1887

Abstract

Pseudorabies virus (PRV), also known as suid herpesvirus, is the aetiological agent of Aujeszky's disease in swine. In other animals, except higher-order primates, PRV infection is often fatal. The mechanisms of PRV pathogenesis and immune modulation are largely unknown. PRV codes for 11 glycoproteins. Among them, glycoprotein G (gG) is the most abundant PRV protein found in the supernatant of PRV-infected cell cultures. PRV-gG has low amino acid sequence similarity with gG from other animal alphaherpesviruses and its function is unknown. gG from other animal alphaherpesviruses, with the exception of at least equine herpesvirus 4, binds to chemokines. We show here that PRV-gG binds to the human chemokine CL1 and several CC and CXC human chemokines with high affinity. Chemokine-binding activity can be detected in the supernatants of PRV-infected cell cultures, and insertional inactivation of the gene encoding gG from the PRV genome results in loss of chemokine-binding activity. Binding of PRV-gG to chemokines inhibits chemokine-mediated cell migration, suggesting a role for PRV-gG in immune evasion.

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2010-01-01
2019-11-18
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References

  1. Alcami, A., Symons, J. A., Collins, P. D., Williams, T. J. & Smith, G. L. ( 1998; ). Blockade of chemokine activity by a soluble chemokine binding protein from vaccinia virus. J Immunol 160, 624–633.
    [Google Scholar]
  2. Alejo, A., Ruiz-Arguello, M. B., Ho, Y., Smith, V. P., Saraiva, M. & Alcami, A. ( 2006; ). A chemokine-binding domain in the tumor necrosis factor receptor from variola (smallpox) virus. Proc Natl Acad Sci U S A 103, 5995–6000.[CrossRef]
    [Google Scholar]
  3. Bennett, L. M., Timmins, J. G., Thomsen, D. R. & Post, L. E. ( 1986; ). The processing of pseudorabies virus glycoprotein gX in infected cells and in an uninfected cell line. Virology 155, 707–715.[CrossRef]
    [Google Scholar]
  4. Brukman, A. & Enquist, L. W. ( 2006; ). Pseudorabies virus EP0 protein counteracts an interferon-induced antiviral state in a species-specific manner. J Virol 80, 10871–10873.[CrossRef]
    [Google Scholar]
  5. Bryant, N. A., Davis-Poynter, N., Vanderplasschen, A. & Alcami, A. ( 2003; ). Glycoprotein G isoforms from some alphaherpesviruses function as broad-spectrum chemokine binding proteins. EMBO J 22, 833–846.[CrossRef]
    [Google Scholar]
  6. Costes, B., Ruiz-Arguello, M. B., Bryant, N. A., Alcami, A. & Vanderplasschen, A. ( 2005; ). Both soluble and membrane-anchored forms of Felid herpesvirus 1 glycoprotein G function as a broad-spectrum chemokine-binding protein. J Gen Virol 86, 3209–3214.[CrossRef]
    [Google Scholar]
  7. Crump, M. P., Gong, J. H., Loetscher, P., Rajarathnam, K., Amara, A., Arenzana-Seisdedos, F., Virelizier, J. L., Baggiolini, M., Sykes, B. D. & Clark-Lewis, I. ( 1997; ). Solution structure and basis for functional activity of stromal cell-derived factor-1; dissociation of CXCR4 activation from binding and inhibition of HIV-1. EMBO J 16, 6996–7007.[CrossRef]
    [Google Scholar]
  8. Demmin, G. L., Clase, A. C., Randall, J. A., Enquist, L. W. & Banfield, B. W. ( 2001; ). Insertions in the gG gene of pseudorabies virus reduce expression of the upstream Us3 protein and inhibit cell-to-cell spread of virus infection. J Virol 75, 10856–10869.[CrossRef]
    [Google Scholar]
  9. Devlin, J. M., Browning, G. F., Hartley, C. A., Kirkpatrick, N. C., Mahmoudian, A., Noormohammadi, A. H. & Gilkerson, J. R. ( 2006; ). Glycoprotein G is a virulence factor in infectious laryngotracheitis virus. J Gen Virol 87, 2839–2847.[CrossRef]
    [Google Scholar]
