Glycoprotein G from pseudorabies virus binds to chemokines with high affinity and inhibits their function

Journal of General Virology

Volumn 91, Issue 1, 2010, Pages 23-31

  Viejo Borbolla, Abel ^a   Muñoz, Ana ^a   Tabarés, Enrique ^a   Alcamí, Antonio ^a,b  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CHEMOKINE; BETA CHEMOKINE; CHEMOKINE; CHEMOKINE CL1; THROMBOSPONDIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING ASSAY; CELL MIGRATION; CONTROLLED STUDY; GENE INSERTION; HERPES VIRUS INFECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PSEUDORABIES HERPETOVIRUS; SUPERNATANT; VIRUS GENOME; VIRUS INACTIVATION;

ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; CHEMOKINES; HERPESVIRUS 1, SUID; HUMANS; PROTEIN BINDING; VIRAL ENVELOPE PROTEINS;

ANIMALIA; EQUID HERPESVIRUS 4; HERPESVIRIDAE; PRIMATES; SUID HERPESVIRUS 1; SUIDAE;

EID: 73149110358     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.011940-0     Document Type: Article

References (40)

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.
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.
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.
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.
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.
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.
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.
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.
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.
10. Enquist, L. W. (1999). Life beyond eradication: veterinary viruses in basic science. Arch Virol Suppl 15, 87-109.
11. Fallon, P. G. & Alcami, A. (2006). Pathogen-derived immunomodulatory molecules: future immunotherapeutics? Trends Immunol 27, 470-476.
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.
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.
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.
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.
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.
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.
18. McGeoch, D. J. (1990). Evolutionary relationships of virion glycoprotein genes in the S regions of alphaherpesvirus genomes. J Gen Virol 71, 2361-2367.
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.
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.
21. Moser, B., Wolf, M., Walz, A. & Loetscher, P. (2004). Chemokines: multiple levels of leukocyte migration control. Trends Immunol 25, 75-84.
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.
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.
24. Proudfoot, A. E. (2002). Chemokine receptors: multifaceted therapeutic targets. Nat Rev Immunol 2, 106-115.
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.
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.
27. Rot, A. (1992). Endothelial cell binding of NAP-1/IL-8: role in neutrophil emigration. Immunol Today 13, 291-294.
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.
29. Seet, B. T. & McFadden, G. (2002). Viral chemokine-binding proteins. J Leukoc Biol 72, 24-34.
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.
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.
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.
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.
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.
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.
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.
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.
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.
40. Zlotnik, A., Yoshie, O. & Nomiyama, H. (2006). The chemokine and chemokine receptor superfamilies and their molecular evolution. Genome Biol 7, 243.