Epigenetic modulation of gene expression from quiescent herpes simplex virus genomes

Journal of Virology

Volumn 83, Issue 17, 2009, Pages 8514-8524

  Ferenczy, Michael W ^a   DeLuca, Neal A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROCHROMATIN PROTEIN 1; HISTONE H3; LYSINE; MICROCOCCAL NUCLEASE; RNA; VIRUS PROTEIN; HISTONE; IMMEDIATE EARLY PROTEIN; MESSENGER RNA; THYMIDINE KINASE; UBIQUITIN PROTEIN LIGASE; VIRUS RNA; VMW110 PROTEIN, HUMAN HERPESVIRUS 1;

ACETYLATION; ARTICLE; CELL TYPE; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; HERPES SIMPLEX VIRUS; HETEROCHROMATIN; HUMAN; HUMAN CYTOMEGALOVIRUS; METHYLATION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; VERO CELL; VIRUS GENOME; VIRUS MUTANT; WILD TYPE; ANIMAL; BIOSYNTHESIS; CELL LINE; CERCOPITHECUS; CYTOMEGALOVIRUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY;

HUMAN HERPESVIRUS 5; SIMPLEXVIRUS;

ACETYLATION; ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; CYTOMEGALOVIRUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, VIRAL; HETEROCHROMATIN; HISTONES; HUMANS; IMMEDIATE-EARLY PROTEINS; METHYLATION; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; RNA, VIRAL; SIMPLEXVIRUS; THYMIDINE KINASE; TRANSCRIPTION, GENETIC; UBIQUITIN-PROTEIN LIGASES; VIRAL PROTEINS;

EID: 69249216590     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00785-09     Document Type: Article

References (65)

