[en] Glycoprotein G (gG) orthologues have been described in several alphaherpesviruses. gG is expressed both as a membrane-anchored form on infected cells and as a secreted form. Recently, we reported that both forms of gG encoded by alphaherpesviruses infecting large herbivores and by Felid herpesvirus 1 (FeHV-1) bind with high affinity to a broad range of CXC, CC and C-chemokines. Based on the viral species, gG has been reported either as a structural or a non-structural protein. To date, the incorporation of FeHV-1 gG into virions has never been tested, nor the property of alphaherpesvirus structural gG to bind chemokines on the virion surface. In the present study, to address these questions, various FeHV-1 gG recombinant strains were produced using an original technique based on an infectious FeHV-1 BAC clone and restriction endonuclease mediated recombination. Using the recombinants produced, we were able to determine that FeHV-1 gG is a structural protein that acts as a chemokine-binding protein on the virion surface. In the light of these results, putative roles of gG in alphaherpesvirus infections are discussed, and an evolutionary scenario is proposed to explain the structural versus non-structural property of gG amongst alphaherpesviruses.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Costes, Bérénice ; Université de Liège - ULiège > Immunologie et vaccinologie
Thirion, Muriel ; Université de Liège - ULiège > Immunologie et vaccinologie
Dewals, Benjamin G ; Université de Liège - ULiège > Immunologie et vaccinologie
Alcami A. Viral mimicry of cytokines, chemokines and their receptors. Nat. Rev. Immunol. 3 (2003) 36-50
Lalani A.S., and McFadden G. Evasion and exploitation of chemokines by viruses. Cytokine Growth Factor Rev. 10 (1999) 219-233
Murphy P.M. Viral exploitation and subversion of the immune system through chemokine mimicry. Nat. Immunol. 2 (2001) 116-122
Costes B., Ruiz-Arguello M.B., Bryant N.A., Alcami A., and Vanderplasschen A. Both soluble and membrane-anchored forms of Felid herpesvirus 1 glycoprotein G function as a broad-spectrum chemokine-binding protein. J. Gen. Virol. 86 (2005) 3209-3214
Bryant N.A., Davis-Poynter N., Vanderplasschen A., and Alcami A. Glycoprotein G isoforms from some alphaherpesviruses function as broad-spectrum chemokine binding proteins. EMBO J. 22 (2003) 833-846
Balan P., Davis-Poynter N., Bell S., Atkinson H., Browne H., and Minson T. An analysis of the in vitro and in vivo phenotypes of mutants of herpes simplex virus type 1 lacking glycoproteins gG, gE, gI or the putative gJ. J. Gen. Virol. 75 Pt 6 (1994) 1245-1258
Baranowski E., Keil G., Lyaku J., Rijsewijk F.A., van Oirschot J.T., Pastoret P.P., and Thiry E. Structural and functional analysis of bovine herpesvirus 1 minor glycoproteins. Vet. Microbiol. 53 (1996) 91-101
Drummer H.E., Studdert M.J., and Crabb B.S. Equine herpesvirus-4 glycoprotein G is secreted as a disulphide-linked homodimer and is present as two homodimeric species in the virion. J. Gen. Virol. 79 (1998) 1205-1213
Richman D.D., Buckmaster A., Bell S., Hodgman C., and Minson A.C. Identification of a new glycoprotein of herpes simplex virus type 1 and genetic mapping of the gene that codes for it. J. Virol. 57 (1986) 647-655
Su H.K., Eberle R., and Courtney R.J. Processing of the herpes simplex virus type 2 glycoprotein gG-2 results in secretion of a 34,000-Mr cleavage product. J. Virol. 61 (1987) 1735-1737
Ackermann M., Longnecker R., Roizman B., and Pereira L. Identification, properties, and gene location of a novel glycoprotein specified by herpes simplex virus 1. Virology 150 (1986) 207-220
Roizman B., and Pellet P.E. The family Herpesviridae: a brief introduction. In: Knipe D.M., and Howley P.M. (Eds). Fields Virology (2001), Lippincott, Williams and Wilkins, Philadelphia 2381-2397
Stiles J. Feline herpesvirus. Clin. Tech. Small Anim. Pract. 18 (2003) 178-185
Andrew S.E. Ocular manifestations of feline herpesvirus. J. Feline Med. Surg. 3 (2001) 9-16
Gaskell, R. Studies on feline viral rhinotracheitis with particular reference to the carrier state, PhD thesis, University of Bristol, Bristol, UK, 1975.
