A nuclear localization signal in herpesvirus protein VP1-2 is essential for infection via capsid routing to the nuclear pore

Journal of Virology

Volumn 86, Issue 17, 2012, Pages 8998-9014

  Abaitua, F ^a   Hollinshead, M ^a   Bolstad, M ^a   Crump, C M ^b   O'Hare, P ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN VP1; PROTEIN VP2; STRUCTURAL PROTEIN;

ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENETIC CONSERVATION; HERPES VIRUS; HERPES VIRUS INFECTION; IMMUNOFLUORESCENCE TEST; MICROTUBULE ORGANIZING CENTER; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; UL36 GENE; VERO CELL; VIRION; VIROGENESIS; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS ENTRY; VIRUS GENE; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS PLAQUE;

AMINO ACID SEQUENCE; CAPSID; CELL LINE; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PORE; SEQUENCE ALIGNMENT; VIRAL PROTEINS; VIRUS ASSEMBLY;

HERPESVIRIDAE; MIRIDAE; SIMPLEXVIRUS;

EID: 84866184239     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01209-12     Document Type: Article

References (62)

1. Abaitua F, Daikoku T, Crump CM, Bolstad M, O'Hare P. 2011. A single mutation responsible for temperature sensitive entry and assembly defects in the VP1-2 protein of HSV. J. Virol. 85:2024-2036.
2. Abaitua F, O'Hare P. 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.
3. Abaitua F, Souto RN, Browne H, Daikoku T, O'Hare P. 2009. Characterization of the herpes simplex virus (HSV)-1 tegument protein VP1-2 during infection with the HSV temperature-sensitive mutant tsB7. J. Gen. Virol. 90:2353-2363.
4. Batterson W, Furlong D, Roizman B. 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.
5. Batterson W, Roizman B. 1983. Characterization of the herpes simplex virion-associated factor responsible for the induction of alpha genes. J. Virol. 46:371-377.
6. Bolstad M, Abaitua F, Crump CM, O'Hare P. 2011. Autocatalytic activity of the ubiquitin-specific protease domain of HSV-1 VP1-2. J. Virol. 85:8738-8751.
7. Bottcher S, et al. 2007. Identification of functional domains within the essential large tegument protein pUL36 of pseudorabies virus. J. Virol. 81:13403-13411.
8. Bottcher S, et al. 2006. Identification of a 709-amino-acid internal nonessential region within the essential conserved tegument protein (p)UL36 of pseudorabies virus. J. Virol. 80:9910-9915.
9. Cohen S, Au S, Pante N. 2011. How viruses access the nucleus. Biochim. Biophys. Acta 1813:1634-1645.
10. Coller KE, Lee JI, Ueda A, Smith GA. 2007. The capsid and tegument of the alpha herpesviruses are linked by an interaction between the UL25 and VP1-2 proteins. J. Virol. 81:11790-11797.
11. Copeland AM, Newcomb WW, Brown JC. 2009. Herpes simplex virus replication: roles of viral proteins and nucleoporins in capsid-nucleus attachment. J. Virol. 83:1660-1668.
12. Dammermann A, Merdes A. 2002. Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J. Cell Biol. 159:255-266.
13. Desai PJ. 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.
14. Flint SJ, Enquist LW, Krug RM, Racaniello VR, Skalka AM. 2009. Principles of virology. ASM Press, Washington, DC.
15. Fuchs W, Klupp BG, Granzow H, Mettenleiter TC. 2004. Essential function of the pseudorabies virus UL36 gene product is independent of its interaction with the UL37 protein. J. Virol. 78:11879-11889.
16. Gierasch WW, et al. 2006. Construction and characterisation of bacterial artificial chromosomes containing HSV-1 strains 17 and KOS. J. Virol. Methods 135:197-206.