1. Arthur, J. L., C. G. Scarpini, V. Connor, R. H. Lachmann, A. M. Tolkovsky, and S. Efstathiou. 2001. Herpes simplex virus type 1 promoter activity during latency establishment, maintenance, and reactivation in primary dorsal root neurons in vitro. J. Virol. 75:3885-3895.
2. Bannister, A. J., P. Zegerman, J. F. Partridge, E. A. Miska, J. O. Thomas, R. C. Allshire, and T. Kouzarides. 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120-124. (Pubitemid 32225848)
3. Barski, A., S. Cuddapah, K. Cui, T. Y. Roh, D. E. Schones, Z. Wang, G. Wei, I. Chepelev, and K. Zhao. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129:823-837. (Pubitemid 46802390)
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. (Pubitemid 36936079)
5. Buschhausen, G., M. Graessmann, and A. Graessmann. 1985. Inhibition of herpes simplex thymidine kinase gene expression by DNA methylation is an indirect effect. Nucleic Acids Res. 13:5503-5513.
6. Cliffe, A. R., and D. M. Knipe. 2008. Herpes simplex virus ICP0 promotes both histone removal and acetylation on viral DNA during lytic infection. J. Virol. 82:12030-12038.
7. Coleman, H. M., V. Connor, Z. S. Cheng, F. Grey, C. M. Preston, and S. Efstathiou. 2008. Histone modifications associated with herpes simplex virus type 1 genomes during quiescence and following ICP0-mediated de-repression. J. Gen. Virol. 89:68-77.
8. Deshmane, S. L., and N. W. Fraser. 1989. During latency, herpes simplex virus type 1 DNA is associated with nucleosomes in a chromatin structure. J. Virol. 63:943-947.
9. Everett, R. D. 2000. ICP0, a regulator of herpes simplex virus during lytic and latent infection. Bioessays 22:761-770. (Pubitemid 30613308)
10. Everett, R. D., W. C. Earnshaw, J. Findlay, and P. Lomonte. 1999. Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110. EMBO J. 18:1526-1538. (Pubitemid 29127066)
11. 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.
12. 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.
13. 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.
14. Grant, P. A., A. Eberharter, S. John, R. G. Cook, B. M. Turner, and J. L. Workman. 1999. Expanded lysine acetylation specificity of Gcn5 in native complexes. J. Biol. Chem. 274:5895-5900.
15. 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.
16. Gu, H., and B. Roizman. 2007. Herpes simplex virus-infected cell protein 0 blocks the silencing of viral DNA by dissociating histone deacetylases from the CoREST REST complex. Proc. Natl. Acad. Sci. USA 104:17134-17139.
17. Gu, H., and B. Roizman. 2003. The degradation of promyelocytic leukemia and Sp100 proteins by herpes simplex virus 1 is mediated by the ubiquitin-conjugating enzyme UbcH5a. Proc. Natl. Acad. Sci. USA 100:8963-8968.
18. Gu, H., and B. Roizman. 2009. Engagement of the lysine-specific demethylase/ HDAC1/CoREST/REST complex by herpes simplex virus 1. J. Virol. 83:4376-4385.
19. Gu, H., and B. Roizman. 2009. The two functions of herpes simplex virus 1 ICP0, inhibition of silencing by the CoREST/REST/HDAC complex and degradation of PML, are executed in tandem. J. Virol. 83:181-187.
20. Herrera, F. J., and S. J. Triezenberg. 2004. VP16-dependent association of chromatin-modifying coactivators and underrepresentation of histones at immediate-early gene promoters during herpes simplex virus infection. J. Virol. 78:9689-9696.
21. Hobbs, W. E., D. E. Brough, I. Kovesdi, and N. A. DeLuca. 2001. Efficient activation of viral genomes by levels of herpes simplex virus ICP0 insufficient to affect cellular gene expression or cell survival. J. Virol. 75:3391-3403.
22. Hobbs, W. E., and N. A. DeLuca. 1999. Perturbation of cell cycle progression and cellular gene expression as a function of herpes simplex virus ICP0. J. Virol. 73:8245-8255.
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. 76:1417-1431.
24. Kent, J. R., P. Y. Zeng, D. Atanasiu, J. Gardner, N. W. Fraser, and S. L. Berger. 2004. During lytic infection herpes simplex virus type 1 is associated with histones bearing modifications that correlate with active transcription. J. Virol. 78:10178-10186.
25. Knipe, D. M., and A. Cliffe. 2008. Chromatin control of herpes simplex virus lytic and latent infection. Nat. Rev. Microbiol. 6:211-221.
