Herpesvirus capsid association with the nuclear pore complex and viral DNA release involve the nucleoporin CAN/Nup214 and the capsid protein pUL25

Journal of Virology

Volumn 83, Issue 13, 2009, Pages 6610-6623

  Pasdeloup, David ^a,b   Blondel, Danielle ^b   Isidro, Anabela L ^b,c   Rixon, Frazer J ^a  

^a INSTITUTE OF VIROLOGY   (United Kingdom)

^b CNRS   (France)

^c INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CAPSID PROTEIN PUL25; CAPSID PROTEIN PUL36; CAPSID PROTEIN PUL6; COAT PROTEIN; NUCLEOPORIN; NUCLEOPORIN CAN; NUCLEOPORIN HCG1; NUCLEOPORIN NUP214; UNCLASSIFIED DRUG; VIRUS DNA; DNA CLEAVAGE AND PACKAGING PROTEINS, HERPESVIRUS; NUCLEAR PROTEIN; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN; NUP214 PROTEIN, HUMAN; NUPL2 PROTEIN, HUMAN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; GENE SILENCING; HERPES SIMPLEX VIRUS 1; HERPES VIRUS; HUMAN; HUMAN CELL; MICROTUBULE ASSEMBLY; NONHUMAN; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS PARTICLE; VIRUS REPLICATION; ANIMAL; CERCOPITHECUS; HAMSTER; HELA CELL; METABOLISM; NUCLEAR PORE; PHYSIOLOGY; VERO CELL; VIROLOGY;

HERPESVIRIDAE; HUMAN HERPESVIRUS 1; MIRIDAE;

ANIMALS; CAPSID PROTEINS; CERCOPITHECUS AETHIOPS; CRICETINAE; DNA, VIRAL; HELA CELLS; HERPESVIRUS 1, HUMAN; HUMANS; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; NUCLEAR PROTEINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; VERO CELLS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 67449089967     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02655-08     Document Type: Article

References (66)

