Nuclear import of the varicella-zoster virus latency-associated protein ORF63 in primary neurons requires expression of the lytic protein ORF61 and occurs in a proteasome-dependent manner

Journal of Virology

Volumn 82, Issue 17, 2008, Pages 8673-8686

  Walters, Matthew S ^a   Kyratsous, Christos A ^a   Wan, Shilin ^a   Silverstein, Saul ^a  

^a Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LATENCY ASSOCIATED PEPTIDE; OPEN READING FRAME 61 PROTEIN; OPEN READING FRAME 63 PROTEIN; PROTEASOME; VIRUS LARGE T ANTIGEN; VIRUS PROTEIN;

ADENOVIRUS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; GUINEA PIG; HERPES ZOSTER; HETEROLOGOUS EXPRESSION; NERVE CELL; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SIMIAN VIRUS 40; VARICELLA ZOSTER VIRUS;

ACTIVE TRANSPORT, CELL NUCLEUS; ADENOVIRIDAE; AMINO ACID SEQUENCE; ANIMALS; CELL LINE, TRANSFORMED; CELL NUCLEUS; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; ENTERIC NERVOUS SYSTEM; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GANGLIA; GLUTATHIONE TRANSFERASE; GUINEA PIGS; HERPES ZOSTER; HERPESVIRUS 3, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; LUCIFERASES, RENILLA; MOLECULAR SEQUENCE DATA; NEURONS; PLASMIDS; PROTEASOME ENDOPEPTIDASE COMPLEX; RECOMBINANT FUSION PROTEINS; SUBCELLULAR FRACTIONS; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS; VIRUS LATENCY;

ADENOVIRIDAE; CAVIA; HUMAN HERPESVIRUS 3; SIMIAN VIRUS 40;

EID: 50149084461     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00685-08     Document Type: Article

References (68)

