An Interleukin 12 Adjuvanted Herpes Simplex Virus 2 DNA Vaccine Is More Protective Than a Glycoprotein D Subunit Vaccine in a High-Dose Murine Challenge Model

Viral Immunology

Volumn 30, Issue 3, 2017, Pages 178-195

  Bagley, Kenneth C ^a   Schwartz, Jennifer A ^a   Andersen, Hanne ^b   Eldridge, John H ^c   Xu, Rong ^c   Ota Setlik, Ayuko ^c   Geltz, Joshua J ^d   Halford, William P ^d   Fouts, Timothy R ^a  

^a Profectus Biosciences   (United States)

^b BIOQUAL INC   (United States)

^c Profectus Biosciences   (United States)

^d SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

adjuvant; DNA vaccine; herpes; HSV 2; virus

Indexed keywords

ADJUVANT; ALUMINUM POTASSIUM SULFATE; DNA VACCINE; GLYCOPROTEIN D; INTERLEUKIN 12; PHOSPHORYL LIPID A; SUBUNIT VACCINE; GLYCOPROTEIN; HERPES VACCINE; IMMUNOLOGICAL ADJUVANT; MEMBRANE PROTEIN; RECOMBINANT VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ARTICLE; DNA IMMUNIZATION; ELECTROPORATION; FLOW CYTOMETRY; GENETIC TRANSFECTION; HERPES SIMPLEX VIRUS 2; IMMUNE RESPONSE; MOUSE; NONHUMAN; SYSTEMATIC REVIEW; TH1 CELL; VACCINATION; VIRAL CLEARANCE; VIRUS NEUTRALIZATION; VIRUS SHEDDING; ANIMAL; COMPARATIVE STUDY; DISEASE MODEL; GENITAL HERPES; IMMUNOLOGY; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; DISEASE MODELS, ANIMAL; GLYCOPROTEINS; HERPES GENITALIS; HERPESVIRUS 2, HUMAN; HERPESVIRUS VACCINES; INTERLEUKIN-12; MEMBRANE PROTEINS; MICE; SURVIVAL ANALYSIS; TREATMENT OUTCOME; VACCINES, DNA; VACCINES, SUBUNIT; VACCINES, SYNTHETIC;

EID: 85017366365     PISSN: 08828245     EISSN: 15578976     Source Type: Journal    
DOI: 10.1089/vim.2016.0136     Document Type: Article

References (93)

