Development of a novel, guinea pig-specific IFN-γ ELISPOT assay and characterization of guinea pig cytomegalovirus GP83-specific cellular immune responses following immunization with a modified vaccinia virus Ankara (MVA)-vectored GP83 vaccine

Vaccine

Volumn 32, Issue 31, 2014, Pages 3963-3970

  Gillis, Peter A ^a   Hernandez Alvarado, Nelmary ^a   Gnanandarajah, Josephine S ^a   Wussow, Felix ^b   Diamond, Don J ^b   Schleiss, Mark R ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

CMV pp65; Congenital CMV infection; Cytomegalovirus vaccine; ELISPOT; Glycoprotein B; Guinea pig; Guinea pig cytokine; Guinea pig immunology; IFN ; Interferon gamma; Placenta; Pp65; TORCH infection

Indexed keywords

CYTOMEGALOVIRUS ANTIGEN PP65; CYTOMEGALOVIRUS VACCINE; GAMMA INTERFERON; GAMMA INTERFERON ANTIBODY; GLYCOPROTEIN B; GUINEA PIG CYTOMEGALOVIRUS GP83; UNCLASSIFIED DRUG; VIRUS VECTOR; EPITOPE; MATRIX PROTEIN; VIRUS VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN BINDING; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; GAMMA INTERFERON ENZYME LINKED IMMUNOSPOT ASSAY; GUINEA PIG MODEL; HUMAN CYTOMEGALOVIRUS; HUMORAL IMMUNITY; IMMUNOGENICITY; IN VIVO STUDY; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; SPLEEN CELL; VACCINATION; VACCINIA VIRUS; VIRUS TRANSMISSION; ANIMAL; CYTOLOGY; CYTOMEGALOVIRUS INFECTIONS; DISEASE MODEL; GUINEA PIG; IMMUNOLOGY; ROSEOLOVIRUS; SPLEEN;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS INFECTIONS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSPOT ASSAY; EPITOPES, T-LYMPHOCYTE; GUINEA PIGS; IMMUNITY, CELLULAR; INTERFERON-GAMMA; ROSEOLOVIRUS; SPLEEN; VACCINIA VIRUS; VIRAL MATRIX PROTEINS; VIRAL VACCINES;

EID: 84902000439     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2014.05.011     Document Type: Article

References (56)