26. Koch, C. M., R. M. Andrews, P. Flicek, S. C. Dillon, U. Karaoz, G. K. Clelland, S. Wilcox, D. M. Beare, J. C. Fowler, P. Couttet, K. D. James, G. C. Lefebvre, A. W. Bruce, O. M. Dovey, P. D. Ellis, P. Dhami, C. F. Langford, Z. Weng, E. Birney, N. P. Carter, D. Vetrie, and I. Dunham. 2007. The landscape of histone modifications across 1% of the human genome in five human cell lines. Genome Res. 17:691-707.
27. Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
28. Kubat, N. J., R. K. Tran, P. McAnany, and D. C. Bloom. 2004. Specific histone tail modification and not DNA methylation is a determinant of herpes simplex virus type 1 latent gene expression. J. Virol. 78:1139-1149.
29. Lachner, M., D. O'Carroll, S. Rea, K. Mechtler, and T. Jenuwein. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116-120. (Pubitemid 32225847)
30. Lehming, N., A. Le Saux, J. Schuller, and M. Ptashne. 1998. Chromatin components as part of a putative transcriptional repressing complex. Proc. Natl. Acad. Sci. USA 95:7322-7326.
31. Leinbach, S. S., and W. C. Summers. 1980. The structure of herpes simplex virus type 1 DNA as probed by micrococcal nuclease digestion. J. Gen. Virol. 51:45-59.
32. Lentine, A. F., and S. L. Bachenheimer. 1990. Intracellular organization of herpes simplex virus type 1 DNA assayed by staphylococcal nuclease sensitivity. Virus Res. 16:275-292.
33. Lomberk, G., L. Wallrath, and R. Urrutia. 2006. The heterochromatin protein 1 family. Genome Biol. 7:228.
34. Lomonte, P., K. F. Sullivan, and R. D. Everett. 2001. Degradation of nucleosome-associated centromeric histone H3-like protein CENP-A induced by herpes simplex virus type 1 protein ICP0. J. Biol. Chem. 276:5829-5835.
35. 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. (Pubitemid 38781511)
36. Maul, G. G., and R. D. Everett. 1994. The nuclear location of PML, a cellular member of the C3HC4 zinc-binding domain protein family, is rearranged during herpes simplex virus infection by the C3HC4 viral protein ICP0. J. Gen. Virol. 75:1223-1233.
37. Melroe, G. T., L. Silva, P. A. Schaffer, and D. M. Knipe. 2007. Recruitment of activated IRF-3 and CBP/p300 to herpes simplex virus ICP0 nuclear foci: potential role in blocking IFN-beta induction. Virology 360:305-321.
38. Mossman, K. L., and J. R. Smiley. 1999. Truncation of the C-terminal acidic transcriptional activation domain of herpes simplex virus VP16 renders expression of the immediate-early genes almost entirely dependent on ICP0. J. Virol. 73:9726-9733.
39. Muggeridge, M. I., and N. W. Fraser. 1986. Chromosomal organization of the herpes simplex virus genome during acute infection of the mouse central nervous system. J. Virol. 59:764-767. (Pubitemid 16011145)
40. Nakayama, J., J. C. Rice, B. D. Strahl, C. D. Allis, and S. I. Grewal. 2001. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292:110-113. (Pubitemid 32289138)
41. Neumann, D. M., P. S. Bhattacharjee, N. V. Giordani, D. C. Bloom, and J. M. Hill. 2007. In vivo changes in the patterns of chromatin structure associated with the latent herpes simplex virus type 1 genome in the mouse trigeminal ganglia can be detected at early times after butyrate treatment. J. Virol. 81:13248-13253.
42. Oh, J., and N. W. Fraser. 2008. Temporal association of the herpes simplex virus genome with histone proteins during a lytic infection. J. Virol. 82:3530-3537.
43. Pinnoji, R. C., G. R. Bedadala, B. George, T. C. Holland, J. M. Hill, and S. C. Hsia. 2007. Repressor element-1 silencing transcription factor/neuronal restrictive silencer factor (REST/NRSF) can regulate HSV-1 immediate-early transcription via histone modification. Virol. J. 4:56.
44. Pluta, A. F., W. C. Earnshaw, and I. G. Goldberg. 1998. Interphase-specific association of intrinsic centromere protein CENP-C with HDaxx, a death domain-binding protein implicated in Fas-mediated cell death. J. Cell Sci. 111:2029-2041.
45. Poon, A. P., Y. Liang, and B. Roizman. 2003. Herpes simplex virus 1 gene expression is accelerated by inhibitors of histone deacetylases in rabbit skin cells infected with a mutant carrying a cDNA copy of the infected-cell protein no. 0. J. Virol. 77:12671-12678.
