Journal of General Virology, Vol 80, 1283-1291, Copyright © 1999 by Society for General Microbiology

ARTICLES

Antibody-induced endocytosis of viral glycoproteins and major histocompatibility complex class I on pseudorabies virus-infected monocytes

HW Favoreel, HJ Nauwynck, HM Halewyck, P Van Oostveldt, TC Mettenleiter and MB Pensaert
Laboratory of Virology, Faculty of Veterinary Medicine, University of Gent, Salisburylaan 133, B-9820 Merelbeke, Belgium

Purified porcine monocytes, the natural carrier cells of pseudorabies virus (PrV) in the pig, were inoculated in vitro with PrV. At different time-points post-inoculation (p.i.) (from 7 to 17 h p.i.), the cells were washed and incubated with fluorescein isothiocyanate-labelled porcine PrV-specific polyclonal antibodies (IgG) at 37 degrees C. At all time-points tested p.i., 1 h of antibody incubation induced passive patching and subsequent internalization of the plasma membrane-anchored viral glycoproteins in approximately 65% of the infected monocytes. This endocytosis process is antibody-dependent, since biotinylated glycoproteins did not undergo spontaneous endocytosis. The process is fast and efficient, since only very low amounts of viral glycoproteins on the plasma membrane (7 h p.i.) and a minimal concentration of antibodies (0.04 mg IgG/ml) were needed to induce endocytosis. Experiments with PrV strains carrying deletions in the genes encoding the 11 different viral glycoproteins showed that viral glycoproteins gB and gD play a very important role in endocytosis (80% reduction with deletion mutants, P <0.001), while the gE:gI Fc receptor complex, but not gE or gI alone, has a significant but lesser effect (45% reduction, P <0.05). Double staining of viral glycoproteins and major histocompatibility complex class I (MHC I) showed a clear co-localization and co-endocytosis of MHC I with the viral glycoproteins, suggesting a possible role of the process in immune evasion of the virus.

This article has been cited by other articles:

				I. Beitia Ortiz de Zarate, L. Cantero-Aguilar, M. Longo, C. Berlioz-Torrent, and F. Rozenberg Contribution of Endocytic Motifs in the Cytoplasmic Tail of Herpes Simplex Virus Type 1 Glycoprotein B to Virus Replication and Cell-Cell Fusion J. Virol., December 15, 2007; 81(24): 13889 - 13903. [Abstract] [Full Text] [PDF]

				A. Calistri, P. Sette, C. Salata, E. Cancellotti, C. Forghieri, A. Comin, H. Gottlinger, G. Campadelli-Fiume, G. Palu, and C. Parolin Intracellular Trafficking and Maturation of Herpes Simplex Virus Type 1 gB and Virus Egress Require Functional Biogenesis of Multivesicular Bodies J. Virol., October 15, 2007; 81(20): 11468 - 11478. [Abstract] [Full Text] [PDF]

				M. Krzyzaniak, M. Mach, and W. J. Britt The Cytoplasmic Tail of Glycoprotein M (gpUL100) Expresses Trafficking Signals Required for Human Cytomegalovirus Assembly and Replication J. Virol., October 1, 2007; 81(19): 10316 - 10328. [Abstract] [Full Text] [PDF]

				S. Costers, P. L. Delputte, and H. J. Nauwynck Porcine reproductive and respiratory syndrome virus-infected alveolar macrophages contain no detectable levels of viral proteins in their plasma membrane and are protected against antibody-dependent, complement-mediated cell lysis. J. Gen. Virol., August 1, 2006; 87(Pt 8): 2341 - 2351. [Abstract] [Full Text] [PDF]

				H. L. Dewerchin, E. Cornelissen, and H. J. Nauwynck Feline infectious peritonitis virus-infected monocytes internalize viral membrane-bound proteins upon antibody addition J. Gen. Virol., June 1, 2006; 87(6): 1685 - 1690. [Abstract] [Full Text] [PDF]

				J. Ficinska, G. Van Minnebruggen, H. J. Nauwynck, K. Bienkowska-Szewczyk, and H. W. Favoreel Pseudorabies Virus Glycoprotein gD Contains a Functional Endocytosis Motif That Acts in Concert with an Endocytosis Motif in gB To Drive Internalization of Antibody-Antigen Complexes from the Surface of Infected Monocytes J. Virol., June 1, 2005; 79(11): 7248 - 7254. [Abstract] [Full Text] [PDF]