  10. Enquist, L. W. ( 1999; ). Life beyond eradication: veterinary viruses in basic science. Arch Virol Suppl 15, 87–109.
    [Google Scholar]
  11. Fallon, P. G. & Alcami, A. ( 2006; ). Pathogen-derived immunomodulatory molecules: future immunotherapeutics? Trends Immunol 27, 470–476.[CrossRef]
    [Google Scholar]
  12. Fernandez, A., Menendez del Campo, A. M., Fernandez, S., Camacho, A., Castro, J. M. & Tabares, E. ( 1999; ). Conversion of US3-encoded protein kinase gene from pseudorabies virus in a diploid gene located within inverted repeats by genetic recombination between the viral genome isomers. Virus Res 61, 125–135.[CrossRef]
    [Google Scholar]
  13. Gomez-Sebastian, S. & Tabares, E. ( 2004; ). Negative regulation of herpes simplex virus type 1 ICP4 promoter by IE180 protein of pseudorabies virus. J Gen Virol 85, 2125–2130.[CrossRef]
    [Google Scholar]
  14. Graham, K. A., Lalani, A. S., Macen, J. L., Ness, T. L., Barry, M., Liu, L. Y., Lucas, A., Clark-Lewis, I., Moyer, R. W. & McFadden, G. ( 1997; ). The T1/35kDa family of poxvirus-secreted proteins bind chemokines and modulate leukocyte influx into virus-infected tissues. Virology 229, 12–24.[CrossRef]
    [Google Scholar]
  15. Johnson, Z., Schwarz, M., Power, C. A., Wells, T. N. & Proudfoot, A. E. ( 2005; ). Multi-faceted strategies to combat disease by interference with the chemokine system. Trends Immunol 26, 268–274.[CrossRef]
    [Google Scholar]
  16. Kimman, T. G., de Wind, N., Oei-Lie, N., Pol, J. M., Berns, A. J. & Gielkens, A. L. ( 1992; ). Contribution of single genes within the unique short region of Aujeszky's disease virus (suid herpesvirus type 1) to virulence, pathogenesis and immunogenicity. J Gen Virol 73, 243–251.[CrossRef]
    [Google Scholar]
  17. Klupp, B. G., Hengartner, C. J., Mettenleiter, T. C. & Enquist, L. W. ( 2004; ). Complete, annotated sequence of the pseudorabies virus genome. J Virol 78, 424–440.[CrossRef]
    [Google Scholar]
  18. McGeoch, D. J. ( 1990; ). Evolutionary relationships of virion glycoprotein genes in the S regions of alphaherpesvirus genomes. J Gen Virol 71, 2361–2367.[CrossRef]
    [Google Scholar]
  19. McGeoch, D. J., Moss, H. W., McNab, D. & Frame, M. C. ( 1987; ). DNA sequence and genetic content of the HindIII l region in the short unique component of the herpes simplex virus type 2 genome: identification of the gene encoding glycoprotein G, and evolutionary comparisons. J Gen Virol 68, 19–38.[CrossRef]
    [Google Scholar]
  20. Mettenleiter, T. C. ( 2000; ). Aujeszky's disease (pseudorabies) virus: the virus and molecular pathogenesis – state of the art, June 1999. Vet Res 31, 99–115.
    [Google Scholar]
  21. Moser, B., Wolf, M., Walz, A. & Loetscher, P. ( 2004; ). Chemokines: multiple levels of leukocyte migration control. Trends Immunol 25, 75–84.[CrossRef]
    [Google Scholar]
  22. Nauwynck, H., Glorieux, S., Favoreel, H. & Pensaert, M. ( 2007; ). Cell biological and molecular characteristics of pseudorabies virus infections in cell cultures and in pigs with emphasis on the respiratory tract. Vet Res 38, 229–241.[CrossRef]
    [Google Scholar]
  23. Parry, C. M., Simas, J. P., Smith, V. P., Stewart, C. A., Minson, A. C., Efstathiou, S. & Alcami, A. ( 2000; ). A broad spectrum secreted chemokine binding protein encoded by a herpesvirus. J Exp Med 191, 573–578.[CrossRef]
    [Google Scholar]
  24. Proudfoot, A. E. ( 2002; ). Chemokine receptors: multifaceted therapeutic targets. Nat Rev Immunol 2, 106–115.[CrossRef]
    [Google Scholar]
  25. Proudfoot, A. E., Handel, T. M., Johnson, Z., Lau, E. K., LiWang, P., Clark-Lewis, I., Borlat, F., Wells, T. N. & Kosco-Vilbois, M. H. ( 2003; ). Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc Natl Acad Sci U S A 100, 1885–1890.[CrossRef]
    [Google Scholar]
  26. Rea, T. J., Timmins, J. G., Long, G. W. & Post, L. E. ( 1985; ). Mapping and sequence of the gene for the pseudorabies virus glycoprotein which accumulates in the medium of infected cells. J Virol 54, 21–29.
