[en] All gammaherpesviruses encode a glycoprotein positionally homologous to the Epstein-Barr virus gp350 and the Kaposi's Sarcoma associated herpesvirus (KSHV) K8.1. In this study, we characterized that of Bovine Herpesvirus-4 (BoHV-4), encoded by the Bo10 gene. We identified a 180 kDa gene product, gp180, which was incorporated into the virion envelope. A Bo10 deletion virus was viable, but showed a growth deficit associated with reduced binding to epithelial cells. This seemed to reflect an interaction of gp180 with glycosaminoglycans (GAGs), since the Bo10 mutant was both less infectious for GAG(+) cells than the wild-type and more infectious for GAG(-) cells. However, we could not identify a direct interaction between gp180 and GAGs, implying that any direct interaction must be of low affinity. This function of gp180 was very similar to that previously identified for the Murid Herpesvirus 4 gp150, and also to the Epstein-Barr virus gp350 that promotes CD21(+) cell infection and inhibits CD21(-) cell infection. We propose that such proteins generally regulate virion attachment both by binding to cells and by covering another receptor-binding protein until they are displaced. Thus they regulate viral tropism both positively and negatively depending upon the presence or absence of their receptor.
Disciplines :
Microbiology
Author, co-author :
Machiels, Bénédicte ; Université de Liège - ULiège > Immunologie et vaccinologie
Lété, Céline ; Université de Liège - ULiège > Immunologie et vaccinologie
Defays, Katalin; Université de Liège - ULiège > Immunologie et vaccinologie
Mast, Jan; Université de Liège - ULiège
Dewals, Benjamin G ; Université de Liège - ULiège > Immunologie et vaccinologie
Stevenson, Philip G.; University of Cambridge (UK) > Department of Pathology > Division of Virology
Baeuerle, P. A., and W. B. Huttner. 1986. Chlorate-a potent inhibitor of protein sulfation in intact cells. Biochem. Biophys. Res. Commun. 141:870-877.
Birkmann, A., K. Mahr, A. Ensser, S. Yaguboglu, F. Titgemeyer, B. Fleckenstein, and F. Neipel. 2001. Cell surface heparan sulfate is a receptor for human herpesvirus 8 and interacts with envelope glycoprotein K8.1. J. Virol. 75:11583-11593.
Boerner, B., W. Weigelt, H. J. Buhk, G. Castrucci, and H. Ludwig. 1999. Asensitive and specific PCR/Southern blot assay for detection of bovine herpesvirus 4 in calves infected experimentally. J. Virol. Methods 83:169-180.
Borza, C. M., and L. M. Hutt-Fletcher. 2002. Alternate replication in B cells and epithelial cells switches tropism of Epstein-Barr virus. Nat. Med. 8:594-599
Bublot, M., M. F. Van Bressem, E. Thiry, J. Dubuisson, and P. P. Pastoret. 1990. Bovine herpesvirus 4 genome: cloning, mapping and strain variation analysis. J. Gen. Virol. 71:133-142.
Chandran, B., C. Bloomer, S. R. Chan, L. Zhu, E. Goldstein, and R. Horvat. 1998. Human herpesvirus-8 ORF K8.1 gene encodes immunogenic glycoproteins generated by spliced transcripts. Virology 249:140-149.
de Lima, B. D., J. S. May, and P. G. Stevenson. 2004. Murine gammaherpesvirus 68 lacking gp150 shows defective virion release but establishes normal latency in vivo. J. Virol. 78:5103-5112.
Dingwell, K. S., C. R. Brunetti, R. L. Hendricks, Q. Tang, M. Tang, A. J. Rainbow, and D. C. Johnson. 1994. Herpes simplex virus glycoproteins E and I facilitate cell-to-cell spread in vivo and across junctions of cultured cells. J. Virol. 68:834-845.
Dubuisson, J., I. Koromyslov, P. P. Pastoret, and E. Thiry. 1992. Proteins of bovine herpesvirus type 4 released into the culture medium of productively infected cells: identification of a 135K glycoprotein involved in viral attachment. J. Gen. Virol. 73:189-194.
