The herpes simplex virus immediate-early ubiquitin ligase ICP0 induces degradation of the ICP0 repressor protein E2FBP1

Journal of Virology

Volumn 85, Issue 7, 2011, Pages 3356-3366

  Fukuyo, Yayoi ^a,b   Horikoshi, Nobuo ^c   Ishov, Alexander M ^d   Silverstein, Saul J ^e   Nakajima, Takuma ^b  

^a CALIFORNIA PACIFIC MEDICAL CENTER   (United States)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^e Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

E2F BINDING PROTEIN 1; INFECTED CELL PROTEIN 0; REPRESSOR PROTEIN; RNA; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ARTICLE; AT RICH SEQUENCE; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; EMBRYO; FETUS; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; VIRUS REPLICATION;

CELL LINE; DNA-BINDING PROTEINS; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMEDIATE-EARLY PROTEINS; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES; VIRULENCE FACTORS;

HERPES; HUMAN HERPESVIRUS 1; SIMPLEXVIRUS;

EID: 79952584958     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02105-10     Document Type: Article

References (75)

1. Boutell, C., et al. 2008. Herpes simplex virus type 1 ICP0 phosphorylation mutants impair the E3 ubiquitin ligase activity of ICP0 in a cell type-dependent manner. J. Virol. 82:10647-10656. (Pubitemid 352691194)
2. Brand, P., T. Lenser, and P. Hemmerich. 2010. Assembly dynamics of PML nuclear bodies in living cells. PMC Biophys. 3:3.
3. Chelbi-Alix, M. K., and H. de Thé. 1999. Herpes virus induced proteasome-dependent degradation of the nuclear bodies-associated PML and Sp100 proteins. Oncogene 18:935-941. (Pubitemid 29086270)
4. Chen, J., C. Panagiotidis, and S. Silverstein. 1992. Multimerization of ICP0, a herpes simplex virus immediate-early protein. J. Virol. 66:5598-5602.
5. 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.
6. Deng, L., et al. 2000. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103:351-361.
7. Dent, A. L., et al. 1996. LYSP100-associated nuclear domains (LANDs): description of a new class of subnuclear structures and their relationship to PML nuclear bodies. Blood 88:1423-1426.
8. de The, H., et al. 1991. The PML-RAR alpha fusion mRNA generated by the t(15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR. Cell 66:675-684.
9. Everett, R. D. 2010. Depletion of CoREST does not improve the replication of ICP0 null mutant herpes simplex virus type 1. J. Virol. 84:3695-3698.
10. Everett, R. D. 2000. ICP0, a regulator of herpes simplex virus during lytic and latent infection. Bioessays 22:761-770. (Pubitemid 30613308)
11. Everett, R. D. 2006. Interactions between DNA viruses, ND10 and the DNA damage response. Cell. Microbiol. 8:365-374.
12. Everett, R. D., and M. K. Chelbi-Alix. 2007. PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89:819-830.
13. Everett, R. D., et al. 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. (Pubitemid 28323974)
14. Everett, R. D., P. Lomonte, T. Sternsdorf, R. van Driel, and A. Orr. 1999. Cell cycle regulation of PML modification and ND10 composition. J. Cell Sci. 112:4581-4588. (Pubitemid 30034807)
15. 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)
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. Everett, R. D., and A. Orr. 2009. Herpes simplex virus type 1 regulatory protein ICP0 aids infection in cells with a preinduced interferon response but does not impede interferon-induced gene induction. J. Virol. 83:4978-4983.
18. Everett, R. D., C. Parada, P. Gripon, H. Sirma, and A. Orr. 2008. Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J. Virol. 82:2661-2672. (Pubitemid 351329157)
19. Everett, R. D., M. L. Parsy, and A. Orr. 2009. Analysis of the functions of herpes simplex virus type 1 regulatory protein ICP0 that are critical for lytic infection and derepression of quiescent viral genomes. J. Virol. 83:4963-4977.
20. Everett, R. D., et al. 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)
21. Everett, R. D., D. F. Young, R. E. Randall, and A. Orr. 2008. STAT-1- and IRF-3-dependent pathways are not essential for repression of ICP0-null mutant herpes simplex virus type 1 in human fibroblasts. J. Virol. 82:8871-8881.
22. Everett, R. D., and A. Zafiropoulos. 2004. Visualization by live-cell microscopy of disruption of ND10 during herpes simplex virus type 1 infection. J. Virol. 78:11411-11415. (Pubitemid 39299684)