1. Abdulhaqq SA, and Weiner DB. DNA vaccines: developing new strategies to enhance immune responses. Immunol Res 2008;42:219-232.
2. Aihara H, and Miyazaki J. Gene transfer into muscle by electroporation in vivo. Nat Biotechnol 1998;16:867-870.
3. Akhtar J, and Shukla D. Viral entry mechanisms: cellular and viral mediators of herpes simplex virus entry. FEBS J 2009;276:7228-7236.
4. Arrington J, Braun RP, Dong L, et al. Plasmid vectors encoding cholera toxin or the heat-labile enterotoxin from Escherichia coli are strong adjuvants for DNA vaccines. J Virol 2002;76:4536-4546.
5. Ashley R, Mertz G, Clark H, et al. Humoral immune response to herpes simplex virus type 2 glycoproteins in patients receiving a glycoprotein subunit vaccine. J Virol 1985;56:475-481.
6. Avitabile E, Forghieri C, and Campadelli-Fiume G. 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 2009;83:10752-10760.
7. Awasthi S, Lubinski JM, and Friedman HM. Immunization with HSV-1 glycoprotein C prevents immune evasion from complement and enhances the efficacy of an HSV-1 glycoprotein D subunit vaccine. Vaccine 2009;27:6845-6853.
8. Awasthi S, Lubinski JM, Shaw CE, 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.
9. Awasthi S, Mahairas GG, Shaw CE, et al. A dual-modality herpes simplex virus 2 vaccine for preventing genital herpes by using glycoprotein C and D subunit antigens to induce potent antibody responses and adenovirus vectors containing capsid and tegument proteins as T cell immunogens. J Virol 2015;89:8497-8509.
10. Babiuk S, Baca-Estrada ME, Foldvari M, et al. Electroporation improves the efficacy of DNA vaccines in large animals. Vaccine 2002;20:3399-3408.
11. Babiuk S, Mookherjee N, Pontarollo R, et al. TLR9-/-And TLR9+/+ mice display similar immune responses to a DNA vaccine. Immunology 2004;113:114-120.
12. Babiuk S, van Drunen Littel-van den Hurk S, and Babiuk LA. Delivery of DNA vaccines using electroporation. Methods Mol Med 2006;127:73-82.
13. Bagley KC, Shata MT, Onyabe DY, et al. Immunogenicity of DNA vaccines that direct the coincident expression of the 120 kDa glycoprotein of human immunodeficiency virus and the catalytic domain of cholera toxin. Vaccine 2003;21:3335-3341.
14. Belshe RB, Leone PA, Bernstein DI, et al. Efficacy results of a trial of a herpes simplex vaccine. N Engl J Med 2012; 366:34-43.
15. Bialuk I, Whitney S, Andresen V, et al. Vaccine induced antibodies to the first variable loop of human immunodeficiency virus type 1 gp120, mediate antibody-dependent virus inhibition in macaques. Vaccine 2011;30:78-94.
16. Bourne N, Bravo FJ, Francotte M, et al. Herpes simplex virus (HSV) type 2 glycoprotein D subunit vaccines and protection against genital HSV-1 or HSV-2 disease in guinea pigs. J Infect Dis 2003;187:542-549.
17. Bourne N, Milligan GN, Stanberry LR, et al. Impact of immunization with glycoprotein D2/AS04 on herpes simplex virus type 2 shedding into the genital tract in guinea pigs that become infected. J Infect Dis 2005;192:2117-2123.
18. Bright H, Perez DL, Christy C, et al. The efficacy of HSV-2 vaccines based on gD and gB is enhanced by the addition of ICP27. Vaccine 2012;30:7529-7535.
19. Broker M, Abel KJ, Kohler R, et al. Escherichia coliderived envelope protein gD but not gC antigens of herpes simplex virus protect mice against a lethal challenge with HSV-1 and HSV-2. Med Microbiol Immunol 1990;179: 145-159.
20. Buchan S, Gronevik E, Mathiesen I, et al. Electroporation as a prime/boost strategy for naked DNA vaccination against a tumor antigen. J Immunol 2005;174:6292-6298.
21. Campadelli-Fiume G, Amasio M, Avitabile E, et al. The multipartite system that mediates entry of herpes simplex virus into the cell. Rev Med Virol 2007;17:313-326.
22. CDC. Seroprevalence of herpes simplex virus type 2 among persons aged 14-49 years-United States, 2005-2008. MMWR Morb Mortal Wkly Rep 2010;59:456-459.
23. Chentoufi AA, Kritzer E, Yu DM, et al. Towards a rational design of an asymptomatic clinical herpes vaccine: The old, the new, and the unknown. Clin Dev Immunol 2012;2012: 187585.
24. Chiarella P, Massi E, De Robertis M, et al. Electroporation of skeletal muscle induces danger signal release and antigen-presenting cell recruitment independently of DNA vaccine administration. Expert Opin Biol Ther 2008;8: 1645-1657.