1. Ambagala, A. P., and J. I. Cohen. 2007. Varicella-zoster virus IE63, a major viral latency protein, is required to inhibit the alpha interferon-induced antiviral response. J. Virol. 81:7844-7851.
2. Baiker, A., C. Bagowski, H. Ito, M. Sommer, L. Zerboni, K. Fabel, J. Hay, W. Ruyechan, and A. M. Arvin. 2004. The immediate-early 63 protein of varicella-zoster virus: analysis of functional domains required for replication in vitro and for T-cell and skin tropism in the SCIDhu model in vivo. J. Virol. 78:1181-1194.
3. Beals, C. R., N. A. Clipstone, S. N. Ho, and G. R. Crabtree. 1997. Nuclear localization of NF-ATc by a calcineurin-dependent, cyclosporin- sensitive intramolecular interaction. Genes Dev. 11:824-834.
4. Beg, A. A., S. M. Ruben, R. I. Scheinman, S. Haskill, C. A. Rosen, and A. S. Baldwin, Jr. 1992. I kappa B interacts with the nuclear localization sequences of the subunits of NF-kappa B: a mechanism for cytoplasmic retention. Genes Dev. 6:1899-1913.
5. Bontems, S., E. Di Valentin, L. Baudoux, B. Rentier, C. Sadzot-Delvaux, and J. Piette. 2002. Phosphorylation of varicella-zoster virus IE63 protein by casein kinases influences its cellular localization and gene regulation activity. J. Biol. Chem. 277:21050-21060.
6. Boutell, C., S. Sadis, and R. D. Everett. 2002. Herpes simplex virus type 1 immediate-early protein ICP0 and is isolated RING finger domain act as ubiquitin E3 ligases in vitro. J. Virol. 76:841-850.
7. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
8. 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-S78.
9. Cohen, J. I., E. Cox, L. Pesnicak, S. Srinivas, and T. Krogmann. 2004. The varicella-zoster virus open reading frame 63 latency-associated protein is critical for establishment of latency. J. Virol. 78:11833- 11840.
10. Cohen, J. I., T. Krogmann, S. Bontems, C. Sadzot-Delvaux, and L. Pesnicak. 2005. Regions of the varicella-zoster virus open reading frame 63 latency-associated protein important for replication in vitro are also critical for efficient establishment of latency. J. Virol. 79:5069-5077.
11. 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.
12. 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.
13. Cohrs, R. J., and D. H. Gilden. 2007. Prevalence and abundance of latently transcribed varicella-zoster virus genes in human ganglia. J. Virol. 81:2950-2956.
14. Cohrs, R. J., and D. H. Gilden. 2003. Varicella zoster virus transcription in latently-infected human ganglia. Anticancer Res. 23:2063-2069.
15. 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.
16. Cohrs, R. J., J. Randall, J. Smith, D. H. Gilden, C. Dabrowski, H. van Der Keyl, and R. Tal-Singer. 2000. Analysis of individual human trigeminal ganglia for latent herpes simplex virus type 1 and varicella-zoster virus nucleic acids using real-time PCR. J. Virol. 74:11464-11471.
17. 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.
18. 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.
19. 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.
20. Davison, A. J., and J. E. Scott. 1986. The complete DNA sequence of varicella-zoster virus. J. Gen. Virol. 67:1759-1816.
21. Debrus, S., C. Sadzot-Delvaux, A. F. Nikkels, J. Piette, and B. Rentier. 1995. Varicella-zoster virus gene 63 encodes an immediate-early protein that is abundantly expressed during latency. J. Virol. 69:3240-3245.
22. Desloges, N., M. Rahaus, and M. H. Wolff. 2005. The varicella-zoster virus-mediated delayed host shutoff: open reading frame 17 has no major function, whereas immediate-early 63 protein represses heterologous gene expression. Microbes Infect. 7:1519-1529.
23. 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.
24. Di Valentin, E., S. Bontems, L. Habran, O. Jolois, N. Markine-Goriaynoff, A. Vanderplasschen, C. Sadzot-Delvaux, and J. Piette. 2005. Varicella-zoster virus IE63 protein represses the basal transcription machinery by disorganizing the pre-initiation complex. Biol. Chem. 386:255-267.
25. Everett, R. D., P. Freemont, H. Saitoh, M. Dasso, A. Orr, M. Kathoria, and J. Parkinson. 1998. The disruption of ND10 during herpes simplex virus infection correlates with the Vmw110- and proteasome-dependent loss of several PML isoforms. J. Virol. 72:6581-6591.
26. 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.
27. Fang, X., T. Chen, K. Tran, and C. S. Parker. 2001. Developmental regulation of the heat shock response by nuclear transport factor karyopherin-alpha3. Development 128:3349-3358.
28. Gilden, D. H., R. J. Cohrs, and R. Mahalingam. 2003. Clinical and molecular pathogenesis of varicella virus infection. Viral Immunol. 16:243-258.
29. Grinfeld, E., and P. G. Kennedy. 2004. Translation of varicella-zoster virus genes during human ganglionic latency. Virus Genes 29:317-319.
30. Habran, L., S. Bontems, E. Di Valentin, C. Sadzot-Delvaux, and J. Piette. 2005. Varicella-zoster virus IE63 protein phosphorylation by roscovitine-sensitive cyclin-dependent kinases modulates its cellular localization and activity. J. Biol. Chem. 280:29135-29143.
31. Habran, L., N. El Mjiyad, E. Di Valentin, C. Sadzot-Delvaux, S. Bontems, and J. Piette. 2007. The varicella-zoster virus immediate-early 63 protein affects chromatin-controlled gene transcription in a cell-type dependent manner. BMC Mol. Biol. 8:99.
32. Hahn, H., and A. C. Palmenberg. 1995. Encephalomyocarditis viruses with short poly(C) tracts are more virulent than their mengovirus counterparts. J. Virol. 69:2697-2699.
33. Heineman, T. C., and J. I. Cohen. 1995. The varicella-zoster virus (VZV) open reading frame 47 (ORF47) protein kinase is dispensable for viral replication and is not required for phosphorylation of ORF63 protein, the VZV homolog of herpes simplex virus ICP22. J. Virol. 69:7367-7370.
34. Hood, C., A. L. Cunningham, B. Slobedman, A. M. Arvin, M. H. Sommer, P. R. Kinchington, and A. Abendroth. 2006. Varicella-zoster virus ORF63 inhibits apoptosis of primary human neurons. J. Virol. 80:1025-1031.