23. Fukuyo, Y., K. Mogi, Y. Tsunematsu, and T. Nakajima. 2004. E2FBP1/hDril1 modulates cell growth through downregulation of promyelocytic leukemia bodies. Cell Death Differ. 11:747-759. (Pubitemid 39023121)
24. Gregory, S. L., R. D. Kortschak, B. Kalionis, and R. Saint. 1996. Characterization of the dead ringer gene identifies a novel, highly conserved family of sequence-specific DNA-binding proteins. Mol. Cell. Biol. 16:792-799.
25. Hagglund, R., and B. Roizman. 2004. Role of ICP0 in the strategy of conquest of the host cell by herpes simplex virus 1. J. Virol. 78:2169-2178. (Pubitemid 38228910)
26. Halford, W. P., and P. A. Schaffer. 2001. ICP0 is required for efficient reactivation of herpes simplex virus type 1 from neuronal latency. J. Virol. 75:3240-3249.
27. 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.
28. Herrscher, R. F., et al. 1995. The immunoglobulin heavy-chain matrix-associating regions are bound by Bright: a B cell-specific trans-activator that describes a new DNA-binding protein family. Genes Dev. 9:3067-3082. (Pubitemid 26018141)
29. Hobbs, S., S. Jitrapakdee, and J. C. Wallace. 1998. Development of a bicistronic vector driven by the human polypeptide chain elongation factor 1alpha promoter for creation of stable mammalian cell lines that express very high levels of recombinant proteins. Biochem. Biophys. Res. Commun. 252:368-372.
30. Huang, T. H., et al. 1996. Repression by a differentiation-specific factor of the human cytomegalovirus enhancer. Nucleic Acids Res. 24:1695-1701. (Pubitemid 26137928)
31. Jiang, W. Q., and N. Ringertz. 1997. Altered distribution of the promyelocytic leukemia-associated protein is associated with cellular senescence. Cell Growth Differ. 8:513-522. (Pubitemid 27273062)
32. Kim, D., L. Probst, C. Das, and P. W. Tucker. 2007. REKLES is an ARID3-restricted multifunctional domain. J. Biol. Chem. 282:15768-15777.
33. Kim, D., and P. W. Tucker. 2006. A regulated nucleocytoplasmic shuttle contributes to Bright's function as a transcriptional activator of immunoglobulin genes. Mol. Cell. Biol. 26:2187-2201.
34. Kortschak, R. D., et al. 1998. The human dead ringer/bright homolog, DRIL1: cDNA cloning, gene structure, and mapping to D19S886, a marker on 19p13.3 that is strictly linked to the Peutz-Jeghers syndrome. Genomics 51:288-292. (Pubitemid 28395036)
35. Kortschak, R. D., P. W. Tucker, and R. Saint. 2000. ARID proteins come in from the desert. Trends Biochem. Sci. 25:294-299.
36. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
37. Lallemand-Breitenbach, V., and H. de The. 2010. PML nuclear bodies. Cold Spring Harb. Perspect. Biol. 2:a000661.
38. Lee, F., R. Mulligan, P. Berg, and G. Ringold. 1981. Glucocorticoids regulate expression of dihydrofolate reductase cDNA in mouse mammary tumour virus chimaeric plasmids. Nature 294:228-232.
39. Lin, D., et al. 2007. Bright/ARID3A contributes to chromatin accessibility of the immunoglobulin heavy chain enhancer. Mol. Cancer 6:23.
40. Lin, L., et al. 2008. Cross talk between Id1 and its interactive protein Dril1 mediate fibroblast responses to transforming growth factor-beta in pulmonary fibrosis. Am. J. Pathol. 173:337-346.
41. Lindsay, C. R., V. M. Morozov, and A. M. Ishov. 2008. PML NBs (ND10) and Daxx: from nuclear structure to protein function. Front. Biosci. 13:7132-7142.
42. Lium, E. K., C. A. Panagiotidis, X. Wen, and S. Silverstein. 1996. Repression of the alpha0 gene by ICP4 during a productive herpes simplex virus infection. J. Virol. 70:3488-3496. (Pubitemid 26000241)
43. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
44. Lopez, P., R. J. Jacob, and B. Roizman. 2002. Overexpression of promyelocytic leukemia protein precludes the dispersal of ND10 structures and has no effect on accumulation of infectious herpes simplex virus 1 or its proteins. J. Virol. 76:9355-9367. (Pubitemid 34919893)
45. Lopez, P., C. Van Sant, and B. Roizman. 2001. Requirements for the nuclear-cytoplasmic translocation of infected-cell protein 0 of herpes simplex virus 1. J. Virol. 75:3832-3840. (Pubitemid 32246392)
46. Lukashchuk, V., and R. D. Everett. 2010. Regulation of ICP0-null mutant herpes simplex virus type 1 infection by ND10 components ATRX and hDaxx. J. Virol. 84:4026-4040.
47. Ma, K., et al. 2003. E2FBP1/DRIL1, an AT-rich interaction domain-family transcription factor, is regulated by p53. Mol. Cancer Res. 1:438-444.
48. Maul, G. G. 1998. Nuclear domain 10, the site of DNA virus transcription and replication. Bioessays 20:660-667. (Pubitemid 28422226)
