[en] Intramolecular recombination is a frequent event during the replication cycle of bovine herpesvirus 1 (BoHV-1). Recombinant viruses frequently arise and survive in cattle after concomitant nasal infections with two BoHV-1 mutants. The consequences of this process, related to herpesvirus evolution, have to be assessed in the context of large use of live marker vaccines based on glycoprotein E (gE) gene deletion. In natural conditions, double nasal infections by vaccine and wild-type strains are likely to occur. This situation might generate virulent recombinant viruses inducing a serological response indistinguishable from the vaccine one. This question was addressed by generating in vitro BoHV-1 recombinants deleted in the gE gene from seven wild-type BoHV-1 strains and one mutant strain deleted in the genes encoding gC and gE. In vitro growth properties were assessed by virus production, one step growth kinetics and plaque size assay. Heterogeneity in the biological properties was shown among the investigated recombinant viruses. The results demonstrated that some recombinants. in spite of their gE minus phenotype, have biological characteristics close to wild-type BoHV-1. (c) 2005 Elsevier B.V. All rights reserved.
Disciplines :
Veterinary medicine & animal health Microbiology
Author, co-author :
Muylkens, Benoît ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Virologie, épidémiologie et pathologie des maladies virales
Meurens, F.
Schynts, F.
de Fays, K.
Pourchet, A.
Thiry, Julien ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Virologie, épidémiologie et pathologie des maladies virales
Antoine, Nadine ; Université de Liège - ULiège > Département de morphologie et pathologie > Histologie
Thiry, Etienne ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Virologie, épidémiologie et pathologie des maladies virales
Language :
English
Title :
Biological characterization of bovine herpesvirus 1 recombinants possessing the vaccine glycoprotein E negative phenotype
Baranowski, E., Keil, G., Lyaku, J., Rijsewijk, F.A., Van Oirschot, J.T., Pastoret, P.P., Thiry, E., Structural and functional analysis of bovine herpesvirus 1 minor glycoproteins (1996) Vet. Microbiol., 53, pp. 91-101
Brack, A.R., Klupp, B.G., Granzow, H., Tirabassi, R., Enquist, L.W., Mettenleiter, T.C., Role of the cytoplasmic tail of pseudorabies virus glycoprotein e in virion formation (2000) J. Virol., 74, pp. 4004-4016
Brandt, C.R., Kolb, A.W., Shah, D.D., Pumfery, A.M., Kintner, R.L., Jaehnig, E., Van Gompel, J.J., Multiple determinants contribute to the virulence of HSV ocular and CNS infection and identification of serine 34 of the US1 gene as an ocular disease determinant (2003) Invest. Ophthalmol. Vis. Sci., 44, pp. 2657-2668
Chowdhury, S.I., Ross, C.S., Lee, B.J., Hall, V., Chu, H.J., Construction and characterization of a glycoprotein e gene-deleted bovine herpesvirus type 1 recombinant (1999) Am. J. Vet. Res., 60, pp. 227-232
Edwards, S., White, H., Nixon, P., A study of the predominant genotypes of bovid herpesvirus 1 found in the U.K. (1990) Vet. Microbiol., 22, pp. 213-223
Engels, M., Giuliani, C., Wild, P., Beck, T.M., Loepfe, E., Wyler, R., The genome of bovine herpesvirus 1 (BHV-1) strains exhibiting a neuropathogenic potential compared to known BHV-1 strains by restriction site mapping and cross-hybridization (1986) Virus Res., 6, pp. 57-73
Fehler, F., Herrman, J.M., Saalmüller, A., Mettenleiter, T.C., Keil, G.M., Glycoprotein IV of bovine herpesvirus 1-expressing cell line complements and rescues a conditionally lethal viral mutant (1992) J. Virol., 66, pp. 831-839
