Heavily isotype-dependent protective activities of human antibodies against vaccinia virus extracellular virion antigen B5

Journal of Virology

Volumn 83, Issue 23, 2009, Pages 12355-12367

  Benhnia, Mohammed Rafii El Idrissi ^a   McCausland, Megan M ^a,c   Laudenslager, John ^b   Granger, Steven W ^b   Rickert, Sandra ^b,d   Koriazova, Lilia ^b   Tahara, Tomoyuki ^b   Kubo, Ralph T ^a,b   Kato, Shinichiro ^b   Crotty, Shane ^a  

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

^b KYOWA HAKKO KOGYO CO LTD   (Japan)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VERTEX PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B5 ANTIGEN; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C5; FC RECEPTOR; HUMAN MONOCLONAL ANTIBODY B5 H101; HUMAN MONOCLONAL ANTIBODY B5 H102; HUMAN MONOCLONAL ANTIBODY B5 H104; HUMAN MONOCLONAL ANTIBODY B5 H106; IMMUNOGLOBULIN G ANTIBODY; ISOTOPE; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; POLYCLONAL ANTIBODY; RECOMBINANT B5 PROTEIN; RECOMBINANT PROTEIN; SMALLPOX VACCINE; UNCLASSIFIED DRUG; VIRUS ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BINDING AFFINITY; COMPLEMENT DEPENDENT CYTOTOXICITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNITY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SMALLPOX; VACCINIA; VACCINIA VIRUS; VIRION; VIRUS IMMUNITY; VIRUS NEUTRALIZATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; BODY WEIGHT; COMPLEMENT C1Q; COMPLEMENT C3; FEMALE; HUMANS; IMMUNOGLOBULIN ISOTYPES; MICE; MICE, INBRED BALB C; MODELS, BIOLOGICAL; NEUTRALIZATION TESTS; SMALLPOX; SURVIVAL ANALYSIS; VACCINIA VIRUS; VIRAL MATRIX PROTEINS;

ANIMALIA; VACCINIA VIRUS; VARIOLA VIRUS;

EID: 70450175846     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01593-09     Document Type: Article

References (110)

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. (Pubitemid 40617230)
2. Aldaz-Carroll, L., Y. Xiao, J. C. Whitbeck, M. P. de Leon, H. Lou, M. Kim, J. Yu, E. L. Reinherz, S. N. Isaacs, R. J. Eisenberg, and G. H. Cohen. 2007. Major neutralizing sites on vaccinia virus glycoprotein B5 are exposed differently on variola virus ortholog B6. J. Virol. 81:8131-8139.
3. Amanna, I. J., M. K. Slifka, and S. Crotty. 2006. Immunity and immunological memory following smallpox vaccination. Immunol. Rev. 211:320-337.
4. Angal, S., D. J. King, M. W. Bodmer, A. Turner, A. D. Lawson, G. Roberts, B. Pedley, and J. R. Adair. 1993. A single amino acid substitution abolishes the heterogeneity of chimeric mouse/human (IgG4) antibody. Mol. Immunol. 30:105-108.
5. 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. (Pubitemid 38902805)
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. Benhnia, M. R., M. M. McCausland, J. Moyron, J. Laudenslager, S. Granger, S. Rickert, L. Koriazova, R. Kubo, S. Kato, and S. Crotty. 2009. Vaccinia virus extracellular enveloped virion neutralization in vitro and protection in vivo depend on complement. J. Virol. 83:1201-1215.
8. Benhnia, M. R., M. M. McCausland, H. P. Su, K. Singh, J. Hoffmann, D. H. Davies, P. Felgner, S. Head, A. Sette, D. N. Garboczi, and S. Crotty. 2008. Redundancy and plasticity of neutralizing antibody responses are cornerstone attributes of the human immune response to the smallpox vaccine. J. Virol. 82:3751-3768.
9. Berry, D. M., and J. D. Almeida. 1968. The morphological and biological effects of various antisera on avian infectious bronchitis virus. J. Gen. Virol. 3:97-102.
10. Bindon, C. I., G. Hale, M. Bruggemann, and H. Waldmann. 1988. Human monoclonal IgG isotypes differ in complement activating function at the level of C4 as well as C1q. J. Exp. Med. 168:127-142.
