Redundancy and plasticity of neutralizing antibody responses are cornerstone attributes of the human immune response to the smallpox vaccine

Journal of Virology

Volumn 82, Issue 7, 2008, Pages 3751-3768

  Benhnia, Mohammed Rafii El Idrissi ^a   McCausland, Megan M ^a   Su, Hua Poo ^b   Singh, Kavita ^b   Hoffmann, Julia ^c   Davies, D Huw ^d   Felgner, Philip L ^d   Head, Steven ^c   Sette, Alessandro ^a   Garboczi, David N ^b   Crotty, Shane ^a  

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

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; NEUTRALIZING ANTIBODY; SMALLPOX VACCINE;

ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN SPECIFICITY; ARTICLE; CORRELATION ANALYSIS; HELA CELL; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGLOBULIN PRODUCTION; INFECTION PREVENTION; NONHUMAN; PRIORITY JOURNAL; SMALLPOX; STATISTICAL SIGNIFICANCE; STEREOTYPY; VACCINIA VIRUS; VIRION; VIRUS NEUTRALIZATION; VIRUS STRAIN;

ANTIBODIES, VIRAL; CARRIER PROTEINS; HUMANS; IMMUNOGLOBULIN G; NEUTRALIZATION TESTS; SMALLPOX VACCINE; VACCINIA VIRUS; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS; VIRION;

MUS; VACCINIA VIRUS; VARIOLA VIRUS;

EID: 41149110035     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02244-07     Document Type: Article

References (61)

