B7 costimulation molecules encoded by replication-defective, vhs-deficient HSV-1 improve vaccine-induced protection against corneal disease

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Schrimpf, Jane E ^a   Tu, Eleain M ^a   Wang, Hong ^a   Wong, Yee M ^a   Morrison, Lynda A ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; HERPES SIMPLEX VACCINE; INFECTED CELL PROTEIN 8; UNCLASSIFIED DRUG; VIRION HOST SHUTOFF PROTEIN; VIRUS PROTEIN; CD86 ANTIGEN; INTERLEUKIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL ACTIVITY; CELL INFILTRATION; CELL STIMULATION; CENTRAL NERVOUS SYSTEM INFECTION; CONTROLLED STUDY; CORNEA DISEASE; CORRELATION ANALYSIS; DRUG EFFICACY; FEMALE; HERPES SIMPLEX VIRUS 1; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; KERATITIS; LYMPH NODE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RISK REDUCTION; T LYMPHOCYTE; TRIGEMINUS GANGLION; VACCINATION; VIRUS REPLICATION; ANIMAL; CELL LINE; CERCOPITHECUS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETICS; HERPES SIMPLEX KERATITIS; IMMUNOLOGY; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; VIROLOGY;

HERPES; HUMAN HERPESVIRUS 1;

ANIMALS; ANTIGENS, CD80; ANTIGENS, CD86; B7 ANTIGENS; BLOTTING, SOUTHERN; CELL LINE; CERCOPITHECUS AETHIOPS; CORNEAL DISEASES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HERPESVIRUS 1, HUMAN; INTERLEUKIN-2; KERATITIS, HERPETIC; MICE; REAL-TIME POLYMERASE CHAIN REACTION; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 79961090075     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022772     Document Type: Article

References (64)

1. Xu F, Sternberg MR, Kottiri BJ, McQuillan GM, Lee FK, et al. (2006) Trends in herpes simplex virus type 1 and type 2 seroprevalence in the United States. JAMA 296: 964-973.
2. Liesegang TJ, Melton LJ III, Daly PJ, Ilstrup DM, (1989) Epidemiology of ocular herpes simplex. Incidence in Rochester, Minn, 1950 through 1982. Arch Ophthalmol 107: 1155-1159.
3. Dana MR, Qian Y, Hamrah P, (2000) Twenty-five-year panorama of corneal immunology: emerging concepts in the immunopathogenesis of microbial keratitis, peripheral ulcerative keratitis, and corneal transplant rejection. Cornea 19: 625-643.
4. Inoue T, Inoue Y, Nakamura T, Yoshida A, Takahashi K, et al. (2000) Preventive effect of local plasmid DNA vaccine encoding gD or gD-IL-2 on herpetic keratitis. Invest Ophthalmol Vis Sci 41: 4209-4215.
5. Dasgupta G, Chentoufi AA, Nesburn AB, Wechsler SL, BenMohamed L, (2009) New concepts in herpes simplex virus vaccine development: notes from the battlefield. Expert Rev Vaccines 8: 1023-1035.
6. Frye TD, Chiou HC, Hull BE, Bigley NJ, (2002) The efficacy of a DNA vaccine encoding herpes simplex virus type 1 (HSV-1) glycoprotein D in decreasing ocular disease severity following corneal HSV-1 challenge. Arch Virol 147: 1747-1759.
7. Bettahi I, Nesburn AB, Yoon S, Zhang X, Mohebbi A, et al. (2007) Protective immunity against ocular herpes infection and disease induced by highly immunogenic self-adjuvanting glycoprotein D lipopeptide vaccines. Invest Ophthalmol Vis Sci 48: 4643-4653.
8. Osorio Y, Cohen J, Ghiasi H, (2004) Improved protection from primary ocular HSV-1 infection and establishment of latency using multigenic DNA vaccines. Invest Ophthalmol Vis Sci 45: 506-514.
9. Osorio Y, Ghiasi H, (2005) Recombinant herpes simplex virus type 1 (HSV-1) codelivering interleukin-12p35 as a molecular adjuvant enhances the protective immune response against ocular HSV-1 challenge. J Virol 79: 3297-3308.
