Intradermal immune response after infection with Vaccinia virus.

Administration, Cutaneous; Animals; CD4-Positive T-Lymphocytes/immunology; CD8-Positive T-Lymphocytes/immunology; Cell Count; Gene Rearrangement, delta-Chain T-Cell Antigen Receptor; Gene Rearrangement, gamma-Chain T-Cell Antigen Receptor; Granulocytes/immunology; Killer Cells, Natural/immunology; Lymphocytes/immunology; Macrophages/immunology; Mice; Mice, Inbred BALB C; Skin/immunology; Smallpox Vaccine/administration & dosage/immunology; T-Lymphocytes/immunology; Time Factors; Vaccination; Vaccinia/immunology; Vaccinia virus/immunology

Abstract :

[en] Although Vaccinia virus (VACV) was used to eradicate smallpox by dermal vaccination, there is little information available about the immune response induced at the vaccination site. Previously, an intradermal murine model that mimics smallpox vaccination was established. Here, this model was used to investigate which leukocytes are recruited to the infected lesion and what are the kinetics of recruitment. Data presented show that VACV infection induced the infiltration of macrophages, followed by granulocytes and lymphocytes. Up to 4 days post-infection, the major lymphocyte population was TCRgammadelta T cells, but thereafter, there was a large recruitment of CD4(+) and CD8(+) T cells. Interestingly, the majority of T cells expressed the natural killer-cell marker DX5. This report is the first to characterize the local immune response sequence to VACV infection and represents a benchmark against which the responses induced by genetically modified VACVs may be compared.

Disciplines :

Immunology & infectious disease

Author, co-author :

Jacobs, Nathalie ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Anatomie et cytologie pathologiques

Chen, Ron A-J

Gubser, Caroline

Najarro, Pilar

Smith, Geoffrey L

Language :

English

Title :

Intradermal immune response after infection with Vaccinia virus.

Publication date :

2006

Journal title :

Journal of General Virology

ISSN :

0022-1317

eISSN :

1465-2099

Publisher :

Society for General Microbiology, London, United Kingdom

Volume :

Issue :

Pt 5

Pages :

1157-61

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

Wellcome Trust [GB]

Available on ORBi :