Gillet L., Daix V., Donofrio G., Wagner M., Koszinowski U.H., China B., Ackermann M., Markine-Goriaynoff N., and Vanderplasschen A. Development of bovine herpesvirus 4 as an expression vector using bacterial artificial chromosome cloning. J. Gen. Virol. 86 (2005) 907-917
Markine-Goriaynoff N., Gillet L., Karlsen O.A., Haarr L., Minner F., Pastoret P.P., Fukuda M., and Vanderplasschen A. The core 2 beta-1,6-N-acetylglucosaminyltransferase-M encoded by bovine herpesvirus 4 is not essential for virus replication despite contributing to post-translational modifications of structural proteins. J. Gen. Virol. 85 (2004) 355-367
Vanderplasschen A., Markine-Goriaynoff N., Lomonte P., Suzuki M., Hiraoka N., Yeh J.C., Bureau F., Willems L., Thiry E., Fukuda M., and Pastoret P.P. A multipotential beta -1,6-N-acetylglucosaminyl-transferase is encoded by bovine herpesvirus type 4. Proc. Natl. Acad. Sci. USA 97 (2000) 5756-5761
Wagner M., Ruzsics Z., and Koszinowski U.H. Herpesvirus genetics has come of age. Trends Microbiol. 10 (2002) 318-324
Arii J., Hushur O., Kato K., Kawaguchi Y., Tohya Y., and Akashi H. Construction of an infectious clone of canine herpesvirus genome as a bacterial artificial chromosome. Microbes Infect. 8 (2006) 1054-1063
Keil G.M., Engelhardt T., Karger A., and Enz M. Bovine herpesvirus 1 U(s) open reading frame 4 encodes a glycoproteoglycan. J. Virol. 70 (1996) 3032-3038
Mettenleiter T.C., Kern H., and Rauh I. Isolation of a viable herpesvirus (pseudorabies virus) mutant specifically lacking all four known nonessential glycoproteins. Virology 179 (1990) 498-503
Sharp P.M. Origins of human virus diversity. Cell 108 (2002) 305-312
Davison A.J. Evolution of the herpesviruses. Vet. Microbiol. 86 (2002) 69-88
McGeoch D.J., Dolan A., and Ralph A.C. Toward a comprehensive phylogeny for mammalian and avian herpesviruses. J. Virol. 74 (2000) 10401-10406
Willoughby K., Bennett M., McCracken C.M., and Gaskell R.M. Molecular phylogenetic analysis of felid herpesvirus 1. Vet. Microbiol. 69 (1999) 93-97
Kumar S., and Hedges S.B. A molecular timescale for vertebrate evolution. Nature 392 (1998) 917-920
Cardin A.D., and Weintraub H.J. Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9 (1989) 21-32
Seet B.T., Barrett J., Robichaud J., Shilton B., Singh R., and McFadden G. Glycosaminoglycan binding properties of the myxoma virus CC-chemokine inhibitor, M-T1. J. Biol. Chem. 276 (2001) 30504-30513
Tran L.C., Kissner J.M., Westerman L.E., and Sears A.E. A herpes simplex virus 1 recombinant lacking the glycoprotein G coding sequences is defective in entry through apical surfaces of polarized epithelial cells in culture and in vivo. Proc. Natl. Acad. Sci. USA 97 (2000) 1818-1822