25. Chong SY, Egan MA, Kutzler MA, et al. Comparative ability of plasmid IL-12 and IL-15 to enhance cellular and humoral immune responses elicited by a SIVgag plasmid DNA vaccine and alter disease progression following SHIV(89.6P) challenge in rhesus macaques. Vaccine 2007; 25:4967-4982.
26. Chu CF, Meador MG, Young CG, et al. 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.
27. Cohen J. Immunology. Painful failure of promising genital herpes vaccine. Science 2010;330:304.
28. Connolly SA, Jackson JO, Jardetzky TS, et al. Fusing structure and function: A structural view of the herpesvirus entry machinery. Nat Rev Microbiol 2011;9:369-381.
29. Dasgupta G, Chentoufi AA, Nesburn AB, et al. New concepts in herpes simplex virus vaccine development: notes from the battlefield. Expert Rev Vaccines 2009;8:1023-1035.
30. Dix RD, and Mills J. Acute and latent herpes simplex virus neurological disease in mice immunized with purified virus-specific glycoproteins gB or gD. J Med Virol 1985; 17:9-18.
31. Donnelly JJ, Wahren B, and Liu MA. DNA vaccines: progress and challenges. J Immunol 2005;175:633-639.
32. Egan MA, Charini WA, Kuroda MJ, et al. Simian immunodeficiency virus (SIV) gag DNA-vaccinated rhesus monkeys develop secondary cytotoxic T-lymphocyte responses and control viral replication after pathogenic SIV infection. J Virol 2000;74:7485-7495.
33. Egan MA, Chong SY, Megati S, et al. Priming with plasmid DNAs expressing interleukin-12 and simian immunodeficiency virus gag enhances the immunogenicity and efficacy of an experimental AIDS vaccine based on recombinant vesicular stomatitis virus. AIDS Res Hum Retroviruses 2005;21:629-643.
34. Egan MA, Megati S, Roopchand V, et al. Rational design of a plasmid DNA vaccine capable of eliciting cell-mediated immune responses to multiple HIV antigens in mice. Vaccine 2006;24:4510-4523.
35. Eisenberg RJ, Atanasiu D, Cairns TM, et al. Herpes virus fusion and entry: A story with many characters. Viruses 2012;4:800-832.
36. Ferraro B, Morrow MP, Hutnick NA, et al. Clinical applications of DNA vaccines: current progress. Clin Infect Dis 2011;53:296-302.
37. Forrester A, Farrell H, Wilkinson G, et al. Construction and properties of a mutant of herpes simplex virus type 1 with glycoprotein H coding sequences deleted. J Virol 1992;66: 341-348.
38. Fotouhi F, Soleimanjahi H, Roostaee MH, et al. Enhancement of protective humoral immune responses against Herpes simplex virus-2 in DNA-immunized guinea-pigs using protein boosting. FEMS Immunol Med Microbiol 2008;54:18-26.
39. Fouts TR, Bagley K, Prado IJ, et al. Balance of cellular and humoral immunity determines the level of protection by HIV vaccines in rhesus macaque models of HIV infection. Proc Natl Acad Sci U S A 2015;112:E992-E999.
40. Geltz JJ, Gershburg E, and Halford WP. Herpes simplex virus 2 (HSV-2) infected cell proteins are among the most dominant antigens of a live-Attenuated HSV-2 vaccine. PLoS One 2015;10:e0116091.
41. Gorander S, Ekblad M, Bergstrom T, et al. Anti-glycoprotein g antibodies of herpes simplex virus 2 contribute to complete protection after vaccination in mice and induce antibodydependent cellular cytotoxicity and complement-mediated cytolysis. Viruses 2014;6:4358-4372.
42. Halford WP. Antigenic breadth: A missing ingredient in HSV-2 subunit vaccines? Expert Rev Vaccines 2014;13:691-710.
43. Halford WP, Puschel R, Gershburg E, et al. A liveattenuated HSV-2 ICP0 virus elicits 10 to 100 times greater protection against genital herpes than a glycoprotein D subunit vaccine. PLoS One 2011;6:e17748.
44. Halford WP, Puschel R, and Rakowski B. Herpes simplex virus 2 ICP0 mutant viruses are avirulent and immunogenic: implications for a genital herpes vaccine. PLoS One 2010;5:e12251.
45. Haynes JR, Arrington J, Dong L, et al. Potent protective cellular immune responses generated by a DNA vaccine encoding HSV-2 ICP27 and the E. coli heat labile enterotoxin. Vaccine 2006;24:5016-5026.
46. Heller LC, Ugen K, and Heller R. Electroporation for targeted gene transfer. Expert Opin Drug Deliv 2005;2: 255-268.