1. Alber, F., S. Dokudovskaya, L. M. Veenhoff, W. Zhang, J. Kipper, D. Devos, A. Suprapto, O. Karni-Schmidt, R. Williams, B. T. Chait, A. Sali, and M. P. Rout. 2007. The molecular architecture of the nuclear pore complex. Nature 450:695-701. (Pubitemid 350207701)
2. 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.
3. Beck, M., F. Forster, M. Ecke, J. M. Plitzko, F. Melchior, G. Gerisch, W. Baumeister, and O. Medalia. 2004. Nuclear pore complex structure and dynamics revealed by cryoelectron tomography. Science 306:1387-1390. (Pubitemid 39532518)
4. Belgareh, N., G. Rabut, S. W. Bai, M. van Overbeek, J. Beaudouin, N. Daigle, O. V. Zatsepina, F. Pasteau, V. Labas, M. Fromont-Racine, J. Ellenberg, and V. Doye. 2001. An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. J. Cell Biol. 154:1147-1160. (Pubitemid 34286193)
5. Bernad, R., H. van der Velde, M. Fornerod, and H. Pickersgill. 2004. Nup358/RanBP2 attaches to the nuclear pore complex via association with Nup88 and Nup214/CAN and plays a supporting role in CRM1-mediated nuclear protein export. Mol. Cell. Biol. 24:2373-2384.
6. Bowman, B. R., R. L. Welschhans, H. Jayaram, N. D. Stow, V. G. Preston, and F. A. Quiocho. 2006. Structural characterization of the UL25 DNA-packaging protein from herpes simplex virus type 1. J. Virol. 80:2309-2317. (Pubitemid 43271536)
7. Cardone, G., D. C. Winkler, B. L. Trus, N. Cheng, J. E. Heuser, W. W. Newcomb, J. C. Brown, and A. C. Steven. 2007. Visualization of the herpes simplex virus portal in situ by cryo-electron tomography. Virology 361:426-434. (Pubitemid 46574843)
8. Chang, J. T., M. F. Schmid, F. J. Rixon, and W. Chiu. 2007. Electron cryotomography reveals the portal in the herpesvirus capsid. J. Virol. 81: 2065-2068. (Pubitemid 46214478)
9. Coller, K. E., J. I. 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. (Pubitemid 47623811)
10. Copeland, A. M., W. W. Newcomb, and J. C. Brown. 2009. Herpes simplex virus replication: roles of viral proteins and nucleoporins in capsid-nucleus attachment. J. Virol. 83:1660-1668.
11. Cronshaw, J. M., A. N. Krutchinsky, W. Zhang, B. T. Chait, and M. J. Matunis. 2002. Proteomic analysis of the mammalian nuclear pore complex. J. Cell Biol. 158:915-927. (Pubitemid 35001082)
12. Cunningham, C., and A. J. Davison. 1993. A cosmid-based system for constructing mutants of herpes simplex virus type 1. Virology 197:116-124. (Pubitemid 23313539)
13. D'Angelo, M. A., and M. W. Hetzer. 2008. Structure, dynamics and function of nuclear pore complexes. Trends Cell Biol. 18:456-466.
14. Davis, L. I., and G. Blobel. 1987. Nuclear pore complex contains a family of glycoproteins that includes p62: glycosylation through a previously unidentified cellular pathway. Proc. Natl. Acad. Sci. USA 84:7552-7556.
15. Davison, M. J., V. G. Preston, and D. J. McGeoch. 1984. Determination of the sequence alteration in the DNA of the herpes simplex virus type 1 temperature-sensitive mutant ts K. J. Gen. Virol. 65(Pt. 5):859-863.
16. 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. (Pubitemid 32222309)
17. Everett, R. D., and J. Murray. 2005. ND10 components relocate to sites associated with herpes simplex virus type 1 nucleoprotein complexes during virus infection. J. Virol. 79:5078-5089. (Pubitemid 40464258)
18. Everett, R. D., S. Rechter, P. Papior, N. Tavalai, T. Stamminger, and A. Orr. 2006. PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J. Virol. 80:7995-8005. (Pubitemid 44182300)
19. Everett, R. D., G. Sourvinos, and A. Orr. 2003. Recruitment of herpes simplex virus type 1 transcriptional regulatory protein ICP4 into foci juxtaposed to ND10 in live, infected cells. J. Virol. 77:3680-3689. (Pubitemid 36297287)
20. Granzow, H., B. G. Klupp, and T. C. Mettenleiter. 2005. Entry of pseudorabies virus: an immunogold-labeling study. J. Virol. 79:3200-3205. (Pubitemid 40270601)
21. Greber, U. F., and A. Fassati. 2003. Nuclear import of viral DNA genomes. Traffic 4:136-143. (Pubitemid 36621706)
22. Hutten, S., and R. H. Kehlenbach. 2006. Nup214 is required for CRM1- dependent nuclear protein export in vivo. Mol. Cell. Biol. 26:6772-6785.