since 18 August 2009

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Bibliography

Amara, R. R., Nigam, P., Sharma, S., Liu, J. & Bostik, V. (2004). Long-lived poxvirus immunity, robust CD4 help, and better persistence of CD4 than CD8 T cells. J Virol 78, 3811-3816.
Asarnow, D. M., Kuziel, W. A., Bonyhadi, M., Tigelaar, R. E., Tucker, P. W. & Allison, J. P. (1988). Limited diversity of γδ antigen receptor genes of Thy-1+ dendritic epidermal cells. Cell 55, 837-847.
Belkaid, Y., Jouin, H. & Milon, G. (1996). A method to recover, enumerate and identify lymphomyeloid cells present in an inflammatory dermal site: a study in laboratory mice. J Immunol Methods 199, 5-25.
Belkaid, Y., Kamhawi, S., Modi, G., Valenzuela, J., Noben-Trauth, N., Rowton, E., Ribeiro, J. & Sacks, D. L. (1998). Development of a natural model of cutaneous leishmaniasis: powerful effects of vector saliva and saliva preexposure on the long-term outcome of Leishmania major infection in the mouse ear dermis. J Exp Med 188, 1941-1953.
Belshe, R. B., Newman, F. K., Frey, S. E., Couch, R. B., Treanor, J. J., Tacket, C. O. & Yan, L. (2004). Dose-dependent neutralizing-antibody responses to vaccinia. J Infect Dis 189, 493-497.
Belyakov, I. M., Earl, P., Dzutsev, A. & 8 other authors (2003). Shared modes of protection against poxvirus infection by attenuated and conventional smallpox vaccine viruses. Proc Natl Acad Sci U S A 100, 9458-9463.
Bukowski, J. F., Woda, B. A., Habu, S., Okumura, K. & Welsh, R. M. (1983). Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo. J Immunol 131, 1531-1538.
Combadiere, B., Boissonnas, A., Carcelain, G., Lefranc, E., Samri, A., Bricaire, F., Debre, P. & Autran, B. (2004). Distinct time effects of vaccination on long-term proliferative and IFN-γ-producing T cell memory to smallpox in humans. J Exp Med 199, 1585-1593.
Crotty, S., Felgner, P., Davies, H., Glidewell, J., Villarreal, L. & Ahmed, R. (2003). Cutting edge: long-term B cell memory in humans after smallpox vaccination. J Immunol 171, 4969-4973.
Davies, D. H., McCausland, M. M., Valdez, C. & 7 other authors (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.
Dupasquier, M., Stoitzner, P., Oudenaren, A., Romani, N. & Leenen, P. J. M. (2004). Macrophages and dendritic cells constitute a major subpopulation of cells in the mouse dermis. J Invest Dermatol 123, 876-879.
Earl, P. L., Americo, J. L., Wyatt, L. S. & 15 other authors (2004). Immunogenicity of a highly attenuated MVA smallpox vaccine and protection against monkeypox. Nature 428, 182-185.
Fogg, C., Lustig, S., Whitbeck, J. C., Eisenberg, R. J., Cohen, G. H. & Moss, B. (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.
Frey, S. E., Newman, F. K., Yan, L., Lottenbach, K. R. & Belshe, R. B. (2003). Response to smallpox vaccine in persons immunized in the distant past. JAMA 289, 3295-3299.
Greenberg, R. N., Kennedy, J. S., Clanton, D. J., Plummer, E. A., Hague, L., Cruz, J., Ennis, F. A., Blackwelder, W. C. & Hopkins, R. J. (2005). Safety and immunogenicity of new cell-cultured smallpox vaccine compared with calf-lymph derived vaccine: a blind, single-centre, randomised controlled trial. Lancet 365, 398-409.
Hammarlund, E., Lewis, M. W., Hansen, S. G., Strelow, L. I., Nelson, J. A., Sexton, G. J., Hanifin, J. M. & Slifka, M. K. (2003). Duration of antiviral immunity after smallpox vaccination. Nat Med 9, 1131-1137.
Hawlisch, H., Belkaid, Y., Baelder, R., Hildeman, D., Gerard, C. & Köhl, J. (2005). C5a negatively regulates Toll-like receptor 4-induced immune responses. Immunity 22, 415-426.
Kambayashi, T., Assarsson, E., Chambers, B. J. & Ljunggren, H. G. (2001). Expression of the DX5 antigen on CD8+ T cells is associated with activation and subsequent cell death or memory during influenza virus infection. Eur J Immunol 31, 1523-1530.
Kennedy, M. K., Glaccum, M., Brown, S. N. & 13 other authors (2000). Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 191, 771-780.
Moss, B. & Shisler, J. L. (2001). Immunology 101 at poxvirus U: immune evasion genes. Semin Immunol 13, 59-66.
Natuk, R. J. & Welsh, R. M. (1987). Accumulation and chemotaxis of natural killer/large granular lymphocytes at sites of virus replication. J Immunol 138, 877-883.
Ninomiya, T., Takimoto, H., Matsuzaki, G., Hamano, S., Yoshida, H., Yoshikai, Y., Kimura, G. & Nomoto, K. (2000). Vγ1+ γδ T cells play protective roles at an early phase of murine cytomegalovirus infection through production of interferon-γ. Immunology 99, 187-194.
Prlic, M., Gibbs, J. & Jameson, S. C. (2005). Characteristics of NK cell migration early after vaccinia infection. J Immunol 175, 2152-2157.
Pütz, M. M., Alberini, I., Midgley, C. M., Manini, I., Montomoli, E. & Smith, G. L. (2005). Prevalence of antibodies to Vaccinia virus after smallpox vaccination in Italy. J Gen Virol 86, 2955-2960.
Reading, P. C. & Smith, G. L (2003). A kinetic analysis of immune mediators in the lungs of mice infected with vaccinia virus and comparison with intradermal infection. J Gen Virol 84, 1973-1983.
Rock, M. T., Yoder, S. M., Wright, P. F., Talbot, T. R., Edwards, K. M. & Crowe, J. E., Jr (2005). Differential regulation of granzyme and perforin in effector and memory T cells following smallpox immunization. J Immunol 174, 3757-3764.
Selin, L. K., Santolucito, P. A., Pinto, A. K., Szomolanyi-Tsuda, E. & Welsh, R. M. (2001). Innate immunity to viruses: control of vaccinia virus infection by γδ T cells. J Immunol 166, 6784-6794.
Slifka, M. K., Pagarigan, R. R. & Whitton, J. L. (2000). NK markers are expressed on a high percentage of virus-specific CD8+ and CD4+ T cells. J Immunol 164, 2009-2015.
Smith, G. L., Mackett, M. & Moss, B. (1983). Infectious vaccinia virus recombinants that express hepatitis B virus surface antigen. Nature 302, 490-495.
Smith, G. L., Symons, J. A., Khanna, A., Vanderplasschen, A. & Alcami, A. (1997). Vaccinia virus immune evasion. Immunol Rev 159, 137-154.
Symons, J. A., Adams, E., Tscharke, D. C., Reading, P. C., Waldmann, H. & Smith, G. L. (2002). The vaccinia virus C12L protein inhibits mouse IL-18 and promotes virus virulence in the murine intranasal model. J Gen Virol 83, 2833-2844.
Tscharke, D. C. & Smith, G. L. (1999). A model for vaccinia virus pathogenesis and immunity based on intradermal injection of mouse ear pinnae. J Gen Virol 80, 2751-2755.
Tscharke, D. C., Reading, P. C. & Smith, G. L. (2002). Dermal infection with vaccinia virus reveals roles for virus proteins not seen using other inoculation routes. J Gen Virol 83, 1977-1986.
Wang, T., Scully, E., Yin, Z. & 7 other authors (2003). IFN-γ-producing γδ T cells help control murine West Nile virus infection. J Immunol 171, 2524-2531.
Wilcock, D., Duncan, S. A., Traktman, P., Zhang, W.-H. & Smith, G. L. (1999). The vaccinia virus A40R gene product is a nonstructural, type II membrane glycoprotein that is expressed at the cell surface. J Gen Virol 80, 2137-2148.
Xu, R., Johnson, A. J., Liggitt, D. & Bevan, M. J. (2004). Cellular and humoral immunity against vaccinia virus infection of mice. J Immunol 172, 6265-6271.