Vaccinia virus H3L envelope protein is a major target of neutralizing antibodies in humans and elicits protection against lethal challenge in mice

Journal of Virology

Volumn 79, Issue 18, 2005, Pages 11724-11733

  Davies, D Huw ^a   McCausland, Megan M ^b   Valdez, Conrad ^a   Huynh, Devan ^a   Hernandez, Jenny E ^a   Mu, Yunxiang ^a   Hirst, Siddiqua ^a   Villarreal, Luis ^a   Felgner, Philip L ^a,c   Crotty, Shane ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^c 3221 McGaugh Hall ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUTRALIZING ANTIBODY; PROTEIN H3L; SMALLPOX VACCINE; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN SPECIFICITY; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; FEMALE; HUMORAL IMMUNITY; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; LETHALITY; MOUSE; NONHUMAN; PASSIVE TRANSPORT; PRIORITY JOURNAL; PROTECTION; PROTEIN FUNCTION; PROTEIN MICROARRAY; PROTEIN TARGETING; VACCINIA VIRUS; VIRION; VIRUS RESISTANCE;

ADMINISTRATION, INTRANASAL; ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; CARRIER PROTEINS; FEMALE; HUMANS; IMMUNIZATION, PASSIVE; IMMUNODOMINANT EPITOPES; MICE; MICE, INBRED BALB C; NEUTRALIZATION TESTS; PROTEIN ARRAY ANALYSIS; PROTEOME; VACCINIA; VACCINIA VIRUS; VIRAL ENVELOPE PROTEINS;

POXVIRIDAE; VACCINIA; VACCINIA VIRUS; VARIOLA VIRUS;

EID: 24644490503     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.18.11724-11733.2005     Document Type: Article

References (70)

