Therapeutic vaccines and antibodies for treatment of orthopoxvirus infections

Viruses

Volumn 2, Issue 10, 2010, Pages 2381-2403

  Xiao, Yuhong ^a   Isaacs, Stuart N ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Dryvax; Lister; Modified vaccinia ankara (MVA); Monkeypox virus; Monoclonal antibodies; Orthopoxvirus; Post exposure vaccination; Vaccinia immune globulin (VIG); Vaccinia virus; Variola virus

Indexed keywords

ANTIBODY; IMMUNOGLOBULIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY A33; MONOCLONAL ANTIBODY B5; MONOCLONAL ANTIBODY C3; MONOCLONAL ANTIBODY L1; ORTHOPOXVIRUS VACCINE; POLYCLONAL ANTIBODY A33; POLYCLONAL ANTIBODY B5; POLYCLONAL ANTIBODY L1; SMALLPOX VACCINE; UNCLASSIFIED DRUG; VACCINIA ANTIBODY; VACCINIA VACCINE;

ADAPTIVE IMMUNITY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG EXPOSURE; DRUG POTENCY; DRUG TOLERABILITY; ECZEMA; HUMAN; INFECTION PREVENTION; INNATE IMMUNITY; MONKEYPOX; MOUSEPOX; NONHUMAN; ORTHOPOXVIRUS; POXVIRUS INFECTION; PROTECTION; REPEATED DRUG DOSE; REVIEW; SINGLE DRUG DOSE; SMALLPOX; VACCINATION; VACCINIA; VIRUS IMMUNITY;

ANIMALIA; MONKEYPOX VIRUS; ORTHOPOXVIRUS; VACCINIA VIRUS; VARIOLA; VARIOLA VIRUS;

EID: 79952143412     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v2102381     Document Type: Review

References (79)