23. Jamieson, D. R., L. H. Robinson, J. I. Daksis, M. J. Nicholl, and C. M. Preston. 1995. Quiescent viral genomes in human fibroblasts after infection with herpes simplex virus type 1 Vmw65 mutants. J. Gen. Virol. 76(Pt. 6):1417-1431.
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. Kuhn, J., T. Leege, B. G. Klupp, H. Granzow, W. Fuchs, and T. C. Mettenleiter. 2008. Partial functional complementation of a pseudorabies virus UL25 deletion mutant by herpes simplex virus type 1 pUL25 indicates overlapping functions of alphaherpesvirus pUL25 proteins. J. Virol. 82: 5725-5734. (Pubitemid 351822248)
26. Lee, J. H., V. Vittone, E. Diefenbach, A. L. Cunningham, and R. J. Diefenbach. 2008. Identification of structural protein-protein interactions of herpes simplex virus type 1. Virology 378:347-354.
27. Le Rouzic, E., A. Mousnier, C. Rustum, F. Stutz, E. Hallberg, C. Dargemont, and S. Benichou. 2002. Docking of HIV-1 Vpr to the nuclear envelope is mediated by the interaction with the nucleoporin hCG1. J. Biol. Chem. 277:45091-45098.
28. Lim, R. Y., and B. Fahrenkrog. 2006. The nuclear pore complex up close. Curr. Opin. Cell Biol. 18:342-347.
29. Lowenstein, P. R., E. E. Morrison, D. Bain, P. Hodge, C. M. Preston, P. Clissold, N. D. Stow, T. A. McKee, and M. G. Castro. 1994. Use of recombinant vectors derived from herpes simplex virus 1 mutant tsK for short-term expression of transgenes encoding cytoplasmic and membrane anchored proteins in postmitotic polarized cortical neurons and glial cells in vitro. Neuroscience 60:1059-1077. (Pubitemid 24180164)
30. Luxton, G. W., 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.
31. Luxton, G. W., J. I. 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.
32. Macara, I. G. 2001. Transport into and out of the nucleus. Microbiol. Mol. Biol. Rev. 65:570-594.
33. McBride, K. M., G. Banninger, C. McDonald, and N. C. Reich. 2002. Regulated nuclear import of the STAT1 transcription factor by direct binding of importin-alpha. EMBO J. 21:1754-1763. (Pubitemid 34614631)
34. McNab, A. R., P. Desai, S. Person, L. L. Roof, D. R. Thomsen, W. W. Newcomb, J. C. Brown, and F. L. Homa. 1998. The product of the herpes simplex virus type 1 UL25 gene is required for encapsidation but not for cleavage of replicated viral DNA. J. Virol. 72:1060-1070. (Pubitemid 28116885)
35. Murray, J., C. Loney, L. B. Murphy, S. Graham, and R. P. Yeo. 2001. Characterization of monoclonal antibodies raised against recombinant respiratory syncytial virus nucleocapsid (N) protein: identification of a region in the carboxy terminus of N involved in the interaction with P protein. Virology 289:252-261. (Pubitemid 33141005)
36. Newcomb, W. W., F. P. Booy, and J. C. Brown. 2007. Uncoating the herpes simplex virus genome. J. Mol. Biol. 370:633-642.
37. Newcomb, W. W., F. L. Homa, and J. C. Brown. 2006. Herpes simplex virus capsid structure: DNA packaging protein UL25 is located on the external surface of the capsid near the vertices. J. Virol. 80:6286-6294. (Pubitemid 43927431)
38. Newcomb, W. W., R. M. Juhas, D. R. Thomsen, F. L. Homa, A. D. Burch, S. K. Weller, and J. C. Brown. 2001. The UL6 gene product forms the portal for entry of DNA into the herpes simplex virus capsid. J. Virol. 75:10923-10932. (Pubitemid 33031559)
39. Ojala, P. M., B. Sodeik, M. W. Ebersold, U. Kutay, and A. Helenius. 2000. Herpes simplex virus type 1 entry into host cells: reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro. Mol. Cell. Biol. 20:4922-4931.
40. Pante, N., R. Bastos, I. McMorrow, B. Burke, and U. Aebi. 1994. Interactions and three-dimensional localization of a group of nuclear pore complex proteins. J. Cell Biol. 126:603-617. (Pubitemid 24241375)
41. Patel, S. S., B. J. Belmont, J. M. Sante, and M. F. Rexach. 2007. Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 129:83-96. (Pubitemid 46507580)
42. Peters, R. 2005. Translocation through the nuclear pore complex: selectivity and speed by reduction-of-dimensionality. Traffic 6:421-427. (Pubitemid 40542768)