1. Alcami, A., and G. L. Smith. 1992. A soluble receptor for interleukin-1 beta encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. Cell 71:153-167.
2. Bachmann, M. F., U. Kalinke, A. Althage, G. Freer, C. Burkhart, H. Roost, M. Aguet, H. Hengartner, and R. M. Zinkernagel. 1997. The role of antibody concentration and avidity in antiviral protection. Science 276:2024-2027.
3. Bell, E., M. Shamim, J. C. Whitbeck, G. Sfyroera, J. D. Lambris, and S. N. Isaacs. 2004. Antibodies against the extracellular enveloped virus B5R protein are mainly responsible for the EEV neutralizing capacity of vaccinia immune globulin. Virology 325:425-431.
4. Belyakov, I. M., P. Earl, A. Dzutsev, V. A. Kuznetsov, M. Lemon, L. S. Wyatt, J. T. Snyder, J. D. Ahlers, G. Franchini, B. Moss, and J. A. Berzofsky. 2003. Shared modes of protection against poxvirus infection by attenuated and conventional smallpox vaccine viruses. Proc. Natl. Acad. Sci. USA 100:9458-9463.
5. Bernasconi, N. L., E. Traggiai, and A. Lanzavecchia. 2002. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298:2199-2202.
6. Blanden, R. V. 1970. Mechanisms of recovery from a generalized viral infection: mousepox. I. The effects of anti-thymocyte serum. J. Exp. Med. 132:1035-1054.
7. Blasco, R., and B. Moss. 1992. Role of cell-associated enveloped vaccinia virus in cell-to-cell spread. J. Virol. 66:4170-4179.
8. Boulanger, D., P. Green, B. Jones, G. Henriquet, L. G. Hunt, S. M. Laidlaw, P. Monaghan, and M. A. Skinner. 2002. Identification and characterization of three immunodominant structural proteins of fowlpox virus. J. Virol. 76:9844-9855.
9. Burleson, F. G., T. M. Chambers, and D. L. Weidbrauk. 1992. Virology: a laboratory manual. Academic Press, New York, N.Y.
10. Chertov, O., I. N. Telezhinskaya, E. V. Zaitseva, T. B. Golubeva, V. V. Zinov'ev, L. G. Ovechkina, L. B. Mazkova, and E. G. Malygin. 1991. Amino acid sequence determination of vaccinia virus immunodominant protein p35 and identification of the gene. Biomed. Sci. 2:151-154.
11. Crotty, S., and R. Ahmed. 2004. Immunological memory in humans. Semin. Immunol. 16:197-203.
12. Crotty, S., P. Felgner, H. Davies, J. Glidewell, L. Villarreal, and R. Ahmed. 2003. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J. Immunol. 171:4969-4973.
13. da Fonseca, F. G., E. J. Wolffe, A. Weisberg, and B. Moss. 2000. Characterization of the vaccinia virus H3L envelope protein: topology and posttranslational membrane insertion via the C-terminal hydrophobic tail. J. Virol. 74:7508-7517.
14. da Fonseca, F. G., E. J. Wolffe, A. Weisberg, and B. Moss. 2000. Effects of deletion or stringent repression of the H3L envelope gene on vaccinia virus replication. J. Virol. 74:7518-7528.
15. Davies, D. H., X. Liang, J. E. Hernandez, A. Randall, S. Hirst, Y. Mu, K. M. Romero, T. T. Nguyen, M. Kalantari-Dehaghi, S. Crotty, P. Baldi, L. P. Villarreal, and P. L. Felgner. 2005. Profiling the humoral immune response to infection by using proteome microarrays: high-throughput vaccine and diagnostic antigen discovery. Proc. Natl. Acad. Sci. USA 102:547-552.
16. Demkowicz, W. E., Jr., R. A. Littaua, J. Wang, and F. A. Ennis. 1996. Human cytotoxic T-cell memory: long-lived responses to vaccinia virus. J. Virol. 70:2627-2631.
17. Demkowicz, W. E., J. S. Maa, and M. Esteban. 1992. Identification and characterization of vaccinia virus genes encoding proteins that are highly antigenic in animals and are immunodominant in vaccinated humans. J. Virol. 66:386-398.
18. Dietzschold, B., M. Kao, Y. M. Zheng, Z. Y. Chen, G. Maul, Z. F. Fu, C. E. Rupprecht, and H. Koprowski. 1992. Delineation of putative mechanisms involved in antibody-mediated clearance of rabies virus from the central nervous system. Proc. Natl. Acad. Sci. USA 89:7252-7256.
19. Edghill-Smith, Y., M. Bray, C. A. Whitehouse, D. Miller, E. Mucker, J. Manischewitz, L. R. King, M. Robert-Guroff, A. Hryniewicz, D. Venzon, C. Meseda, J. Weir, A. Nalca, V. Livingston, J. Wells, M. G. Lewis, J. Huggins, S. H. Zwiers, H. Golding, and G. Franchini. 2005. Smallpox vaccine does not protect macaques with AIDS from a lethal monkeypox virus challenge. J. Infect. Dis. 191:372-381.
20. Fenner, F., D. A. Henderson, I. Arita, Z. Jezek, and I. D. Ladnyi. 1988. Smallpox and its eradication. World Health Organization, Geneva, Switzerland.
21. Fogg, C., S. Lustig, J. C. Whitbeck, R. J. Eisenberg, G. H. Cohen, and B. Moss. 2004. Protective immunity to vaccinia virus induced by vaccination with multiple recombinant outer membrane proteins of intracellular and extracellular virions. J. Virol. 78:10230-10237.
