1887

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Volume 91, Issue 9

Inner tegument protein pUL37 of herpes simplex virus type 1 is involved in directing capsids to the -Golgi network for envelopment Open Access

Abstract

Secondary envelopment of herpes simplex virus type 1 has been demonstrated as taking place at the -Golgi network (TGN). The inner tegument proteins pUL36 and pUL37 and the envelope glycoproteins gD and gE are known to be important for secondary envelopment. We compared the cellular localizations of capsids from a virus mutant lacking the UL37 gene with those of a virus mutant lacking the genes encoding gD and gE. Although wild-type capsids accumulated at the TGN, capsids of the pUL37 mutant were distributed throughout the cytoplasm and showed no association with TGN-derived vesicles. This was in contrast to capsids from a gDgE mutant, which accumulated in the vicinity of TGN vesicles, but did not colocalize with them, suggesting that they were transported to the TGN but were unable to undergo envelopment. We conclude that the inner tegument protein pUL37 is required for directing capsids to the TGN, where secondary envelopment occurs.

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2010-09-01
2024-04-19
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References

  1. Baines, J. D. & Roizman, B.(1992). The UL11 gene of herpes simplex virus 1 encodes a function that facilitates nucleocapsid envelopment and egress from cells. J Virol 66, 5168–5174. [Google Scholar]
  2. Baines, J. D., Ward, P. L., Campadelli-Fiume, G. & Roizman, B.(1991). The UL20 gene of herpes simplex virus 1 encodes a function necessary for viral egress. J Virol 65, 6414–6424. [Google Scholar]
  3. Bechtel, J. T. & Shenk, T.(2002). Human cytomegalovirus UL47 tegument protein functions after entry and before immediate-early gene expression. J Virol 76, 1043–1050.[CrossRef] [Google Scholar]
  4. Brack, A. R., Dijkstra, J. M., Granzow, H., Klupp, B. G. & Mettenleiter, T. C.(1999). Inhibition of virion maturation by simultaneous deletion of glycoproteins E, I, and M of pseudorabies virus. J Virol 73, 5364–5372. [Google Scholar]
  5. Campadelli, G., Brandimarti, R., Di Lazzaro, C., Ward, P. L., Roizman, B. & Torrisi, M. R.(1993). Fragmentation and dispersal of Golgi proteins and redistribution of glycoproteins and glycolipids processed through the Golgi apparatus after infection with herpes simplex virus 1. Proc Natl Acad Sci U S A 90, 2798–2802.[CrossRef] [Google Scholar]
  6. Cohen, G. H., Katze, M., Hydrean-Stern, C. & Eisenberg, R. J.(1978). Type-common CP-1 antigen of herpes simplex virus is associated with a 59,000-molecular-weight envelope glycoprotein. J Virol 27, 172–181. [Google Scholar]
  7. Coller, K. E., Lee, J. I., Ueda, A. & Smith, G. A.(2007). The capsid and tegument of the alphaherpesviruses are linked by an interaction between the UL25 and VP1/2 proteins. J Virol 81, 11790–11797.[CrossRef] [Google Scholar]
  8. Copeland, A. M., Newcomb, W. W. & Brown, J. C.(2009). Herpes simplex virus replication: roles of viral proteins and nucleoporins in capsid-nucleus attachment. J Virol 83, 1660–1668.[CrossRef] [Google Scholar]
  9. Desai, P. J.(2000). A null mutation in the UL36 gene of herpes simplex virus type 1 results in accumulation of unenveloped DNA-filled capsids in the cytoplasm of infected cells. J Virol 74, 11608–11618.[CrossRef] [Google Scholar]