1. Fenner, F.; Henderson, D.A.; Arita, I.; Jezek, Z.; Ladnyi, I.D. Smallpox and Its Eradication, 1st ed.; World Health Organization: Geneva, Switzerland, 1988; Preface, ix-xii; Chapter 27, 1227-1262.
2. Atlas, R.M. The threat of bioterrorism returns the fear of smallpox. Curr. Opin. Microbiol. 1998, 1, 719-721.
3. Henderson, D.A. The looming threat of bioterrorism. Science 1999, 283, 1279-1282.
4. Hammarlund, E.; Lewis, M.W.; Hansen, S.G.; Strelow, L.I.; Nelson, J.A.; Sexton, G.J.; Hanifin, J.M.; Slifka, M.K. Duration of antiviral immunity after smallpox vaccination. Nat. Med. 2003, 9, 1131-1137.
5. Crotty, S.; Felgner, P.; Davies, H.; Glidewell, J.; Villarreal, L.; Ahmed, R. Cutting edge: Long-term B cell memory in humans after smallpox vaccination. J. Immunol. 2003, 171, 4969-4973.
6. Miller, J.D.; Van der Most, R.G.; Akondy, R.S.; Glidewell, J.T.; Albott, S.; Masopust, D.; Murali-Krishna, K.; Mahar, P.L.; Edupuganti, S.; Lalor, S.; Germon, S.; Del Rio, C.; Mulligan, M.J.; Staprans, S.I.; Altman, J.D.; Feinberg, M.B.; Ahmed, R. Human effector and memory CD8+ T cell responses to smallpox and yellow fever vaccines. Immunity 2008, 28, 710-722.
7. Fulginiti, V.A.; Papier, A.; Lane, J.M.; Neff, J.M.; Henderson, D.A. Smallpox vaccination: A review, part II. Adverse events. Clin. Infect. Dis. 2003, 37, 251-271.
8. Lutwick, L.I. Postexposure prophylaxis. Infect. Dis. Clin. North Am. 1996, 10, 899-915.
9. Dixon, C.W. Smallpox; Churchill: London, UK, 1962; Chapter 14, 296-360.
10. Hanna, W.; Baxby, D. Studies in smallpox and vaccination. 1913. Rev. Med. Virol. 2002, 12, 201-209.
11. Rao, A.R. Smallpox; Korhari Book Depot: Bombay, India; 1972; Chapter 17, 130-150.
12. Heiner, G.G.; Fatima, N.; McCrumb, F.R., Jr. A study of intrafamilial transmission of smallpox. Am. J. Epidemiol. 1971, 94, 316-326.
13. Mack, T.M.; Thomas, D.B.; Ali, A.; Muzaffar Khan, M. Epidemiology of smallpox in West Pakistan. I. Acquired immunity and the distribution of disease. Am. J. Epidemiol. 1972, 95, 157-168.
14. Mortimer, P.P. Can postexposure vaccination against smallpox succeed? Clin. Infect. Dis. 2003, 36, 622-629.
15. Staib, C.; Suezer, Y.; Kisling, S.; Kalinke, U.; Sutter, G. Short-term, but not post-exposure, protection against lethal orthopoxvirus challenge after immunization with modified vaccinia virus Ankara. J. Gen. Virol. 2006, 87, 2917-2921.
16. Stittelaar, K.J.; Neyts, J.; Naesens, L.; van Amerongen, G.; Van Lavieren, R.F.; Holy, A.; De Clercq, E.; Niesters, H.G.; Fries, E.; Maas, C.; Mulder, P.G.; Van der Zeijst, B.A.; Osterhaus, A.D. Antiviral treatment is more effective than smallpox vaccination upon lethal monkeypox virus infection. Nature 2006, 439, 745-748.
17. Paran, N.; Suezer, Y.; Lustig, S.; Israely, T.; Schwantes, A.; Melamed, S.; Katz, L.; Preuss, T.; Hanschmann, K.M.; Kalinke, U.; Erez, N.; Levin, R.; Velan, B.; Lower, J.; Shafferman, A.; Sutter, G. Postexposure immunization with modified vaccinia virus Ankara or conventional Lister vaccine provides solid protection in a murine model of human smallpox. J. Infect. Dis. 2009, 199, 39-48.
18. Kennedy, J.S.; Greenberg, R.N. IMVAMUNE: Modified vaccinia Ankara strain as an attenuated smallpox vaccine. Expert Rev. Vaccines 2009, 8, 13-24.
19. Earl, P.L.; Americo, J.L.; Wyatt, L.S.; Espenshade, O.; Bassler, J.; Gong, K.; Lin, S.; Peters, E.; Rhodes, L., Jr.; Spano, Y.E.; Silvera, P.M.; Moss, B. Rapid protection in a monkeypox model by a single injection of a replication-deficient vaccinia virus. Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 10889-10894.
20. Samuelsson, C.; Hausmann, J.; Lauterbach, H.; Schmidt, M.; Akira, S.; Wagner, H.; Chaplin, P.; Suter, M.; O'Keeffe, M.; Hochrein, H. Survival of lethal poxvirus infection in mice depends on TLR9, and therapeutic vaccination provides protection. J. Clin. Invest. 2008, 118, 1776-1784.