1. Hickey A.J. Guinea pig model of infectious disease - viral infections. Curr Drug Targets 2011, 12:1018-1023.
2. Padilla-Carlin D.J., McMurray D.N., Hickey A.J. The guinea pig as a model of infectious diseases. Comp Med 2008, 58:324-340.
3. Kaufmann S.H.E., Gengenbacher M. Recombinant live vaccine candidates against tuberculosis. Curr Opin Biotechnol 2012, 23:900-907.
4. Skerry C., Pokkali S., Pinn M., Be N.A., Harper J., Karakousis P.C., et al. Vaccination with recombinant mycobacterium tuberculosis PknD attenuates bacterial dissemination to the brain in guinea pigs. PLOS ONE 2013, 8.
5. Lin F., Shen X.F., McCoy J.R., Mendoza J.M., Yan J., Kemmerrer S.V., et al. A novel prototype device for electroporation-enhanced DNA vaccine delivery simultaneously to both skin and muscle. Vaccine 2011, 29:6771-6780.
6. Lan S.Y., Schelde L.M., Wang J.L., Kumar N., Ly H., Liang Y.Y. Development of infectious clones for virulent and avirulent pichinde viruses: a model virus to study arenavirus-induced hemorrhagic fevers. J Virol 2009, 83:6357-6362.
7. McLay L., Lan S., Ansari A., Liang Y., Ly H. Identification of virulence determinants within the L genomic segment of the pichinde arenavirus. J Virol 2013, 87:6635-6643.
8. Hashimoto K., Yamada S., Katano H., Fukuchi S., Sato Y., Kato M., et al. Effects of immunization of pregnant guinea pigs with guinea pig cytomegalovirus glycoprotein B on viral spread in the placenta. Vaccine 2013, 31:3199-3205.
9. Crumpler M.M., Choi K.Y., McVoy M.A., Schleiss M.R. A live guinea pig cytomegalovirus vaccine deleted of three putative immune evasion genes is highly attenuated but remains immunogenic in a vaccine/challenge model of congenital cytomegalovirus infection. Vaccine 2009, 27:4209-4218.
10. Choi Y.C., Hsiung G.D. Cytomegalovirus-infection in guinea-pigs. 2. Transplacental and horizontal transmission. J Infect Dis 1978, 138:197-202.
11. Schleiss M.R., Bourne N., Jensen N.J., Bravo F., Bernstein D.I. Immunogenicity evaluation of DNA vaccines that target guinea pig cytomegalovirus proteins glycoprotein B and UL83. Viral Immunol 2000, 13:155-167.
12. Olejniczak M.J., Choi K.Y., McVoy M.A., Cui X., Schleiss M.R. Intravaginal cytomegalovirus (CMV) challenge elicits maternal viremia results in congenital transmission in a guinea pig model. Virol J 2011, 8.
13. Cranage M.P., Kouzarides T., Bankier A.T., Satchwell S., Weston K., Tomlinson P., et al. Identification of the human cytomegalovirus glycoprotein-B gene and induction of neutralizing antibodies via its expression in recombinant vaccinia virus. EMBO J 1986, 5:3057-3063.
14. Schleiss M.R., Bourne N., Stroup G., Bravo F.J., Jensen N.J., Bernstein D.I. Protection against congenital cytomegalovirus infection and disease in guinea pigs, conferred by a purified recombinant glycoprotein B vaccine. J Infect Dis 2004, 189:1374-1381.
15. Wills M.R., Carmichael A.J., Mynard K., Jin X., Weekes M.P., Plachter B., et al. The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J Virol 1996, 70:7569-7579.
16. Schleiss M.R., Lacayo J.C., Belkaid Y., McGregor A., Stroup G., Rayner J., et al. Preconceptual administration of an alphavirus replicon UL83 (pp65 homolog) vaccine induces humoral and cellular immunity and improves pregnancy outcome in the guinea pig model of congenital cytomegalovirus infection. J Infect Dis 2007, 195:789-798.
17. Kallas E.G., Reynolds K., Andrews J., Fitzgerald T., Kasper M., Menegus M., et al. Cytomegalovirus-specific IFN gamma and IL-4 are produced by antigen expanded human blood lymphocytes from seropositive volunteers. Immunol Lett 1998, 64:63-69.
18. Eid A.J., Brown R.A., Hogan W.J., Lahr B.D., Eckel-Passow J.E., Litzow M.R., et al. Kinetics of interferon-gamma producing cytomegalovirus (CMV)-specific CD4+and CD8+T lymphocytes and the risk of subsequent CMV viremia after allogeneic hematopoietic stem cell transplantation. Transpl Infect Dis 2009, 11:519-528.
19. Hodson E.M., Jones C.A., Strippoli G.F.M., Webster A.C., Craig J.C. Immunoglobulins, vaccines or interferon for preventing cytomegalovirus disease in solid organ transplant recipients. Cochrane Database Syst Rev 2007, (2):CD005129.
20. Sinclair E., Tan Q.X., Sharp M., Girling V., Poon C., Van Natta M., et al. Protective immunity to cytomegalovirus (CMV) retinitis in AIDS is associated with CMV-specific T cells that express interferon-G and interleukin-2 and have a CD8(+) cell early maturational phenotype. J Infect Dis 2006, 194:1537-1546.
