1887

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Volume 95, Issue 12

Human herpesvirus 6 gM/gN complex interacts with v-SNARE in infected cells Free

Abstract

Human herpesvirus 6 (HHV-6) glycoprotein M (gM) is an envelope glycoprotein that associates with glycoprotein N (gN), forming the gM/gN protein complex, in a similar manner to the other herpesviruses. Liquid chromatography-MS/MS analysis showed that the HHV-6 gM/gN complex interacts with the v-SNARE protein, vesicle-associated membrane protein 3 (VAMP3). VAMP3 colocalized with the gM/gN complex at the -Golgi network and other compartments, possibly the late endosome in HHV-6-infected cells, and its expression gradually increased during the late phase of virus infection. Finally, VAMP3 was incorporated into mature virions and may be transported with the gM/gN complex.

  • Received:
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© 2014 The Authors
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2014-12-01
2024-04-26
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References

  1. Ablashi D. V., Balachandran N., Josephs S. F., Hung C. L., Krueger G. R., Kramarsky B., Salahuddin S. Z., Gallo R. C. 1991; Genomic polymorphism, growth properties, and immunologic variations in human herpesvirus-6 isolates. Virology 184:545–552 [View Article][PubMed]
     [Google Scholar]
  2. Ablashi D., Agut H., Alvarez-Lafuente R., Clark D. A., Dewhurst S., Diluca D., Flamand L., Frenkel N., Gallo R.other authors 2014; Classification of HHV-6A and HHV-6B as distinct viruses. Arch Virol 159:863–870 [View Article][PubMed]
     [Google Scholar]
  3. Akkapaiboon P., Mori Y., Sadaoka T., Yonemoto S., Yamanishi K. 2004; Intracellular processing of human herpesvirus 6 glycoproteins Q1 and Q2 into tetrameric complexes expressed on the viral envelope. J Virol 78:7969–7983 [View Article][PubMed]
     [Google Scholar]
  4. Aubin J. T., Collandre H., Candotti D., Ingrand D., Rouzioux C., Burgard M., Richard S., Huraux J. M., Agut H. 1991; Several groups among human herpesvirus 6 strains can be distinguished by Southern blotting and polymerase chain reaction. J Clin Microbiol 29:367–372[PubMed]
     [Google Scholar]
  5. Baines J. D., Roizman B. 1991; The open reading frames UL3, UL4, UL10, and UL16 are dispensable for the replication of herpes simplex virus 1 in cell culture. J Virol 65:938–944[PubMed]
     [Google Scholar]
  6. Borisovska M., Zhao Y., Tsytsyura Y., Glyvuk N., Takamori S., Matti U., Rettig J., Südhof T., Bruns D. 2005; v-SNAREs control exocytosis of vesicles from priming to fusion. EMBO J 24:2114–2126 [View Article][PubMed]
     [Google Scholar]
  7. Campadelli-Fiume G., Guerrini S., Xiaoming L., Foà-Tomasi L. 1993; Monoclonal antibodies to glycoprotein B differentiate human herpesvirus 6 into two clusters, variants A and B. J Gen Virol 74:2257–2262 [View Article][PubMed]
     [Google Scholar]
  8. Chandran B., Tirawatnapong S., Pfeiffer B., Ablashi D. V. 1992; Antigenic relationships among human herpesvirus-6 isolates. J Med Virol 37:247–254 [View Article][PubMed]
     [Google Scholar]
  9. Dijkstra J. M., Visser N., Mettenleiter T. C., Klupp B. G. 1996; Identification and characterization of pseudorabies virus glycoprotein gM as a nonessential virion component. J Virol 70:5684–5688[PubMed]
     [Google Scholar]
  10. Galli T., Chilcote T., Mundigl O., Binz T., Niemann H., De Camilli P. 1994; Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells. J Cell Biol 125:1015–1024 [View Article][PubMed]