  10. Desai, P. & Person, S.(1998). Incorporation of the green fluorescent protein into the herpes simplex virus type 1 capsid. J Virol 72, 7563–7568. [Google Scholar]
  11. Desai, P., Sexton, G. L., McCaffery, J. M. & Person, S.(2001). A null mutation in the gene encoding the herpes simplex virus type 1 UL37 polypeptide abrogates virus maturation. J Virol 75, 10259–10271.[CrossRef] [Google Scholar]
  12. Desai, P., Sexton, G. L., Huang, E. & Person, S.(2008). Localization of herpes simplex virus type 1 UL37 in the Golgi complex requires UL36 but not capsid structures. J Virol 82, 11354–11361.[CrossRef] [Google Scholar]
  13. Elliott, G., Mouzakitis, G. & O'Hare, P.(1995). VP16 interacts via its activation domain with VP22, a tegument protein of herpes simplex virus, and is relocated to a novel macromolecular assembly in coexpressing cells. J Virol 69, 7932–7941. [Google Scholar]
  14. Farnsworth, A., Goldsmith, K. & Johnson, D. C.(2003). Herpes simplex virus glycoproteins gD and gE/gI serve essential but redundant functions during acquisition of the virion envelope in the cytoplasm. J Virol 77, 8481–8494.[CrossRef] [Google Scholar]
  15. Foster, T. P., Melancon, J. M., Baines, J. D. & Kousoulas, K. G.(2004). The herpes simplex virus type 1 UL20 protein modulates membrane fusion events during cytoplasmic virion morphogenesis and virus-induced cell fusion. J Virol 78, 5347–5357.[CrossRef] [Google Scholar]
  16. Fuchs, W., Klupp, B. G., Granzow, H. & Mettenleiter, T. C.(2004). Essential function of the pseudorabies virus UL36 gene product is independent of its interaction with the UL37 protein. J Virol 78, 11879–11889.[CrossRef] [Google Scholar]
  17. Gross, S. T., Harley, C. A. & Wilson, D. W.(2003). The cytoplasmic tail of herpes simplex virus glycoprotein H binds to the tegument protein VP16 in vitro and in vivo. Virology 317, 1–12.[CrossRef] [Google Scholar]
  18. Homa, F. L. & Brown, J. C.(1997). Capsid assembly and DNA packaging in herpes simplex virus. Rev Med Virol 7, 107–122.[CrossRef] [Google Scholar]
  19. Klupp, B. G., Granzow, H., Mundt, E. & Mettenleiter, T. C.(2001). Pseudorabies virus UL37 gene product is involved in secondary envelopment. J Virol 75, 8927–8936.[CrossRef] [Google Scholar]
  20. Klupp, B. G., Fuchs, W., Granzow, H., Nixdorf, R. & Mettenleiter, T. C.(2002). Pseudorabies virus UL36 tegument protein physically interacts with the UL37 protein. J Virol 76, 3065–3071.[CrossRef] [Google Scholar]
  21. Ko, D. H., Cunningham, A. L. & Diefenbach, R. J.(2009). The major determinant for addition of tegument protein pUL48 (VP16) to capsids in herpes simplex virus type 1 is the presence of the major tegument protein pUL36 (VP1/2). J Virol 84, 1397–1405. [Google Scholar]
  22. Lee, J. H., Vittone, V., Diefenbach, E., Cunningham, A. L. & Diefenbach, R. J.(2008). Identification of structural protein–protein interactions of herpes simplex virus type 1. Virology 378, 347–354.[CrossRef] [Google Scholar]
  23. Leege, T., Fuchs, W., Granzow, H., Kopp, M., Klupp, B. G. & Mettenleiter, T. C.(2009). Effects of simultaneous deletion of pUL11 and glycoprotein M on virion maturation of herpes simplex virus type 1. J Virol 83, 896–907.[CrossRef] [Google Scholar]
  24. Ligas, M. W. & Johnson, D. C.(1988). A herpes simplex virus mutant in which glycoprotein D sequences are replaced by β-galactosidase sequences binds to but is unable to penetrate into cells. J Virol 62, 1486–1494. [Google Scholar]