22. Frey, S. E., F. K. Newman, J. Cruz, W. B. Shelton, J. M. Tennant, T. Polach, A. L. Rothman, J. S. Kennedy, M. Wolff, R. B. Belshe, and F. A. Ennis. 2002. Dose-related effects of smallpox vaccine. N. Engl. J. Med. 346:1275-1280.
23. Fulginiti, V. A., A. Papier, J. M. Lane, J. M. Neff, and D. A. Henderson. 2003. Smallpox vaccination: a review, part II. Adverse events. Clin. Infect. Dis. 37:251-271.
24. Galmiche, M. C., J. Goenaga, R. Wittek, and L. Rindisbacher. 1999. Neutralizing and protective antibodies directed against vaccinia virus envelope antigens. Virology 254:71-80.
25. Gordon, J., T. Kovala, and S. Dales. 1988. Molecular characterization of a prominent antigen of the vaccinia virus envelope. Virology 167:361-369.
26. Gordon, J., A. Mohandas, S. Wilton, and S. Dales. 1991. A prominent antigenic surface polypeptide involved in the biogenesis and function of the vaccinia virus envelope. Virology 181:671-686.
27. Hammarlund, E., M. W. Lewis, S. G. Hansen, L. I. Strelow, J. A. Nelson, G. J. Sexton, J. M. Hanifin, and M. K. Slifka. 2003. Duration of antiviral immunity after smallpox vaccination. Nat. Med. 9:1131-1137.
28. Heine, H. G., M. P. Stevens, A. J. Foord, and D. B. Boyle. 1999. A capripoxvirus detection PCR and antibody ELISA based on the major antigen P32, the homolog of the vaccinia virus H3L gene. J. Immunol. Methods 227:187-196.
29. Henderson, D. A., T. V. Inglesby, J. G. Bartlett, M. S. Ascher, E. Eitzen, P. B. Jahrling, J. Hauer, M. Layton, J. McDade, M. T. Osterholm, T. O'Toole, G. Parker, T. Perl, P. K. Russell, K. Tonat, et al. 1999. Smallpox as a biological weapon: medical and public health management. JAMA 281:2127-2137.
30. Hooper, J. W., D. M. Custer, C. S. Schmaljohn, and A. L. Schmaljohn. 2000. DNA vaccination with vaccinia virus L1R and A33R genes protects mice against a lethal poxvirus challenge. Virology 266:329-339.
31. Hooper, J. W., D. M. Custer, and E. Thompson. 2003. Four-gene-combination DNA vaccine protects mice against a lethal vaccinia virus challenge and elicits appropriate antibody responses in nonhuman primates. Virology 306:181-195.
32. Hooper, J. W., E. Thompson, C. Wilhelmsen, M. Zimmerman, M. A. Ichou, S. E. Steffen, C. S. Schmaljohn, A. L. Schmaljohn, and P. B. Jahrling. 2004. Smallpox DNA vaccine protects nonhuman primates against lethal monkeypox. J. Virol. 78:4433-4443.
33. Housawi, F. M., G. M. Roberts, J. A. Gilray, I. Pow, H. W. Reid, P. F. Nettleton, K. J. Sumption, M. H. Hibma, and A. A. Mercer. 1998. The reactivity of monoclonal antibodies against orf virus with other parapoxviruses and the identification of a 39 kDa immunodominant protein. Arch. Virol. 143:2289-2303.
34. Hsiao, J. C., C. S. Chung, and W. Chang. 1999. Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. J. Virol. 73:8750-8761.
35. Ichihashi, Y., and M. Oie. 1996. Neutralizing epitope on penetration protein of vaccinia virus. Virology 220:491-494.
36. Ichihashi, Y., T. Takahashi, and M. Oie. 1994. Identification of a vaccinia virus penetration protein. Virology 202:834-843.
37. + T lymphocytes and macrophage subsets in the control of a generalized virus infection. J. Virol. 70:8301-8309.
38. Kempe, C. H. 1960. Studies of smallpox and complications of smallpox vaccination. Pediatrics 26:176-189.
39. Kempe, C. H., C. Bowles, G. Meiklejohn, T. O. Berge, L. St Vincent, B. V. Babu, S. Govindarajan, N. R. Ratnakannan, A. W. Downie, and V. R. Murthy. 1961. The use of vaccinia hyperimmune gamma-globulin in the prophylaxis of smallpox. Bull. World Health Organ. 25:41-48.
40. Lai, C. F., S. C. Gong, and M. Esteban. 1991. The purified 14-kilodalton envelope protein of vaccinia virus produced in Escherichia coli induces virus immunity in animals. J. Virol. 65:5631-5635.
41. Lane, J. M., F. L. Ruben, J. M. Neff, and J. D. Millar. 1969. Complications of smallpox vaccination, 1968. N. Engl. J. Med. 281:1201-1208.
42. Law, M., and G. L. Smith. 2001. Antibody neutralization of the extracellular enveloped form of vaccinia virus. Virology 280:132-142.
43. Levine, B., J. M. Hardwick, B. D. Trapp, T. O. Crawford, R. C. Bollinger, and D. E. Griffin. 1991. Antibody-mediated clearance of alphavirus infection from neurons. Science 254:856-860.
44. Lin, C. L., C. S. Chung, H. G. Heine, and W. Chang. 2000. Vaccinia virus envelope H3L protein binds to cell surface heparan sulfate and is important for intracellular mature virion morphogenesis and virus infection in vitro and in vivo. J. Virol. 74:3353-3365.
45. Mathew, A., M. Terajima, K. West, S. Green, A. L. Rothman, F. A. Ennis, and J. S. Kennedy. 2005. Identification of murine poxvirus-specific CD8+ CTL epitopes with distinct functional profiles. J. Immunol. 174:2212-2219.
