. Virol. 27:59-65.
52. Belshe RB, Leone PA, Bernstein DI, Wald A, Levin MJ, Stapleton JT, Gorfinkel I, Morrow RL, Ewell MG, Stokes-Riner A, Dubin G, Heineman TC, Schulte JM, Deal CD. 2012. Efficacy results of a trial of a herpes simplex vaccine. N. Engl. J. Med. 366:34-43. http://dx.doi.org/10.1056 /NEJMoa1103151.
53. Johnston C, Koelle DM, Wald A. 2014. Current status and prospects for development of an HSV vaccine. Vaccine 20:1553-1560. http://dx.doi.org /10.1016/j.vaccine.2013.08.066.
54. Goade DE, Bell R, Yamada T, Mertz GJ, Jenison S. 1996. Locations of herpes simplex virus type 2 glycoprotein B epitopes recognized by human serum immunoglobulin G antibodies. J. Virol. 70:2950-2956.
55. Wittekindt C, Fleckenstein B, Wiesmuller K, Eing BR, Kuhn JE. 2000. Detection of human serum antibodies against type-specifically reactive peptides from the N terminus of glycoprotein B of herpes simplex virus type 1 and type 2 by surface plasmon resonance. J. Virol. Methods 87:133-144 http://dx.doi.org/10.1016/S0166-0934(00)00160-9.
56. Adamiak B, Trybala E, Mardberg K, Johansson M, Liljeqvist JA, Olofsson S, Grabowska A, Bienkowska-Szewczyk K, Szewczyk B, Bergstrom T. 2010. Human antibodies to herpes simplex virus type 1 glycoprotein C are neutralizing and target the heparan sulfate-binding domain. Virology 400:197-206. http://dx.doi.org/10.1016/j.virol.2010.01.032.
57. Svennerholm B, Jeansson S, Vahlne A, Lycke E. 1991. Involvement of glycoprotein C (gC) in adsorption of herpes simplex virus type 1 (HSV-1) to the cell. Arch. Virol. 120:273-279.
58. Weir JP, Bennett M, Allen EM, Elkins KL, Martin S, Rouse BT. 1989. Recombinant vaccinia virus expressing the herpes simplex virus type 1 glycoprotein C protects mice against herpes simplex virus challenge. J. Gen. Virol. 70(Part 10):2587-2594.
59. Awasthi S, Lubinski JM, Shaw CE, Barrett SM, Cai M, Wang F, Betts M, Kingsley S, Distefano DJ, Balliet JW, Flynn JA, Casimiro DR, Bryan JT, Friedman HM. 2011. Immunization with a vaccine combining herpes simplex virus 2 (HSV-2) glycoprotein C (gC) and gD subunits improves the protection of dorsal root ganglia in mice and reduces the frequency of recurrent vaginal shedding of HSV-2 DNA in guinea pigs compared to immunization with gD alone. J. Virol. 85:10472-10486. http://dx.doi.org /10.1128/JVI.00849-11.
60. Showalter SD, Zweig M, Hampar B. 1981. Monoclonal antibodies to herpes simplex virus type 1 proteins, including the immediate-early protein ICP 4. Infect. Immun. 34:684-692.
61. Buckmaster EA, Gompels U, Minson A. 1984. Characterisation and physical mapping of an HSV-1 glycoprotein of approximately 115x10(3) molecular weight. Virology 139:408-413.
62. Gompels U, Minson A. 1986. The properties and sequence of glycoprotein H of herpes simplex virus type 1. Virology 153:230-247.