1. Aldaz-Carroll, L., J. C. Whitbeck, M. Ponce de Leon, H. Lou, L. Hirao, S. N. Isaacs, B. Moss, R. J. Eisenberg, and G. H. Cohen. 2005. Epitope-mapping studies define two major neutralization sites on the vaccinia virus extracellular enveloped virus glycoprotein B5R. J. Virol. 79:6260-6271.
2. Aldaz-Carroll, L., J. C. Whitbeck, M. Ponce de Leon, H. Lou, L. K. Pannell, J. Lebowitz, C. Fogg, C. L. White, B. Moss, G. H. Cohen, and R. J. Eisenberg. 2005. Physical and immunological characterization of a recombinant secreted form of the membrane protein encoded by the vaccinia virus L1R gene. Virology 341:59-71.
3. Alibek, K. 27 March 1998. Russia's deadly expertise, p. A19. In The New York Times. The New York Times Co., New York, NY.
4. Alibek, K., and S. Handelman. 1999. Biohazard. Random House, New York, NY.
5. Amanna, I. J., M. K. Slifka, and S. Crotty. 2006. Immunity and immunological memory following smallpox vaccination. Immunol. Rev. 211:320-337.
6. 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.
7. 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.
8. Chiu, W. L., C. L. Lin, M. H. Yang, D. L. Tzou, and W. Chang. 2007. Vaccinia virus 4c (A26L) protein on intracellular mature virus binds to the extracellular cellular matrix laminin. J. Virol. 81:2149-2157.
9. Chung, C. S., C. H. Chen, M. Y. Ho, C. Y. Huang, C. L. Liao, and W. Chang. 2006. Vaccinia virus proteome: identification of proteins in vaccinia virus intracellular mature virion particles. J. Virol. 80:2127-2140.
10. Condit, R. C., N. Moussatche, and P. Traktman. 2006. In a nutshell: structure and assembly of the vaccinia virion. Adv. Virus Res. 66:31-124.
11. 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.
12. 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.
13. Davies, D. H., M. M. McCausland, C. Valdez, D. Huynh, J. E. Hernandez, Y. Mu, S. Hirst, L. Villarreal, P. L. Felgner, and S. Crotty. 2005. Vaccinia virus H3L envelope protein is a major target of neutralizing antibodies in humans and elicits protection against lethal challenge in mice. J. Virol. 79:11724-11733.
14. 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.
15. Edghill-Smith, Y., H. Golding, J. Manischewitz, L. R. King, D. Scott, M. Bray, A. Nalca, J. W. Hooper, C. A. Whitehouse, J. E. Schmitz, K. A. Reimann, and G. Franchini. 2005. Smallpox vaccine-induced antibodies are necessary and sufficient for protection against monkeypox virus. Nat. Med. 11:740-747.
16. Fenner, F., D. A. Henderson, I. Arita, Z. Jezek, and I. D. Ladnyi. 1988. Smallpox and its eradication. World Health Organization, Geneva, Switzerland.
17. 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.
18. 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.
19. Hammarlund, E., M. W. Lewis, S. V. Carter, I. Amanna, S. G. Hansen, L. I. Strelow, S. W. Wong, P. Yoshihara, J. M. Hanifin, and M. K. Slifka. 2005. Multiple diagnostic techniques identify previously vaccinated individuals with protective immunity against monkeypox. Nat. Med. 11:1005-1011.
20. 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.
21. He, Y., J. Manischewitz, C. A. Meseda, M. Merchlinsky, R. A. Vassell, L. Sirota, I. Berkower, H. Golding, and C. D. Weiss. 2007. Antibodies to the A27 protein of vaccinia virus neutralize and protect against infection but represent a minor component of Dryvax vaccine-induced immunity. J. Infect. Dis. 196:1026-1032.
22. Henderson, D. A. 1999. Smallpox and vaccinia, p. 74-97. In S. A. Plotkin and W. A. Orenstein (ed.), Vaccines, 3rd ed. W. B. Saunders, Philadelphia, PA.
23. 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.
24. Heuser, J. 2005. Deep-etch EM reveals that the early poxvirus envelope is a single membrane bilayer stabilized by a geodetic "honeycomb" surface coat. J. Cell Biol. 169:269-283.
25. Hobday, T. L. 1962. Antivaccinial gamma-globulin in the control of smallpox. Lancet i:907-908.
26. 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.
27. Hopkins, D. R. 1983. Princes and peasants. Smallpox in history. University of Chicago Press, Chicago, IL.
28. Hopkins, R. J., and J. M. Lane. 2004. Clinical efficacy of intramuscular vaccinia immune globulin: a literature review. Clin. Infect. Dis. 39:819-826.
29. 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.
30. Ichihashi, Y., and M. Oie. 1996. Neutralizing epitope on penetration protein of vaccinia virus. Virology 220:491-494.
31. Ichihashi, Y., T. Takahashi, and M. Oie. 1994. Identification of a vaccinia virus penetration protein. Virology 202:834-843.