11. Botto, M., C. Dell'Agnola, A. E. Bygrave, E. M. Thompson, H. T. Cook, F. Petry, M. Loos, P. P. Pandolfi, and M. J. Walport. 1998. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19:56-59.
12. Botto, M., and M. J. Walport. 2002. C1q, autoimmunity and apoptosis. Immunobiology 205:395-406.
13. Botto, M., and M. J. Walport. 1993. Hereditary deficiency of C3 in animals and humans. Int. Rev. Immunol. 10:37-50.
14. Brier, A. M., C. Wohlenberg, J. Rosenthal, M. Mage, and A. L. Notkins. 1971. Inhibition or enhancement of immunological injury of virus-infected cells. Proc. Natl. Acad. Sci. USA 68:3073-3077.
15. Celik, I., C. Stover, M. Botto, S. Thiel, S. Tzima, D. Kunkel, M. Walport, W. Lorenz, and W. Schwaeble. 2001. Role of the classical pathway of complement activation in experimentally induced polymicrobial peritonitis. Infect. Immun. 69:7304-7309.
16. Chen, Z., P. Earl, J. Americo, I. Damon, S. K. Smith, F. Yu, A. Sebrell, S. Emerson, G. Cohen, R. J. Eisenberg, I. Gorshkova, P. Schuck, W. Satterfield, B. Moss, and R. Purcell. 2007. Characterization of chimpanzee/human monoclonal antibodies to vaccinia virus A33 glycoprotein and its variola virus homolog in vitro and in a vaccinia virus mouse protection model. J. Virol. 81:8989-8995. (Pubitemid 47311442)
17. Chen, Z., P. Earl, J. Americo, I. Damon, S. K. Smith, Y. H. Zhou, F. Yu, A. Sebrell, S. Emerson, G. Cohen, R. J. Eisenberg, J. Svitel, P. Schuck, W. Satterfield, B. Moss, and R. Purcell. 2006. Chimpanzee/human mAbs to vaccinia virus B5 protein neutralize vaccinia and smallpox viruses and protect mice against vaccinia virus. Proc. Natl. Acad. Sci. USA 103:1882-1887.
18. 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.
19. Da Costa, X. J., M. A. Brockman, E. Alicot, M. Ma, M. B. Fischer, X. Zhou, D. M. Knipe, and M. C. Carroll. 1999. Humoral response to herpes simplex virus is complement-dependent. Proc. Natl. Acad. Sci. USA 96:12708-12712.
20. 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.
21. 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.
22. Davies, D. H., D. Molina, J. Wrammert, J. Miller, S. Hirst, Y. Mu, J. Pablo, B. Unal, R. Nakajima-Sasaki, X. Liang, S. Crotty, K. Karem, I. Damon, R. Ahmed, L. Villarreal, and P. Felgner. 2007. Proteome-wide analysis of the serological response to vaccinia and smallpox. Proteomics 7:1678-1686.
23. Davies, D. H., L. S. Wyatt, F. K. Newman, P. L. Earl, S. Chun, J. E. Hernandez, D. Molina, S. Hirst, B. Moss, S. E. Frey, and P. L. Felgner. 2008. Antibody profiling by proteome microarray reveals the immunogenicity of the attenuated smallpox vaccine modified vaccinia virus Ankara is comparable to that of Dryvax. J. Virol. 82:652-663.
24. Downie, A. W., and K. McCarthy. 1958. The antibody response in man following infection with viruses of the pox group. III. Antibody response in smallpox. J. Hyg. (London) 56:479-487.
25. Duke-Cohan, J. S., K. Wollenick, E. A. Witten, M. S. Seaman, L. R. Baden, R. Dolin, and E. L. Reinherz. 2009. The heterogeneity of human antibody responses to vaccinia virus revealed through use of focused protein arrays. Vaccine 27:1154-1165.
26. Duncan, A. R., and G. Winter. 1988. The binding site for C1q on IgG. Nature 332:738-740.
27. 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.
28. Engelstad, M., S. T. Howard, and G. L. Smith. 1992. A constitutively expressed vaccinia gene encodes a 42-kDa glycoprotein related to complement control factors that forms part of the extracellular virus envelope. Virology 188:801-810.
29. Fang, M., H. Cheng, Z. Dai, Z. Bu, and L. J. Sigal. 2006. Immunization with a single extracellular enveloped virus protein produced in bacteria provides partial protection from a lethal orthopoxvirus infection in a natural host. Virology 345:231-243.