10. Walker J, Leib DA, (1998) Protection from primary infection and establishment of latency by vaccination with a herpes simplex virus type 1 recombinant deficient in the virion host shutoff (vhs) function. Vaccine 16: 1-5.
11. Awasthi S, Lubinski JM, Eisenberg RJ, Cohen GH, Friedman HM, (2008) An HSV-1 gD mutant virus as an entry-impaired live virus vaccine. Vaccine 26: 1195-1203.
12. Dambach MJ, Trecki J, Martin N, Markovitz NS, (2006) Oncolytic viruses derived from the gamma34.5-deleted herpes simplex virus recombinant R3616 encode a truncated UL3 protein. Mol Ther 13: 891-898.
13. Dudek T, Knipe DM, (2006) Replication-defective viruses as vaccines and vaccine vectors. Virology 344: 230-239.
14. Morrison LA, Knipe DM, (1994) Immunization with replication-defective mutants of herpes simplex virus type 1: sites of immune intervention in pathogenesis of challenge virus infection. J Virol 68: 689-696.
15. Brehm MA, Bonneau RH, Knipe DM, Tevethia SS, (1997) Immunization with a replication-deficient mutant of herpes simplex virus type 1 (HSV-1) induces a CD8+ cytotoxic T-lymphocyte response and confers a level of protection comparable to that of wild-type HSV-1. J Virol 71: 3534-3544.
16. Morrison LA, Knipe DM, (1997) Contributions of antibody and T cell subsets to protection elicited by immunization with a replication-defective mutant of herpes simplex virus type 1. Virology 239: 315-326.
17. Stuart PM, Summers B, Morris JE, Morrison LA, Leib DA, (2004) CD8(+) T cells control corneal disease following ocular infection with herpes simplex virus type 1. J Gen Virol 85: 2055-2063.
18. Tigges MA, Leng S, Johnson DC, Burke RL, (1996) Human herpes simplex virus (HSV)-specific CD8+ CTL clones recognize HSV-2-infected fibroblasts after treatment with IFN-gamma or when virion host shutoff functions are disabled. J Immunol 156: 3901-3910.
19. Samady L, Costigliola E, MacCormac L, McGrath Y, Cleverley S, et al. (2003) Deletion of the virion host shutoff protein (vhs) from herpes simplex virus (HSV) relieves the viral block to dendritic cell activation: potential of vhs- HSV vectors for dendritic cell-mediated immunotherapy. J Virol 77: 3768-3776.
20. Cotter CR, Nguyen ML, Yount JS, Lopez CB, Blaho JA, et al. (2010) The virion host shut-off (vhs) protein blocks a TLR-independent pathway of herpes simplex virus type 1 recognition in human and mouse dendritic cells. PLoS One 5: e8684.
21. Prechtel AT, Turza NM, Kobelt DJ, Eisemann JI, Coffin RS, et al. (2005) Infection of mature dendritic cells with herpes simplex virus type 1 dramatically reduces lymphoid chemokine-mediated migration. J Gen Virol 86: 1645-1657.
22. Geiss BJ, Smith TJ, Leib DA, Morrison LA, (2000) Disruption of virion host shutoff activity improves the immunogenicity and protective capacity of a replication-incompetent herpes simplex virus type 1 vaccine strain. J Virol 74: 11137-11144.
23. Thebeau LG, Morrison LA, (2002) B7 costimulation plays an important role in protection from herpes simplex virus type 2-mediated pathology. J Virol 76: 2563-2566.
24. Thebeau LG, Vagvala SP, Wong YM, Morrison LA, (2007) B7 costimulation molecules expressed from the herpes simplex virus 2 genome rescue immune induction in B7-deficient mice. J Virol 81: 12200-12209.
25. Vagvala SP, Thebeau LG, Wilson SR, Morrison LA, (2009) Virus-encoded b7-2 costimulation molecules enhance the protective capacity of a replication-defective herpes simplex virus type 2 vaccine in immunocompetent mice. J Virol 83: 953-960.
26. Strelow LI, Leib DA, (1995) Role of the virion host shutoff (vhs) of herpes simplex virus type 1 in latency and pathogenesis. J Virol 69: 6779-6786.
