Anti-glycoprotein g antibodies of herpes simplex virus 2 contribute to complete protection after vaccination in mice and induce antibody-dependent cellular cytotoxicity and complement-mediated cytolysis

Viruses

Volumn 6, Issue 11, 2014, Pages 4358-4372

  Görander, Staffan ^a,b   Ekblad, Maria ^a,b   Bergström, Tomas ^a,b   Liljeqvist, Jan Åke ^a,b  

^a Department of Infectious Diseases Section of Virology   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Antibodies; Glycoprotein G; Herpes simplex virus 2; Vaccination

Indexed keywords

ANTISERUM; CPG OLIGODEOXYNUCLEOTIDE; GAMMA INTERFERON; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2B; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN G ANTIBODY; COMPLEMENT; GLYCOPROTEIN G, HERPES SIMPLEX VIRUS TYPE 2; HERPES SIMPLEX VACCINE; IMMUNOGLOBULIN G; IMMUNOLOGICAL ADJUVANT; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

AGMK CELL LINE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY TITER; BHK CELL LINE; CD4+ T LYMPHOCYTE; CELL PROLIFERATION ASSAY; CELLULAR IMMUNITY; COMPLEMENT DEPENDENT CYTOTOXICITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ACTIVITY SCORE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 2; MOUSE; NONHUMAN; PASSIVE IMMUNIZATION; PLAQUE FORMING CELL ASSAY; REVIEW; SURVIVAL RATE; VACCINATION; VAGINITIS; VIRUS LOAD; VIRUS NEUTRALIZATION; VIRUS REPLICATION; WESTERN BLOTTING; ANIMAL; BLOOD; C57BL MOUSE; CELL PROLIFERATION; IMMUNOLOGY; INTRAMUSCULAR DRUG ADMINISTRATION; SECRETION (PROCESS); SUBCUTANEOUS DRUG ADMINISTRATION; SURVIVAL;

HUMAN HERPESVIRUS 2; MUS;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, VIRAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; COMPLEMENT SYSTEM PROTEINS; FEMALE; HERPES SIMPLEX; HERPES SIMPLEX VIRUS VACCINES; HERPESVIRUS 2, HUMAN; IMMUNIZATION, PASSIVE; IMMUNOGLOBULIN G; INJECTIONS, INTRAMUSCULAR; INJECTIONS, SUBCUTANEOUS; INTERFERON-GAMMA; MICE, INBRED C57BL; SURVIVAL ANALYSIS; VIRAL ENVELOPE PROTEINS;

EID: 84910151882     PISSN: 19994915     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v6114358     Document Type: Review

References (39)

