Recombinant Modified Vaccinia Virus Ankara Expressing A Soluble Form of Glycoprotein B Causes Durable Immunity and Neutralizing Antibodies against Multiple Strains of Human Cytomegalovirus

Journal of Virology

Volumn 78, Issue 8, 2004, Pages 3965-3976

  Wang, Zhongde ^a   La Rosa, Corinna ^a   Maas, Rebecca ^a   Ly, Heang ^a   Brewer, John ^a   Mekhoubad, Shahram ^a   Daftarian, Pirouz ^a   Longmate, Jeff ^a   Britt, William J ^b   Diamond, Don J ^a  

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

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOMEGALOVIRUS VACCINE; GLYCOPROTEIN B; NEUTRALIZING ANTIBODY; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; CYTOTOXIC T LYMPHOCYTE; HUMAN CYTOMEGALOVIRUS; IMMUNIZATION; LATENT VIRUS INFECTION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; VACCINIA VIRUS; VIRUS NEUTRALIZATION; VIRUS REACTIVATION; VIRUS STRAIN;

ANIMALS; ANTIBODIES, VIRAL; BASE SEQUENCE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DNA, VIRAL; FEMALE; GENOTYPE; HUMANS; IMMUNOGLOBULIN G; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEUTRALIZATION TESTS; PREGNANCY; SOLUBILITY; T-LYMPHOCYTES; T-LYMPHOCYTES, CYTOTOXIC; VACCINES, ATTENUATED; VACCINES, SYNTHETIC; VACCINIA VIRUS; VIRAL ENVELOPE PROTEINS; VIRAL VACCINES;

EID: 12144289541     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.8.3965-3976.2004     Document Type: Article

References (67)

