Differing roles of inner tegument proteins pUL36 and pUL37 during entry of herpes simplex virus type

Journal of Virology

Volumn 83, Issue 1, 2009, Pages 105-116

  Roberts, Ashley P E ^a   Abaitua, Fernando ^b   O'Hare, Peter ^b   McNab, David ^a   Rixon, Frazer J ^a   Pasdeloup, David ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b MARIE CURIE RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

UL36 PROTEIN; UL37 PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN; UL36 PROTEIN, HUMAN HERPESVIRUS 1; UL37 PROTEIN, HUMAN HERPESVIRUS 1;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; DNA REPLICATION; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; INFECTION; INTEGUMENT; MUTANT; PRIORITY JOURNAL; PROTEIN FUNCTION; VIRION; VIRUS CAPSID; VIRUS ENTRY; VIRUS TRANSMISSION; CELL CULTURE; GENE DELETION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN BINDING; VIRUS ASSEMBLY;

HUMAN HERPESVIRUS 1; MIRIDAE; SIMPLEXVIRUS;

CELLS, CULTURED; GENE DELETION; HERPESVIRUS 1, HUMAN; HUMANS; PROTEIN BINDING; VIRAL PROTEINS; VIRAL STRUCTURAL PROTEINS; VIRUS ASSEMBLY; VIRUS INTERNALIZATION;

EID: 58149393193     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01032-08     Document Type: Article

References (59)