Fabian, K., R. Ivanics, M. Terenyi, and L. Egyed. 2005. Detection of bovine herpesvirus 4 in CD11b+ leukocytes of experimentally infected rabbits. Acta Vet. Hung. 53:265-273.
Gillet, L., H. Adler, and P. G. Stevenson. 2007. Glycosaminoglycan interactions in murine gammaherpesvirus-68 infection. PLoS One 2:e347.
Gillet, L., S. Colaco, and P. G. Stevenson. 2008. The murid herpesvirus-4 gH/gL binds to glycosaminoglycans. PLoS One 3:e1669.
Gillet, L., V. Daix, G. Donofrio, M. Wagner, U. H. Koszinowski, B. China, M. Ackermann, N. Markine-Goriaynoff, and A. Vanderplasschen. 2005. Development of bovine herpesvirus 4 as an expression vector using bacterial artificial chromosome cloning. J. Gen. Virol. 86:907-917.
Gillet, L., J. S. May, S. Colaco, and P. G. Stevenson. 2007. Glycoprotein L disruption reveals two functional forms of the murine gammaherpesvirus 68 glycoprotein H. J. Virol. 81:280-291.
Gillet, L., J. S. May, S. Colaco, and P. G. Stevenson. 2007. The murine gammaherpesvirus-68 gp150 acts as an immunogenic decoy to limit virion neutralization. PLoS One 2:e705.
Gillet, L., J. S. May, and P. G. Stevenson. 2009. In vivo importance of heparan sulfate-binding glycoproteins for murid herpesvirus-4 infection. J. Gen. Virol. 90:602-613.
Gillet, L., F. Minner, B. Detry, F. Farnir, L. Willems, M. Lambot, E. Thiry, P. P. Pastoret, F. Schynts, and A. Vanderplasschen. 2004. Investigation of the susceptibility of human cell lines to bovine herpesvirus 4 infection: demonstration that human cells can support a nonpermissive persistent infection which protects them against tumor necrosis factor alpha-induced apoptosis. J. Virol. 78:2336-2347.
Gillet, L., H. Schroeder, J. Mast, M. Thirion, J. C. Renauld, B. Dewals, and A. Vanderplasschen. 2009. Anchoring tick salivary anti-complement proteins IRAC I and IRAC II to membrane increases their immunogenicity. Vet. Res. 40:51.
Gillet, L., and P. G. Stevenson. 2007. Antibody evasion by the N terminus of murid herpesvirus-4 glycoprotein B. EMBO J. 26:5131-5142.
Gillet, L., and P. G. Stevenson. 2007. Evidence for a multiprotein gamma-2 herpesvirus entry complex. J. Virol. 81:13082-13091.
Habuchi, H., O. Habuchi, and K. Kimata. 2004. Sulfation pattern in glycosaminoglycan: does it have a code? Glycoconj. J. 21:47-52.
Heldwein, E. E., and C. Krummenacher. 2008. Entry of herpesviruses into mammalian cells. Cell. Mol. Life Sci. 65:1653-1668.
Herrold, R. E., A. Marchini, S. Fruehling, and R. Longnecker. 1996. Glycoprotein 110, the Epstein-Barr virus homolog of herpes simplex virus glycoprotein B, is essential for Epstein-Barr virus replication in vivo. J. Virol. 70:2049-2054.
Hutt-Fletcher, L. M. 2007. Epstein-Barr virus entry. J. Virol. 81:7825-7832.
Janz, A., M. Oezel, C. Kurzeder, J. Mautner, D. Pich, M. Kost, W. Hammerschmidt, and H. J. Delecluse. 2000. Infectious Epstein-Barr virus lacking major glycoprotein BLLF1 (gp350/220) demonstrates the existence of additional viral ligands. J. Virol. 74:10142-10152.
Johannsen, E., M. Luftig, M. R. Chase, S. Weicksel, E. Cahir-McFarland, D. Illanes, D. Sarracino, and E. Kieff. 2004. Proteins of purified Epstein-Barr virus. Proc. Natl. Acad. Sci. U. S. A. 101:16286-16291.
Karger, A., U. Schmidt, and U. J. Buchholz. 2001. Recombinant bovine respiratory syncytial virus with deletions of the G or SH genes: G and F proteins bind heparin. J. Gen. Virol. 82:631-640.