47. Hosken N, McGowan P, Meier A, et al. Diversity of the CD8+ T-cell response to herpes simplex virus type 2 proteins among persons with genital herpes. J Virol 2006;80: 5509-5515.
48. Hung CF, Monie A, Alvarez RD, et al. DNA vaccines for cervical cancer: from bench to bedside. Exp Mol Med 2007;39:679-689.
49. Jimenez GS, Planchon R, Wei Q, et al. Vaxfectinformulated influenza DNA vaccines encoding NP and M2 viral proteins protect mice against lethal viral challenge. Hum Vaccin 2007;3:157-164.
50. Jondal M. Antibody-dependent cellular cytotoxicity (ADCC) against Epstein-Barr virus-determined antigens II. Induction of ADCC by FC-FC receptor bridging. Clin Exp Immunol 1977;29:1-10.
51. Jonsson MK, and Wahren B. Sexually transmitted herpes simplex viruses. Scand J Infect Dis 2004;36:93-101.
52. Kalams SA, Parker SD, Elizaga M, et al. Safety and comparative immunogenicity of an HIV-1 DNA vaccine in combination with plasmid interleukin 12 and impact of intramuscular electroporation for delivery. J Infect Dis 2013;208:818-829.
53. Kaushic C, Ashkar AA, Reid LA, et al. Progesterone increases susceptibility and decreases immune responses to genital herpes infection. J Virol 2003;77:4558-4565.
54. Kim JJ, Yang JS, Dentchev T, et al. Chemokine gene adjuvants can modulate immune responses induced by DNA vaccines. J Interferon Cytokine Res 2000;20:487-498.
55. Koelle DM, and Corey L. Herpes simplex: insights on pathogenesis and possible vaccines. Annu Rev Med 2008; 59:381-395.
56. Kutzler MA, andWeiner DB. Developing DNA vaccines that call to dendritic cells. J Clin Invest 2004;114:1241-1244.
57. Laddy DJ, Yan J, Khan AS, et al. Electroporation of synthetic DNA antigens offers protection in nonhuman primates challenged with highly pathogenic avian influenza virus. J Virol 2009;83:4624-4630.
58. Luckay A, Sidhu MK, Kjeken R, et al. Effect of plasmid DNA vaccine design and in vivo electroporation on the resulting vaccine-specific immune responses in rhesus macaques. J Virol 2007;81:5257-5269.
59. Macphail S. The class of antibody involved in the antibodydependent cell-mediated lysis of chicken erythrocytes. Immunology 1976;31:697-705.
60. Manickan E, Francotte M, Kuklin N, et al. Vaccination with recombinant vaccinia viruses expressing ICP27 induces protective immunity against herpes simplex virus through CD4+ Th1+ T cells. J Virol 1995;69:4711-4716.
61. Manservigi R, Boero A, Argnani R, et al. Immunotherapeutic activity of a recombinant combined gB-gD-gE vaccine against recurrent HSV-2 infections in a guinea pig model. Vaccine 2005;23:865-872.
62. McKendall RR, and Woo W. Antibody activity to herpes simplex virus in mouse Ig classes and IgG subclasses. Arch Virol 1988;98:225-233.
63. Mertz GJ, Schmidt O, Jourden JL, et al. Frequency of acquisition of first-episode genital infection with herpes simplex virus from symptomatic and asymptomatic source contacts. Sex Transm Dis 1985;12:33-39.
64. Mester JC, Twomey TA, Tepe ET, et al. Immunity induced by DNA immunization with herpes simplex virus type 2 glycoproteins B and C. Vaccine 1999;18:875-883.
65. Mpendo J, Mutua G, Nyombayire J, et al. A phase I double blind, placebo-controlled, randomized study of the safety and immunogenicity of electroporated HIV DNA with or without interleukin 12 in prime-boost combinations with an Ad35 HIV vaccine in healthy HIV-seronegative African adults. PLoS One 2015;10:e0134287.
66. Nicola AV, Willis SH, Naidoo NN, et al. Structure-function analysis of soluble forms of herpes simplex virus glycoprotein D. J Virol 1996;70:3815-3822.
67. Parr MB, Kepple L, McDermott MR, et al. A mouse model for studies of mucosal immunity to vaginal infection by herpes simplex virus type 2. Lab Invest 1994;70:369-380.
68. Peng T, Ponce-de-Leon M, Jiang H, et al. The gH-gL complex of herpes simplex virus (HSV) stimulates neutralizing antibody and protects mice against HSV type 1 challenge. J Virol 1998;72:65-72.
69. Posavad CM, Remington M, Mueller DE, et al. Detailed characterization of T cell responses to herpes simplex virus-2 in immune seronegative persons. J Immunol 2010; 184:3250-3259.
70. Posavad CM, Wald A, Hosken N, et al. T cell immunity to herpes simplex viruses in seronegative subjects: silent infection or acquired immunity? J Immunol 2003;170:4380-4388.