Fujita, K., Maeda, K., Yokoyama, N., Miyazawa, T., Kai, C., Mikami, T., In vitro recombination of feline herpesvirus type 1 (1998) Arch. Virol., 143, pp. 25-34
Glazenburg, K.L., Moormann, R.J., Kimman, T.G., Gielkens, A.L., Peeters, B.P., In vivo recombination of pseudorabies virus strains in mice (1994) Virus Res., 34, pp. 115-126
Han, M.G., Kim, S.J., Analysis of Korean strains of infectious laryngo-tracheitis virus by nucleotide sequences and restriction fragment length polymorphism (2001) Vet. Microbiol., 83, pp. 321-331
Henderson, L.M., Katz, J.B., Erickson, G.A., Mayfield, J.E., In vivo and in vitro genetic recombination between conventional and gene-deleted vaccine strains of pseudorabies virus (1990) Am. J. Vet. Res., 51, pp. 1656-1662
Hollander, M., Wolfe, D.A., (1973) Non Parametric Statistical Methods, , Wiley New York
Javier, R.T., Sedarati, F., Stevens, J.G., Two avirulent herpes simplex viruses generate lethal recombinants in vivo (1986) Science, 234, pp. 746-748
Kaashoek, M.J., Straver, P.H., Van Rooij, E.M., Quak, J., Van Oirschot, J.T., Virulence, immunogenicity and reactivation of seven bovine herpesvirus 1.1 strains: Clinical and virological aspects (1996) Vet. Rec., 139, pp. 416-421
König, P., Giesow, K., Keil, G.M., Glycoprotein M of bovine herpesvirus 1 (BHV-1) is non-essential for replication in cell culture and is involved in inhibition of bovine respiratory syncytial virus F protein induced syncytium formation in recombinant BHV-1 infected cells (2002) Vet. Microbiol., 86, pp. 37-49
Lemaire, M., Schynts, F., Meyer, G., Thiry, E., Antibody response to glycoprotein e after bovine herpesvirus type 1 infection in passively immunised, glycoprotein e negative calves (1999) Vet. Rec., 144, pp. 172-174
Leung-Tack, P., Audonnet, J.C., Riviere, M., The complete DNA sequence and the genetic organization of the short unique region (US) of the bovine herpesvirus type 1 (ST strain) (1994) Virology
Mahony, T.J., McCarthy, F.M., Gravel, J.L., West, L., Young, P.L., Construction and manipulation of an infectious clone of the bovine herpesvirus 1 genome maintained as a bacterial artificial chromosome (2002) J. Virol., 76, pp. 6660-6668
McGeoch, D.J., Evolutionary relationships of virion glycoprotein genes in the S regions of alphaherpesvirus genomes (1990) J. Gen. Virol., 71, pp. 2361-2367
Mechor, G.D., Rousseaux, C.G., Radostits, O.M., Babiuk, L.A., Petrie, L., Protection of newborn calves against fatal multisystemic infectious bovine rhinotracheitis by feeding colostrums from vaccinated cows (1987) Can. J. Vet. Res., 51, pp. 452-459
Meurens, F., Schynts, F., Keil, G.M., Muylkens, B., Vanderplasschen, A., Gallego, P., Thiry, E., Superinfection prevents recombination of the alphaherpesvirus bovine herpesvirus 1 (2004) J. Virol., 78, pp. 3872-3879
Meurens, F., Keil, G.M., Muylkens, B., Gogev, S., Schynts, F., Negro, S., Wiggers, L., Thiry, E., Interspecific recombination between two ruminant alphaherpesviruses, bovine herpesviruses 1 and 5 (2004) J. Virol., 78, pp. 9828-9836
Miller, J.M., Van Der Maaten, M.J., Reproductive tract lesions in heifers after intrauterine inoculation with infectious bovine rhinotracheitis virus (1984) Am. J. Vet. Res., 45, pp. 790-794
Nishiyama, Y., Kimura, H., Daikoku, T., Complementary lethal invasion of the central nervous system by non-neuroinvasive herpes simplex virus types 1 and 2 (1991) J. Virol., 65, pp. 4520-4524