  25. McLauchlan, J., Liefkens, K. & Stow, N. D.(1994). The herpes simplex virus type 1 UL37 gene product is a component of virus particles. J Gen Virol 75, 2047–2052.[CrossRef] [Google Scholar]
  26. Mettenleiter, T. C., Klupp, B. G. & Granzow, H.(2006). Herpesvirus assembly: a tale of two membranes. Curr Opin Microbiol 9, 423–429.[CrossRef] [Google Scholar]
  27. Mijatov, B., Cunningham, A. L. & Diefenbach, R. J.(2007). Residues F593 and E596 of HSV-1 tegument protein pUL36 (VP1/2) mediate binding of tegument protein pUL37. Virology 368, 26–31.[CrossRef] [Google Scholar]
  28. Mossman, K. L., Sherburne, R., Lavery, C., Duncan, J. & Smiley, J. R.(2000). Evidence that herpes simplex virus VP16 is required for viral egress downstream of the initial envelopment event. J Virol 74, 6287–6299.[CrossRef] [Google Scholar]
  29. Pasdeloup, D., Blondel, D., Isidro, A. L. & Rixon, F. J.(2009). Herpesvirus capsid association with the nuclear pore complex and viral DNA release involve the nucleoporin CAN/Nup214 and the capsid protein pUL25. J Virol 83, 6610–6623.[CrossRef] [Google Scholar]
  30. Rixon, F. J., Addison, C. & McLauchlan, J.(1992). Assembly of enveloped tegument structures (L particles) can occur independently of virion maturation in herpes simplex virus type 1-infected cells. J Gen Virol 73, 277–284.[CrossRef] [Google Scholar]
  31. Roberts, A. P., Abaitua, F., O'Hare, P., McNab, D., Rixon, F. J. & Pasdeloup, D.(2009). Differing roles of inner tegument proteins pUL36 and pUL37 during entry of herpes simplex virus type 1. J Virol 83, 105–116.[CrossRef] [Google Scholar]
  32. Rozen, R., Sathish, N., Li, Y. & Yuan, Y.(2008). Virion-wide protein interactions of Kaposi's sarcoma-associated herpesvirus. J Virol 82, 4742–4750.[CrossRef] [Google Scholar]
  33. Sugimoto, K., Uema, M., Sagara, H., Tanaka, M., Sata, T., Hashimoto, Y. & Kawaguchi, Y.(2008). Simultaneous tracking of capsid, tegument, and envelope protein localization in living cells infected with triply fluorescent herpes simplex virus 1. J Virol 82, 5198–5211.[CrossRef] [Google Scholar]
  34. Szilagyi, J. F. & Cunningham, C.(1991). Identification and characterization of a novel non-infectious herpes simplex virus-related particle. J Gen Virol 72, 661–668.[CrossRef] [Google Scholar]
  35. Turcotte, S., Letellier, J. & Lippe, R.(2005). Herpes simplex virus type 1 capsids transit by the trans-Golgi network, where viral glycoproteins accumulate independently of capsid egress. J Virol 79, 8847–8860.[CrossRef] [Google Scholar]
  36. Uetz, P., Dong, Y. A., Zeretzke, C., Atzler, C., Baiker, A., Berger, B., Rajagopala, S. V., Roupelieva, M., Rose, D. & other authors(2006). Herpesviral protein networks and their interaction with the human proteome. Science 311, 239–242.[CrossRef] [Google Scholar]
  37. Vittone, V., Diefenbach, E., Triffett, D., Douglas, M. W., Cunningham, A. L. & Diefenbach, R. J.(2005). Determination of interactions between tegument proteins of herpes simplex virus type 1. J Virol 79, 9566–9571.[CrossRef] [Google Scholar]
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Inner tegument protein pUL37 of herpes simplex virus type 1 is involved in directing capsids to the trans-Golgi network for envelopment
J. Gen. Virol. 91, 2145 (2010); https://doi.org/10.1099/vir.0.022053-0
/content/journal/jgv/10.1099/vir.0.022053-0
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