30. Fenner, F., D. A. Henderson, I. Arita, Z. Jezek, and I. D. Ladnyi. 1988. Smallpox and its eradication. World Health Organization, Geneva, Switzerland.
31. Reference deleted.
32. Figueroa, J. E., and P. Densen. 1991. Infectious diseases associated with complement deficiencies. Clin. Microbiol. Rev. 4:359-395.
33. Flamand, A., H. Raux, Y. Gaudin, and R. W. Ruigrok. 1993. Mechanisms of rabies virus neutralization. Virology 194:302-313.
34. 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. (Pubitemid 39258347)
35. Fogg, C. N., J. L. Americo, P. L. Earl, W. Resch, L. Aldaz-Carroll, R. J. Eisenberg, G. H. Cohen, and B. Moss. 2008. Disparity between levels of in vitro neutralization of vaccinia virus by antibody to the A27 protein and protection of mice against intranasal challenge. J. Virol. 82:8022-8029.
36. 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. (Pubitemid 29391715)
37. Girgis, N. M., B. C. Dehaven, X. Fan, K. M. Viner, M. Shamim, and S. N. Isaacs. 2008. Cell surface expression of the vaccinia virus complement control protein is mediated by interaction with the viral A56 protein and protects infected cells from complement attack. J. Virol. 82:4205-4214.
38. Glass, D., D. Raum, D. Gibson, J. S. Stillman, and P. H. Schur. 1976. Inherited deficiency of the second component of complement. Rheumatic disease associations. J. Clin. Investig. 58:853-861.
39. He, Y., J. Manischewitz, C. Meseda, M. Merchlinsky, R. Vassell, L. Sirota, I. Berkower, H. Golding, and C. 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.
40. Heraud, J. M., Y. Edghill-Smith, V. Ayala, I. Kalisz, J. Parrino, V. S. Kalyanaraman, J. Manischewitz, L. R. King, A. Hryniewicz, C. J. Trindade, M. Hassett, W. P. Tsai, D. Venzon, A. Nalca, M. Vaccari, P. Silvera, M. Bray, B. S. Graham, H. Golding, J. W. Hooper, and G. Franchini. 2006. Subunit recombinant vaccine protects against monkeypox. J. Immunol. 177:2552-2564. (Pubitemid 44201014)
41. Hessell, A. J., L. Hangartner, M. Hunter, C. E. Havenith, F. J. Beurskens, J. M. Bakker, C. M. Lanigan, G. Landucci, D. N. Forthal, P. W. Parren, P. A. Marx, and D. R. Burton. 2007. Fc receptor but not complement binding is important in antibody protection against HIV. Nature 449:101-104.
42. Hicks, J. T., F. A. Ennis, E. Kim, and M. Verbonitz. 1978. The importance of an intact complement pathway in recovery from a primary viral infection: influenza in decomplemented and in C5-deficient mice. J. Immunol. 121:1437-1445.
43. Hobday, T. L. 1962. Antivaccinial gamma-globulin in the control of smallpox. Lancet i:907-908.
44. 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.
45. 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.
46. 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.
47. Hopkins, R. J., and J. M. Lane. 2004. Clinical efficacy of intramuscular vaccinia immune globulin: a literature review. Clin. Infect. Dis. 39:819-826.
48. Isaacs, S. N., G. J. Kotwal, and B. Moss. 1992. Vaccinia virus complement-control protein prevents antibody-dependent complement-enhanced neutralization of infectivity and contributes to virulence. Proc. Natl. Acad. Sci. USA 89:628-632.
49. Isaacs, S. N., E. J. Wolffe, L. G. Payne, and B. Moss. 1992. Characterization of a vaccinia virus-encoded 42-kilodalton class I membrane glycoprotein component of the extracellular virus envelope. J. Virol. 66:7217-7224.
50. Ishida, I., K. Tomizuka, H. Yoshida, T. Tahara, N. Takahashi, A. Ohguma, S. Tanaka, M. Umehashi, H. Maeda, C. Nozaki, E. Halk, and N. Lonberg. 2002. Production of human monoclonal and polyclonal antibodies in Trans-Chromo animals. Cloning Stem Cells 4:91-102. (Pubitemid 34437643)
51. Johnson, J. B., G. A. Capraro, and G. D. Parks. 2008. Differential mechanisms of complement-mediated neutralization of the closely related paramyxoviruses simian virus 5 and mumps virus. Virology 376:112-123.
