Development of eczema vaccinatum in atopic mouse models and efficacy of MVA vaccination against lethal poxviral infection

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Knitlova, Jarmila ^a   Hajkova, Vera ^a   Voska, Ludek ^b   Elsterova, Jana ^a,c   Obrova, Barbora ^a   Melkova, Zora ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b INSTITUTE FOR CLINICAL AND EXPERIMENTAL MEDICINE   (Czech Republic)

^c UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

MODIFIED VACCINIA VIRUS ANKARA 5T4 VACCINE; OVALBUMIN; SMALLPOX VACCINE; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATOPIC DERMATITIS; CONTROLLED STUDY; DISEASE COURSE; DRUG EFFICACY; ECZEMA; ECZEMA VACCINATUM; EOSINOPHIL; FEMALE; MALE; MAST CELL; MOUSE; MOUSE MODEL; MOUSE STRAIN; NONHUMAN; POXVIRUS INFECTION; SINGLE DRUG DOSE; SKIN DEFECT; SKIN SENSITIZATION; VACCINATION; VACCINIA VIRUS; VIRUS STRAIN; ANIMAL; BLOOD; DISEASE MODEL; GENETICS; IMMUNIZATION; IMMUNOLOGY; KAPOSI VARICELLIFORM ERUPTION; MORTALITY; PATHOLOGY; POXVIRIDAE INFECTIONS; SKIN;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; DERMATITIS, ATOPIC; DISEASE MODELS, ANIMAL; FEMALE; IMMUNIZATION; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; KAPOSI VARICELLIFORM ERUPTION; MALE; MICE; POXVIRIDAE INFECTIONS; SKIN; SMALLPOX VACCINE; VACCINIA VIRUS;

EID: 84915822406     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114374     Document Type: Article

References (55)