1. Adler, S. P., S. H. Hempfling, S. E. Starr, S. A. Plotkin, and S. Riddell. 1998. Safety and immunogenicity of the Towne strain cytomegalovirus vaccine. Pediatr. Infect. Dis. J. 17:200-206.
2. Adler, S. P., S. A. Plotkin, E. Gonczol, M. Cadoz, C. Meric, J. B. Wang, P. Dellamonica, A. M. Best, J. Zahradnik, S. Pincus, K. Berencsi, W. I. Cox, and Z. Gyulai. 1999. A canarypox vector expressing cytomegalovirus (CMV) glycoprotein B primes for antibody responses to a live attenuated CMV vaccine (Towne). J. Infect. Dis. 180:843-846.
3. Amara, R. R., F. Villinger, J. D. Altman, S. L. Lydy, S. P. O'Neil, S. I. Staprans, D. C. Montefiori, Y. Xu, J. G. Herndon, et al. 2001. Control of a mucosal challenge and preventions of AIDS by a multiprotein DNA/MVA vaccine. Science 292:69-74.
4. Andreoni, M., M. Faircloth, L. Vugler, and W. J. Britt. 1989. A rapid microneutralization assay for the measurement of neutralizing antibody reactive with human cytomegalovirus. J. Virol. Methods 23:157-167.
5. Aquino, V. H., and L. T. Figueiredo. 2000. High prevalence of renal transplant recipients infected with more than one cytomegalovirus glycoprotein B genotype. J. Med. Virol. 61:138-142.
6. Arribillaga, L., A. L. De Cerio, P. Sarobe, N. Casares, M. Gorraiz, A. Vales, O. Bruna-Romero, F. Borras-Cuesta, G. Paranhos-Baccala, J. Prieto, J. Ruiz, and J. J. Lasarte. 2002. Vaccination with an adenoviral vector encoding hepatitis C virus (HCV) NS3 protein protects against infection with HCV-recombinant vaccinia virus. Vaccine 21:202-210.
7. Banks, T., B. Huo, K. Kousoulas, R. Spaete, C. Pachl, and L. Pereira. 1989. A major neutralizing domain maps within the carboxyl-terminal half of the cleaved cytomegalovirus B glycoprotein. J. Gen. Virol. 70:979-985.
8. Belyakov, I. M., B. Moss, W. Strober, and J. A. Berzofsky. 1999. Mucosal vaccination overcomes the barrier to recombinant vaccinia immunization caused by preexisting poxvirus immunity. Proc. Natl. Acad. Sci. USA 96:4512-4517.
9. Berencsi, K., R. F. Rando, C. deTaisne, E. Paoletti, S. A. Plotkin, and E. Gonczol. 1993. Murine cytotoxic T cell response specific for human cytomegalovirus glycoprotein B (gB) induced by adenovirus and vaccinia virus recombinants expressing gB. J. Gen. Virol. 74:2507-2512.
10. Boppana, S. B., and W. J. Britt. 1996. Recognition of human cytomegalovirus gene products by HCMV-specific cytotoxic T cells. Virology 222:293-296.
11. Boppana, S. B., K. B. Fowler, W. J. Britt, S. Stagno, and R. F. Pass. 1999. Symptomatic congenital cytomegalovirus infection in infants born to mothers with preexisting immunity to cytomegalovirus. Pediatrics 104:55-60.
12. Boppana, S. B., L. B. Rivera, K. B. Fowler, M. Mach, and W. J. Britt. 2001. Intrauterine transmission of cytomegalovirus to infants of women with preconceptional immunity. N. Engl. J. Med. 344:1366-1371.
13. Britt, W., J. Fay, J. Seals, and C. Kensil. 1995. Formulation of an immunogenic human cytomegalovirus vaccine: responses in mice. J. Infect. Dis. 171:18-25.
14. Britt, W. J. 1984. Neutralizing antibodies detect a disulfide-linked glycoprotein complex within the envelope of human cytomegalovirus. Virology 135:369-378.
15. Britt, W. J., and C. A. Alford. 1996. Cytomegalovirus, p. 2493-2523. In B. N. Fields, D. Knipe, and P. M. Howley (ed.), Fields virology. Lippincott-Raven, Philadelphia, Pa.
16. Britt, W. J., L. Vugler, E. J. Butfiloski, and E. B. Stephens. 1990. Cell surface expression of human cytomegalovirus (HCMV) gp55-116 (gB): use of HCMV-recombinant vaccinia virus-infected cells in analysis of the human neutralizing antibody response. J. Virol. 64:1079-1085.
17. Britt, W. J., and L. G. Vugler. 1989. Processing of the gp55-116 envelope glycoprotein complex (gB) of human cytomegalovirus. J. Virol. 63:403-410.
18. Carlson, C., W. J. Britt, and T. Compton. 1997. Expression, purification, and characterization of a soluble form of human cytomegalovirus glycoprotein B. Virology 239:198-205.