35. Hoover, S. E., R. J. Cohrs, Z. G. Rangel, D. H. Gilden, P. Munson, and J. I. Cohen. 2006. Downregulation of varicella-zoster virus (VZV) immediate-early ORF62 transcription by VZV ORF63 correlates with virus replication in vitro and with latency. J. Virol. 80:3459-3468.
36. Kalderon, D., B. L. Roberts, W. D. Richardson, and A. E. Smith. 1984. A short amino acid sequence able to specify nuclear location. Cell 39:499-509.
37. 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.
38. Kennedy, P. G., E. Grinfeld, S. Bontems, and C. Sadzot-Delvaux. 2001. Varicella-zoster virus gene expression in latently infected rat dorsal root ganglia. Virology 289:218-223.
39. Kenyon, T. K., E. Homan, J. Storlie, M. Ikoma, and C. Grose. 2003. Comparison of varicella-zoster virus ORF47 protein kinase and casein kinase II and their substrates. J. Med. Virol. 70(Suppl. 1):S95-S102.
40. Kenyon, T. K., J. Lynch, J. Hay, W. Ruyechan, and C. Grose. 2001. Varicella-zoster virus ORF47 protein serine kinase: characterization of a cloned, biologically active phosphotransferase and two viral substrates, ORF62 and ORF63. J. Virol. 75:8854-8858.
41. 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.
42. Kost, R. G., H. Kupinsky, and S. E. Straus. 1995. Varicella-zoster virus gene 63: transcript mapping and regulatory activity. Virology 209:218-224.
43. Kyratsous, C. A., and S. J. Silverstein. 2007. BAG3, a host cochaperone, facilitates varicella-zoster virus replication. J. Virol. 81:7491-7503.
44. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
45. Li, M., C. L. Brooks, F. Wu-Baer, D. Chen, R. Baer, and W. Gu. 2003. Monoversus polyubiquitination: differential control of p53 fate by Mdm2, Science 302:1972-1975.
46. 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.
47. Lynch, J. M., T. K. Kenyon, C. Grose, J. Hay, and W. T. Ruyechan. 2002. Physical and functional interaction between the varicella zoster virus IE63 and IE62 proteins. Virology 302:71-82.
48. Mahalingam, R., M. Wellish, R. Cohrs, S. Debrus, J. Piette, B. Rentier, and D. H. Gilden. 1996. Expression of protein encoded by varicella-zoster virus open reading frame 63 in latently infected human ganglionic neurons. Proc. Natl. Acad. Sci. USA 93:2122-2124.
49. 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.
50. Moriuchi, H., M. Moriuchi, and J. I. Cohen. 1994. The RING finger domain of the varicella-zoster virus open reading frame 61 protein is required for its transregulatory functions. Virology 205:238-246.
51. Moriuchi, H., M. Moriuchi, H. A. Smith, S. E. Straus, and J. I. Cohen. 1992. Varicella-zoster virus open reading frame 61 protein is functionally homologous to herpes simplex virus type 1 ICP0. J. Virol. 66:7303-7308.
52. Moriuchi, H., M. Moriuchi, S. E. Straus, and J. I. Cohen. 1993. Varicella-zoster virus (VZV) open reading frame 61 protein transactivates VZV gene promoters and enhances the infectivity of VZV DNA. J. Virol. 67:4290-4295.
53. 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.
54. Panagiotidis, C. A., and S. J. Silverstein. 1995. pALEX, a dual-tag prokaryotic expression vector for the purification of full-length proteins. Gene 164:45-47.
55. Perry, L. J., F. J. Rixon, R. D. Everett, M. C. Frame, and D. J. McGeoch. 1986. Characterization of the IE110 gene of herpes simplex virus type 1. J. Gen. Virol. 67:2365-2380.
56. Pouton, C. W., K. M. Wagstaff, D. M. Roth, G. W. Moseley, and D. A. Jans. 2007. Targeted delivery to the nucleus. Adv. Drug Deliv. Rev. 59:698-717.
57. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31-40.
58. Sommer, M. H., E. Zagha, O. K. Serrano, C. C. Ku, L. Zerboni, A. Baiker, R. Santos, M. Spengler, J. Lynch, C. Grose, W. Ruyechan, J. Hay, and A. M. Arvin. 2001. Mutational analysis of the repeated open reading frames, ORFs 63 and 70 and ORFs 64 and 69, of varicella-zoster virus. J. Virol. 75:8224-8239.
59. Stallings, C. L., G. J. Duigou, A. A. Gershon, M. D. Gershon, and S. J. Silverstein. 2006. The cellular localization pattern of varicella-zoster virus ORF29p is influenced by proteasome-mediated degradation. J. Virol. 80:1497-1512.
60. Stevenson, D., K. L. Colman, and A. J. Davison. 1992. Characterization of the varicella-zoster virus gene 61 protein. J. Gen. Virol. 73:521-530.
61. Stevenson, D., M. Xue, J. Hay, and W. T. Ruyechan. 1996. Phosphorylation and nuclear localization of the varicella-zoster virus gene 63 protein. J. Virol. 70:658-662.
62. Stewart, M. 2007. Molecular mechanism of the nuclear protein import cycle. Nat. Rev. Mol. Cell Biol. 8:195-208.
63. Terry, L. J., E. B. Shows, and S. R. Wente. 2007. Crossing the nuclear envelope: hierarchical regulation of nucleocytoplasmic transport. Science 318:1412-1416.
64. Traenckner, E. B., S. Wilk, and P. A. Baeuerle. 1994. A proteasome inhibitor prevents activation of NF-kappa B and stabilizes a newly phosphorylated form of I kappa B-alpha that is still bound to NF-kappa B. EMBO J. 13:5433-5441.
65. Trotman, L. C., X. Wang, A. Alimonti, Z. Chen, J. Teruya-Feldstein, H. Yang, N. P. Pavletich, B. S. Carver, C. Cordon-Cardo, H. Erdjument-Bromage, P. Tempst, S. G. Chi, H. J. Kim, T. Misteli, X. Jiang, and P. P. Pandolfi. 2007. Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell 128:141-156.
66. 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.
67. Xiao, C. Y., S. Hubner, and D. A. Jans. 1997. SV40 large tumor antigen nuclear import is regulated by the double-stranded DNA-dependent protein kinase site (serine 120) flanking the nuclear localization sequence. J. Biol. Chem. 272:22191-22198.
68. Zuranski, T., H. Nawar, D. Czechowski, J. M. Lynch, A. Arvin, J. Hay, and W. T. Ruyechan. 2005. Cell-type-dependent activation of the cellular EF-1alpha promoter by the varicella-zoster virus IE63 protein. Virology 338:35-42.