46. Moss, B. 2001. Poxviridae: the viruses and their replication. In D. M. Knipe and P. Howley (ed.), Fundamental virology, 4th ed. Lippincott, Williams & Wilkins, Philadelphia, Pa.
47. Newman, F. K., S. E. Frey, T. P. Blevins, M. Mandava, A. Bonifacio, Jr., L. Yan, and R. B. Belshe. 2003. Improved assay to detect neutralizing antibody following vaccination with diluted or undiluted vaccinia (Dryvax) vaccine. J. Clin. Microbiol. 41:3154-3157.
48. Payne, L. G. 1980. Significance of extracellular enveloped virus in the in vitro and in vivo dissemination of vaccinia. J. Gen. Virol. 50:89-100.
49. Plotkin, S. A. 2003. Vaccines, vaccination, and vaccinology. J Infect. Dis. 187:1349-1359.
50. Ramirez, J. C., E. Tapia, and M. Esteban. 2002. Administration to mice of a monoclonal antibody that neutralizes the intracellular mature virus form of vaccinia virus limits virus replication efficiently under prophylactic and therapeutic conditions. J. Gen. Virol. 83:1059-1067.
51. Rappuoli, R., H. I. Miller, and S. Falkow. 2002. Medicine. The intangible value of vaccination. Science 297:937-939.
52. Reading, P. C., and G. L. Smith. 2003. A kinetic analysis of immune mediators in the lungs of mice infected with vaccinia virus and comparison with intradermal infection. J. Gen. Virol. 84:1973-1983.
53. Rodriguez, J. F., and M. Esteban. 1987. Mapping and nucleotide sequence of the vaccinia virus gene that encodes a 14-kilodalton fusion protein. J. Virol. 61:3550-3554.
54. Rodriguez, J. F., R. Janeczko, and M. Esteban. 1985. Isolation and characterization of neutralizing monoclonal antibodies to vaccinia virus. J. Virol. 56:482-488.
55. Roos, N., M. Cyrklaff, S. Cudmore, R. Blasco, J. Krijnse-Locker, and G. Griffiths. 1996. A novel immunogold cryoelectron microscopic approach to investigate the structure of the intracellular and extracellular forms of vaccinia virus. EMBO J. 15:2343-2355.
56. Slifka, M. K. 2004. Immunological memory to viral infection. Curr. Opin. Immunol. 16:443-450.
57. Smith, G. L., A. Vanderplasschen, and M. Law. 2002. The formation and function of extracellular enveloped vaccinia virus. J. Gen. Virol. 83:2915-2931.
58. + T-cell peptide epitope of vaccinia and variola viruses. J. Virol. 78:7052-7060.
59. Terajima, M., J. Cruz, G. Raines, E. D. Kilpatrick, J. S. Kennedy, A. L. Rothman, and F. A. Ennis. 2003. Quantitation of CD8+ T cell responses to newly identified HLA-A*0201-restricted T cell epitopes conserved among vaccinia and variola (smallpox) viruses. J. Exp. Med. 197:927-932.
60. Tscharke, D. C., G. Karupiah, J. Zhou, T. Palmore, K. R. Irvine, S. M. Haeryfar, S. Williams, J. Sidney, A. Sette, J. R. Bennink, and J. W. Yewdell. 2005. Identification of poxvirus CD8+ T cell determinants to enable rational design and characterization of smallpox vaccines. J. Exp. Med. 201:95-104.
61. Tyler, K. L., M. A. Mann, B. N. Fields, and H. W. T. Virgin. 1993. Protective anti-reovirus monoclonal antibodies and their effects on viral pathogenesis. J. Virol. 67:3446-3453.
62. Wallengren, K., C. Risco, J. Krijnse-Locker, M. Esteban, and D. Rodriguez. 2001. The A17L gene product of vaccinia virus is exposed on the surface of IMV. Virology 290:143-152.
63. Welsh, R. M., L. K. Selin, and E. Szomolanyi-Tsuda. 2004. Immunological memory to viral infections. Annu. Rev. Immunol. 22:711-743.
64. Wilton, S., J. Gordon, and S. Dales. 1986. Identification of antigenic determinants by polyclonal and hybridoma antibodies induced during the course of infection by vaccinia virus. Virology 148:84-96.
65. Wolffe, E. J., S. Vijaya, and B. Moss. 1995. A myristylated membrane protein encoded by the vaccinia virus L1R open reading frame is the target of potent neutralizing monoclonal antibodies. Virology 211:53-63.
66. Wright, K. E., and M. J. Buchmeier. 1991. Antiviral antibodies attenuate T-cell-mediated immunopathology following acute lymphocytic choriomeningitis virus infection. J. Virol. 65:3001-3006.
67. Wyatt, L. S., P. L. Earl, L. A. Eller, and B. Moss. 2004. Highly attenuated smallpox vaccine protects mice with and without immune deficiencies against pathogenic vaccinia virus challenge. Proc. Natl. Acad. Sci. USA 101:4590-4595.
68. Xu, R., A. J. Johnson, D. Liggitt, and M. J. Bevan. 2004. Cellular and humoral immunity against vaccinia virus infection of mice. J. Immunol. 172:6265-6271.
69. Zhang, W. H., D. Wilcock, and G. L. Smith. 2000. Vaccinia virus F12L protein is required for actin tail formation, normal plaque size, and virulence. J. Virol. 74:11654-11662.
70. Zinoviev, V. V., N. A. Tchikaev, O. Chertov, and E. G. Malygin. 1994. Identification of the gene encoding vaccinia virus immunodominant protein p35. Gene 147:209-214.