21. Lauterbach, H.; Kassub, R.; Patzold, J.; Korner, J.; Bruckel, M.; Verschoor, A.; Chaplin, P.; Suter, M.; Hochrein, H. Immune requirements of post-exposure immunization with modified vaccinia Ankara of lethally infected mice. PLoS ONE 2010, 5, e9659.
22. Panchanathan, V.; Chaudhri, G.; Karupiah, G. Interferon function is not required for recovery from a secondary poxvirus infection. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 12921-12926.
23. Panchanathan, V.; Chaudhri, G.; Karupiah, G. Protective immunity against secondary poxvirus infection is dependent on antibody but not on CD4 or CD8 T-cell function. J. Virol. 2006, 80, 6333-6338.
24. Panchanathan, V.; Chaudhri, G.; Karupiah, G. Antiviral protection following immunization correlates with humoral but not cell-mediated immunity. Immun. Cell Biol. 2010, 88, 461-467.
25. Wittek, R. Vaccinia immune globulin: Current policies, preparedness, and product safety and efficacy. Int. J. Infect. Dis. 2006, 10, 193-201.
26. Hopkins, R.J.; Kramer, W.G.; Blackwelder, W.C.; Ashtekar, M.; Hague, L.; Winker-La Roche, S.D.; Berezuk, G.; Smith, D.; Leese, P.T. Safety and pharmacokinetic evaluation of intravenous vaccinia immune globulin in healthy volunteers. Clin. Infect. Dis. 2004, 39, 759-766.
27. Napolitano, P.G.; Ryan, M.A.; Grabenstein, J.D. Pregnancy discovered after smallpox vaccination: Is vaccinia immune globulin appropriate? Am. J. Obstet. Gynecol. 2004, 191, 1863-1867.
28. Bell, E.; Shamim, M.; Whitbeck, J.C.; Sfyroera, G.; Lambris, J.D.; Isaacs, S.N. Antibodies against the extracellular enveloped virus B5R protein are mainly responsible for the EEV neutralizing capacity of vaccinia immune globulin. Virology 2004, 325, 425-431.
29. Putz, M.M.; Midgley, C.M.; Law, M.; Smith, G.L. Quantification of antibody responses against multiple antigens of the two infectious forms of Vaccinia virus provides a benchmark for smallpox vaccination. Nat. Med. 2006, 12, 1310-1315.
30. Adamo, J.E.; Meseda, C.A.; Weir, J.P.; Merchlinsky, M.J. Smallpox vaccines induce antibodies to the immunomodulatory, secreted vaccinia virus complement control protein. J. Gen. Virol. 2009, 90, 2604-2608.
31. Davies, D.H.; Liang, X.; Hernandez, J.E.; Randall, A.; Hirst, S.; Mu, Y.; Romero, K.M.; Nguyen, T.T.; Kalantari-Dehaghi, M.; Crotty, S.; Baldi, P.; Villarreal, L.P.; Felgner, P.L. Profiling the humoral immune response to infection by using proteome microarrays: High-throughput vaccine and diagnostic antigen discovery. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 547-552.
32. Jones-Trower, A.; Garcia, A.; Meseda, C.A.; He, Y.; Weiss, C.; Kumar, A.; Weir, J.P.; Merchlinsky, M. Identification and preliminary characterization of vaccinia virus (Dryvax) antigens recognized by vaccinia immune globulin. Virology 2005, 343, 128-140.
33. Kempe, C.H. Studies on smallpox and complications of smallpox vaccination. Pediatrics 1960, 26, 176-189.
34. Kempe, C.H. Passive immunity to vaccinia in newborns. I. Placental transmission of antibodies. Yale J. Biol. Med. 1952, 24, 328-333.
35. Bray, M. Henry Kempe and the birth of vaccinia immune globulin. Clin. Infect. Dis. 2004, 39, 767-769.
36. Fulginiti, V.A.; Hathaway, W.E.; Pearlman, D.; Sieber, O.; Eller, J.; Joyner, J.; Robinson, A. Progressive vaccinia in immunologically deficient individuals. Birth Defects 1968, 4, 128-151.
37. Kempe, C.H. Acceptance of the Howland award. Pediat. Res. 1980, 14, 1155-1161.
38. Howell, M.D.; Jones, J.F.; Kisich, K.O.; Streib, J.E.; Gallo, R.L.; Leung, D.Y. Selective killing of vaccinia virus by LL-37: Implications for eczema vaccinatum. J. Immunol. 2004, 172, 1763-1767.
39. Kawakami, Y.; Tomimori, Y.; Yumoto, K.; Hasegawa, S.; Ando, T.; Tagaya, Y.; Crotty, S.; Kawakami, T. Inhibition of NK cell activity by IL-17 allows vaccinia virus to induce severe skin lesions in a mouse model of eczema vaccinatum. J. Exp. Med. 2009, 206, 1219-1225.