19. Carroll, M. W., and B. Moss. 1995. E. coli beta-glucuronidase (GUS) as a marker for recombinant vaccinia viruses. BioTechniques 19:352-354, 356.
20. Chakrabarti, S., K. Brechling, and B. Moss. 1985. Vaccinia virus expression vector: coexpression of beta-galactosidase provides visual screening of recombinant virus plaques. Mol. Cell. Biol. 5:3403-3409.
21. Chou, S. W., and K. M. Dennison. 1991. Analysis of interstrain variation in cytomegalovirus glycoprotein B sequences encoding neutralization-related epitopes. J. Infect. Dis. 163:1229-1234.
22. Coutelier, J. P., J. T. van der Logt, F. W. Heessen, G. Warnier, and J. Van Snick. 1987. IgG2a restriction of murine antibodies elicited by viral infections. J. Exp. Med. 165:64-69.
23. Cranage, M. P., T. Kouzarides, A. T. Bankier, S. Satchwell, K. Weston, P. Tomlinson, B. Barrell, H. Hart, S. E. Bell, A. C. Minson, et al. 1986. Identification of the human cytomegalovirus glycoprotein B gene and induction of neutralizing antibodies via its expression in recombinant vaccinia virus. EMBO J. 5:3057-3063.
24. Degano, P., J. Schneider, C. M. Hannan, S. C. Gilbert, and A. V. Hill. 1999. Gene gun intradermal DNA immunization followed by boosting with modified vaccinia virus Ankara: enhanced CD8+ T cell immunogenicity and protective efficacy in the influenza and malaria models. Vaccine 18:623-632.
25. Drew, W. L., S. Chou, R. C. Miner, B. A. Mohr, M. P. Busch, C. M. van der Horst, D. M. Asmuth, and L. A. Kalish. 2002. Cytomegalovirus glycoprotein B groups in human immunodeficiency virus-infected patients with incident retinitis. J. Infect. Dis. 186:114-117.
26. Endresz, V., K. Burian, K. Berencsi, Z. Gyulai, L. Kari, H. Horton, D. Virok, C. Meric, S. A. Plotkin, and E. Gonczol. 2001. Optimization of DNA immunization against human cytomegalovirus. Vaccine 19:3972-3980.
27. Endresz, V., L. Kari, K. Berencsi, C. Kari, Z. Gyulai, C. Jeney, S. Pincus, U. Rodeck, C. Meric, S. A. Plotkin, and E. Gonczol. 1999. Induction of human cytomegalovirus (HCMV)-glycoprotein B (gB)-specific neutralizing antibody and phosphoprotein 65 (pp65)-specific cytotoxic T lymphocyte responses by naked DNA immunization. Vaccine 17:50-58.
28. Espenschied, J., J. Lamont, J. Longmate, S. Pendas, Z. Wang, D. J. Diamond, and J. D. Ellenhorn. 2003. CTLA-4 blockade enhances the therapeutic effect of an attenuated poxvirus vaccine targeting p53 in an established murine tumor model. J. Immunol. 170:3401-3407.
29. Frey, S. E., C. Harrison, R. F. Pass, E. Yang, D. Boken, R. E. Sekulovich, S. Percell, A. E. Izu, S. Hirabayashi, R. L. Burke, and A. M. Duliege. 1999. Effects of antigen dose and immunization regimens on antibody responses to a cytomegalovirus glycoprotein B subunit vaccine. J. Infect. Dis. 180:1700-1703.
30. Frey, S. E., F. K. Newman, L. Yan, K. R. Lottenbach, and R. B. Belshe. 2003. Response to smallpox vaccine in persons immunized in the distant past. JAMA 289:3295-3299.
31. Gonczol, E., K. Berensci, S. Pincus, V. Endresz, C. Meric, E. Paoletti, and S. A. Plotkin. 1995. Preclinical evaluation of an ALVAC (canarypox)-human cytomegalovirus glycoprotein B vaccine candidate. Vaccine 13:1080-1085.
32. Gyulai, Z., V. Endresz, K. Burian, S. Pincus, J. Toldy, W. I. Cox, C. Meri, S. Plotkin, and K. Berencsi. 2000. Cytotoxic T lymphocyte (CTL) responses to human cytomegalovirus pp65, IE1-Exon4, gB, pp150, and pp28 in healthy individuals: reevaluation of prevalence of IE1-specific CTLs. J. Infect. Dis. 181:1537-1546.
33. Hanke, T., A. J. McMichael, M. Mwau, E. G. Wee, I. Ceberej, S. Patel, J. Sutton, M. Tomlinson, and R. V. Samuel. 2002. Development of a DNA-MVA/HIVA vaccine for Kenya. Vaccine 20:1995-1998.
34. Harlow, E., and D. Lane. 1988. Immunoaffinity purification, p., 519-551. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