Kit, S., M. Kit, H. Ichimura, R. Crandell, and S. McConnell. 1986. Induction of thymidine kinase activity by viruses with group B DNA genomes: bovine cytomegalovirus (bovine herpesvirus 4). Virus Res. 4:197-212.
Kolset, S. O. 1987. Proteoglycans in normal and neoplastic monocytes. Exp. Cell Res. 168:318-324.
Li, M., J. MacKey, S. C. Czajak, R. C. Desrosiers, A. A. Lackner, and J. U. Jung. 1999. Identification and characterization of Kaposi's sarcoma-associated herpesvirus K8.1 virion glycoprotein. J. Virol. 73:1341-1349.
Lomonte, P., M. Bublot, V. van Santen, G. M. Keil, P. P. Pastoret, and E. Thiry. 1995. Analysis of bovine herpesvirus 4 genomic regions located outside the conserved gammaherpesvirus gene blocks. J. Gen. Virol. 76:1835-1841.
Lomonte, P., P. Filee, J. R. Lyaku, M. Bublot, P. P. Pastoret, and E. Thiry. 1997. Analysis of the biochemical properties of, and complex formation between, glycoproteins H and L of the gamma2 herpesvirus bovine herpesvirus-4. J. Gen. Virol. 78:2015-2023.
Lopez, O. J., J. A. Galeota, and F. A. Osorio. 1996. Bovine herpesvirus type-4 (BHV-4) persistently infects cells of the marginal zone of spleen in cattle. Microb. Pathog. 21:47-58.
Luna, R. E., F. Zhou, A. Baghian, V. Chouljenko, B. Forghani, S. J. Gao, and K. G. Kousoulas. 2004. Kaposi's sarcoma-associated herpesvirus glycoprotein K8.1 is dispensable for virus entry. J. Virol. 78:6389-6398.
Markine-Goriaynoff, N., L. Gillet, O. A. Karlsen, L. Haarr, F. Minner, P. P. Pastoret, M. Fukuda, and A. Vanderplasschen. 2004. The core 2 beta-1,6-N-acetylglucosaminyltransferase-M encoded by bovine herpesvirus 4 is not essential for virus replication despite contributing to translational modifications of structural proteins. J. Gen. Virol. 85:355-367.
Marsh, M., and A. Helenius. 2006. Virus entry: open sesame. Cell 124:729-740.
Maruo, S., L. Yang, and K. Takada. 2001. Roles of Epstein-Barr virus glycoproteins gp350 and gp25 in the infection of human epithelial cells. J. Gen. Virol. 82:2373-2383.
Mast, J., C. Nanbru, T. van den Berg, and G. Meulemans. 2005. Ultrastructural changes of the tracheal epithelium after vaccination of day-old chickens with the La Sota strain of Newcastle disease virus. Vet. Pathol. 42:559-565.
Means, R. E. 2004. Characterization of the herpesvirus saimiri Orf51 protein. Virology 326:67-78.
Molesworth, S. J., C. M. Lake, C. M. Borza, S. M. Turk, and L. M. Hutt-Fletcher. 2000. Epstein-Barr virus gH is essential for penetration of B cells but also plays a role in attachment of virus to epithelial cells. J. Virol. 74:6324-6332.
Nemerow, G. R., C. Mold, V. K. Schwend, V. Tollefson, and N. R. Cooper. 1987. Identification of gp350 as the viral glycoprotein mediating attachment of Epstein-Barr virus (EBV) to the EBV/C3d receptor of B cells: sequence homology of gp350 and C3 complement fragment C3d. J. Virol. 61:1416-1420.
Pertel, P. E. 2002. Human herpesvirus 8 glycoprotein B (gB), gH, and gL can mediate cell fusion. J. Virol. 76:4390-4400.
Rosa, G. T., L. Gillet, C. M. Smith, B. D. de Lima, and P. G. Stevenson. 2007. IgG Fc receptors provide an alternative infection route for murine gammaherpesvirus-68. PLoS One 2:e560.
