The cellular localization pattern of varicella-zoster virus ORF29p is influenced by proteasome-mediated degradation

Journal of Virology

Volumn 80, Issue 3, 2006, Pages 1497-1512

  Stallings, Christina L ^a   Duigou, Gregory J ^a   Gershon, Anne A ^a   Gershon, Michael D ^a   Silverstein, Saul J ^a,b  

^a College of Physicians and Surgeons ^*  (United States)

^b Department of Microbiology ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN; IMMEDIATE EARLY PROTEIN; PROTEASOME;

ARTICLE; ASTROCYTOMA; CELL NUCLEUS; CELL SPECIFICITY; CELL TYPE; CONTROLLED STUDY; GENE TRANSLOCATION; GUINEA PIG; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; INTESTINE INNERVATION; LATENT PERIOD; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OPEN READING FRAME; OPEN READING FRAME 29; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; VARICELLA ZOSTER VIRUS;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; DNA-BINDING PROTEINS; ENTERIC NERVOUS SYSTEM; EXONS; GUINEA PIGS; HERPESVIRUS 1, HUMAN; HERPESVIRUS 3, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; LEUPEPTINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTATION; OPEN READING FRAMES; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA, MESSENGER; RNA, VIRAL; SUBCELLULAR FRACTIONS; TISSUE CULTURE TECHNIQUES; UBIQUITIN-PROTEIN LIGASES; VIRAL PROTEINS;

CAVIA PORCELLUS; HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 3;

EID: 31144471071     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.3.1497-1512.2006     Document Type: Article

References (69)