27. Gao M, Knipe DM, (1989) Genetic evidence for multiple nuclear functions of the herpes simplex virus ICP8 DNA-binding protein. J Virol 63: 5258-5267.
28. Morrison LA, Knipe DM, (1996) Mechanisms of immunization with a replication-defective mutant of herpes simplex virus 1. Virology 220: 402-413.
29. Hoggan MD, Roizman B, (1959) The isolation and properties of a variant of Herpes simplex producing multinucleated giant cells in monolayer cultures in the presence of antibody. Am J Hyg 70: 208-219.
30. Knipe DM, Spang AE, (1982) Definition of a series of stages in the association of two herpesviral proteins with the cell nucleus. J Virol 43: 314-324.
31. Borriello F, Sethna MP, Boyd SD, Schweitzer AN, Tivol EA, et al. (1997) B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity 6: 303-313.
32. Bonneau RH, Salvucci LA, Johnson DC, Tevethia SS, (1993) Epitope specificity of H-2Kb-restricted, HSV-1-, and HSV-2-cross-reactive cytotoxic T lymphocyte clones. Virology 195: 62-70.
33. Hanke T, Graham FL, Rosenthal KL, Johnson DC, (1991) Identification of an immunodominant cytotoxic T-lymphocyte recognition site in glycoprotein B of herpes simplex virus by using recombinant adenovirus vectors and synthetic peptides. J Virol 65: 1177-1186.
34. Mosmann T, (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63.
35. Morrison LA, Da Costa XJ, Knipe DM, (1998) Influence of mucosal and parenteral immunization with a replication-defective mutant of HSV-2 on immune responses and protection from genital challenge. Virology 243: 178-187.
36. Ramachandran S, Davoli KA, Yee MB, Hendricks RL, Kinchington PR, (2010) Delaying the expression of herpes simplex virus type 1 glycoprotein B (gB) to a true late gene alters neurovirulence and inhibits the gB-CD8+ T-cell response in the trigeminal ganglion. J Virol 84: 8811-8820.
37. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
38. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
39. Gangappa S, Deshpande SP, Rouse BT, (2000) Bystander activation of CD4+ T cells accounts for herpetic ocular lesions. Invest Ophthalmol Vis Sci 41: 453-459.
40. Gangappa S, Babu JS, Thomas J, Daheshia M, Rouse BT, (1998) Virus-induced immunoinflammatory lesions in the absence of viral antigen recognition. J Immunol 161: 4289-4300.
41. Panoutsakopoulou V, Sanchirico ME, Huster KM, Jansson M, Granucci F, et al. (2001) Analysis of the relationship between viral infection and autoimmune disease. Immunity 15: 137-147.
42. Wallace ME, Keating R, Heath WR, Carbone FR, (1999) The cytotoxic T-cell response to herpes simplex virus type 1 infection of C57BL/6 mice is almost entirely directed against a single immunodominant determinant. J Virol 73: 7619-7626.
43. Lang A, Nikolich-Zugich J, (2005) Development and migration of protective CD8+ T cells into the nervous system following ocular herpes simplex virus-1 infection. J Immunol 174: 2919-2925.
44. He J, Ichimura H, Iida T, Minami M, Kobayashi K, et al. (1999) Kinetics of cytokine production in the cornea and trigeminal ganglion of C57BL/6 mice after corneal HSV-1 infection. J Interferon Cytokine Res 19: 609-615.
45. Valyi-Nagy T, Deshmane S, Dillner A, Fraser NW, (1991) Induction of cellular transcription factors in trigeminal ganglia of mice by corneal scarification, herpes simplex virus type 1 infection, and explantation of trigeminal ganglia. J Virol 65: 4142-4152.
46. LaVail JH, Johnson WE, Spencer LC, (1993) Immunohistochemical identification of trigeminal ganglion neurons that innervate the mouse cornea: relevance to intercellular spread of herpes simplex virus. J Comp Neurol 327: 133-140.
47. Mott KR, Bresee CJ, Allen SJ, BenMohamed L, Wechsler SL, et al. (2009) Level of herpes simplex virus type 1 latency correlates with severity of corneal scarring and exhaustion of CD8+ T cells in trigeminal ganglia of latently infected mice. J Virol 83: 2246-2254.