1. Looker, K.J.; Garnett, G.P.; Schmid, G.P. An estimate of the global prevalence and incidence of herpes simplex virus type 2 infection. Bull. World Health Organ. 2008, 86, 805-812.
2. Belshe, R.B.; Leone, P.A.; Bernstein, D.I.; Wald, A.; Levin, M.J.; Stapleton, J.T.; Gorfinkel, I.; Morrow, R.L.; Ewell, M.G.; Stokes-Riner, A.; et al. Efficacy results of a trial of a herpes simplex vaccine. N. Engl. J. Med. 2012, 366, 34-43.
3. Cohen, J. Immunology. Painful failure of promising genital herpes vaccine. Science 2010, 330, 304.
4. Corey, L.; Langenberg, A.G.; Ashley, R.; Sekulovich, R.E.; Izu, A.E.; Douglas, J.M., Jr.; Handsfield, H.H.; Warren, T.; Marr, L.; Tyring, S.; et al. Recombinant glycoprotein vaccine for the prevention of genital HSV-2 infection: Two randomized controlled trials. Chiron HSV vaccine study group. JAMA 1999, 282, 331-340.
5. Stanberry, L.R.; Spruance, S.L.; Cunningham, A.L.; Bernstein, D.I.; Mindel, A.; Sacks, S.; Tyring, S.; Aoki, F.Y.; Slaoui, M.; Denis, M.; et al. Glycoprotein-D-adjuvant vaccine to prevent genital herpes. N. Engl. J. Med. 2002, 347, 1652-1661.
6. Gorander, S.; Svennerholm, B.; Liljeqvist, J.A. Secreted portion of glycoprotein G of herpes simplex virus type 2 is a novel antigen for type-discriminating serology. J. Clin. Microbiol. 2003, 41, 3681-3686.
7. Ho, D.W.; Field, P.R.; Sjogren-Jansson, E.; Jeansson, S.; Cunningham, A.L. Indirect ELISA for the detection of HSV-2 specific IgG and IgM antibodies with glycoprotein G (gG-2). J. Virol. Methods 1992, 36, 249-264.
8. Lee, F.K.; Coleman, R.M.; Pereira, L.; Bailey, P.D.; Tatsuno, M.; Nahmias, A.J. Detection of herpes simplex virus type 2-specific antibody with glycoprotein G. J. Clin. Microbiol. 1985, 22, 641-644.
9. Svennerholm, B.; Olofsson, S.; Jeansson, S.; Vahlne, A.; Lycke, E. Herpes simplex virus type-selective enzyme-linked immunosorbent assay with helix pomatia lectin-purified antigens. J. Clin. Microbiol. 1984, 19, 235-239.
10. Ashley, R.L.; Militoni, J.; Lee, F.; Nahmias, A.; Corey, L. Comparison of western blot (immunoblot) and glycoprotein G-specific immunodot enzyme assay for detecting antibodies to herpes simplex virus type 1 and 2 in human sera. J. Clin. Microbiol. 1988, 26, 662-667.
11. Gorander, S.; Harandi, A.M.; Lindqvist, M.; Bergstrom, T.; Liljeqvist, J.A. Glycoprotein G of herpes simplex virus 2 as a novel vaccine antigen for immunity to genital and neurological disease. J. Virol. 2012, 86, 7544-7553.
12. Balachandran, N.; Bacchetti, S.; Rawls, W.E. Protection against lethal challenge of BALB/c mice by passive transfer of monoclonal antibodies to five glycoproteins of herpes simplex virus type 2. Infect. Immun. 1982, 37, 1132-1137.
13. Bystricka, M.; Petrikova, M.; Zatovicova, M.; Solarikova, L.; Kostolansky, F.; Mucha, V.; Russ, G. Monoclonal antibodies to the distinct antigenic sites on glycoproteins C and B and their protective abilities in herpes simplex virus infection. Acta Virol. 1997, 41, 5-12.
14. Belshe, R.B.; Heineman, T.C.; Bernstein, D.I.; Bellamy, A.R.; Ewell, M.; van der Most, R.; Deal, C.D. Correlate of immune protection against HSV-1 genital disease in vaccinated women. J. Infect. Dis. 2014, 209, 828-836.
15. Awasthi, S.; Belshe, R.B.; Friedman, H.M. Better neutralization of herpes simplex virus type 1 (HSV-1) than HSV-2 by antibody from recipients of glaxosmithkline HSV-2 glycoprotein D2 subunit vaccine. J. Infect. Dis. 2014, 210, 571-575.
16. Kitamura, D.; Roes, J.; Kuhn, R.; Rajewsky, K. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 1991, 350, 423-426.
17. Olofsson, S.; Jeansson, S.; Lycke, E. Unusual lectin-binding properties of a herpes simplex virus type 1-specific glycoprotein. J. Virol. 1981, 38, 564-570.
18. Liljeqvist, J.A.; Trybala, E.; Svennerholm, B.; Jeansson, S.; Sjogren-Jansson, E.; Bergstrom, T. Localization of type-specific epitopes of herpes simplex virus type 2 glycoprotein G recognized by human and mouse antibodies. J. Gen. Virol 1998, 79, 1215-1224.
19. Kohl, S.; Cahall, D.L.; Walters, D.L.; Schaffner, V.E. Murine antibody-dependent cellular cytotoxicity to herpes simplex virus-infected target cells. J. Immunol. 1979, 123, 25-30.
20. Sigma plot 12, 12.0 Build 12.0.0.182; Systat Software Inc: San Jose, CA, USA, 2010.