1. Abaitua, F., and P. O'Hare. 2008. Identification of a highly conserved functional nuclear localization signal within the N-terminal region of herpes simplex virus type 1 VP1-2 tegument protein. J. Virol. 82:5234-5244.
2. L16 are dispensable for the replication of herpes simplex virus 1 in cell culture. J. Virol. 65:938-944.
3. Batterson, W., D. Furlong, and B. Roizman. 1983. Molecular genetics of herpes simplex virus. VIII. Further characterization of a temperature-sensitive mutant defective in release of viral DNA and in other stages of the viral reproductive cycle. J. Virol. 45:397-407.
4. Brack, A. R., J. M. Dijkstra, H. Granzow, B. G. Klupp, and T. C. Mettenleiter. 1999. Inhibition of virion maturation by simultaneous deletion of glycoproteins E, I, and M of pseudorabies virus. J. Virol. 73:5364-5372.
5. Bucks, M. A., K. J. O'Regan, M. A. Murphy, J. W. Wills, and R. J. Courtney. 2007. Herpes simplex virus type 1 tegument proteins VP1/2 and UL37 are associated with intranuclear capsids. Virology 361:316-324.
6. Chen, D. H., H. Jiang, M. Lee, F. Y. Liu, and Z. H. Zhou. 1999. Three-dimensional visualization of tegument/capsid interactions in the intact human cytomegalovirus. Virology 260:10-16.
7. Clarke, R. W., N. Monnier, H. T. Li, D. J. Zhou, H. Browne, and D. Klenerman. 2007. Two-color fluorescence analysis of individual virions determines the distribution of the copy number of proteins in herpes simplex virus particles. Biophys. J. 93:1329-1337.
8. Coller, K. E., J. I.-H. Lee, A. Ueda, and G. A. Smith. 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.
9. Cunningham, C., and A. J. Davison. 1993. A cosmid-based system for constructing mutants of herpes simplex virus type 1. Virology 197:116-124.
10. Delboy, M. G., D. G. Roller, and A. V. Nicola. 2008. Cellular proteasome activity facilitates herpes simplex virus entry at a postpenetration step. J. Virol. 82:3381-3390.
11. del Rio, T., T. H. Ch'ng, E. A. Flood, S. P. Gross, and L. W. Enquist. 2005. Heterogeneity of a fluorescent tegument component in single pseudorabies virus virions and enveloped axonal assemblies. J. Virol. 79:3903-3919.
12. Desai, P., N. A. Deluca, J. C. Glorioso, and S. Person. 1993. Mutations in herpes simplex virus type 1 genes encoding VP5 and VP23 abrogate capsid formation and cleavage of replicated DNA. J. Virol. 67:1357-1364.
13. Desai, P., G. L. Sexton, J. M. McCaffery, and S. Person. 2001. A null mutation in the gene encoding the herpes simplex virus type 1 UL37 polypeptide abrogates virus maturation. J. Virol. 75:10259-10271.
14. 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.
15. Elliott, G., D. O'Reilly, and P. O'Hare. 1996. Phosphorylation of the herpes simplex virus type-I tegument protein VP22. Virology 226:140-145.
16. Everett, R. D., J. Murray, A. Orr, and C. M. Preston. 2007. Herpes simplex virus type 1 genomes are associated with ND10 nuclear substructures in quiescently infected human fibroblasts. J. Virol. 81:10991-11004.
17. Fuchs, W., B. G. Klupp, H. Granzow, and T. C. Mettenleiter. 2004. Essential function of the pseudorabies virus UL36 gene product is independent of its interaction with the UL37 protein. J. Virol. 78:11879-11889.
18. Fuchs, W., B. G. Klupp, H. Granzow, N. Osterrieder, and T. C. Mettenleiter. 2002. The interacting UL31 and UL34 gene products of pseudorabies virus are involved in egress from the host-cell nucleus and represent components of primary enveloped but not mature virions. J. Virol. 76:364-378.
19. Gibson, W., and B. Roizman. 1972. Proteins specified by herpes simplex virus. VIII. Characterization and composition of multiple capsid forms of subtypes 1 and 2. J. Virol. 10:1044-1052.
20. Granzow, H., B. G. Klupp, and T. C. Mettenleiter. 2005. Entry of pseudorabies virus: an immunogold-labeling study. J. Virol. 79:3200-3205.
21. Granzow, H., B. G. Klupp, and T. C. Mettenleiter. 2004. The pseudorabies virus US3 protein is a component of primary and of mature virions. J. Virol. 78:1314-1323.
22. Grunewald, K., P. Desai, D. C. Winkler, J. B. Heymann, D. M. Belnap, W. Baumeister, and A. C. Steven. 2003. Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 302:1396-1398.
23. Homa, F. L., and J. C. Brown. 1997. Capsid assembly and DNA packaging in herpes simplex virus. Rev. Med. Virol. 7:107-122.
24. Jovasevic, V., L. Liang, and B. Roizman. 2008. Proteolytic cleavage of VP1-2 is required for release of herpes simplex virus 1 DNA into the nucleus. J. Virol. 82:3311-3319.
25. Klupp, B. G., W. Fuchs, H. Granzow, R. Nixdorf, and T. C. Mettenleiter. 2002. Pseudorabies virus UL36 tegument protein physically interacts with the UL37 protein. J. Virol. 76:3065-3071.
26. Klupp, B. G., H. Granzow, E. Mundt, and T. C. Mettenleiter. 2001. Pseudorabies virus UL37 gene product is involved in secondary envelopment. J. Virol. 75:8927-8936.
27. Lamberti, C., and S. K. Weller. 1998. The herpes simplex virus type 1 cleavage/packaging protein, UL32, is involved in efficient localization of capsids to replication compartments. J. Virol. 72:2463-2473.
28. Lewis, L., and G. Albrechtbuehler. 1987. Distribution of multiple centrospheres determines migration of BHK syncytia. Cell Motil. Cytoskelet. 7:282-290.
29. Luxton, G. W. G., S. Haverlock, K. E. Coller, S. E. Antinone, A. Pincetic, and G. A. Smith. 2005. Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc. Natl. Acad. Sci. USA 102:5832-5837.