17. Goldfarb DS, Corbett AH, Mason DA, Harreman MT, Adam SA. 2004. Importin alpha: a multipurpose nuclear-transport receptor. Trends Cell Biol. 14:505-514.
18. Gorlich D, Kutay U. 1999. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15:607-660.
19. Granzow H, Klupp BG, Mettenleiter TC. 2005. Entry of pseudorabies virus: an immunogold-labeling study. J. Virol. 79:3200-3205.
20. Greber UF, Fassati A. 2003. Nuclear import of viral DNA genomes. Traffic 4:136-143.
21. Greber UF, Fornerod M. 2005. Nuclear import in viral infections. Curr. Top. Microbiol. Immunol. 285:109-138.
22. Hanz S, et al. 2003. Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40:1095-1104.
23. Heine JW, Honess RW, Cassai E, Roizman B. 1974. Proteins specified by herpes simplex virus. XII. The virion polypeptides of type 1 strains. J. Virol. 14:640-651.
24. Jarosinski K, Kattenhorn L, Kaufer B, Ploegh H, Osterrieder N. 2007. A herpesvirus ubiquitin-specific protease is critical for efficient T cell lymphoma formation. Proc. Natl. Acad. Sci. U. S. A. 104:20025-20030.
25. Jovasevic V, Liang L, Roizman B. 2008. Proteolytic cleavage of VP1-2 is required for release of herpes simplex virus 1 DNA into the nucleus. J. Virol. 82:3311-3319.
26. Kalt A, Schliwa M. 1993. Molecular components of the centrosome. Trends Cell Biol. 3:118-128.
27. Kann M, Sodeik B, Vlachou A, Gerlich WH, Helenius A. 1999. Phosphorylation-dependent binding of hepatitis B virus core particles to the nuclear pore complex. J. Cell Biol. 145:45-55.
28. Kattenhorn LM, Korbel GA, Kessler BM, Spooner E, Ploegh HL. 2005. A deubiquitinating enzyme encoded by HSV-1 belongs to a family of cysteine proteases that is conserved across the family Herpesviridae. Mol. Cell 19:547-557.
29. Kelly BJ, Diefenbach E, Fraefel C, Diefenbach RJ. 2012. Identification of host cell proteins which interact with herpes simplex virus type 1 tegument protein pUL37. Biochem. Biophys. Res. Commun. 417:961-965.
30. Klupp BG, Fuchs W, Granzow H, Nixdorf R, Mettenleiter TC. 2002. Pseudorabies virus UL36 tegument protein physically interacts with the UL37 protein. J. Virol. 76:3065-3071.
31. Knipe DM, Batterson W, Nosal C, Roizman B, Buchan A. 1981. Molecular genetics of herpes simplex virus. VI. Characterization of a temperature-sensitive mutant defective in the expression of all early viral gene products. J. Virol. 38:539-547.
32. Ko DH, Cunningham AL, Diefenbach RJ. 2010. 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.
33. Kollman JM, Merdes A, Mourey L, Agard DA. 2011. Microtubule nucleation by gamma-tubulin complexes. Nat. Rev. Mol. Cell Biol. 12:709-721.
34. Lee JI, Luxton GW, Smith GA. 2006. Identification of an essential domain in the herpesvirus VP1/2 tegument protein: the carboxy terminus directs incorporation into capsid assemblons. J. Virol. 80:12086-12094.
35. Lee JI, et al. 2009. A herpesvirus encoded deubiquitinase is a novel neuroinvasive determinant. PLoS Pathog. 5:e1000387. doi:10.1371/journal.ppat.1000387.
36. Levin A, Loyter A, Bukrinsky M. 2011. Strategies to inhibit viral protein nuclear import: HIV-1 as a target. Biochim. Biophys. Acta 1813:1646-1653.
37. Luxton GW, et al. 2005. Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc. Natl. Acad. Sci. U. S. A. 102:5832-5837.
38. Luxton GW, Lee JI, Haverlock-Moyns S, Schober JM, Smith GA. 2006. The pseudorabies virus VP1/2 tegument protein is required for intracellular capsid transport. J. Virol. 80:201-209.
39. Mettenleiter T. 2002. Herpesvirus assembly and egress. J. Virol. 76:1537-1547.