35. Hopkins, J. I., A. N. Fiander, A. S. Evans, M. Delchambre, D. Gheysen, and L. K. Borysiewicz. 1996. Cytotoxic T cell immunity to human cytomegalovirus glycoprotein B. J. Med. Virol. 49:124-131.
36. La Rosa, C., Z. Wang, J. C. Brewer, S. F. Lacey, M. C. Villacres, R. Sharan, R. Krishnan, M. Crooks, S. Markel, R. Maas, and D. J. Diamond. 2002. Preclinical development of an adjuvant-free peptide vaccine with activity against CMV pp65 in HLA transgenic mice. Blood 100:3681-3689.
37. Lopper, M., and T. Compton. 2002. Disulfide bond configuration of human cytomegalovirus glycoprotein B. J. Virol. 76:6073-6082.
38. Marshall, G. S., M. Li, G. G. Stout, M. V. Louthan, A. M. Duliege, R. L. Burke, and L. A. Hunt. 2000. Antibodies to the major linear neutralizing domains of cytomegalovirus glycoprotein B among natural seropositives and CMV subunit vaccine recipients. Viral Immunol. 13:329-341.
39. Marshall, G. S., G. P. Rabalais, G. G. Stout, and S. L. Waldeyer. 1992. Antibodies to recombinant-derived glycoprotein B after natural human cytomegalovirus infection correlate with neutralizing activity. J. Infect. Dis. 165:381-384.
40. Marshall, G. S., R. P. Ricciardi, R. F. Rando, J. Puck, R. W. Ge, S. A. Plotkin, and E. Gonczol. 1990. An adenovirus recombinant that expresses the human cytomegalovirus major envelope glycoprotein and induces neutralizing antibodies. J. Infect. Dis, 162:1177-1181.
41. Mayr, A., H. Stickl, H. K. Muller, K. Danner, and H. Singer. 1978. The smallpox vaccination strain MVA: marker, genetic structure, experience gained with the parenteral vaccination and behavior in organisms with a debilitated defence mechanism (author's translation). Zentbl. Bakteriol. B 167:375-390. (In German.)
42. McConkey, S. J., W. H. Reece, V. S. Moorthy, D. Webster, S. Dunachie, G. Butcher, J. M. Vuola, T. J. Blanchard, P. Gothard, K. Watkins, C. M. Hannan, S. Everaere, K. Brown, K. E. Kester, J. Cummings, J. Williams, D. G. Heppner, A. Pathan, K. Flanagan, N. Arulanantham, M. T. Roberts, M. Roy, G. L. Smith, J. Schneider, T. Peto, R. E. Sinden, S. C. Gilbert, and A. V. Hill. 2003. Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat. Med. 9:729-735.
43. Mocarski, E. S. 1996. Cytomegalovirus and their replication, p. 2447-2492. In B. N. Fields, D. Knipe, and P. M. Howley (ed.), Fields virology. Lippincott-Raven, Philadelphia, Pa.
44. Moss, B., and P. L. Earl. 1998. Expression of proteins in mammalian cells using vaccinia virus vectors, p. 16.15.1-16.21.9. In J. E. Coligan, A. M. Kruisbeek, D. H. Margulies, E. Shevach, and W. Strober (ed.), Current protocols in immunology. John Wiley & Sons, Inc., New York, N.Y.
45. Murata, K., M. Lechmann, M. Qiao, T. Gunji, H. J. Alter, and T. J. Liang. 2003. Immunization with hepatitis C virus-like particles protects mice from recombinant hepatitis C virus-vaccinia infection. Proc. Natl. Acad. Sci. USA 100:6753-6758.
46. Navarro, D., P. Paz, S. Tugizov, K. Topp, J. La Vail, and L. Pereira. 1993. Glycoprotein B of human cytomegalovirus promotes virion penetration into cells, transmission of infection from cell to cell, and fusion of infected cells. Virology 197:143-158.
47. Pancholi, P., M. Perkus, N. Tricoche, Q. Liu, and A. M. Prince. 2003. DNA immunization with hepatitis C virus (HCV) polycistronic genes or immunization by HCV DNA priming-recombinant canarypox virus boosting induces immune responses and protection from recombinant HCV-vaccinia virus infection in HLA-A2.1-transgenic mice. J. Virol. 77:382-390.
48. Pass, R. F., A. M. Duliege, S. Boppana, R. Sekulovich, S. Percell, W. Britt, and R. L. Burke. 1999. A subunit cytomegalovirus vaccine based on recombinant envelope glycoprotein B and a new adjuvant. J. Infect. Dis. 180:970-975.
49. Ramirez, J. C., M. M. Gherardi, and M. Esteban. 2000. Biology of attenuated modified vaccinia virus Ankara recombinant vector in mice: virus fate and activation. J. Virol. 74:923-933.