32. Kempe, C. H. 1960. Studies on smallpox and complications of smallpox vaccination. Pediatrics 25:176-189.
33. Kempe, C. H., T. O. Berge, and B. England. 1956. Hyperimmune vaccinial gamma globulin. Pediatrics 18:177-188.
34. 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.
35. 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.
36. Lustig, S., C. Fogg, J. C. Whitbeck, R. J. Eisenberg, G. H. Cohen, and B. Moss. 2005. Combinations of polyclonal or monoclonal antibodies to proteins of the outer membranes of the two infectious forms of vaccinia virus protect mice against a lethal respiratory challenge. J. Virol. 79:13454-13462.
37. Mack, T. M., J. Noble, Jr., and D. B. Thomas. 1972. A prospective study of serum antibody and protection against smallpox. Am. J. Trop. Med. Hyg. 21:214-218.
38. Marennikova, S. S. 1962. The use of hyperimmune antivaccinia gammaglobulin for the prevention and treatment of smallpox. Bull. World Health Organ. 27:325-330.
39. Miner, J. N., and D. E. Hruby. 1989. Rifampicin prevents virosome localization of L65, an essential vaccinia virus polypeptide. Virology 170:227-237.
40. Moss, B. 2006. Poxviridae: the viruses and their replication, p. 2849-2883. In D. M. Knipe, P. Howley, D. Griffin, and R. Lamb (ed.), Fundamental virology, 5th ed. Lippincott Williams & Wilkins, Hagerstown, MD.
41. 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.
42. Ojeda, S., A. Domi, and B. Moss. 2006. Vaccinia virus G9 protein is an essential component of the poxvirus entry-fusion complex. J. Virol. 80:9822-9830.
43. Ojeda, S., T. G. Senkevich, and B. Moss. 2006. Entry of vaccinia virus and cell-cell fusion require a highly conserved cysteine-rich membrane protein encoded by the A16L gene. J. Virol. 80:51-61.
44. O'Toole, T., M. Mair, and T. V. Inglesby. 2002. Shining light on "Dark Winter." Clin. Infect. Dis. 34:972-983.
45. Putz, M. M., C. M. Midgley, M. Law, and G. L. Smith. 2006. Quantification of antibody responses against multiple antigens of the two infectious forms of Vaccinia virus provides a benchmark for smallpox vaccination. Nat. Med. 12:1310-1315.
46. 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.
47. Rappuoli, R., H. I. Miller, and S. Falkow. 2002. Medicine. The intangible value of vaccination. Science 297:937-939.
48. Resch, W., K. K. Hixson, R. J. Moore, M. S. Lipton, and B. Moss. 2007. Protein composition of the vaccinia virus mature virion. Virology 358:233-247.
49. Robinson, W. H., C. DiGennaro, W. Hueber, B. B. Haab, M. Kamachi, E. J. Dean, S. Fournel, D. Fong, M. C. Genovese, H. E. de Vegvar, K. Skriner, D. L. Hirschberg, R. I. Morris, S. Muller, G. J. Pruijn, W. J. van Venrooij, J. S. Smolen, P. O. Brown, L. Steinman, and P. J. Utz. 2002. Autoantigen microarrays for multiplex characterization of autoantibody responses. Nat. Med. 8:295-301.
50. 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.
51. Rodriguez, J. F., R. Janeczko, and M. Esteban. 1985. Isolation and characterization of neutralizing monoclonal antibodies to vaccinia virus. J. Virol. 56:482-488.
52. Sakhatskyy, P., S. Wang, T. H. Chou, and S. Lu. 2006. Immunogenicity and protection efficacy of monovalent and polyvalent poxvirus vaccines that include the D8 antigen. Virology 355:167-174.
53. Sarkar, J. K., A. C. Mitra, and M. K. Mukherjee. 1975. The minimum protective level of antibodies in smallpox. Bull. World Health Organ. 52:307-311.
54. Senkevich, T. G., S. Ojeda, A. Townsley, G. E. Nelson, and B. Moss. 2005. Poxvirus multiprotein entry-fusion complex. Proc. Natl. Acad. Sci. USA 102:18572-18577.
55. Smith, G. L., A. Vanderplasschen, and M. Law. 2002. The formation and function of extracellular enveloped vaccinia virus. J. Gen. Virol. 83:2915-2931.
56. Su, H. P., S. C. Garman, T. J. Allison, C. Fogg, B. Moss, and D. N. Garboczi. 2005. The 1.51-Angstrom structure of the poxvirus L1 protein, a target of potent neutralizing antibodies. Proc. Natl. Acad. Sci. USA 102:4240-4245.
57. Szajner, P., A. S. Weisberg, J. Lebowitz, J. Heuser, and B. Moss. 2005. External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. J. Cell Biol. 170:971-981.
58. Tsung, K., J. H. Yim, W. Marti, R. M. Buller, and J. A. Norton. 1996. Gene expression and cytopathic effect of vaccinia virus inactivated by psoralen and long-wave UV light. J. Virol. 70:165-171.
59. 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.
60. Wittek, R. 2006. Vaccinia immune globulin: current policies, preparedness, and product safety and efficacy. Int. J. Infect. Dis. 10:193-201.
61. 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.