1. Arvin, A. M. 1996. Varicella-zoster virus. Clin. Microbiol. Rev. 9:361-381.
2. Assouline, J. G., M. J. Levin, E. O. Major, B. Forghani, S. E. Straus, and J. M. Ostrove. 1990. Varicella-zoster virus infection of human astrocytes, Schwann cells, and neurons. Virology 179:834-844.
3. Boucaud, D., H. Yoshitake, J. Hay, and W. Ruyechan. 1998. The varicella-zoster virus (VZV) open-reading frame 29 protein acts as a modulator of a late VZV gene promoter. J Infect. Dis. 178(Suppl. 1):S34-S38.
4. Boutell, C., A. Orr, and R. D. Everett. 2003. PML residue lysine 160 is required for the degradation of PML induced by herpes simplex virus type 1 regulatory protein ICP0. J. Virol. 77:8686-8694.
5. Boutell, C., S. Sadis, and R. D. Everett. 2002. Herpes simplex virus type 1 immediate-early protein ICP0 and its isolated RING finger domain act as ubiquitin E3 ligases in vitro. J. Virol. 76:841-850.
6. Burch, A. D., and S. K. Weller. 2004. Nuclear sequestration of cellular chaperone and proteasomal machinery during herpes simplex virus type 1 infection. J. Virol. 78:7175-7185.
7. Burkham, J., D. M. Coen, C. B. Hwang, and S. K. Weller. 2001. Interactions of herpes simplex virus type 1 with ND10 and recruitment of PML to replication compartments. J. Virol. 75:2353-2367.
8. Chen, J., and S. Silverstein. 1992. Herpes simplex viruses with mutations in the gene encoding ICP0 are defective in gene expression. J. Virol. 66:2916-2927.
9. Chen, J. J., A. A. Gershon, Z. S. Li, O. Lungu, and M. D. Gershon. 2003. Latent and lytic infection of isolated guinea pig enteric ganglia by varicella zoster virus. J. Med. Virol. 70(Suppl. 1):S71-S8.
10. Cohrs, R. J., M. Barbour, and D. H. Gilden. 1996. Varicella-zoster virus (VZV) transcription during latency in human ganglia: detection of transcripts mapping to genes 21, 29, 62, and 63 in a cDNA library enriched for VZV RNA. J. Virol. 70:2789-2796.
11. Cohrs, R. J., M. B. Barbour, R. Mahalingam, M. Wellish, and D. H. Gilden. 1995. Varicella-zoster virus (VZV) transcription during latency in human ganglia: prevalence of VZV gene 21 transcripts in latently infected human ganglia. J. Virol. 69:2674-2678.
12. Cohrs, R. J., D. H. Gilden, P. R. Kinchington, E. Grinfeld, and P. G. Kennedy. 2003. Varicella-zoster virus gene 66 transcription and translation in latently infected human ganglia. J. Virol. 77:6660-6665.
13. Cohrs, R. J., K. Srock, M. B. Barbour, G. Owens, R. Mahalingam, M. E. Devlin, M. Wellish, and D. H. Gilden. 1994. Varicella-zoster virus (VZV) transcription during latency in human ganglia: construction of a cDNA library from latently infected human trigeminal ganglia and detection of a VZV transcript. J. Virol. 68:7900-7908.
14. Cohrs, R. J., J. Wischer, C. Essman, and D. H. Gilden. 2002. Characterization of varicella-zoster virus gene 21 and 29 proteins in infected cells. J. Virol. 76:7228-7238.
15. Croen, K. D., J. M. Ostrove, L. J. Dragovic, and S. E. Straus. 1988. Patterns of gene expression and sites of latency in human nerve ganglia are different for varicella-zoster and herpes simplex viruses. Proc. Natl. Acad. Sci. USA 85:9773-9777.
16. Croen, K. D., and S. E. Straus. 1991. Varicella-zoster virus latency. Annu. Rev. Microbiol. 45:265-282.
17. Diao, L., B. Zhang, J. Fan, X. Gao, S. Sun, K. Yang, D. Xin, N. Jin, Y. Geng, and C. Wang. 2005. Herpes virus proteins ICP0 and BICP0 can activate NF-kappaB by catalyzing IkappaBalpha ubiquitination. Cell Signal. 17:217-229.
18. Eom, C. Y., W. D. Heo, M. L. Craske, T. Meyer, and I. R. Lehman. 2004. The neural F-box protein NFB42 mediates the nuclear export of the herpes simplex virus type 1 replication initiator protein (UL9 protein) after viral infection. Proc. Natl. Acad. Sci. USA 101:4036-4040.
19. Eom, C. Y., and I. R. Lehman. 2003. Replication-initiator protein (UL9) of the herpes simplex virus 1 binds NFB42 and is degraded via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 100:9803-9807.
20. Everett, R. D. 2000. ICP0, a regulator of herpes simplex virus during lytic and latent infection. Bioessays 22:761-770.
21. Everett, R. D. 1986. The products of herpes simplex virus type 1 (HSV-1) immediate early genes 1, 2 and 3 can activate HSV-1 gene expression in trans. J. Gen. Virol. 67:2507-2513.
22. Everett, R. D., A. Orr, and C. M. Preston. 1998. A viral activator of gene expression functions via the ubiquitin-proteasome pathway. EMBO J. 17:7161-7169.
23. Gelman, I. H., and S. Silverstein. 1986. Co-ordinate regulation of herpes simplex virus gene expression is mediated by the functional interaction of two immediate early gene products. J. Mol. Biol. 191:395-409.
