Antibody inhibition of a viral type 1 interferon decoy receptor cures a viral disease by restoring interferon signaling in the liver

PLoS Pathogens

Volumn 8, Issue 1, 2012, Pages

  Xu, Ren Huan ^a   Rubio, Daniel ^a,b   Roscoe, Felicia ^a   Krouse, Tracy E ^c   Truckenmiller, Mary Ellen ^c   Norbury, Christopher C ^c   Hudson, Paul N ^d   Damon, Inger K ^d   Alcamí, Antonio ^b   Sigal, Luis J ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b CSIC   (Spain)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

^d NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIVIRAL THERAPY; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; ECTROMELIA VIRUS; FEMALE; IN VIVO STUDY; LIVER; LIVER PROTECTION; MOUSE; MOUSEPOX; NONHUMAN; SIGNAL TRANSDUCTION; SPLEEN;

ANIMALS; ANTIBODIES, VIRAL; CELL LINE; CRICETINAE; ECTROMELIA VIRUS; ECTROMELIA, INFECTIOUS; FEMALE; LIVER; MICE; MICE, INBRED BALB C; MICE, SCID; RECEPTOR, INTERFERON ALPHA-BETA; SPLEEN; VARIOLA VIRUS; VIRAL PROTEINS; VIRULENCE FACTORS; VIRUS ATTACHMENT;

ECTROMELIA VIRUS; VARIOLA VIRUS;

EID: 84857462069     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002475     Document Type: Article

References (65)