43. Preston, C. M. 1979. Control of herpes simplex virus type 1 mRNA synthesis in cells infected with wild-type virus or the temperature-sensitive mutant tsK. J. Virol. 29:275-284.
44. Preston, V. G., J. Murray, C. M. Preston, I. M. McDougall, and N. D. Stow. 2008. The UL25 gene product of herpes simplex virus type 1 is involved in uncoating of the viral genome. J. Virol. 82:6654-6666. (Pubitemid 351875142)
45. Raux, H., A. Flamand, and D. Blondel. 2000. Interaction of the rabies virus P protein with the LC8 dynein light chain. J. Virol. 74:10212-10216. (Pubitemid 30780831)
46. Ribbeck, K., and D. Gorlich. 2001. Kinetic analysis of translocation through nuclear pore complexes. EMBO J. 20:1320-1330. (Pubitemid 32233972)
47. Roberts, A. P., F. Abaitua, P. O'Hare, D. McNab, F. J. Rixon, and D. Pasdeloup. 2009. Differing roles of inner tegument proteins pUL36 and pUL37 during entry of herpes simplex virus type 1. J. Virol. 83:105-116.
48. Roth, M. B., A. M. Zahler, and J. A. Stolk. 1991. A conserved family of nuclear phosphoproteins localized to sites of polymerase II transcription. J. Cell Biol. 115:587-596. (Pubitemid 21909914)
49. Rout, M. P., J. D. Aitchison, M. O. Magnasco, and B. T. Chait. 2003. Virtual gating and nuclear transport: the hole picture. Trends Cell Biol. 13:622-628. (Pubitemid 37415027)
50. Schwartz, T. U. 2005. Modularity within the architecture of the nuclear pore complex. Curr. Opin. Struct. Biol. 15:221-226.
51. Shahin, V., W. Hafezi, H. Oberleithner, Y. Ludwig, B. Windoffer, H. Schillers, and J. E. Kuhn. 2006. The genome of HSV-1 translocates through the nuclear pore as a condensed rod-like structure. J. Cell Sci. 119:23-30. (Pubitemid 43169295)
52. 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. (Pubitemid 27131733)
53. Stow, N. D. 2001. Packaging of genomic and amplicon DNA by the herpes simplex virus type 1 UL25-null mutant KUL25NS. J. Virol. 75:10755-10765. (Pubitemid 33031545)
54. Thurlow, J. K., M. Murphy, N. D. Stow, and V. G. Preston. 2006. Herpes simplex virus type 1 DNA-packaging protein UL17 is required for efficient binding of UL25 to capsids. J. Virol. 80:2118-2126. (Pubitemid 43271519)
55. Tran, E. J., and S. R. Wente. 2006. Dynamic nuclear pore complexes: life on the edge. Cell 125:1041-1053. (Pubitemid 43866205)
56. Trotman, L. C., N. Mosberger, M. Fornerod, R. P. Stidwill, and U. F. Greber. 2001. Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat. Cell Biol. 3:1092-1100.
57. Trus, B. L., N. Cheng, W. W. Newcomb, F. L. Homa, J. C. Brown, and A. C. Steven. 2004. Structure and polymorphism of the UL6 portal protein of herpes simplex virus type 1. J. Virol. 78:12668-12671. (Pubitemid 39458785)
58. Trus, B. L., W. W. Newcomb, N. Cheng, G. Cardone, L. Marekov, F. L. Homa, 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. (Pubitemid 46765180)
59. Walther, T. C., H. S. Pickersgill, V. C. Cordes, M. W. Goldberg, T. D. Allen, I. W. Mattaj, and M. Fornerod. 2002. The cytoplasmic filaments of the nuclear pore complex are dispensable for selective nuclear protein import. J. Cell Biol. 158:63-77. (Pubitemid 34886722)
60. Whittaker, G. R., M. Kann, and A. Helenius. 2000. Viral entry into the nucleus. Annu. Rev. Cell Dev. Biol. 16:627-651.
61. Wilken, N., J. L. Senecal, U. Scheer, and M. C. Dabauvalle. 1995. Localization of the Ran-GTP binding protein RanBP2 at the cytoplasmic side of the nuclear pore complex. Eur. J. Cell Biol. 68:211-219.
62. 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.
63. Wu, J., M. J. Matunis, D. Kraemer, G. Blobel, and E. Coutavas. 1995. Nup358, a cytoplasmically exposed nucleoporin with peptide repeats, Ran- GTP binding sites, zinc fingers, a cyclophilin A homologous domain, and a leucine-rich region. J. Biol. Chem. 270:14209-14213.
64. Yokoyama, N., N. Hayashi, T. Seki, N. Pante, T. Ohba, K. Nishii, K. Kuma, T. Hayashida, T. Miyata, U. Aebi, et al. 1995. A giant nucleopore protein that binds Ran/TC4. Nature 376:184-188.
65. 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. (Pubitemid 29135713)
66. 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. (Pubitemid 30257740)