71. Prudhomme GJ, Glinka Y, Khan AS, et al. Electroporationenhanced nonviral gene transfer for the prevention or treatment of immunological, endocrine and neoplastic diseases. Curr Gene Ther 2006;6:243-273.
72. Ramanathan MP, Kutzler MA, Kuo YC, et al. Coimmunization with an optimized IL15 plasmid adjuvant enhances humoral immunity via stimulating B cells induced by genetically engineered DNA vaccines expressing consensus JEV and WNV E DIII. Vaccine 2009;27:4370-4380.
73. Robinson HL. Non-neutralizing antibodies in prevention of HIV infection. Expert Opin Biol Ther 2013;13:197-207.
74. Samaniego LA, Neiderhiser L, and DeLuca NA. Persistence and expression of the herpes simplex virus genome in the absence of immediate-early proteins. J Virol 1998;72: 3307-3320.
75. Schadeck EB, Sidhu M, Egan MA, et al. A dose sparing effect by plasmid encoded IL-12 adjuvant on a SIVgagplasmid DNA vaccine in rhesus macaques. Vaccine 2006; 24:4677-4687.
76. Scheerlinck JP, Karlis J, Tjelle TE, et al. In vivo electroporation improves immune responses to DNA vaccination in sheep. Vaccine 2004;22:1820-1825.
77. Selby M, Goldbeck C, Pertile T, et al. Enhancement of DNA vaccine potency by electroporation in vivo. J Biotechnol 2000;83:147-152.
78. Shao HJ, Chen L, Shen MS, et al. Enhancement of immune responses to the hepatitis B virus core protein through DNA vaccines with a DNA fragment encoding human IL-1beta 163-171 peptide. Acta Virol 2003;47:217-221.
79. Sin JI, Bagarazzi M, Pachuk C, et al. DNA priming-protein boosting enhances both antigen-specific antibody and Th1-Type cellular immune responses in a murine herpes simplex virus-2 gD vaccine model. DNA Cell Biol 1999;18: 771-779.
80. Sin JI, Kim J, Dang K, et al. LFA-3 plasmid DNA enhances Ag-specific humoral-And cellular-mediated protective immunity against herpes simplex virus-2 in vivo: involvement of CD4+ T cells in protection. Cell Immunol 2000;203: 19-28.
81. Sin JI, Kim JJ, Arnold RL, et al. IL-12 gene as a DNA vaccine adjuvant in a herpes mouse model: IL-12 enhances Th1-Type CD4+ T cell-mediated protective immunity against herpes simplex virus-2 challenge. J Immunol 1999;162: 2912-2921.
82. Sin JI, Kim JJ, Boyer JD, et al. In vivo modulation of vaccine-induced immune responses toward a Th1 phenotype increases potency and vaccine effectiveness in a herpes simplex virus type 2 mouse model. J Virol 1999;73: 501-509.
83. Solomon L, Cannon MJ, Reyes M, et al. Epidemiology of recurrent genital herpes simplex virus types 1 and 2. Sex Transm Infect 2003;79:456-459.
84. Stanberry LR, Spruance SL, Cunningham AL, et al. Glycoprotein-D-Adjuvant vaccine to prevent genital herpes. N Engl J Med 2002;347:1652-1661.
85. Stephenson J. Genital herpes vaccine shows limited promise. JAMA 2000;284:1913-1914.
86. Straus SE, Wald A, Kost RG, et al. Immunotherapy of recurrent genital herpes with recombinant herpes simplex virus type 2 glycoproteins D and B: results of a placebocontrolled vaccine trial. J Infect Dis 1997;176:1129-1134.
87. Wald A, Corey L, Cone R, et al. Frequent genital herpes simplex virus 2 shedding in immunocompetent women. Effect of acyclovir treatment. J Clin Invest 1997;99:1092-1097.
88. Wald A, Zeh J, Selke S, et al. Reactivation of genital herpes simplex virus type 2 infection in asymptomatic seropositive persons. N Engl J Med 2000;342:844-850.
89. Wang S, Zhang C, Zhang L, et al. The relative immunogenicity of DNA vaccines delivered by the intramuscular needle injection, electroporation and gene gun methods. Vaccine 2008;26:2100-2110.
90. Xu F, Sternberg MR, Kottiri BJ, et al. Trends in herpes simplex virus type 1 and type 2 seroprevalence in the United States. JAMA 2006;296:964-973.
91. Xu R, Megati S, Roopchand V, et al. Comparative ability of various plasmid-based cytokines and chemokines to adjuvant the activity of HIV plasmid DNA vaccines. Vaccine 2008;26:4819-4829.
92. Youssef S, Maor G, Wildbaum G, et al. C-C chemokineencoding DNA vaccines enhance breakdown of tolerance to their gene products and treat ongoing adjuvant arthritis. J Clin Invest 2000;106:361-371.
93. Zhu XP, Muhammad ZS, Wang JG, et al. HSV-2 vaccine: current status and insight into factors for developing an efficient vaccine. Viruses 2014;6:371-390.