1. Theofilopoulos AN, Baccala R, Beutler B, Kono DH, (2005) Type I interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol 23: 307-336.
2. Fields BN, Knipe DM, Howley PM, Griffin DE, eds. (2001) Fields' Virology.4th edition. Philadelphia Lippincott Williams & Wilkins.
3. Flint SJ, American Society for Microbiology. (2009) Principles of virology. Washington, DC ASM Press.
4. Symons JA, Alcami A, Smith GL, (1995) Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 81: 551-560.
5. Smith VP, Alcami A, (2002) Inhibition of interferons by ectromelia virus. J Virol 76: 1124-1134.
6. Fernandez de Marco Mdel M, Alejo A, Hudson P, Damon IK, Alcami A, (2010) The highly virulent variola and monkeypox viruses express secreted inhibitors of type I interferon. FASEB J 24: 1479-1488.
7. Colamonici OR, Domanski P, Sweitzer SM, Larner A, Buller RM, (1995) Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon alpha transmembrane signaling. J Biol Chem 270: 15974-15978.
8. Ueda Y, Morikawa S, Matsuura Y, (1990) Identification and nucleotide sequence of the gene encoding a surface antigen induced by vaccinia virus. Virology 177: 588-594.
9. Assarsson E, Greenbaum JA, Sundstrom M, Schaffer L, Hammond JA, et al. (2008) Kinetic analysis of a complete poxvirus transcriptome reveals an immediate-early class of genes. Proc Natl Acad Sci U S A 105: 2140-2145.
10. Xu RH, Cohen M, Tang Y, Lazear E, Whitbeck JC, et al. (2008) The orthopoxvirus type I IFN binding protein is essential for virulence and an effective target for vaccination. J Exp Med 205: 981-992.
11. Burton DR, (2002) Antibodies, viruses and vaccines. Nat Rev Immunol 2: 706-713.
12. Amanna IJ, Slifka MK, (2009) Wanted, dead or alive: new viral vaccines. Antiviral Res 84: 119-130.
13. Benhnia MR, McCausland MM, Laudenslager J, Granger SW, Rickert S, et al. (2009) Heavily isotype-dependent protective activities of human antibodies against vaccinia virus extracellular virion antigen B5. J Virol 83: 12355-12367.
14. Walker PD, (1992) Bacterial vaccines: old and new, veterinary and medical. Vaccine 10: 977-990.
15. Alcami A, (2003) Viral mimicry of cytokines, chemokines and their receptors. Nat Rev Immunol 3: 36-50.
16. Virgin HW, (2007) Pathogenesis of viral infection. In: Fields BN, Knipe DM, Howley PM, editors. Fields' virology 5th edition. Philadelphia Wolters kluwer/Lippincott Williams & Wilkins pp. 335-336.
17. Fenner F, (1949) Mouse-pox; infectious ectromelia of mice; a review. J Immunol 63: 341-373.
18. Bosma GC, Custer RP, Bosma MJ, (1983) A severe combined immunodeficiency mutation in the mouse. Nature 301: 527-530.
19. Alcami A, Symons JA, Smith GL, (2000) The vaccinia virus soluble alpha/beta interferon (IFN) receptor binds to the cell surface and protects cells from the antiviral effects of IFN. J Virol 74: 11230-11239.
20. McEvoy LM, Sun H, Frelinger JG, Butcher EC, (1997) Anti-CD43 inhibition of T cell homing. J Exp Med 185: 1493-1498.
21. Davison AJ, Moss B, (1989) Structure of vaccinia virus early promoters. J Mol Biol 210: 749-769.
22. Roper RL, Wolffe EJ, Weisberg A, Moss B, (1998) The envelope protein encoded by the A33R gene is required for formation of actin-containing microvilli and efficient cell-to-cell spread of vaccinia virus. J Virol 72: 4192-4204.
23. Nimmerjahn F, Ravetch JV, (2008) Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 8: 34-47.
24. Parren P, Burton DR, (2001) The antiviral activity of antibodies in vitro and in vivo. Adv Immunol 77: 195-262.
25. Liptakova H, Kontsekova E, Alcami A, Smith GL, Kontsek P, (1997) Analysis of an interaction between the soluble vaccinia virus-coded type I interferon (IFN)-receptor and human IFN-alpha1 and IFN-alpha2. Virology 232: 86-90.
26. Palframan RT, Jung S, Cheng G, Weninger W, Luo Y, et al. (2001) Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J Exp Med 194: 1361-1373.
27. Sallusto F, Baggiolini M, (2008) Chemokines and leukocyte traffic. Nat Immunol 9: 949-952.
28. Thelen M, Stein JV, (2008) How chemokines invite leukocytes to dance. Nat Immunol 9: 953-959.
29. Lee SH, Girard S, Macina D, Busa M, Zafer A, et al. (2001) Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat Genet 28: 42-45.
30. Willfuhr KU, Hirschfeld U, Westermann J, Pabst R, (1990) The in vitro lymphocyte/endothelium binding assay. An improved method employing light microscopy. J Immunol Methods 130: 201-207.
31. Medzhitov R, Janeway C Jr, (2000) Innate immune recognition: mechanisms and pathways. Immunol Rev 173: 89-97.
32. Fang M, Lanier LL, Sigal LJ, (2008) A role for NKG2D in NK cell-mediated resistance to poxvirus disease. PLoS Pathog 4: e30.
33. Fang M, Roscoe F, Sigal LJ, (2010) Age-dependent susceptibility to a viral disease due to decreased natural killer cell numbers and trafficking. J Exp Med 207: 2369-2381.
34. Janeway C, (2005) Immunobiology: the immune system in health and disease. New York Garland Science. xxiii, 823.
35. Xu R-H, Fang M, Klein-Szanto A, Sigal LJ, (2007) Memory CD8+ T cells are gatekeepers of the lymph node draining the site of viral infection. Proc Natl Acad Sci U S A 104: 10992-10997.
36. Seet BT, Johnston JB, Brunetti CR, Barrett JW, Everett H, et al. (2003) Poxviruses and immune evasion. Annu Rev Immunol 21: 377-423.