30. Luxton, G. W. G., J. I. H. Lee, S. Haverlock-Moyns, J. M. Schober, and G. A. Smith. 2006. The pseudorabies virus VP1/2 tegument protein is required for intracellular capsid transport. J. Virol. 80:201-209.
31. McClelland, D. A., J. D. Aitken, D. Bhella, D. McNab, J. Mitchell, S. M. Kelly, N. C. Price, and F. J. Rixon. 2002. pH reduction as a trigger for dissociation of herpes simplex virus type 1 scaffolds. J. Virol. 76:7407-7417.
32. McGeoch, D. J., M. A. Dalrymple, A. J. Davison, A. Dolan, M. C. Frame, D. McNab, L. J. Perry, J. E. Scott, and P. Taylor. 1988. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J. Gen. Virol. 69:1531-1574.
33. McLauchlan, J. 1997. The abundance of the herpes simplex virus type 1 UL37 tegument protein in virus particles is closely controlled. J. Gen. Virol. 78:189-194.
34. McLauchlan, J., K. Liefkens, and N. D. Stow. 1994. The herpes simplex virus type 1 UL37 gene-product is a component of virus particles. J. Gen. Virol. 75:2047-2052.
35. McLauchlan, J., and F. J. Rixon. 1992. Characterization of enveloped tegument structures (L-particles) produced by alphaherpesviruses: integrity of the tegument does not depend on the presence of capsid or envelope. J. Gen. Virol. 73:269-276.
36. Mettenleiter, T. C. 2002. Herpesvirus assembly and egress. J. Virol. 76:1537-1547.
37. Mijatov, B., A. L. Cunningham, and R. J. Diefenbach. 2007. Residues F593 and E596 of HSV-1 tegument protein pUL36 (VP1/2) mediate binding of tegument protein pUL37. Virology 368:26-31.
38. Naldinho-Souto, R., H. Browne, and T. Minson. 2006. Herpes simplex virus tegument protein VP16 is a component of primary enveloped virions. J. Virol. 80:2582-2584.
39. Nicholson, P., C. Addison, A. M. Cross, J. Kennard, V. G. Preston, and F. J. Rixon. 1994. Localization of the herpes simplex virus type 1 major capsid protein VP5 to the cell nucleus requires the abundant scaffolding protein VP22a. J. Gen. Virol. 75:1091-1099.
40. L34 proteins of herpes simplex virus type 1 form a complex that accumulates at the nuclear rim and is required for envelopment of nucleocapsids. J. Virol. 75:8803-8817.
41. Reynolds, A. E., E. G. Wills, R. J. Roller, B. J. Ryckman, and J. D. Baines. 2002. Ultrastructural localization of the herpes simplex virus type 1 UL31, UL34, and US3 proteins suggests specific roles in primary envelopment and egress of nucleocapsids. J. Virol. 76:8939-8952.
42. Rixon, F. J. 1993. Structure and assembly of herpesviruses. Semin. Virol. 4:135-144.
43. Rixon, F. J., C. Addison, and J. McLauchlan. 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.
44. L34 gene product is required for viral envelopment. J. Virol. 74:117-129.
45. Schrag, J. D., B. V. V. Prasad, F. J. Rixon, and W. Chiu. 1989. Three-dimensional structure of the HSV-1 nucleocapsid. Cell 56:651-660.
46. Shelton, L. S., A. G. Albright, W. T. Ruyechan, and F. J. Jenkins. 1994. Retention of the herpes simplex virus type 1 (HSV-1) UL37 protein on single-stranded DNA columns requires the HSV-1 ICP8 protein. J. Virol. 68:521-525.
47. Siegel, R. W., R. Jain, and A. Bradbury. 2001. Using an in vivo phagemid system to identify non-compatible loxP sequences. FEBS Lett. 499:147-153.
48. Smith, G. A., and L. W. Enquist. 2000. A self-recombining bacterial artificial chromosome and its application for analysis of herpesvirus pathogenesis. Proc. Natl. Acad. Sci. USA 97:4873-4878.
49. Sodeik, B., M. W. Ebersold, and A. Helenius. 1997. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol. 136:1007-1021.
50. Steven, A. C., and P. G. Spear. 1997. Herpesvirus capsid assembly and envelopment, p. 312-351. In W. Chiu, R. M. Burnett, and R. Garcea (ed.), Structural biology of viruses. Oxford University Press, Oxford, United Kingdom.
51. Stow, N. D., and N. M. Wilkie. 1976. An improved technique for obtaining enhanced infectivity with herpes simplex virus type 1 DNA. J. Gen. Virol. 33:447-458.
52. Szilagyi, J. F., and C. Cunningham. 1991. Identification and characterization of a novel non-infectious herpes simplex virus-related particle. J. Gen. Virol. 72:661-668.
53. Trus, B. L., W. W. Newcomb, N. Q. Cheng, G. Cardone, L. Marekov, F. L. Horna, J. C. Brown, and A. C. Steven. 2007. Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-filled HSV-1 capsids. Mol. Cell 26:479-489.
54. Vielkind, U., and S. H. Swierenga. 1989. A simple fixation procedure for immunofluorescent detection of different cytoskeletal components within the same cell. Histochemistry 91:81-88.
55. Vittone, V., E. Diefenbach, D. Triffett, M. W. Douglas, A. L. Cunningham, and R. J. Diefenbach. 2005. Determination of interactions between tegument proteins of herpes simplex virus type 1. J. Virol. 79:9566-9571.
56. Wagenaar, F., J. M. A. Pol, B. Peeters, A. L. J. Gielkens, N. Dewind, and T. G. Kimman. 1995. The US3-encoded protein kinase from pseudorabies virus affects egress of virions from the nucleus. J. Gen. Virol. 76:1851-1859.
57. Wolfstein, A., C. H. Nagel, K. Radtke, K. Dohner, V. J. Allan, and B. Sodeik. 2006. The inner tegument promotes herpes simplex virus capsid motility along microtubules in vitro. Traffic 7:227-237.
58. Zhou, Z. H., D. H. Chen, J. Jakana, F. J. Rixon, and W. Chiu. 1999. Visualization of tegument-capsid interactions and DNA in intact herpes simplex virus type 1 virions. J. Virol. 73:3210-3218.
59. Zhou, Z. H., M. Dougherty, J. Jakana, J. He, F. J. Rixon, and W. Chiu. 2000. Seeing the herpesvirus capsid at 8.5 Å. Science 288:877-880.