48. Banerjee K, Biswas PS, Kumaraguru U, Schoenberger SP, Rouse BT, (2004) Protective and pathological roles of virus-specific and bystander CD8+ T cells in herpetic stromal keratitis. J Immunol 173: 7575-7583.
49. Banerjee K, Biswas PS, Rouse BT, (2005) Elucidating the protective and pathologic T cell species in the virus-induced corneal immunoinflammatory condition herpetic stromal keratitis. J Leukoc Biol 77: 24-32.
50. Sheridan BS, Knickelbein JE, Hendricks RL, (2007) CD8 T cells and latent herpes simplex virus type 1: keeping the peace in sensory ganglia. Expert Opin Biol Ther 7: 1323-1331.
51. Liu T, Khanna KM, Chen X, Fink DJ, Hendricks RL, (2000) CD8(+) T cells can block herpes simplex virus type 1 (HSV-1) reactivation from latency in sensory neurons. J Exp Med 191: 1459-1466.
52. Schroder K, Hertzog PJ, Ravasi T, Hume DA, (2004) Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75: 163-189.
53. Frank GM, Lepisto AJ, Freeman ML, Sheridan BS, Cherpes TL, et al. (2009) Early CD4+ T cell help prevents partial CD8+ T cell exhaustion and promotes maintenance of herpes simplex virus 1 latency. J Immunol 184: 277-286.
54. Janeway CA Jr, Bottomly K, (1994) Signals and signs for lymphocyte responses. Cell 76: 275-285.
55. McAdam AJ, Farkash EA, Gewurz BE, Sharpe AH, (2000) B7 costimulation is critical for antibody class switching and CD8(+) cytotoxic T-lymphocyte generation in the host response to vesicular stomatitis virus. J Virol 74: 203-208.
56. Zajac P, Schutz A, Oertli D, Noppen C, Schaefer C, et al. (1998) Enhanced generation of cytotoxic T lymphocytes using recombinant vaccinia virus expressing human tumor-associated antigens and B7 costimulatory molecules. Cancer Res 58: 4567-4571.
57. Petrulio CA, Kaufman HL, (2006) Development of the PANVAC-VF vaccine for pancreatic cancer. Expert Rev Vaccines 5: 9-19.
58. Hodge JW, Chakraborty M, Kudo-Saito C, Garnett CT, Schlom J, (2005) Multiple costimulatory modalities enhance CTL avidity. J Immunol 174: 5994-6004.
59. Todo T, Martuza RL, Dallman MJ, Rabkin SD, (2001) In situ expression of soluble B7-1 in the context of oncolytic herpes simplex virus induces potent antitumor immunity. Cancer Res 61: 153-161.
60. Lee YS, Kim JH, Choi KJ, Choi IK, Kim H, et al. (2006) Enhanced antitumor effect of oncolytic adenovirus expressing interleukin-12 and B7-1 in an immunocompetent murine model. Clin Cancer Res 12: 5859-5868.
61. Emtage PC, Wan Y, Bramson JL, Graham FL, Gauldie J, (1998) A double recombinant adenovirus expressing the costimulatory molecule B7-1 (murine) and human IL-2 induces complete tumor regression in a murine breast adenocarcinoma model. J Immunol 160: 2531-2538.
62. Mosca JD, Chang YN, Williams G, (2007) Antigen-presenting particle technology using inactivated surface-engineered viruses: induction of immune responses against infectious agents. Retrovirology 4: 32.
63. Marti WR, Oertli D, Meko JB, Norton JA, Tsung K, (1997) Induction of antigen-presenting capacity in tumor cells upon infection with non-replicating recombinant vaccinia virus encoding murine MHC class II and costimulatory molecules. J Immunol Methods 200: 191-198.
64. Oertli D, Marti WR, Norton JA, Tsung K, (1997) Artificial antigen-presenting cells engineered by recombinant vaccinia viruses expressing antigen, MHC class II, and costimulatory molecules elicit proliferation of CD4+ lymphocytes in vitro. Clin Exp Immunol 110: 144-149.