37. Ploegh HL, (1998) Viral strategies of immune evasion. Science 280: 248-253.
38. Alcami A, Koszinowski UH, (2000) Viral mechanisms of immune evasion. Trends Microbiol 8: 410-418.
39. Alcami A, (2010) The interaction of viruses with host immune defenses. Curr Opin Microbiol 13: 501-502.
40. Zinkernagel RM, Hengartner H, (2006) Protective 'immunity' by pre-existent neutralizing antibody titers and preactivated T cells but not by so-called 'immunological memory'. Immunol Rev 211: 310-319.
41. Mack TM, Noble J Jr, Thomas DB, (1972) A prospective study of serum antibody and protection against smallpox. Am J Trop Med Hyg 21: 214-218.
42. Sarkar JK, Mitra AC, Mukherjee MK, (1975) The minimum protective level of antibodies in smallpox. Bull World Health Organ 52: 307-311.
43. Benhnia MR, McCausland MM, Moyron J, Laudenslager J, Granger S, et al. (2009) Vaccinia virus extracellular enveloped virion neutralization in vitro and protection in vivo depend on complement. J Virol 83: 1201-1215.
44. Panchanathan V, Chaudhri G, Karupiah G, (2005) Interferon function is not required for recovery from a secondary poxvirus infection. Proc Natl Acad Sci U S A 102: 12921-12926.
45. Paran N, Suezer Y, Lustig S, Israely T, Schwantes A, et al. (2009) Postexposure immunization with modified vaccinia virus Ankara or conventional Lister vaccine provides solid protection in a murine model of human smallpox. J Infect Dis 199: 39-48.
46. Yang G, Pevear DC, Davies MH, Collett MS, Bailey T, et al. (2005) An orally bioavailable antipoxvirus compound (ST-246) inhibits extracellular virus formation and protects mice from lethal orthopoxvirus Challenge. J Virol 79: 13139-13149.
47. Ciesla SL, Trahan J, Wan WB, Beadle JR, Aldern KA, et al. (2003) Esterification of cidofovir with alkoxyalkanols increases oral bioavailability and diminishes drug accumulation in kidney. Antiviral Res 59: 163-171.
48. Huggins J, Goff A, Hensley L, Mucker E, Shamblin J, et al. (2009) Non-human primates are protected from smallpox virus or monkeypox virus challenges by the antiviral drug ST-246. Antimicrob Agents Chemother 53: 2620-2625.
49. De Clercq E, (2009) Another ten stories in antiviral drug discovery (part C): "Old" and "new" antivirals, strategies, and perspectives. Med Res Rev 29: 611-645.
50. Jordan R, Goff A, Frimm A, Corrado ML, Hensley LE, et al. (2009) ST-246(R) Antiviral Efficacy in a Non-Human Primate Monkeypox Model: Determination of the Minimal Effective Dose and Human Dose Justification. Antimicrob Agents Chemother 53: 1817-1822.
51. Parker S, Touchette E, Oberle C, Almond M, Robertson A, et al. (2008) Efficacy of therapeutic intervention with an oral ether-lipid analogue of cidofovir (CMX001) in a lethal mousepox model. Antiviral Res 77: 39-49.
52. Parker S, Schriewer J, Oberle C, Robertson A, Lanier R, et al. (2008) Using biomarkers to stage disease progression in a lethal mousepox model treated with CMX001. Antivir Ther 13: 863-873.
53. Quenelle DC, Buller RM, Parker S, Keith KA, Hruby DE, et al. (2007) Efficacy of delayed treatment with ST-246 given orally against systemic orthopoxvirus infections in mice. Antimicrob Agents Chemother 51: 689-695.
54. Buller RM, Owens G, Schriewer J, Melman L, Beadle JR, et al. (2004) Efficacy of oral active ether lipid analogs of cidofovir in a lethal mousepox model. Virology 318: 474-481.
55. Gammon DB, Snoeck R, Fiten P, Krecmerova M, Holy A, et al. (2008) Mechanism of antiviral drug resistance of vaccinia virus: identification of residues in the viral DNA polymerase conferring differential resistance to antipoxvirus drugs. J Virol 82: 12520-12534.
56. Becker MN, Obraztsova M, Kern ER, Quenelle DC, Keith KA, et al. (2008) Isolation and characterization of cidofovir resistant vaccinia viruses. Virol J 5: 58.
57. Kornbluth RS, Smee DF, Sidwell RW, Snarsky V, Evans DH, et al. (2006) Mutations in the E9L polymerase gene of cidofovir-resistant vaccinia virus strain WR are associated with the drug resistance phenotype. Antimicrob Agents Chemother 50: 4038-4043.
58. Andrei G, Gammon DB, Fiten P, De Clercq E, Opdenakker G, et al. (2006) Cidofovir resistance in vaccinia virus is linked to diminished virulence in mice. J Virol 80: 9391-9401.
59. Smee DF, Sidwell RW, Kefauver D, Bray M, Huggins JW, (2002) Characterization of wild-type and cidofovir-resistant strains of camelpox, cowpox, monkeypox, and vaccinia viruses. Antimicrob Agents Chemother 46: 1329-1335.
60. Fang M, Sigal LJ, (2005) Antibodies and CD8+ T Cells Are Complementary and Essential for Natural Resistance to a Highly Lethal Cytopathic Virus. J Immunol 175: 6829-6836.
61. Fang M, Sigal LJ, (2006) Direct CD28 Costimulation Is Required for CD8+ T Cell-Mediated Resistance to an Acute Viral Disease in a Natural Host. J Immunol 177: 8027-8036.
62. Fang M, Cheng H, Dai Z, Bu Z, Sigal LJ, (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.
63. McWhirter SM, Barbalat R, Monroe KM, Fontana MF, Hyodo M, et al. (2009) A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J Exp Med 206: 1899-1911.
64. Fang M, Sigal L, (2010) Studying NK cell responses to ectromelia virus infections in mice. Methods Mol Biol 612: 411-428.
65. Winer J, Jung CK, Shackel I, Williams PM, (1999) Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem 270: 41-49.