Safaiyan, F., S. O. Kolset, K. Prydz, E. Gottfridsson, U. Lindahl, and M. Salmivirta. 1999. Selective effects of sodium chlorate treatment on the sulfation of heparan sulfate. J. Biol. Chem. 274:36267-36273.
Sakamoto, K., H. Asanuma, T. Nakamura, T. Kanno, T. Sata, and H. Katano. 2010. Immune response to intranasal and intraperitoneal immunization with Kaposi's sarcoma-associated herpesvirus in mice. Vaccine 28:3325-3332.
Serafini-Cessi, F., N. Malagolini, M. Nanni, F. Dall'Olio, G. Campadelli-Fiume, J. Tanner, and E. Kieff. 1989. Characterization of N-and O-linked oligosaccharides of glycoprotein 350 from Epstein-Barr virus. Virology 170: 1-10.
Shannon-Lowe, C. D., B. Neuhierl, G. Baldwin, A. B. Rickinson, and H. J. Delecluse. 2006. Resting B cells as a transfer vehicle for Epstein-Barr virus infection of epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 103:7065-7070.
Spear, P. G., and R. Longnecker. 2003. Herpesvirus entry: an update. J. Virol. 77:10179-10185.
Stewart, J. P., N. J. Janjua, S. D. Pepper, G. Bennion, M. Mackett, T. Allen, A. A. Nash, and J. R. Arrand. 1996. Identification and characterization of murine gammaherpesvirus 68 gp150: a virion membrane glycoprotein. J. Virol. 70:3528-3535.
Tanner, J., J. Weis, D. Fearon, Y. Whang, and E. Kieff. 1987. Epstein-Barr virus gp350/220 binding to the B lymphocyte C3d receptor mediates adsorption, capping, and endocytosis. Cell 50:203-213.
Thiry, E., M. Bublot, J. Dubuisson, M. F. Van Bressem, A. S. Lequarre, P. Lomonte, A. Vanderplasschen, and P. P. Pastoret. 1992. Molecular biology of bovine herpesvirus type 4. Vet. Microbiol. 33:79-92.
Thiry, E., P. P. Pastoret, C. Dessy-Doizé, C. Hanzen, and C. M. Calberg-Bacq. 1981. Herpesvirus in infertile bull's testicle. Vet. Rec. 108:426.
Thorley-Lawson, D. A., and C. M. Edson. 1979. Polypeptides of the Epstein-Barr virus membrane antigen complex. J. Virol. 32:458-467.
Thorley-Lawson, D. A., and C. A. Poodry. 1982. Identification and isolation of the main component (gp350-gp220) of Epstein-Barr virus responsible for generating neutralizing antibodies in vivo. J. Virol. 43:730-736.
Turk, S. M., R. Jiang, L. S. Chesnokova, and L. M. Hutt-Fletcher. 2006. Antibodies to gp350/220 enhance the ability of Epstein-Barr virus to infect epithelial cells. J. Virol. 80:9628-9633.
Turnbull, J., A. Powell, and S. Guimond. 2001. Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol. 11:75-82.
Vanderplasschen, A., M. Bublot, J. Dubuisson, P. P. Pastoret, and E. Thiry. 1993. Attachment of the gammaherpesvirus bovine herpesvirus 4 is mediated by the interaction of gp8 glycoprotein with heparinlike moieties on the cell surface. Virology 196:232-240.
van Santen, V. L. 1991. Characterization of the bovine herpesvirus 4 major immediate-early transcript. J. Virol. 65:5211-5224.
Wu, L., R. Renne, D. Ganem, and B. Forghani. 2000. Human herpesvirus 8 glycoprotein K8.1: expression, post-translational modification and localization analyzed by monoclonal antibody. J. Clin. Virol. 17:127-136.
Zhu, L., V. Puri, and B. Chandran. 1999. Characterization of human herpesvirus-8 K8.1A/B glycoproteins by monoclonal antibodies. Virology 262: 237-249.
Zimmermann, W., H. Broll, B. Ehlers, H. J. Buhk, A. Rosenthal, and M. Goltz. 2001. Genome sequence of bovine herpesvirus 4, a bovine Rhadinovirus, and identification of an origin of DNA replication. J. Virol. 75:1186-1194.