21. Bettahi I., Zhang X., Afifi R.E., BenMohamed L. Protective immunity to genital herpes simplex virus type 1 and type 2 provided by self-adjuvanting lipopeptides that drive dendritic cell maturation and elicit a polarized Th1 immune response. Viral Immunol 2006, 19:220-236.
22. van Rooij E.M.A., de Bruin M.G.M., de Visser Y.E., Middel W.G.J., Boersma W.J.A., Bianchi A.T.J. Vaccine-induced T cell-mediated immunity plays a critical role in early protection against pseudorabies virus (suid herpes virus type 1) infection in pigs. Vet Immunol Immunopathol 2004, 99:113-125.
23. Yue Y., Kaur A., Eberhardt M.K., Kassis N., Zhou S.S., Tarantal A.F., et al. Immunogenicity and protective efficacy of DNA vaccines expressing rhesus cytomegalovirus glycoprotein B, phosphoprotein 65-2, and viral interleukin-10 in rhesus macaques. J Virol 2007, 81:1095-1109.
24. Morello C.S., Kelley L.A., Munks M.W., Hill A.B., Spector D.H. DNA immunization using highly conserved murine cytomegalovirus genes encoding homologs of human cytomegalovirus UL54 (DNA polymerase) and UL105 (helicase) elicits strong CD8 T-cell responses and is protective against systemic challenge. J Virol 2007, 81:7766-7775.
25. Gibson L., Piccinini G., Lilleri D., Revello M.G., Wang Z.D., Markel S., et al. Human cytomegalovirus proteins pp65 and immediate early protein 1 are common targets for CD8(+) T cell responses in children with congenital or postnatal human cytomegalovirus infection. J Immunol 2004, 172:2256-2264.
26. Khan N., Cobbold M., Keenan R., Moss P.A.H. Comparative analysis of CD8(+) T cell responses against human cytomegalovirus proteins pp65 and immediate early 1 shows similarities in precursor frequency, oligoclonality, and phenotype. J Infect Dis 2002, 185:1025-1034.
27. Schalich J., Vytvytska O., Zauner W., Fischer M.B., Buschle M., Aichinger G., et al. Analysis of the human cytomegalovirus pp65-directed T-cell response in healthy HLA-A2-positive individuals. Biol Chem 2008, 389:551-559.
28. Schäfer H., Kilem G., Kropp B., Burger R. Monoclonal antibodies to guinea pig interferon-gamma: tools for cytokine detection and neutralization. J Immunol Methods 2007, 328:106-117.
29. Schäfer H., Burger R. Tools for cellular immunology and vaccine research the in the guinea pig: monoclonal antibodies to cell surface antigens and cell lines. Vaccine 2012, 30:5804-5811.
30. Jeevan A., Yoshimura T., Lee K.E., McMurray D.N. Differential expression of gamma interferon mRNA induced by attenuated and virulent Mycobacterium tuberculosis in guinea pig cells after Mycobacterium bovis BCG vaccination. Infect Immun 2003, 71:354-364.
31. Wang Z., La Rosa C., Li Z., Ly H., Krishnan A., Martinez J., et al. Vaccine properties of a novel marker gene-free recombinant modified vaccinia Ankara expressing immunodominant CMV antigens pp65 and IE1. Vaccine 2007, 25:1132-1141.
32. Wang Z.D., La Rosa C., Mekhoubad S., Lacey S.F., Villacres M.C., Markel S., et al. Attenuated poxviruses generate clinically relevant frequencies of CMV-specific T cells. Blood 2004, 104:847-856.
33. Wang Z.D., La Rosa C., Maas R., Ly H., Brewer J., Mekhoubad S., et al. Recombinant modified vaccinia virus Ankara expressing a soluble form of glycoprotein B causes durable immunity and neutralizing antibodies against multiple strains of human cytomegalovirus. J Virol 2004, 78:3965-3976.
34. Schleiss M.R. Cloning and characterization of the guinea-pig cytomegalovirus glycoprotein-B gene. Virology 1994, 202:173-185.
35. Tree J.A., Patel J., Thom R.E., Elmore M.J., Schaefer H., Williams A., et al. Temporal changes in the gene signatures of BCG-vaccinated guinea pigs in response to different mycobacterial antigens. Vaccine 2010, 28:7979-7986.
36. Chen H.T., Liu Y.S. Immunity of foot-and-mouth disease serotype asia 1 by sublingual vaccination. PLOS ONE 2013, 8.
37. Mohana Subramanian B., Madhanmohan M., Sriraman R., Chandrasekhar Reddy R.V., Yuvaraj S., Manikumar K., et al. Development of foot-and-mouth disease virus (FMDV) serotype O virus-like-particles (VLPs) vaccine and evaluation of its potency. Antiviral Res 2012, 96:288-295.
38. Paessler S., Walker D.H. Pathogenesis of the viral hemorrhagic fevers. Annu Rev Pathol 2013, 8:411-440.