52. Kempe, C. H. 1960. Studies on smallpox and complications of smallpox vaccination. Pediatrics 25:176-189.
53. Kempe, C. H., T. O. Berge, and B. England. 1956. Hyperimmune vaccinial gamma globulin. Pediatrics 18:177-188.
54. Kishore, U., and K. B. Reid. 2000. C1q: structure, function, and receptors. Immunopharmacology 49:159-170.
55. Klasse, P. J. 2007. Modeling how many envelope glycoprotein trimers per virion participate in human immunodeficiency virus infectivity and its neutralization by antibody. Virology 369:245-262.
56. Klasse, P. J., and D. Burton. 2007. Antibodies to West Nile virus: a doubleed-ged sword. Cell Host Microbe 1:87-89. (Pubitemid 46554918)
57. Klasse, P. J., and J. P. Moore. 1996. Quantitative model of antibody- and soluble CD4-mediated neutralization of primary isolates and T-cell line-adapted strains of human immunodeficiency virus type 1. J. Virol. 70:3668-3677. (Pubitemid 26157347)
58. Kotwal, G. J., S. N. Isaacs, R. McKenzie, M. M. Frank, and B. Moss. 1990. Inhibition of the complement cascade by the major secretory protein of vaccinia virus. Science 250:827-830.
59. Kotwal, G. J., and B. Moss. 1988. Vaccinia virus encodes a secretory polypeptide structurally related to complement control proteins. Nature 335:176-178.
60. Law, M., R. Hollinshead, and G. L. Smith. 2002. Antibody-sensitive and antibody-resistant cell-to-cell spread by vaccinia virus: role of the A33R protein in antibody-resistant spread. J. Gen. Virol. 83:209-222.
61. Law, M., M. M. Pütz, and G. L. Smith. 2005. An investigation of the therapeutic value of vaccinia-immune IgG in a mouse pneumonia model. J. Gen. Virol. 86:991-1000.
62. Lawrence, S. J., K. R. Lottenbach, F. K. Newman, R. M. Buller, C. J. Bellone, J. J. Chen, G. H. Cohen, R. J. Eisenberg, R. B. Belshe, S. L. Stanley, Jr., and S. E. Frey. 2007. Antibody responses to vaccinia membrane proteins after smallpox vaccination. J. Infect. Dis. 196:220-229.
63. Leddy, J. P., R. L. Simons, and R. G. Douglas. 1977. Effect of selective complement deficiency on the rate of neutralization of enveloped viruses by human sera. J. Immunol. 118:28-34.
64. Lewis, M. J., and M. Botto. 2006. Complement deficiencies in humans and animals: links to autoimmunity. Autoimmunity 39:367-378.
65. Li, L., K. L. Coelingh, and W. J. Britt. 1995. Human cytomegalovirus neutralizing antibody-resistant phenotype is associated with reduced expression of glycoprotein H. J. Virol. 69:6047-6053.
66. 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.
67. Lustig, S., C. Fogg, J. C. Whitbeck, and B. Moss. 2004. Synergistic neutralizing activities of antibodies to outer membrane proteins of the two infectious forms of vaccinia virus in the presence of complement. Virology 328:30-35.
68. 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.
69. Marennikova, S. S. 1962. The use of hyperimmune antivaccinia gammaglobulin for the prevention and treatment of smallpox. Bull. W. H. O. 27:325-330.
70. Marriott, K. A., C. V. Parkinson, S. I. Morefield, R. Davenport, R. Nichols, and T. P. Monath. 2008. Clonal vaccinia virus grown in cell culture fully protects monkeys from lethal monkeypox challenge. Vaccine 26:581-588.
71. Mehlhop, E., and M. S. Diamond. 2006. Protective immune responses against West Nile virus are primed by distinct complement activation pathways. J. Exp. Med. 203:1371-1381.