50. Ramirez, J. C., M. M. Gherardi, D. Rodriguez, and M. Esteban. 2000. Attenuated modified vaccinia virus Ankara can be used as an immunizing agent under conditions of preexisting immunity to the vector. J. Virol. 74:7651-7655.
51. Rasmussen, L., C. Matkin, R. Spaete, C. Pachl, and T. C. Merigan. 1991. Antibody response to human cytomegalovirus glycoproteins gB and gH after natural infection in humans. J. Infect. Dis. 164:835-842.
52. Riddell, S. R., M. Rabin, A. P. Geballe, W. J. Britt, and P. D. Greenberg. 1991. Class I MHC-restricted cytotoxic T lymphocyte recognition of cells infected with human cytomegalovirus does not require endogenous viral gene expression. J. Immunol. 146:2795-2804.
53. Rothe, M., S. Pepperl-Klindworth, D. Lang, R. Vornhagen, W. Hinderer, K. Weise, H. H. Sonneborn, and B. Plachter. 2001. An antigen fragment encompassing the AD2 domains of glycoprotein B from two different strains is sufficient for differentiation of primary vs. recurrent human cytomegalovirus infection by ELISA. J. Med. Virol. 65:719-729.
54. Spaete, R. R. 1991. A recombinant subunit vaccine approach to HCMV vaccine development. Transpl. Proc. 23:90-96.
55. Spaete, R. R., R. M. Thayer, W. S. Probert, F. R. Masiarz, S. H. Chamberlain, L. Rasmussen, T. C. Merigan, and C. Pachl. 1988. Human cytomegalovirus strain Towne glycoprotein B is processed by proteolytic cleavage. Virology 167:207-225.
56. Stickl, H., V. Hochstein-Mintzel, A. Mayr, H. C. Huber, H. Schafer, and A. Holzner. 1974. MVA vaccination against smallpox: clinical tests with an attenuated live vaccinia virus strain (MVA) (author's translation). Dtsch. Med. Wochenschr. 99:2386-2392. (In German.)
57. Stittelaar, K. J., T. Kuiken, R. L. de Swart, G. van Amerongen, H. W. Vos, H. G. Niesters, P. van Schalkwijk, T. van der Kwast, L. S. Wyatt, B. Moss, and A. D. Osterhaus. 2001. Safety of modified vaccinia virus Ankara (MVA) in immune-suppressed macaques. Vaccine 19:3700-3709.
58. Stratton, K. R., J. S. Durch, and R. S. Lawrence. 2001. Vaccines for the 21st century: a tool for decisionmaking. National Academy Press, Bethesda, Md.
59. Sutter, G., and B. Moss. 1992. Nonreplicating vaccinia vector efficiently expresses recombinant genes. Proc. Natl. Acad. Sci. USA 89:10847-10851.
60. Sutter, G., L. S. Wyatt, P. L. Foley, J. R. Bennink, and B. Moss. 1994. A recombinant vector derived from the host range-restricted and highly attenuated MVA strain of vaccinia virus stimulates protective immunity in mice to influenza virus. Vaccine 12:1032-1040.
61. Torok-Storb, B., M. Boeckh, C. Hoy, W. Leisenring, D. Myerson, and T. Gooley. 1997. Association of specific cytomegalovirus genotypes with death from myelosuppression after marrow transplantation. Blood 90:2097-2102.
62. Urban, M., T. Winkler, M. P. Landini, W. Britt, and M. Mach. 1994. Epitope-specific distribution of IgG subclasses against antigenic domains on glycoproteins of human cytomegalovirus. J. Infect. Dis. 169:83-90.
63. Wang, X., S. M. Huong, M. L. Chiu, N. Raab-Traub, and E. S. Huang. 2003. Epidermal growth factor receptor is a cellular receptor for human cytomegalovirus. Nature 424:456-461.
64. Wyatt, L. S., S. T. Shors, B. R. Murphy, and B. Moss. 1996. Development of a replication-deficient recombinant vaccinia virus vaccine effective against parainfluenza virus 3 infection in an animal model. Vaccine 14:1451-1458.
65. Wyatt, L. S., S. S. Whitehead, K. A. Venanzi, B. R. Murphy, and B. Moss. 1999. Priming and boosting immunity to respiratory syncytial virus by recombinant replication-defective vaccinia virus MVA. Vaccine 18:392-397.
66. Yang, Z. Y., L. S. Wyatt, W. P. Kong, Z. Moodie, B. Moss, and G. J. Nabel. 2003. Overcoming immunity to a viral vaccine by DNA priming before vector boosting. J. Virol. 77:799-803.
67. Zinkernagel, R. M. 2002. On differences between immunity and immunological memory. Curr. Opin. Immunol. 14:523-536.