				L. Maresova, T. J. Pasieka, E. Homan, E. Gerday, and C. Grose Incorporation of Three Endocytosed Varicella-Zoster Virus Glycoproteins, gE, gH, and gB, into the Virion Envelope J. Virol., January 15, 2005; 79(2): 997 - 1007. [Abstract] [Full Text] [PDF]

				G. Van Minnebruggen, H. W. Favoreel, and H. J. Nauwynck Internalization of Pseudorabies Virus Glycoprotein B Is Mediated by an Interaction between the YQRL Motif in Its Cytoplasmic Domain and the Clathrin-Associated AP-2 Adaptor Complex J. Virol., August 15, 2004; 78(16): 8852 - 8859. [Abstract] [Full Text] [PDF]

				H. W. Favoreel, T. C. Mettenleiter, and H. J. Nauwynck Copatching and Lipid Raft Association of Different Viral Glycoproteins Expressed on the Surfaces of Pseudorabies Virus-Infected Cells J. Virol., May 15, 2004; 78(10): 5279 - 5287. [Abstract] [Full Text] [PDF]

				H. W. Favoreel, G. R. Van de Walle, H. J. Nauwynck, T. C. Mettenleiter, and M. B. Pensaert Pseudorabies virus (PRV)-specific antibodies suppress intracellular viral protein levels in PRV-infected monocytes J. Gen. Virol., November 1, 2003; 84(11): 2969 - 2973. [Abstract] [Full Text] [PDF]

				G. R. Van de Walle, H. W. Favoreel, H. J. Nauwynck, and M. B. Pensaert Antibody-induced internalization of viral glycoproteins and gE-gI Fc receptor activity protect pseudorabies virus-infected monocytes from efficient complement-mediated lysis J. Gen. Virol., April 1, 2003; 84(4): 939 - 947. [Abstract] [Full Text] [PDF]

				G. R. Van de Walle, H. W. Favoreel, H. J. Nauwynck, T. C. Mettenleiter, and M. B. Pensaert Transmission of pseudorabies virus from immune-masked blood monocytes to endothelial cells J. Gen. Virol., March 1, 2003; 84(3): 629 - 637. [Abstract] [Full Text] [PDF]

				H. W. Favoreel, G. R. Van de Walle, H. J. Nauwynck, and M. B. Pensaert Virus complement evasion strategies J. Gen. Virol., January 1, 2003; 84(1): 1 - 15. [Abstract] [Full Text] [PDF]

				K. M. van der Meulen, H. J. Nauwynck, and M. B. Pensaert Absence of viral antigens on the surface of equine herpesvirus-1-infected peripheral blood mononuclear cells: a strategy to avoid complement-mediated lysis J. Gen. Virol., January 1, 2003; 84(1): 93 - 97. [Abstract] [Full Text] [PDF]

				S. M. Rizvi and M. Raghavan Responses of Herpes Simplex Virus Type 1-Infected Cells to the Presence of Extracellular Antibodies: gE-Dependent Glycoprotein Capping and Enhancement in Cell-to-Cell Spread J. Virol., December 6, 2002; 77(1): 701 - 708. [Abstract] [Full Text] [PDF]

				H. W. Favoreel, G. Van Minnebruggen, H. J. Nauwynck, L. W. Enquist, and M. B. Pensaert A Tyrosine-Based Motif in the Cytoplasmic Tail of Pseudorabies Virus Glycoprotein B Is Important for both Antibody-Induced Internalization of Viral Glycoproteins and Efficient Cell-to-Cell Spread J. Virol., June 5, 2002; 76(13): 6845 - 6851. [Abstract] [Full Text] [PDF]

				G. Reiner, E. Melchinger, M. Kramarova, E. Pfaff, M. Buttner, A. Saalmuller, and H. Geldermann Detection of quantitative trait loci for resistance/susceptibility to pseudorabies virus in swine J. Gen. Virol., January 1, 2002; 83(1): 167 - 172. [Abstract] [Full Text] [PDF]