49. Maul, G. G., D. Negorev, P. Bell, and A. M. Ishov. 2000. Review: properties and assembly mechanisms of ND10, PML bodies, or PODs. J. Struct. Biol. 129:278-287.
50. Muller, S., and A. Dejean. 1999. Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption. J. Virol. 73:5137-5143. (Pubitemid 29246776)
51. Negorev, D. G., O. V. Vladimirova, A. Ivanov, F. Rauscher III, and G. G. Maul. 2006. Differential role of Sp100 isoforms in interferon-mediated repression of herpes simplex virus type 1 immediate-early protein expression. J. Virol. 80:8019-8029.
52. Negorev, D. G., O. V. Vladimirova, and G. G. Maul. 2009. Differential functions of interferon-upregulated Sp100 isoforms: herpes simplex virus type 1 promoter-based immediate-early gene suppression and PML protection from ICP0-mediated degradation. J. Virol. 83:5168-5180.
53. Nystrom, K., et al. 2004. Real time PCR for monitoring regulation of host gene expression in herpes simplex virus type 1-infected human diploid cells. J. Virol. Methods 118:83-94. (Pubitemid 38479737)
54. Parkinson, J., and R. D. Everett. 2000. Alphaherpesvirus proteins related to herpes simplex virus type 1 ICP0 affect cellular structures and proteins. J. Virol. 74:10006-10017.
55. Pearson, M., et al. 2000. PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature 406:207-210.
56. Peeper, D. S., et al. 2002. A functional screen identifies hDRIL1 as an oncogene that rescues RAS-induced senescence. Nat. Cell Biol. 4:148-153.
57. Prieur, A., K. Nacerddine, M. van Lohuizen, and D. S. Peeper. 2009. SUMOylation of DRIL1 directs its transcriptional activity towards leukocyte lineage-specific genes. PLoS One 4:e5542.
58. Rajaiya, J., M. Hatfield, J. C. Nixon, D. J. Rawlings, and C. F. Webb. 2005. Bruton's tyrosine kinase regulates immunoglobulin promoter activation in association with the transcription factor Bright. Mol. Cell. Biol. 25:2073-2084.
59. Roizman, B. 1999. HSV gene functions: what have we learned that could be generally applicable to its near and distant cousins? Acta Virol. 43:75-80.
60. Russell, J., N. D. Stow, E. C. Stow, and C. M. Preston. 1987. Herpes simplex virus genes involved in latency in vitro. J. Gen. Virol. 68:3009-3018.
61. Saffert, R. T., and R. F. Kalejta. 2008. Promyelocytic leukemia-nuclear body proteins: herpesvirus enemies, accomplices, or both? Future Virol. 3:265-277.
62. Salomoni, P., and A. F. Khelifi. 2006. Daxx: death or survival protein? Trends Cell Biol. 16:97-104.
63. Schmittgen, T. D., and K. J. Livak. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3:1101-1108.
64. Sternsdorf, T., T. Grotzinger, K. Jensen, and H. Will. 1997. Nuclear dots: actors on many stages. Immunobiology 198:307-331. (Pubitemid 28021406)
65. Suzuki, M., et al. 1998. A novel E2F binding protein with Myc-type HLH motif stimulates E2F-dependent transcription by forming a heterodimer. Oncogene 17:853-865. (Pubitemid 28430208)
66. Tavalai, N., and T. Stamminger. 2008. New insights into the role of the subnuclear structure ND10 for viral infection. Biochim. Biophys. Acta 1783:2207-2221.
67. Thompson, R. L., and N. M. Sawtell. 2006. Evidence that the herpes simplex virus type 1 ICP0 protein does not initiate reactivation from latency in vivo. J. Virol. 80:10919-10930.
68. Van Sant, C., P. Lopez, S. J. Advani, and B. Roizman. 2001. Role of cyclin D3 in the biology of herpes simplex virus 1 ICP0. J. Virol. 75:1888-1898. (Pubitemid 32110179)
69. Webb, C. F. 2001. The transcription factor, Bright, and immunoglobulin heavy chain expression. Immunol. Res. 24:149-161.
70. Webb, C. F., et al. 2000. The transcription factor Bright associates with Bruton's tyrosine kinase, the defective protein in immunodeficiency disease. J. Immunol. 165:6956-6965. (Pubitemid 32001167)
71. Wileman, T. 2007. Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design? Annu. Rev. Microbiol. 61:149-167.
72. Wilsker, D., A. Patsialou, P. B. Dallas, and E. Moran. 2002. ARID proteins: a diverse family of DNA binding proteins implicated in the control of cell growth, differentiation, and development. Cell Growth Differ. 13:95-106. (Pubitemid 34507099)
73. Wilsker, D., et al. 2005. Nomenclature of the ARID family of DNA-binding proteins. Genomics 86:242-251. (Pubitemid 40917228)
74. Zhu, X. X., J. X. Chen, and S. Silverstein. 1991. Isolation and characterization of a functional cDNA encoding ICP0 from herpes simplex virus type 1. J. Virol. 65:957-960.
75. 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. (Pubitemid 20279862)