21. Awasthi, S.; Lubinski, J.M.; Shaw, C.E.; Barrett, S.M.; Cai, M.; Wang, F.; Betts, M.; Kingsley, S.; Distefano, D.J.; Balliet, J.W.; et al. 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. 2011, 85, 10472-10486.
22. Khodai, T.; Chappell, D.; Christy, C.; Cockle, P.; Eyles, J.; Hammond, D.; Gore, K.; McCluskie, M.J.; Evans, D.M.; Lang, S.; et al. Single and combination herpes simplex virus type 2 glycoprotein vaccines adjuvanted with CpG oligodeoxynucleotides or monophosphoryl lipid A exhibit differential immunity that is not correlated to protection in animal models. Clin. Vaccine Immunol. 2011, 18, 1702-1709.
23. Balachandran, N.; Oba, D.E.; Hutt-Fletcher, L.M. Antigenic cross-reactions among herpes simplex virus types 1 and 2, epstein-barr virus, and cytomegalovirus. J. Virol. 1987, 61, 1125-1135.
24. Para, M.F.; Parish, M.L.; Noble, A.G.; Spear, P.G. Potent neutralizing activity associated with anti-glycoprotein D specificity among monoclonal antibodies selected for binding to herpes simplex virions. J. Virol. 1985, 55, 483-488.
25. Chu, C.F.; Meador, M.G.; Young, C.G.; Strasser, J.E.; Bourne, N.; Milligan, G.N. Antibody-mediated protection against genital herpes simplex virus type 2 disease in mice by Fc gamma receptor-dependent and -independent mechanisms. J. Reprod. Immunol. 2008, 78, 58-67.
26. Kohl, S.; Charlebois, E.D.; Sigouroudinia, M.; Goldbeck, C.; Hartog, K.; Sekulovich, R.E.; Langenberg, A.G.; Burke, R.L. Limited antibody-dependent cellular cytotoxicity antibody response induced by a herpes simplex virus type 2 subunit vaccine. J. Infect. Dis. 2000, 181, 335-339.
27. Ravetch, J.V.; Kinet, J.P. Fc receptors. Annu. Rev. Immunol. 1991, 9, 457-492.
28. Dudley, K.L.; Bourne, N.; Milligan, G.N. Immune protection against HSV-2 in B-cell-deficient mice. Virology 2000, 270, 454-463.
29. Parr, M.B.; Parr, E.L. Immunity to vaginal herpes simplex virus-2 infection in B-cell knockout mice. Immunology 2000, 101, 126-131.
30. Morrison, L.A.; Zhu, L.; Thebeau, L.G. Vaccine-induced serum immunoglobin contributes to protection from herpes simplex virus type 2 genital infection in the presence of immune T cells. J. Virol. 2001, 75, 1195-1204.
31. Homann, D.; Tishon, A.; Berger, D.P.; Weigle, W.O.; von Herrath, M.G.; Oldstone, M.B. Evidence for an underlying CD4 helper and CD8 T-cell defect in B-cell-deficient mice: Failure to clear persistent virus infection after adoptive immunotherapy with virus-specific memory cells from muMT/muMT mice. J. Virol. 1998, 72, 9208-9216.
32. Bourne, N.; Pyles, R.B.; Bernstein, D.I.; Stanberry, L.R. Modification of primary and recurrent genital herpes in guinea pigs by passive immunization. J. Gen. Virol. 2002, 83, 2797-2801.
33. Parr, E.L.; Parr, M.B. Immunoglobulin G is the main protective antibody in mouse vaginal secretions after vaginal immunization with attenuated herpes simplex virus type 2. J. Virol. 1997, 71, 8109-8115.
34. Eis-Hubinger, A.M.; Schmidt, D.S.; Schneweis, K.E. Anti-glycoprotein B monoclonal antibody protects T cell-depleted mice against herpes simplex virus infection by inhibition of virus replication at the inoculated mucous membranes. J. Gen. Virol. 1993, 74, 379-385.
35. Krawczyk, A.; Krauss, J.; Eis-Hubinger, A.M.; Daumer, M.P.; Schwarzenbacher, R.; Dittmer, U.; Schneweis, K.E.; Jager, D.; Roggendorf, M.; Arndt, M.A. Impact of valency of a glycoprotein B-specific monoclonal antibody on neutralization of herpes simplex virus. J. Virol. 2011, 85, 1793-1803.
36. Halford, W.P.; Geltz, J.; Gershburg, E. Pan-HSV-2 IgG antibody in vaccinated mice and guinea pigs correlates with protection against herpes simplex virus 2. PLoS One 2013, 8, e65523.
37. McDermott, M.R.; Brais, L.J.; Evelegh, M.J. Mucosal and systemic antiviral antibodies in mice inoculated intravaginally with herpes simplex virus type 2. J. Gen. Virol. 1990, 71, 1497-1504.
38. Awasthi, S.; Friedman, H.M. A paradigm shift: Vaccine-induced antibodies as an immune correlate of protection against herpes simplex virus type 1 genital herpes. J. Infect. Dis. 2014, 209, 813-815.
39. Excler, J.L.; Ake, J.; Robb, M.L.; Kim, J.H.; Plotkin, S.A. Nonneutralizing functional antibodies: A new “old” paradigm for HIV vaccines. Clin. Vaccine Immunol. 2014, 21, 1023-1036.