     [Google Scholar]
  11. Hobom U., Brune W., Messerle M., Hahn G., Koszinowski U. H. 2000; Fast screening procedures for random transposon libraries of cloned herpesvirus genomes: mutational analysis of human cytomegalovirus envelope glycoprotein genes. J Virol 74:7720–7729 [View Article][PubMed]
     [Google Scholar]
  12. Hu C., Hardee D., Minnear F. 2007; Membrane fusion by VAMP3 and plasma membrane t-SNAREs. Exp Cell Res 313:3198–3209 [View Article][PubMed]
     [Google Scholar]
  13. Jahn R., Scheller R. H. 2006; SNAREs–engines for membrane fusion. Nat Rev Mol Cell Biol 7:631–643 [View Article][PubMed]
     [Google Scholar]
  14. Jahn R., Lang T., Südhof T. C. 2003; Membrane fusion. Cell 112:519–533 [View Article][PubMed]
     [Google Scholar]
  15. Kawabata A., Jasirwan C., Yamanishi K., Mori Y. 2012; Human herpesvirus 6 glycoprotein M is essential for virus growth and requires glycoprotein N for its maturation. Virology 429:21–28 [View Article][PubMed]
     [Google Scholar]
  16. Koshizuka T., Ota M., Yamanishi K., Mori Y. 2010; Characterization of varicella-zoster virus-encoded ORF0 gene–comparison of parental and vaccine strains. Virology 405:280–288 [View Article][PubMed]
     [Google Scholar]
  17. Krzyzaniak M. A., Mach M., Britt W. J. 2009; HCMV-encoded glycoprotein M (UL100) interacts with Rab11 effector protein FIP4. Traffic 10:1439–1457 [View Article][PubMed]
     [Google Scholar]
  18. Lawrence G. L., Nicholas J., Barrell B. G. 1995; Human herpesvirus 6 (strain U1102) encodes homologues of the conserved herpesvirus glycoprotein gM and the alphaherpesvirus origin-binding protein. J Gen Virol 76:147–152 [View Article][PubMed]
     [Google Scholar]
  19. Luftman K., Hasan N., Day P., Hardee D., Hu C. 2009; Silencing of VAMP3 inhibits cell migration and integrin-mediated adhesion. Biochem Biophys Res Commun 380:65–70 [View Article][PubMed]
     [Google Scholar]
  20. McMahon H. T., Ushkaryov Y. A., Edelmann L., Link E., Binz T., Niemann H., Jahn R., Südhof T. C. 1993; Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein. Nature 364:346–349 [View Article][PubMed]
     [Google Scholar]
  21. Mohrmann R., Sørensen J. B. 2012; SNARE requirements en route to exocytosis: from many to few. J Mol Neurosci 48:387–394 [View Article][PubMed]
     [Google Scholar]
  22. Mori Y. 2009; Recent topics related to human herpesvirus 6 cell tropism. Cell Microbiol 11:1001–1006 [View Article][PubMed]
     [Google Scholar]
  23. Mori Y., Akkapaiboon P., Yonemoto S., Koike M., Takemoto M., Sadaoka T., Sasamoto Y., Konishi S., Uchiyama Y., Yamanishi K. 2004; Discovery of a second form of tripartite complex containing gH-gL of human herpesvirus 6 and observations on CD46. J Virol 78:4609–4616 [View Article][PubMed]
     [Google Scholar]
  24. Mori Y., Koike M., Moriishi E., Kawabata A., Tang H., Oyaizu H., Uchiyama Y., Yamanishi K. 2008; Human herpesvirus-6 induces MVB formation, and virus egress occurs by an exosomal release pathway. Traffic 9:1728–1742 [View Article][PubMed]
     [Google Scholar]
  25. Niwa H., Yamamura K., Miyazaki J. 1991; Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193–199 [View Article][PubMed]
     [Google Scholar]
  26. Osterrieder N., Neubauer A., Brandmuller C., Braun B., Kaaden O. R., Baines J. D. 1996; The equine herpesvirus 1 glycoprotein gp21/22a, the herpes simplex virus type 1 gM homolog, is involved in virus penetration and cell-to-cell spread of virions. J Virol 70:4110–4115[PubMed]