    [Google Scholar]
  27. Rot, A. ( 1992; ). Endothelial cell binding of NAP-1/IL-8: role in neutrophil emigration. Immunol Today 13, 291–294.[CrossRef]
    [Google Scholar]
  28. Ruiz-Arguello, M. B., Smith, V. P., Campanella, G. S., Baleux, F., Arenzana-Seisdedos, F., Luster, A. D. & Alcami, A. ( 2008; ). An ectromelia virus protein that interacts with chemokines through their glycosaminoglycan binding domain. J Virol 82, 917–926.[CrossRef]
    [Google Scholar]
  29. Seet, B. T. & McFadden, G. ( 2002; ). Viral chemokine-binding proteins. J Leukoc Biol 72, 24–34.
    [Google Scholar]
  30. Thomsen, D. R., Marchioli, C. C., Yancey, R. J., Jr & Post, L. E. ( 1987; ). Replication and virulence of pseudorabies virus mutants lacking glycoprotein gX. J Virol 61, 229–232.
    [Google Scholar]
  31. van Berkel, V., Barrett, J., Tiffany, H. L., Fremont, D. H., Murphy, P. M., McFadden, G., Speck, S. H. & Virgin, H. I. ( 2000; ). Identification of a gammaherpesvirus selective chemokine binding protein that inhibits chemokine action. J Virol 74, 6741–6747.[CrossRef]
    [Google Scholar]
  32. Van de Walle, G. R., May, M. L., Sukhumavasi, W., von Einem, J. & Osterrieder, N. ( 2007; ). Herpesvirus chemokine-binding glycoprotein G (gG) efficiently inhibits neutrophil chemotaxis in vitro and in vivo. J Immunol 179, 4161–4169.[CrossRef]
    [Google Scholar]
  33. van Rooij, E. M., de Bruin, M. G., de Visser, Y. E., Middel, W. G., Boersma, W. J. & Bianchi, A. T. ( 2004; ). Vaccine-induced T cell-mediated immunity plays a critical role in early protection against pseudorabies virus (suid herpes virus type 1) infection in pigs. Vet Immunol Immunopathol 99, 113–125.[CrossRef]
    [Google Scholar]
  34. van Zijl, M., van der Gulden, H., de Wind, N., Gielkens, A. & Berns, A. ( 1990; ). Identification of two genes in the unique short region of pseudorabies virus; comparison with herpes simplex virus and varicella-zoster virus. J Gen Virol 71, 1747–1755.[CrossRef]
    [Google Scholar]
  35. von Einem, J., Smith, P. M., Van de Walle, G. R., O'Callaghan, D. J. & Osterrieder, N. ( 2007; ). In vitro and in vivo characterization of equine herpesvirus type 1 (EHV-1) mutants devoid of the viral chemokine-binding glycoprotein G (gG). Virology 362, 151–162.[CrossRef]
    [Google Scholar]
  36. Webb, L. M., Clark-Lewis, I. & Alcami, A. ( 2003; ). The gammaherpesvirus chemokine binding protein binds to the N terminus of CXCL8. J Virol 77, 8588–8592.[CrossRef]
    [Google Scholar]
  37. Webb, L. M., Smith, V. P. & Alcami, A. ( 2004; ). The gammaherpesvirus chemokine binding protein can inhibit the interaction of chemokines with glycosaminoglycans. FASEB J 18, 571–573.
    [Google Scholar]
  38. Wittmann, G. & Rziha, H. J. ( 1989; ). Aujeszky's disease (pseudorabies) in pigs. In Herpesvirus Diseases of Cattle, Horses, and Pigs, pp. 230–325. Edited by G. Wittmann. Boston: Kluwer.
  39. Yoshie, O., Imai, T. & Nomiyama, H. ( 2001; ). Chemokines in immunity. Adv Immunol 78, 57–110.
    [Google Scholar]
  40. Zlotnik, A., Yoshie, O. & Nomiyama, H. ( 2006; ). The chemokine and chemokine receptor superfamilies and their molecular evolution. Genome Biol 7, 243 [CrossRef]
    [Google Scholar]
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