40. Michael K, Klupp BG, Mettenleiter TC, Karger A. 2006. Composition of pseudorabies virus particles lacking tegument protein US3, UL47, or UL49 or envelope glycoprotein E. J. Virol. 80:1332-1339.
41. Mijatov B, Cunningham AL, Diefenbach RJ. 2007. Residues F593 and E596 of HSV-1 tegument protein pUL36 (VP1/2) mediate binding of tegument protein pUL37. Virology 368:26-31.
42. Mohl BS, et al. 2010. Random transposon-mediated mutagenesis of the essential large tegument protein pUL36 of pseudorabies virus. J. Virol. 84:8153-8162.
43. Mohl BS, et al. 2009. Intracellular localization of the pseudorabies virus large tegument protein pUL36. J. Virol. 83:9641-9651.
44. Monette A, Pante N, Mouland AJ. 2011. HIV-1 remodels the nuclear pore complex. J. Cell Biol. 193:619-631.
45. Newcomb WW, Brown JC. 2010. Structure and capsid association of the herpesvirus large tegument protein UL36. J. Virol. 84:9408-9414.
46. Ojala PM, Sodeik B, Ebersold MW, Kutay U, Helenius A. 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.
47. Pasdeloup D, Blondel D, Isidro AL, Rixon FJ. 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.
48. Perry RB, Fainzilber M. 2009. Nuclear transport factors in neuronal function. Semin. Cell Dev. Biol. 20:600-606.
49. Preston VG, Murray J, Preston CM, McDougall IM, Stow ND. 2008. The UL25 gene product of herpes simplex virus type 1 is involved in uncoating of the viral genome. J. Virol. 82:6654-6666.
50. Rabe B, et al. 2009. Nuclear entry of hepatitis B virus capsids involves disintegration to protein dimers followed by nuclear reassociation to capsids. PLoS Pathog. 5:e1000563. doi:10.1371/journal.ppat.1000563.
51. Radtke K, et al. 2010. Plus- and minus-end directed microtubule motors bind simultaneously to herpes simplex virus capsids using different inner tegument structures. PLoS Pathog. 6:e1000991. doi:10.1371/journal.ppat.1000991.
52. Roberts AP, et al. 2009. Differing roles of inner tegument proteins pUL36 and pUL37 during entry of herpes simplex virus type 1 (HSV-1). J. Virol. 83:105-116.
53. Schipke J, et al. 2012. The C terminus of the large tegument protein pUL36 contains multiple capsid binding sites that function differently during assembly and cell entry of herpes simplex virus. J. Virol. 86:3682-3700.
54. Schlieker C, et al. 2007. Structure of a herpesvirus-encoded cysteine protease reveals a unique class of deubiquitinating enzymes. Mol. Cell 25:677-687.
55. Shanda SK, Wilson DW. 2008. UL36p is required for efficient transport of membrane-associated herpes simplex virus type 1 along microtubules. J. Virol. 82:7388-7394.
56. Smith GA, Enquist LW. 2002. Break ins and break outs: viral interactions with the cytoskeleton of mammalian cells. Annu. Rev. Cell Dev. Biol. 18:135-161.
57. Tischer BK, von Einem J, Kaufer B, Osterrieder N. 2006. Two-step Red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. Biotechniques 40:191-197.
58. Trotman LC, Mosberger N, Fornerod M, Stidwill RP, Greber UF. 2001. Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat. Cell Biol. 3:1092-1100.
59. Vittone V, et al. 2005. Determination of interactions between tegument proteins of herpes simplex virus type 1. J. Virol. 79:9566-9571.
60. Whittaker GR, Kann M, Helenius A. 2000. Viral entry into the nucleus. Annu. Rev. Cell Dev. Biol. 16:627-651.
61. Wolfstein A, et al. 2006. The inner tegument promotes herpes simplex virus capsid motility along microtubules in vitro. Traffic 7:227-237.
62. Zhou L, et al. 2011. Transportin 3 promotes a nuclear maturation step required for efficient HIV-1 integration. PLoS Pathog. 7:e1002194. doi: 10.1371/journal.ppat.1002194.