72. Mehlhop, E., K. Whitby, T. Oliphant, A. Marri, M. Engle, and M. S. Diamond. 2005. Complement activation is required for induction of a protective antibody response against West Nile virus infection. J. Virol. 79:7466-7477. (Pubitemid 40756783)
73. Miletic, V. D., and M. M. Frank. 1995. Complement-immunoglobulin interactions. Curr. Opin. Immunol. 7:41-47.
74. Mitchell, D. A., M. C. Pickering, J. Warren, L. Fossati-Jimack, J. Cortes- Hernandez, H. T. Cook, M. Botto, and M. J. Walport. 2002. C1q deficiency and autoimmunity: the effects of genetic background on disease expression. J. Immunol. 168:2538-2543. (Pubitemid 34171862)
75. Moss, B. 2006. Poxviridae: the viruses and their replication, p. 2849-2883. In D. M. Knipe, P. Howley, D. Giriffin, and R. Lamb (ed.), Fundamental virology, 5th ed. Lippincott Williams & Wilkins, Hagerstown, MD.
76. Moulton, E. A., J. P. Atkinson, and R. M. Buller. 2008. Surviving mousepox infection requires the complement system. PLoS Pathog. 4:e1000249.
77. Ochsenbein, A. F., D. D. Pinschewer, B. Odermatt, M. C. Carroll, H. Hengartner, and R. M. Zinkernagel. 1999. Protective T cell-independent antiviral antibody responses are dependent on complement. J. Exp. Med. 190:1165-1174.
78. Osofsky, S. G., B. H. Thompson, T. F. Lint, and H. Gewurz. 1977. Hereditary deficiency of the third component of complement in a child with fever, skin rash, and arthralgias: response to transfusion of whole blood. J. Pediatr. 90:180-186.
79. Parren, P. W., and D. R. Burton. 2001. The antiviral activity of antibodies in vitro and in vivo. Adv. Immunol. 77:195-262.
80. Pickering, M. C., P. Macor, J. Fish, P. Durigutto, F. Bossi, F. Petry, M. Botto, and F. Tedesco. 2008. Complement C1q and C8β deficiency in an individual with recurrent bacterial meningitis and adult-onset systemic lupus erythematosus-like illness. Rheumatology (Oxford) 47:1588-1589.
81. Pierson, T. C., Q. Xu, S. Nelson, T. Oliphant, G. E. Nybakken, D. H. Fremont, and M. S. Diamond. 2007. The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe 1:135-145. (Pubitemid 46554914)
82. Pütz, M. M., I. Alberini, C. M. Midgley, I. Manini, E. Montomoli, and G. L. Smith. 2005. Prevalence of antibodies to vaccinia virus after smallpox vaccination in Italy. J. Gen. Virol. 86:2955-2960.
83. Pütz, 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.
84. Radwan, A. I., and D. Burger. 1973. The complement-requiring neutralization of equine arteritis virus by late antisera. Virology 51:71-77.
85. 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.
86. Ravetch, J. V., and J. P. Kinet. 1991. Fc receptors. Annu. Rev. Immunol. 9:457-492.
87. Reddy, M. P., C. A. Kinney, M. A. Chaikin, A. Payne, J. Fishman-Lobell, P. Tsui, P. R. Dal Monte, M. L. Doyle, M. R. Brigham-Burke, D. Anderson, M. Reff, R. Newman, N. Hanna, R. W. Sweet, and A. Truneh. 2000. Elimination of Fc receptor-dependent effector functions of a modified IgG4 monoclonal antibody to human CD4. J. Immunol. 164:1925-1933.
88. Roden, R. B., E. M. Weissinger, D. W. Henderson, F. Booy, R. Kirnbauer, J. F. Mushinski, D. R. Lowy, and J. T. Schiller. 1994. Neutralization of bovine papillomavirus by antibodies to L1 and L2 capsid proteins. J. Virol. 68:7570-7574.
89. Sahu, A., S. N. Isaacs, A. M. Soulika, and J. D. Lambris. 1998. Interaction of vaccinia virus complement control protein with human complement proteins: factor I-mediated degradation of C3b to iC3b1 inactivates the alternative complement pathway. J. Immunol. 160:5596-5604. (Pubitemid 28267854)
90. 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 355:164-174.
