Regulation of histone deposition on the herpes simplex virus type 1 genome during lytic infection

Journal of Virology

Volumn 83, Issue 11, 2009, Pages 5835-5845

  Kutluay, Sebla B ^a,c   Triezenberg, Steven J ^a,b,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c VAN ANDEL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOHEXIMIDE; ETOPOSIDE; HISTONE; RNA POLYMERASE II; IMMEDIATE EARLY PROTEIN; TRANSACTIVATOR PROTEIN;

ARTICLE; CONTROLLED STUDY; GENE DELETION; GENETIC TRANSCRIPTION; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 2; HUMAN; HUMAN CELL; IMMEDIATE EARLY GENE; INFECTION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SUPERINFECTION; VIRUS GENOME; VIRUS TRANSCRIPTION; GENETICS; HELA CELL; METABOLISM;

HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 2;

GENOME, VIRAL; HELA CELLS; HERPES SIMPLEX VIRUS PROTEIN VMW65; HERPESVIRUS 1, HUMAN; HERPESVIRUS 2, HUMAN; HISTONES; HUMANS; IMMEDIATE-EARLY PROTEINS; RNA POLYMERASE II; TRANSCRIPTION, GENETIC;

EID: 66149148358     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00219-09     Document Type: Article

References (69)

1. Amelio, A. L., N. V. Giordani, N. J. Kubat, J. E. O'Neil, and D. C. Bloom. 2006. Deacetylation of the herpes simplex virus type 1 latency-associated transcript (LAT) enhancer and a decrease in LAT abundance precede an increase in ICP0 transcriptional permissiveness at early times postexplant. J. Virol. 80:2063-2068. (Pubitemid 43228747)
2. Belotserkovskaya, R., S. Oh, V. A. Bondarenko, G. Orphanides, V. M. Studitsky, and D. Reinberg. 2003. FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090-1093. (Pubitemid 37022309)
3. Black, J. C., J. E. Choi, S. R. Lombardo, and M. Carey. 2006. A mechanism for coordinating chromatin modification and preinitiation complex assembly. Mol. Cell 23:809-818.
4. Boeger, H., J. Griesenbeck, J. S. Strattan, and R. D. Kornberg. 2003. Nucleosomes unfold completely at a transcriptionally active promoter. Mol. Cell 11:1587-1598.
5. Campbell, M. E., J. W. Palfreyman, and C. M. Preston. 1984. Identification of herpes simplex virus DNA sequences which encode a trans-acting polypeptide responsible for stimulation of immediate early transcription. J. Mol. Biol. 180:1-19. (Pubitemid 16223340)
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. Cohen, G. H., M. Ponce de Leon, H. Diggelmann, W. C. Lawrence, S. K. Vernon, and R. J. Eisenberg. 1980. Structural analysis of the capsid polypeptides of herpes simplex virus types 1 and 2. J. Virol. 34:521-531. (Pubitemid 10104055)
8. 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.
9. Cress, A., and S. J. Triezenberg. 1991. Nucleotide and deduced amino acid sequences of the gene encoding virion protein 16 of herpes simplex virus type 2. Gene 103:235-238.
10. 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. (Pubitemid 19057265)
11. Flaus, A., and T. Owen-Hughes. 2004. Mechanisms for ATP-dependent chromatin remodelling: farewell to the tuna-can octamer? Curr. Opin. Genet. Dev. 14:165-173. (Pubitemid 38520144)
12. Gibson, W., and B. Roizman. 1971. Compartmentalization of spermine and spermidine in the herpes simplex virion. Proc. Natl. Acad. Sci. USA 68:2818-2821.
13. Goodrich, J. A., T. Hoey, C. J. Thut, A. Admon, and R. Tjian. 1993. Drosophila TAFII40 interacts with both a VP16 activation domain and the basal transcription factor TFIIB. Cell 75:519-530. (Pubitemid 2009844)
14. 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.
15. 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. (Pubitemid 350211004)