Pasieka, T.J., Woolson, R.F., Grose, C., Viral induced fusion and syncytium formation: Measurement by the Kolmogorov-Smirnov statistical test (2003) J. Virol. Methods, 111, pp. 157-161
Rebordosa, X., Pinol, J., Perez-Pons, J.A., Lloberas, J., Naval, J., Serra-Hartmann, X., Espuna, E., Querol, E., Glycoprotein e of bovine herpesvirus type 1 is involved in virus transmission by direct cell-to-cell spread (1996) Virus Res., 45, pp. 59-68
Rijsewijk, F.A., Verschuren, S.B., Madic, J., Ruuls, R.C., Renaud, P., Van Oirschot, J.T., Spontaneous BHV1 recombinants in which the gI/gE/US9 region is replaced by a duplication/inversion of the US1.5/US2 region (1999) Arch. Virol., 144, pp. 1527-1537
Schmidt, J., Gerdts, V., Beyer, J., Klupp, B.G., Mettenleiter, T.C., Glycoprotein D-independent infectivity of pseudorabies virus results in an alteration of in vivo host range and correlates with mutations in glycoproteins B and H (2001) J. Virol., 75, pp. 10054-10064
Schröder, C., Linde, G., Fehler, F., Keil, G.M., From essential to beneficial: Glycoprotein D loses importance for replication of bovine herpesvirus 1 in cell culture (1997) J. Virol., 71, pp. 25-33
Schynts, F., Baranowski, E., Lemaire, M., Thiry, E., A specific PCR to differentiate between gE negative vaccine and wild-type bovine herpesvirus type 1 strains (1999) Vet. Microbiol., 66, pp. 187-195
Schynts, F., Vanderplasschen, A., Hanon, E., Rijsewijk, F.A., Van Oirschot, J.T., Thiry, E., Use of PCR and immunofluorescence to detect bovine herpesvirus 1 recombinants (2001) J. Virol. Methods, 92, pp. 99-104
Schynts, F., Meurens, F., Detry, B., Vanderplasschen, A., Thiry, E., Rise and survival of bovine herpesvirus 1 recombinants after primary infection and reactivation from latency (2003) J. Virol., 77, pp. 12535-12542
Smith, G., Young, P., Reed, K., Emergence of a new bovine herpesvirus 1 strain in Australian feedlots (1995) Arch. Virol., 140, pp. 599-603
Thiry, E., Meurens, F., Muylkens, B., McVoy, M., Gogev, S., Thiry, J., Vanderplasschen, A., Schynts, F., Recombination in alphaherpesviruses (2005) Rev. Med. Virol., 15, pp. 89-103
Tikoo, S.K., Campos, M., Babiuk, L.A., Bovine herpesvirus 1 (BHV-1): Biology, pathogenesis, and control (1995) Adv. Virus Res., 45, pp. 191-223
Trapp, S., Osterrieder, N., Keil, G.M., Beer, M., Mutagenesis of a bovine herpesvirus type 1 genome cloned as an infectious bacterial artificial chromosome: Analysis of glycoprotein e and G double deletion mutants (2003) J. Gen. Virol., 84, pp. 301-306
Umene, K., Intermolecular recombination of the herpes simplex virus type 1 genome analysed using two strains differing in restriction enzyme cleavage sites (1985) J. Gen. Virol., 66, pp. 2659-2670
Van Engelenburg, F.A., Kaashoek, M.J., Rijsewijk, F.A., Van Den Burg, L., Moerman, A., Gielkens, A.L., Van Oirschot, J.T., A glycoprotein e deletion mutant of bovine herpesvirus 1 is avirulent in calves (1994) J. Gen. Virol., 75, pp. 2311-2318
Van Oirschot, J.T., Kaasohoek, M.J., Maris-Veldhuis, M.A., Weerd-Meester, K., Rijsewijk, F.A., An enzyme-linked immunosorbent assay to detect antibodies against glycoprotein e of bovine herpesvirus 1 allows differentiation between infected and vaccinated cattle (1997) J. Virol. Methods., 67, pp. 23-34
Whitbeck, J.C., Knapp, A.C., Enquist, L.W., Lawrence, W.C., Bello, L.J., Synthesis, processing, and oligomerization of bovine herpesvirus 1 gE and gI membrane proteins (1996) J. Virol., 70, pp. 7878-7884
York, C.J., Schwartz, A.J., Estela, L.A., The isolation and identification of infectious bovine rhinotracheitis virus in tissue culture (1957) P. S. E. B. M., 94, pp. 740-744