91. Sette, A., M. Moutaftsi, J. Moyron-Quiroz, M. M. McCausland, D. H. Davies, R. J. Johnston, B. Peters, M. Rafii-El-Idrissi Benhnia, J. Hoffmann, H. P. Su, K. Singh, D. N. Garboczi, S. Head, H. Grey, P. Felgner, and S. Crotty. 2008. Selective CD4+ T cell help for antibody responses to a large viral pathogen: deterministic linkage of specificities. Immunity 28:847-858. (Pubitemid 351778408)
92. Sissons, J. G., and M. B. Oldstone. 1980. Killing of virus-infected cells: the role of antiviral antibody and complement in limiting virus infection. J. Infect. Dis. 142:442-448.
93. Smith, G. L., A. Vanderplasschen, and M. Law. 2002. The formation and function of extracellular enveloped vaccinia virus. J. Gen. Virol. 83:2915-2931.
94. Stollar, V. 1975. Immune lysis of Sindbis virus. Virology 66:620-624.
95. Tao, M. H., R. I. Smith, and S. L. Morrison. 1993. Structural features of human immunoglobulin G that determine isotype-specific differences in complement activation. J. Exp. Med. 178:661-667.
96. Taylor, P. R., E. Seixas, M. J. Walport, J. Langhorne, and M. Botto. 2001. Complement contributes to protective immunity against reinfection by Plasmodium chabaudi chabaudi parasites. Infect. Immun. 69:3853-3859.
97. Tomizuka, K., T. Shinohara, H. Yoshida, H. Uejima, A. Ohguma, S. Tanaka, K. Sato, M. Oshimura, and I. Ishida. 2000. Double trans-chromosomic mice: maintenance of two individual human chromosome fragments containing Ig heavy and kappa loci and expression of fully human antibodies. Proc. Natl. Acad. Sci. USA 97:722-727.
98. Vanderplasschen, A., M. Hollinshead, and G. L. Smith. 1997. Antibodies against vaccinia virus do not neutralize extracellular enveloped virus but prevent virus release from infected cells and comet formation. J. Gen. Virol. 78:2041-2048.
99. Vanderplasschen, A., E. Mathew, M. Hollinshead, R. B. Sim, and G. L. Smith. 1998. Extracellular enveloped vaccinia virus is resistant to complement because of incorporation of host complement control proteins into its envelope. Proc. Natl. Acad. Sci. USA 95:7544-7549.
100. Wagenaar, T. R., and B. Moss. 2007. Association of vaccinia virus fusion regulatory proteins with the multicomponent entry/fusion complex. J. Virol. 81:6286-6293.
101. Walker, B. D., and D. R. Burton. 2008. Toward an AIDS vaccine. Science 320:760-764.
102. Walport, M. J. 2002. Complement and systemic lupus erythematosus. Arthritis Res. 4(Suppl. 3):S279-S293.
103. Walport, M. J., K. A. Davies, and M. Botto. 1998. C1q and systemic lupus erythematosus. Immunobiology 199:265-285.
104. Ward, B. M., and B. Moss. 2000. Golgi network targeting and plasma membrane internalization signals in vaccinia virus B5R envelope protein. J. Virol. 74:3771-3780.
105. Ward, E. S., and V. Ghetie. 1995. The effector functions of immunoglobulins: implications for therapy. Ther. Immunol. 2:77-94.
106. Warren, J., P. Mastroeni, G. Dougan, M. Noursadeghi, J. Cohen, M. J. Walport, and M. Botto. 2002. Increased susceptibility of C1q-deficient mice to Salmonella enterica serovar Typhimurium infection. Infect. Immun. 70:551-557.
107. Welsh, R. M., Jr., P. W. Lampert, P. A. Burner, and M. B. Oldstone. 1976. Antibody-complement interactions with purified lymphocytic choriomeningitis virus. Virology 73:59-71.
108. Wolffe, E. J., S. N. Isaacs, and B. Moss. 1993. Deletion of the vaccinia virus B5R gene encoding a 42-kilodalton membrane glycoprotein inhibits extracellular virus envelope formation and dissemination. J. Virol. 67:4732-4741.
109. 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.
110. Xiao, Y., L. Aldaz-Carroll, A. M. Ortiz, J. C. Whitbeck, E. Alexander, H. Lou, H. L. Davis, T. J. Braciale, R. J. Eisenberg, G. H. Cohen, and S. N. Isaacs. 2007. A protein-based smallpox vaccine protects mice from vaccinia and ectromelia virus challenges when given as a prime and single boost. Vaccine 25:1214-1224. (Pubitemid 46027342)