1. Artenstein AW (2008) New generation smallpox vaccines: a review of preclinical and clinical data. Rev Med Virol 18: 217-231.
2. Nalca A, Zumbrun EE (2010) ACAM2000: the new smallpox vaccine for United States Strategic National Stockpile. Drug Des Devel Ther 4: 71-79.
3. Frey SE, Newman FK, Kennedy JS, Sobek V, Ennis FA, et al. (2007) Clinical and immunologic responses to multiple doses of IMVAMUNE (Modified Vaccinia Ankara) followed by Dryvax challenge. Vaccine 25: 8562-8573.
4. von Krempelhuber A, Vollmar J, Pokorny R, Rapp P, Wulff N, et al. (2010) A randomized, doubleblind, dose-finding Phase II study to evaluate immunogenicity and safety of the third generation smallpox vaccine candidate IMVAMUNE. Vaccine 28: 1209-1216.
5. Stittelaar KJ, van Amerongen G, Kondova I, Kuiken T, van Lavieren RF, et al. (2005) Modified vaccinia virus Ankara protects macaques against respiratory challenge with monkeypox virus. J Virol 79: 7845-7851.
6. Townsend MB, Keckler MS, Patel N, Davies DH, Felgner P, et al. (2012) Humoral Immunity to Smallpox Vaccines and Monkeypox virus Challenge; Proteomic Assessment and Clinical Correlations. J Virol doi: 101128/JVI02089-12.
7. Davies DH, Wyatt LS, Newman FK, Earl PL, Chun S, et al. (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.
8. Arness MK, Eckart RE, Love SS, Atwood JE, Wells TS, et al. (2004) Myopericarditis following smallpox vaccination. Am J Epidemiol 160: 642-651.
9. Marcinak J, Vora S, Weber S, Thomson K, Garcia-Houchins S, et al. (2007) Household transmission of vaccinia virus from contact with a military smallpox vaccine-Illinois and Indiana, 2007. MMWR Morb Mortal Wkly Rep 56: 478-481.
10. Wertheimer ER, Olive DS, Brundage JF, Clark LL (2012) Contact transmission of vaccinia virus from smallpox vaccinees in the United States, 2003-2011. Vaccine 30: 985-988.
11. Neff JM, Lane JM, Fulginiti VA, Henderson DA (2002) Contact vaccinia-transmission of vaccinia from smallpox vaccination. Jama 288: 1901-1905.
12. Becker Y (2003) Vaccinia virus pathogenicity in atopic dermatitis is caused by allergen-induced immune response that prevents the antiviral cellular and humoral immunity. Virus Genes 27: 269-282.
13. Leung DY, Bieber T (2003) Atopic dermatitis. Lancet 361: 151-160.
14. De Benedetto A, Agnihothri R, McGirt LY, Bankova LG, Beck LA (2009) Atopic dermatitis: a disease caused by innate immune defects? J Invest Dermatol 129: 14-30.
15. Kawakami T, Ando T, Kimura M, Wilson BS, Kawakami Y (2009) Mast cells in atopic dermatitis. Curr Opin Immunol 21: 666-678.
16. Gutermuth J, Ollert M, Ring J, Behrendt H, Jakob T (2004) Mouse models of atopic eczema critically evaluated. Int Arch Allergy Immunol 135: 262-276.
17. Shiohara T, Hayakawa J, Mizukawa Y (2004) Animal models for atopic dermatitis: are they relevant to human disease? J Dermatol Sci 36: 1-9.
18. Vestergaard C, Yoneyama H, Matsushima K (2000) The NC/Nga mouse: a model for atopic dermatitis. Mol Med Today 6: 209-210.
19. Spergel JM, Mizoguchi E, Brewer JP, Martin TR, Bhan AK, et al. (1998) Epicutaneous sensitization with protein antigen induces localized allergic dermatitis and hyperresponsiveness to methacholine after single exposure to aerosolized antigen in mice. J Clin Invest 101: 1614-1622.
20. Jin H, He R, Oyoshi M, Geha RS (2009) Animal models of atopic dermatitis. J Invest Dermatol 129: 31-40.
21. Watanabe H, Numata K, Ito T, Takagi K, Matsukawa A (2004) Innate immune response in Th1- and Th2-dominant mouse strains. Shock 22: 460-466.
22. Kawakami Y, Tomimori Y, Yumoto K, Hasegawa S, Ando T, et al. (2009) 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 206: 1219-1225.
23. Oyoshi MK, Elkhal A, Kumar L, Scott JE, Koduru S, et al. (2009) Vaccinia virus inoculation in sites of allergic skin inflammation elicits a vigorous cutaneous IL-17 response. Proc Natl Acad Sci U S A 106: 14954-14959.
24. Scott JE, ElKhal A, Freyschmidt EJ, MacArthur DH, McDonald D, et al. (2007) Impaired immune response to vaccinia virus inoculated at the site of cutaneous allergic inflammation. J Allergy Clin Immunol 120: 1382-1388.
25. Meseda CA, Garcia AD, Kumar A, Mayer AE, Manischewitz J, et al. (2005) Enhanced immunogenicity and protective effect conferred by vaccination with combinations of modified vaccinia virus Ankara and licensed smallpox vaccine Dryvax in a mouse model. Virology 339: 164-175.
26. Nemeckova S, Hainz P, Otahal P, Gabriel P, Sroller V, et al. (2001) Early gene expression of vaccinia virus strains replicating (Praha) and non-replicating (modified vaccinia virus strain Ankara, MVA) in mammalian cells. Acta Virol 45: 243-247.
27. Kutinova L, Ludvikova V, Simonova V, Otavova M, Krystofova J, et al. (1995) Search for optimal parent for recombinant vaccinia virus vaccines. Study of three vaccinia virus vaccinal strains and several virus lines derived from them. Vaccine 13: 487-493.