24. Graham, F. L., J. Smiley, W. C. Russell, and R. Nairn. 1977. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 36:59-74.
25. Grinfeld, E., and P. G. Kennedy. 2004. Translation of varicella-zoster virus genes during human ganglionic latency. Virus Genes 29:317-319.
26. Grose, C., and P. A. Brunel. 1978. Varicella-zoster virus: isolation and propagation in human melanoma cells at 36 and 32 degrees C. Infect. Immun. 19:199-203.
27. Gu, H., Y. Liang, G. Mandel, and B. Roizman. 2005. Components of the REST/CoREST/histone deacetylase repressor complex are disrupted, modified, and translocated in HSV-1-infected cells. Proc. Natl. Acad. Sci. USA 102:7571-7576.
28. Hagglund, R., C. Van Sant, P. Lopez, and B. Roizman. 2002. Herpes simplex virus 1-infected cell protein 0 contains two E3 ubiquitin ligase sites specific for different E2 ubiquitin-conjugating enzymes. Proc. Natl. Acad. Sci. USA 99:631-636.
29. Hamamoto, T., S. Gunji, H. Tsuji, and T. Beppu. 1983. Leptomycins A and B, new antifungal antibiotics. I. Taxonomy of the producing strain and their fermentation, purification and characterization. J. Antibiot. (Tokyo) 36:639-645.
30. Harris, R. A., R. D. Everett, X. X. Zhu, S. Silverstein, and C. M. Preston. 1989. Herpes simplex virus type 1 immediate-early protein Vmw110 reactivates latent herpes simplex virus type 2 in an in vitro latency system. J. Virol. 63:3513-3515.
31. Hay, J., and W. T. Ruyechan. 1994. Varicella-zoster virus: a different kind of herpesvirus latency? Semin. Virol. 5:241-248.
32. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
33. Inchauspe, G., S. Nagpal, and J. M. Ostrove. 1989. Mapping of two varicella-zoster virus-encoded genes that activate the expression of viral early and late genes. Virology 173:700-709.
34. Jordan, R., and P. A. Schaffer. 1997. Activation of gene expression by herpes simplex virus type 1 ICP0 occurs at the level of mRNA synthesis. J. Virol. 71:6850-6862.
35. Kamei, Y., S. Yuba, T. Nakayama, and Y. Yoneda. 1999. Three distinct classes of the alpha-subunit of the nuclear pore-targeting complex (importin-alpha) are differentially expressed in adult mouse tissues. J. Histochem Cytochem. 47:363-372.
36. Kennedy, P. G., E. Grinfeld, and J. E. Bell. 2000. Varicella-zoster virus gene expression in latently infected and explanted human ganglia. J. Virol. 74:11893-11898.
37. Kennedy, P. G., E. O. Major, R. K. Williams, and S. E. Straus. 1994. Down-regulation of glial fibrillary acidic protein expression during acute lytic varicella-zoster virus infection of cultured human astrocytes. Virology 205:558-562.
38. Kinchington, P. R., D. Bookey, and S. E. Turse. 1995. The transcriptional regulatory proteins encoded by varicella-zoster virus open reading frames (ORFs) 4 and 63, but not ORF 61, are associated with purified virus particles. J. Virol. 69:4274-4282.
39. Kinchington, P. R., G. Inchauspe, J. H. Subak-Sharpe, F. Robey, J. Hay, and W. T. Ruyechan. 1988. Identification and characterization of a varicella-zoster virus DNA-binding protein by using antisera directed against a predicted synthetic oligopeptide. J. Virol. 62:802-809.
40. Kinchington, P. R., and S. E. Turse. 1998. Regulated nuclear localization of the varicella-zoster virus major regulatory protein, IE62. J. Infect. Dis. 178(Suppl. 1):S16-S21.
41. Kisselev, A. F., and A. L. Goldberg. 2001. Proteasome inhibitors: from research tools to drug candidates. Chem. Biol. 8:739-758.
42. Kohler, M., C. Speck, M. Christiansen, F. R. Bischoff, S. Prehn, H. Haller, D. Gorlich, and E. Hartmann. 1999. Evidence for distinct substrate specificities of importin alpha family members in nuclear protein import. Mol. Cell. Biol. 19:7782-7791.
43. Kudo, N., B. Wolff, T. Sekimoto, E. P. Schreiner, Y. Yoneda, M. Yanagida, S. Horinouchi, and M. Yoshida. 1998. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242:540-547.
44. Lee, D. H., and A. L. Goldberg. 1998. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8:397-403.
45. Lee, S. S., and I. R. Lehman. 1997. Unwinding of the box I element of a herpes simplex virus type 1 origin by a complex of the viral origin binding protein, single-strand DNA binding protein, and single-stranded DNA. Proc. Natl. Acad. Sci. USA 94:2838-2842.
46. Lees-Miller, S. P., M. C. Long, M. A. Kilvert, V. Lam, S. A. Rice, and C. A. Spencer. 1996. Attenuation of DNA-dependent protein kinase activity and its catalytic subunit by the herpes simplex virus type 1 transactivator ICP0. J. Virol. 70:7471-7477.