39. Schleiss M.R. Comparison of vaccine strategies against congenital CMV infection in the guinea pig model. J Clin Virol 2008, 41:224-230.
40. Hopkins J.I., Fiander A.N., Evans A.S., Delchambre M., Gheysen D., Borysiewicz L.K., Cytotoxic T. cell immunity to human cytomegalovirus glycoprotein B. J Med Virol 1996, 49:124-131.
41. Borysiewicz L.K., Hickling J.K., Graham S., Sinclair J., Cranage M.P., Smith G.L., et al. Human cytomegalovirus-specific cytotoxic T cells relative frequency of stage-specific CTL recognizing the 72-kD immediate early protein and glycoprotein B expressed by recombinant vaccinia viruses. J Exp Med 1988, 168:919-931.
42. Walter E.A., Greenberg P.D., Gilbert M.J., Finch R.J., Watanabe K.S., Thomas E.D., et al. Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N Engl J Med 1995, 333:1038-1044.
43. Jeevan A., McFarland C.T., Yoshimura T., Skwor T., Cho H., Lasco T., et al. Production and characterization of guinea pig recombinant gamma interferon and its effect on macrophage activation. Infect Immun 2006, 74:213-224.
44. Davignon J.L., Castanie P., Yorke J.A., Gautier N., Clement D., Davrinche C. Anti-human cytomegalovirus activity of cytokines produced by CD4+ T-cell clones specifically activated by IE1 peptides in vitro. J Virol 1996, 70:2162-2169.
45. Vescovini R., Biasini C., Fagnoni F.F., Telera A.R., Zanlari L., Pedrazzoni M., et al. Massive load of functional effector CD4+ and CD8+ T cells against cytomegalovirus in very old subjects. J Immunol 2007, 179:4283-4291.
46. Zhou W., Longmate J., Lacey S.F., Palmer J.M., Gallez-Hawkins G., Thao L., et al. Impact of donor CMV status on viral infection and reconstitution of multifunction CMV-specific T cells in CMV-positive transplant recipients. Blood 2009, 113:6465-6476.
47. Cantisan S., Lara R., Montejo M., Redel J., Rodriguez-Benot A., Gutierrez-Aroca J., et al. Pretransplant interferon- secretion by CMV-specific CD8+T cells informs the risk of CMV replication after transplantation. Am J Transplant 2013, 13:738-745.
48. Yue Y., Kaur A., Zhou S.S., Barry P.A. Characterization and immunological analysis of the rhesus cytomegalovirus homologue (Rh112) of the human cytomegalovirus UL83 lower matrix phosphoprotein (pp65). J Gen Virol 2006, 87:777-787.
49. Elkington R., Walker S., Crough T., Menzies M., Tellam J., Bharadwaj M., et al. Ex vivo profiling of CD8(+)-T-cell responses to human cytomegalovirus reveals broad and multispecific reactivities in healthy virus carriers. J Virol 2003, 77:5226-5240.
50. Sylwester A.W., Mitchell B.L., Edgar J.B., Taormina C., Pelte C., Ruchti F., et al. Broadly targeted human cytomegalovirus-specific CD4(+) and CD8(+) T cells dominate the memory compartments of exposed subjects. J Exp Med 2005, 202:673-685.
51. Akiyama Y., Maruyama K., Mochizuki T., Sasaki K., Takaue Y., Yamaguchi K. Identification of HLA-A24-restricted CTL epitope encoded by the matrix protein pp65 of human cytomegalovirus. Immunol Lett 2002, 83:21-30.
52. Ohnishi M., Sakurai T., Heike Y., Yamazaki R., Kanda Y., Takaue Y., et al. Evaluation of cytomegalovirus-specific T-cell reconstitution in patients after various allogeneic haematopoietic stem cell transplantation using interferon-gamma-enzyme-linked immunospot and human leucocyte antigen tetramer assays with an immunodominant T-cell epitope. Br J Haematol 2005, 131:472-479.
53. Zaia J.A., Gallez-Hawkins G., Li X.L., Yao Z.Q., Lomeli N., Molinder K., et al. Infrequent occurrence of natural mutations in the pp65(495-503) epitope sequence presented by the HLA A*0201 allele among human cytomegalovirus isolates. J Virol 2001, 75:2472-2474.
54. Provenzano M., Mocellin S., Bettinotti M., Preuss J., Monsurro V., Marincola F.M., et al. Identification of immune dominant cytomegalovirus epitopes using quantitative real-time polymerase chain reactions to measure interferon-gamma production by peptide-stimulated peripheral blood mononuclear cells. J Immunother 2002, 25:342-351.
55. Britten C.M., Meyer R.G., Graf C., Huber C., Wolfel T. Identification of T cell epitopes by the use of rapidly generated mRNA fragments. J Immunol Methods 2005, 299:165-175.
56. Schumacher T.N., De Bruijn M.L., Vernie L.N., Kast W.M., Melief C.J., Neefjes J.J., et al. Peptide selection by MHC class I molecules. Nature 1991, 350:703-706.