40. Freyschmidt, E.J.; Mathias, C.B.; Diaz, N.; MacArthur, D.H.; Laouar, A.; Manjunath, N.; Hofer, M.D.; Wurbel, M.A.; Campbell, J.J.; Chatila, T.A.; Oettgen, H.C. Skin inflammation arising from cutaneous regulatory T cell deficiency leads to impaired viral immune responses. J. Immunol. 2010, 185, 1295-1302.
41. Kempe, C.H.; Berge, T.O.; England, B. Hyperimmune vaccinal gamma globulin: Source, evaluation, and use in prophylaxis and therapy. Pediatrics 1956, 18, 177-188.
42. CDC. Household transmission of vaccinia virus from contact with a military smallpox vaccinee- Illinois and Indiana, 2007. MMWR Morb. Mortal. Wkly. Rep. 2007, 56, 478-481.
43. Barbero, G.J.; Gray, A.; Scott, T.F.; Kempe, C.H. Vaccinia gangrenosa treated with hyperimmune vaccinal gamma globulin. Pediatrics 1955, 16, 609-618.
44. Bray, M.; Wright, M.E. Progressive vaccinia. Clin. Infect. Dis. 2003, 36, 766-774.
45. Keane, J.T.; James, K.; Blankenship, M.L.; Pearson, R.W. Progressive vaccinia associated with combined variable immunodeficiency. Arch. Dermatol. 1983, 119, 404-408.
46. Hanlon, C.A.; Niezgoda, M.; Shankar, V.; Niu, H.S.; Koprowski, H.; Rupprecht, C.E. A recombinant vaccinia-rabies virus in the immunocompromised host: Oral innocuity, progressive parenteral infection, and therapeutics. Vaccine 1997, 15, 140-148.
47. Bauer, D.J.; St. Vincent, L.; Kempe, C.H.; Young, P.A.; Downie, A.W. Prophylaxis of smallpox with methisazone. Am. J. Epidemiol. 1969, 90, 130-145.
48. Shearer, J.D.; Siemann, L.; Gerkovich, M.; House, R.V. Biological activity of an intravenous preparation of human vaccinia immune globulin in mouse models of vaccinia virus infection. Antimicrob. Agents Chemother. 2005, 49, 2634-2641.
49. Belyakov, I.M.; Earl, P.; Dzutsev, A.; Kuznetsov, V.A.; Lemon, M.; Wyatt, L.S.; Snyder, J.T.; Ahlers, J.D.; Franchini, G.; Moss, B.; Berzofsky, J.A. Shared modes of protection against poxvirus infection by attenuated and conventional smallpox vaccine viruses. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 9458-9463.
50. Xu, R.; Johnson, A.J.; Liggitt, D.; Bevan, M.J. Cellular and humoral immunity against vaccinia virus infection of mice. J. Immunol. 2004, 172, 6265-6271.
51. Kempe, C.H.; Bowles, C.; Meiklejohn, G.; Berge, T.O.; St Vincent, L.; Babu, B.V.; Govindarajan, S.; Ratnakannan, N.R.; Downie, A.W.; Murthy, V.R. The use of vaccinia hyperimmune gamma-globulin in the prophylaxis of smallpox. Bull. World Health Organ. 1961, 25, 41-48.
52. Hobday, T.L. Antivaccinial gamma-globulin in the control of smallpox. Lancet 1962, 1, 907-908.
53. Hogben, G.H.; Mc, K.G.; Nicol, C.G. Smallpox in Tottenham; 1957. Lancet 1958, 1, 1061-1064.
54. Peirce, E.R.; Melville, F.S.; Downie, A.W.; Duckworth, M.J. Anti-vaccinial gamma-globulin in smallpox prophylaxis. Lancet 1958, 2, 635-638.
55. Semple, A.B.; Parry, W.H.; Hobday, T.L. Antivaccinial gamma-globulin; a further report on smallpox prophylaxis. Lancet 1959, 2, 34.
56. Marennikova, S.S. The use of hyperimmune antivaccinia gamma-globulin for the prevention and treatment of smallpox. Bull. World Health Organ. 1962, 27, 325-330.
57. Law, M.; Putz, M.M.; Smith, G.L. An investigation of the therapeutic value of vaccinia-immune IgG in a mouse pneumonia model. J. Gen. Virol. 2005, 86, 991-1000.
58. Lustig, S.; Maik-Rachline, G.; Paran, N.; Melamed, S.; Israely, T.; Erez, N.; Orr, N.; Reuveny, S.; Ordentlich, A.; Laub, O.; Shafferman, A.; Velan, B. Effective post-exposure protection against lethal orthopoxviruses infection by vaccinia immune globulin involves induction of adaptive immune response. Vaccine 2009, 27, 1691-1699.
59. CDC. Progressive vaccinia in a military smallpox vaccinee-United States, 2009. MMWR Morb. Mortal. Wkly. Rep. 2009, 58, 532-536.
60. Smith, G.L.; Vanderplasschen, A.; Law, M. The formation and function of extracellular enveloped vaccinia virus. J. Gen. Virol. 2002, 83, 2915-2931.