28. Kutinova L, Ludvikova V, Krystofova J, Otavova M, Simonova V, et al. (1996) Influence of the parental virus strain on the virulence and immunogenicity of recombinant vaccinia viruses expressing HBV preS2-S protein or VZV glycoprotein I. Vaccine 14: 1045-1052.
29. Liskova J, Knitlova J, Honner R, Melkova Z (2011) Apoptosis and necrosis in vaccinia virus-infected HeLa G and BSC-40 cells. Virus Res 160: 40-50.
30. Kalbacova M, Spisakova M, Liskova J, Melkova Z (2008) Lytic infection with vaccinia virus activates caspases in a Bcl-2-inhibitable manner. Virus Res 135: 53-63.
31. Joklik WK (1962) The purification fo four strains of poxvirus. Virology 18: 9-18.
32. Barchichat S, Katz E (2002) Immunization of rabbits with a modified vaccinia Ankara recombinant virus bearing the HIV envelope antigen on its outer membrane. Virus Res 90: 243-251.
33. Humlova Z, Vokurka M, Esteban M, Melkova Z (2002) Vaccinia virus induces apoptosis of infected macrophages. J Gen Virol 83: 2821-2832.
34. Combadiere B, Boissonnas A, Carcelain G, Lefranc E, Samri A, et al. (2004) Distinct time effects of vaccination on long-term proliferative and IFN-gamma-producing T cell memory to smallpox in humans. J Exp Med 199: 1585-1593.
35. Kawakami Y, Yumoto K, Kawakami T (2007) An improved mouse model of atopic dermatitis and suppression of skin lesions by an inhibitor of Tec family kinases. Allergol Int 56: 403-409.
36. Frey SE, Couch RB, Tacket CO, Treanor JJ, Wolff M, et al. (2002) Clinical responses to undiluted and diluted smallpox vaccine. N Engl J Med 346: 1265-1274.
37. Matsumoto M, Ra C, Kawamoto K, Sato H, Itakura A, et al. (1999) IgE hyperproduction through enhanced tyrosine phosphorylation of Janus kinase 3 in NC/Nga mice, a model for human atopic dermatitis. J Immunol 162: 1056-1063.
38. Suto H, Matsuda H, Mitsuishi K, Hira K, Uchida T, et al. (1999) NC/Nga mice: a mouse model for atopic dermatitis. Int Arch Allergy Immunol 120 Suppl 1:: 70-75.
39. Yagi R, Nagai H, Iigo Y, Akimoto T, Arai T, et al. (2002) Development of atopic dermatitis-like skin lesions in STAT6-deficient NC/Nga mice. J Immunol 168: 2020-2027.
40. Mamessier E, Botturi K, Vervloet D, Magnan A (2005) [T regulatory lymphocytes, atopy and asthma: a new concept in three dimensions]. Rev Mal Respir 22: 305-311.
41. Anderson E, Pierre-Louis WS, Wong CJ, Lary JW, Cole JL (2011) Heparin activates PKR by inducing dimerization. J Mol Biol 413: 973-984.
42. Rager KJ, Langland JO, Jacobs BL, Proud D, Marsh DG, et al. (1998) Activation of antiviral protein kinase leads to immunoglobulin E class switching in human B cells. J Virol 72: 1171-1176.
43. Davies MV, Chang HW, Jacobs BL, Kaufman RJ (1993) The E3L and K3L vaccinia virus gene products stimulate translation through inhibition of the double-stranded RNA-dependent protein kinase by different mechanisms. J Virol 67: 1688-1692.
44. Williams BR (1999) PKR; a sentinel kinase for cellular stress. Oncogene 18: 6112-6120.
45. Baixeras E, Cebrian A, Albar JP, Salas J, Martinez AC, et al. (1998) Vaccinia virus-induced apoptosis in immature B lymphocytes: role of cellular Bcl-2. Virus Res 58: 107-113.
46. Engelmayer J, Larsson M, Subklewe M, Chahroudi A, Cox WI, et al. (1999) Vaccinia virus inhibits the maturation of human dendritic cells: a novel mechanism of immune evasion. J Immunol 163: 6762-6768.
47. Haga IR, Bowie AG (2005) Evasion of innate immunity by vaccinia virus. Parasitology 130 Suppl: S11-25.
48. Martin RM, Brady JL, Lew AM (1998) The need for IgG2c specific antiserum when isotyping antibodies from C57BL/6 and NOD mice. J Immunol Methods 212: 187-192.
49. Oyoshi MK, Ramesh N, Geha RS (2011) Vaccinia Ig ameliorates eczema vaccinatum in a murine model of atopic dermatitis. J Invest Dermatol 132: 1299-1301.
50. von Sonnenburg F, Perona P, Darsow U, Ring J, von Krempelhuber A, et al. (2014) Safety and immunogenicity of modified vaccinia Ankara as a smallpox vaccine in people with atopic dermatitis. Vaccine 32: 5696-5702.
51. Guzman E, Cubillos-Zapata C, Cottingham MG, Gilbert SC, Prentice H, et al. (2012) Modified vaccinia virus Ankara-based vaccine vectors induce apoptosis in dendritic cells draining from the skin via both the extrinsic and intrinsic caspase pathways, preventing efficient antigen presentation. J Virol 86: 5452-5466.
52. Perdiguero B, Gomez CE, Najera JL, Sorzano CO, Delaloye J, et al. (2012) Deletion of the viral antiapoptotic gene F1L in the HIV/AIDS vaccine candidate MVA-C enhances immune responses against HIV-1 antigens. PLoS One 7: e48524.
53. Reed JL, Scott DE, Bray M (2012) Eczema vaccinatum. Clin Infect Dis 54: 832-840.
54. Stahlberg A, Hakansson J, Xian X, Semb H, Kubista M. (2004) Properties of the reverse transcription reaction in mRNA quantification. Clin Chem 50: 509-515.
55. Miljkovic Z, Momcilovic M, Miljkovic D, Mostarica-Stojkovic M (2008) Methylprednisolone inhibits IFN-gamma and IL-17 expression and production by cells infiltrating central nervous system in experimental autoimmune encephalomyelitis. J Neuroinflammation 6: 37.