     [Google Scholar]
  27. Polgár J., Chung S. H., Reed G. L. 2002; Vesicle-associated membrane protein 3 (VAMP-3) and VAMP-8 are present in human platelets and are required for granule secretion. Blood 100:1081–1083 [View Article][PubMed]
     [Google Scholar]
  28. Roizmann B., Desrosiers R. C., Fleckenstein B., Lopez C., Minson A. C., Studdert M. J.The Herpesvirus Study Group of the International Committee on Taxonomy of Viruses 1992; The family Herpesviridae: an update. Arch Virol 123:425–449 [View Article][PubMed]
     [Google Scholar]
  29. Rothman J. E. 1994; Mechanisms of intracellular protein transport. Nature 372:55–63 [View Article][PubMed]
     [Google Scholar]
  30. Shevchenko A., Wilm M., Vorm O., Mann M. 1996; Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68:850–858 [View Article][PubMed]
     [Google Scholar]
  31. Söllner T., Whiteheart S. W., Brunner M., Erdjument-Bromage H., Geromanos S., Tempst P., Rothman J. E. 1993; SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318–324 [View Article][PubMed]
     [Google Scholar]
  32. Takemoto M., Koike M., Mori Y., Yonemoto S., Sasamoto Y., Kondo K., Uchiyama Y., Yamanishi K. 2005; Human herpesvirus 6 open reading frame U14 protein and cellular p53 interact with each other and are contained in the virion. J Virol 79:13037–13046 [View Article][PubMed]
     [Google Scholar]
  33. Tang H., Serada S., Kawabata A., Ota M., Hayashi E., Naka T., Yamanishi K., Mori Y. 2013; CD134 is a cellular receptor specific for human herpesvirus-6B entry. Proc Natl Acad Sci U S A 110:9096–9099 [View Article][PubMed]
     [Google Scholar]
  34. Tayeb M. A., Skalski M., Cha M. C., Kean M. J., Scaife M., Coppolino M. G. 2005; Inhibition of SNARE-mediated membrane traffic impairs cell migration. Exp Cell Res 305:63–73 [View Article][PubMed]
     [Google Scholar]
  35. Tischer B. K., Schumacher D., Messerle M., Wagner M., Osterrieder N. 2002; The products of the UL10 (gM) and the UL49.5 genes of Marek’s disease virus serotype 1 are essential for virus growth in cultured cells. J Gen Virol 83:997–1003[PubMed]
     [Google Scholar]
  36. Veale K. J., Offenhäuser C., Lei N., Stanley A. C., Stow J. L., Murray R. Z. 2011; VAMP3 regulates podosome organisation in macrophages and together with Stx4/SNAP23 mediates adhesion, cell spreading and persistent migration. Exp Cell Res 317:1817–1829 [View Article][PubMed]
     [Google Scholar]
  37. Yamagishi Y., Sadaoka T., Yoshii H., Somboonthum P., Imazawa T., Nagaike K., Ozono K., Yamanishi K., Mori Y. 2008; Varicella-zoster virus glycoprotein M homolog is glycosylated, is expressed on the viral envelope, and functions in virus cell-to-cell spread. J Virol 82:795–804 [View Article][PubMed]
     [Google Scholar]
  38. Yamanishi K., Shiraki K., Kondo T., Okuno T., Takahashi M., Asano Y., Kurata T. 1988; Identification of human herpesvirus-6 as a causal agent for exanthem subitum. Lancet 331:1065–1067 [View Article][PubMed]
     [Google Scholar]
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Human herpesvirus 6 gM/gN complex interacts with v-SNARE in infected cells
J. Gen. Virol. 95, 2769 (2014); https://doi.org/10.1099/vir.0.069336-0
/content/journal/jgv/10.1099/vir.0.069336-0
/content/journal/jgv/10.1099/vir.0.069336-0
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