47. Li, M., C. L. Brooks, F. Wu-Baer, D. Chen, R. Baer, and W. Gu. 2003. Mono-versus polyubiquitination: differential control of p53 fate by Mdm2. Science 302:1972-1975.
48. Lomonte, P., J. Thomas, P. Texier, C. Caron, S. Khochbin, and A. L. Epstein. 2004. Functional interaction between class II histone deacetylases and ICP0 of herpes simplex virus type 1. J. Virol. 78:6744-6757.
49. Lungu, O., C. A. Panagiotidis, P. W. Annunziato, A. A. Gershon, and S. J. Silverstein. 1998. Aberrant intracellular localization of Varicella-Zoster virus regulatory proteins during latency. Proc. Natl. Acad. Sci. USA 95:7080-7085.
50. Meier, J. L., R. P. Holman, K. D. Croen, J. E. Smialek, and S. E. Straus. 1993. Varicella-zoster virus transcription in human trigeminal ganglia. Virology 193:193-200.
51. Meier, J. L., X. Luo, M. Sawadogo, and S. E. Straus. 1994. The cellular transcription factor USF cooperates with varicella-zoster virus immediate-early protein 62 to symmetrically activate a bidirectional viral promoter. Mol. Cell. Biol. 14:6896-6906.
52. Meier, J. L., and S. E. Straus. 1995. Interactions between varicella-zoster virus IE62 and cellular transcription factor USF in the coordinate activation of genes 28 and 29. Neurology 4S:S30-S32.
53. Meier, J. L., and S. E. Straus. 1993. Varicella-zoster virus DNA polymerase and major DNA-binding protein genes have overlapping divergent promoters. J. Virol. 67:7573-7581.
54. Ng, P., D. T. Cummings, C. M. Evelegh, and F. L. Graham. 2000. Yeast recombinase FLP functions effectively in human cells for construction of adenovirus vectors. BioTechniques 29:524-526, 528.
55. O'Hare, P, and G. S. Hayward. 1985. Evidence for a direct role for both the 175,000- and 110,000-molecular-weight immediate-early proteins of herpes simplex virus in the transactivation of delayed-early promoters. J. Virol. 53:751-760.
56. O'Hare, P., and G. S. Hayward. 1985. Three trans-acting regulatory proteins of herpes simplex virus modulate immediate-early gene expression in a pathway involving positive and negative feedback regulation. J. Virol. 56:723-733.
57. Parkinson, J., S. P. Lies-Miller, and R. D. Everett. 1999. Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA-dependent protein kinase. J. Virol. 73:650-657.
58. Philipson, L. 1961. Adenovirus assay by the fluorescent cell-counting procedure. Virology 15:263-268.
59. Poon, A. P., S. J. Silverstein, and B. Roizman. 2002. An early regulatory function required in a cell type-dependent manner is expressed by the genomic but not the cDNA copy of the herpes simplex virus 1 gene encoding infected cell protein 0. J. Virol. 76:9744-9755.
60. Roberts, C. R., A. C. Weir, J. Hay, S. E. Straus, and W. T. Ruyechan. 1985. DNA-binding proteins present in varicella-zoster virus-infected cells. J. Virol. 55:45-53.
61. Rost, B., and J. Liu. 2003. The PredictProtein server. Nucleic Acids Res. 31:3300-3304.
62. Stallings, C. L., and S. Silverstein. 2005. Dissection of a novel nuclear localization signal in open reading frame 29 of varicella-zoster virus. J. Virol. 79:13070-13081.
63. Straus, S. E. 1993. Shingles. Sorrows, salves, and solutions. JAMA 269:1836-1839.
64. Taylor, T. J., and D. M. Knipe. 2003. C-terminal region of herpes simplex virus ICP8 protein needed for intranuclear localization. Virology 309:219-231.
65. Van Sant, C., R. Hagglund, P. Lopez, and B. Roizman. 2001. The infected cell protein 0 of herpes simplex virus 1 dynamically interacts with proteasomes, binds and activates the cdc34 E2 ubiquitin-conjugating enzyme, and possesses in vitro E3 ubiquitin ligase activity. Proc. Natl. Acad. Sci. USA 98:8815-8820.
66. Yang, M., J. Hay, and W. T. Ruyechan. 2004. The DNA element controlling expression of the varicella-zoster virus open reading frame 28 and 29 genes consists of two divergent unidirectional promoters which have a common USF site. J. Virol. 78:10939-10952.
67. Zhu, X. X., J. X. Chen, C. S. Young, and S. Silverstein. 1990. Reactivation of latent herpes simplex virus by adenovirus recombinants encoding mutant IE-0 gene products. J. Virol. 64:4489-4498.
68. Zhu, X. X., C. S. Young, and S. Silverstein. 1988. Adenovirus vector expressing functional herpes simplex virus ICP0. J. Virol. 62:4544-4553.
69. Zhu, Z., M. D. Gershon, Y. Hao, R. T. Ambron, C. A. Gabel, and A. A. Gershon. 1995. Envelopment of varicella-zoster virus: targeting of viral glycoproteins to the trans-Golgi network. J. Virol. 69:7951-7959.