61. Condit, R.C.; Moussatche, N.; Traktman, P. In a nutshell: Structure and assembly of the vaccinia virion. Adv. Virus Res. 2006, 66, 31-124.
62. Moss, B. Poxvirus entry and membrane fusion. Virology 2006, 344, 48-54.
63. Rodriguez, J.F.; Janeczko, R.; Esteban, M. Isolation and characterization of neutralizing monoclonal antibodies to vaccinia virus. J. Virol. 1985, 56, 482-488.
64. Nelson, G.E.; Sisler, J.R.; Chandran, D.; Moss, B. Vaccinia virus entry/fusion complex subunit A28 is a target of neutralizing and protective antibodies. Virology 2008, 380, 394-401.
65. Hsiao, J.C.; Chung, C.S.; Chang, W. Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. J. Virol. 1999, 73, 8750-8761.
66. Davies, D.H.; McCausland, M.M.; Valdez, C.; Huynh, D.; Hernandez, J.E.; Mu, Y.; Hirst, S.; Villarreal, L.; Felgner, P.L.; Crotty, S. Vaccinia virus H3L envelope protein is a major target of neutralizing antibodies in humans and elicits protection against lethal challenge in mice. J. Virol. 2005, 79, 11724-11733.
67. Wolffe, E.J.; Vijaya, S.; Moss, B. A myristylated membrane protein encoded by the vaccinia virus L1R open reading frame is the target of potent neutralizing monoclonal antibodies. Virology 1995, 211, 53-63.
68. Ichihashi, Y.; Oie, M. Neutralizing epitope on penetration protein of vaccinia virus. Virology 1996, 220, 491-494.
69. Galmiche, M.C.; Goenaga, J.; Wittek, R.; Rindisbacher, L. Neutralizing and protective antibodies directed against vaccinia virus envelope antigens. Virology 1999, 254, 71-80.
70. Ramirez, J.C.; Tapia, E.; Esteban, M. 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. 2002, 83, 1059-1067.
71. Lustig, S.; Fogg, C.; Whitbeck, J.C.; Eisenberg, R.J.; Cohen, G.H.; Moss, B. 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. 2005, 79, 13454-13462.
72. Xiao, Y.; Isaacs, S.N. University of Pennsylvania, Philadelphia, PA. Unpublished work, 2005.
73. Chen, Z.; Earl, P.; Americo, J.; Damon, I.; Smith, S.K.; Zhou, Y.H.; Yu, F.; Sebrell, A.; Emerson, S.; Cohen, G.; Eisenberg, R.J.; Svitel, J.; Schuck, P.; Satterfield, W.; Moss, B.; Purcell, R. Chimpanzee/human mAbs to vaccinia virus B5 protein neutralize vaccinia and smallpox viruses and protect mice against vaccinia virus. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 1882-1887.
74. Chen, Z.; Earl, P.; Americo, J.; Damon, I.; Smith, S.K.; Yu, F.; Sebrell, A.; Emerson, S.; Cohen, G.; Eisenberg, R.J.; Gorshkova, I.; Schuck, P.; Satterfield, W.; Moss, B.; Purcell, R. 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. 2007, 81, 8989-8995.
75. Lustig, S.; Fogg, C.; Whitbeck, J.C.; Moss, B. Synergistic neutralizing activities of antibodies to outer membrane proteins of the two infectious forms of vaccinia virus in the presence of complement. Virology 2004, 328, 30-35.
76. Benhnia, M.R.; McCausland, M.M.; Moyron, J.; Laudenslager, J.; Granger, S.; Rickert, S.; Koriazova, L.; Kubo, R.; Kato, S.; Crotty, S. Vaccinia virus extracellular enveloped virion neutralization in vitro and protection in vivo depend on complement. J. Virol. 2009, 83, 1201-1215.
77. Benhnia, M.R.; McCausland, M.M.; Laudenslager, J.; Granger, S.W.; Rickert, S.; Koriazova, L.; Tahara, T.; Kubo, R.T.; Kato, S.; Crotty, S. Heavily isotype-dependent protective activities of human antibodies against vaccinia virus extracellular virion antigen B5. J. Virol. 2009, 83, 12355-12367.
78. Seet, B.T.; Johnston, J.B.; Brunetti, C.R.; Barrett, J.W.; Everett, H.; Cameron, C.; Sypula, J.; Nazarian, S.H.; Lucas, A.; McFadden, G. Poxviruses and immune evasion. Annu. Rev. Immunol. 2003, 21, 377-423.
79. Xu, R.H.; Cohen, M.; Tang, Y.; Lazear, E.; Whitbeck, J.C.; Eisenberg, R.J.; Cohen, G.H.; Sigal, L.J. The orthopoxvirus type I IFN binding protein is essential for virulence and an effective target for vaccination. J. Exp. Med. 2008, 205, 981-992.