46. Preston, C. M., R. Mabbs, and M. J. Nicholl. 1997. Construction and characterization of herpes simplex virus type 1 mutants with conditional defects in immediate early gene expression. Virology 229:228-239. (Pubitemid 27243506)
47. Preston, C. M., and M. J. Nicholl. 1997. Repression of gene expression upon infection of cells with herpes simplex virus type 1 mutants impaired for immediate-early protein synthesis. J. Virol. 71:7807-7813.
48. Rice, J. C., and C. D. Allis. 2001. Histone methylation versus histone acetylation: new insights into epigenetic regulation. Curr. Opin. Cell Biol. 13: 263-273.
49. Samaniego, L. A., L. Neiderhiser, and N. A. DeLuca. 1998. Persistence and expression of the herpes simplex virus genome in the absence of immediate-early proteins. J. Virol. 72:3307-3320.
50. Samaniego, L. A., N. Wu, and N. A. DeLuca. 1997. The herpes simplex virus immediate-early protein ICP0 affects transcription from the viral genome and infected-cell survival in the absence of ICP4 and ICP27. J. Virol. 71: 4614-4625.
51. Sampath, P., and N. A. Deluca. 2008. Binding of ICP4, TATA-binding protein, and RNA polymerase II to herpes simplex virus type 1 immediate-early, early, and late promoters in virus-infected cells. J. Virol. 82:2339-2349. (Pubitemid 351293534)
52. Shahbazian, M. D., and M. Grunstein. 2007. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76:75-100.
53. Shi, Y., F. Lan, C. Matson, P. Mulligan, J. R. Whetstine, P. A. Cole, R. A. Casero, and Y. Shi. 2004. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941-953. (Pubitemid 40037608)
54. Spivack, J. G., and N. W. Fraser. 1988. Expression of herpes simplex virus type 1 (HSV-1) latency-associated transcripts and transcripts affected by the deletion in avirulent mutant HFEM: evidence for a new class of HSV-1 genes. J. Virol. 62:3281-3287.
55. Spivack, J. G., and N. W. Fraser. 1988. Expression of herpes simplex virus type 1 latency-associated transcripts in the trigeminal ganglia of mice during acute infection and reactivation of latent infection. J. Virol. 62:1479-1485.
56. Stinski, M. F., and T. J. Roehr. 1985. Activation of the major immediate early gene of human cytomegalovirus by cis-acting elements in the promoter-regulatory sequence and by virus-specific trans-acting components. J. Virol. 55:431-441.
57. Stinski, M. F., D. R. Thomsen, R. M. Stenberg, and L. C. Goldstein. 1983. Organization and expression of the immediate early genes of human cyto-megalovirus. J. Virol. 46:1-14.
58. Sullivan, K. F., M. Hechenberger, and K. Masri. 1994. Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J. Cell Biol. 127:581-592.
59. Terry-Allison, T., C. A. Smith, and N. A. DeLuca. 2007. Relaxed repression of herpes simplex virus type 1 genomes in murine trigeminal neurons. J. Virol. 81:12394-12405. (Pubitemid 350085853)
60. Thomsen, D. R., R. M. Stenberg, W. F. Goins, and M. F. Stinski. 1984. Promoter-regulatory region of the major immediate early gene of human cytomegalovirus. Proc. Natl. Acad. Sci. USA 81:659-663.
61. van Leeuwen, H., M. Okuwaki, R. Hong, D. Chakravarti, K. Nagata, and P. O'Hare. 2003. Herpes simplex virus type 1 tegument protein VP22 interacts with TAF-I proteins and inhibits nucleosome assembly but not regulation of histone acetylation by INHAT. J. Gen. Virol. 84:2501-2510.
62. Verdin, E., F. Dequiedt, and H. G. Kasler. 2003. Class II histone deacetylases: versatile regulators. Trends Genet. 19:286-293. (Pubitemid 36507011)
63. Wang, Q. Y., C. Zhou, K. E. Johnson, R. C. Colgrove, D. M. Coen, and D. M. Knipe. 2005. Herpesviral latency-associated transcript gene promotes assembly of heterochromatin on viral lytic-gene promoters in latent infection. Proc. Natl. Acad. Sci. USA 102:16055-16059.
64. Zabierowski, S., and N. A. DeLuca. 2004. Differential cellular requirements for activation of herpes simplex virus type 1 early (tk) and late (gC) promoters by ICP4. J. Virol. 78:6162-6170. (Pubitemid 38715914)
65. Zhang, Y., and C. Jones. 2001. The bovine herpesvirus 1 immediate-early protein (bICP0) associates with histone deacetylase 1 to activate transcription. J. Virol. 75:9571-9578. (Pubitemid 32900091)