16. Gutierrez, J. L., M. Chandy, M. J. Carrozza, and J. L. Workman. 2007. Activation domains drive nucleosome eviction by SWI/SNF. EMBO J. 26:730-740. (Pubitemid 46253835)
17. Hardy, S., M. Brand, G. Mittler, J. Yanagisawa, S. Kato, M. Meisterernst, and L. Tora. 2002. TATA-binding protein-free TAF-containing complex (TFTC) and p300 are both required for efficient transcriptional activation. J. Biol. Chem. 277:32875-32882. (Pubitemid 34984800)
18. Haushalter, K. A., and J. T. Kadonaga. 2003. Chromatin assembly by DNA-translocating motors. Nat. Rev. Mol. Cell Biol. 4:613-620. (Pubitemid 36934963)
19. Henikoff, S. 2008. Nucleosome destabilization in the epigenetic regulation of gene expression. Nat. Rev. Genet. 9:15-26. (Pubitemid 350277297)
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. (Pubitemid 39187086)
21. Huang, J., J. R. Kent, B. Placek, K. A. Whelan, C. M. Hollow, P. Y. Zeng, N. W. Fraser, and S. L. Berger. 2006. Trimethylation of histone H3 lysine 4 by Set1 in the lytic infection of human herpes simplex virus 1. J. Virol. 80:5740-5746. (Pubitemid 43849152)
22. Ikeda, K., D. J. Steger, A. Eberharter, and J. L. Workman. 1999. Activation domain-specific and general transcription stimulation by native histone acetyltransferase complexes. Mol. Cell. Biol. 19:855-863. (Pubitemid 29018486)
23. Ingles, C. J., M. Shales, W. D. Cress, S. J. Triezenberg, and J. Greenblatt. 1991. Reduced binding of TFIID to transcriptionally compromised mutants of VP16. Nature 351:588-590. (Pubitemid 21896648)
24. Ito, T., T. Ikehara, T. Nakagawa, W. L. Kraus, and M. Muramatsu. 2000. p300-mediated acetylation facilitates the transfer of histone H2A-H2B dimers from nucleosomes to a histone chaperone. Genes Dev. 14:1899-1907. (Pubitemid 30639523)
25. Kaplan, C. D., L. Laprade, and F. Winston. 2003. Transcription elongation factors repress transcription initiation from cryptic sites. Science 301:1096-1099. (Pubitemid 37022311)
26. 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. (Pubitemid 39187135)
27. Klemm, R. D., J. A. Goodrich, S. Zhou, and R. Tjian. 1995. Molecular cloning and expression of the 32-kDa subunit of human TFIID reveals interactions with VP16 and TFIIB that mediate transcriptional activation. Proc. Natl. Acad. Sci. USA 92:5788-5792.
28. Knipe, D. M., and A. Cliffe. 2008. Chromatin control of herpes simplex virus lytic and latent infection. Nat. Rev. Microbiol. 6:211-221.
29. Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128:693-705. (Pubitemid 46273577)
30. Kristjuhan, A., and J. Q. Svejstrup. 2004. Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo. EMBO J. 23:4243-4252. (Pubitemid 39546162)
31. Kubat, N. J., A. L. Amelio, N. V. Giordani, and D. C. Bloom. 2004. The herpes simplex virus type 1 latency-associated transcript (LAT) enhancer/rcr is hyperacetylated during latency independently of LAT transcription. J. Virol. 78:12508-12518. (Pubitemid 39458769)
32. 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. (Pubitemid 38095824)
33. Kulaeva, O. I., D. A. Gaykalova, and V. M. Studitsky. 2007. Transcription through chromatin by RNA polymerase II: histone displacement and exchange. Mutat. Res. 618:116-129. (Pubitemid 46574746)
34. Kundu, T. K., V. B. Palhan, Z. Wang, W. An, P. A. Cole, and R. G. Roeder. 2000. Activator-dependent transcription from chromatin in vitro involving targeted histone acetylation by p300. Mol. Cell 6:551-561.
35. Kutluay, S. B., J. Doroghazi, M. E. Roemer, and S. J. Triezenberg. 2008. Curcumin inhibits herpes simplex virus immediate-early gene expression by a mechanism independent of p300/CBP histone acetyltransferase activity. Virology 373:239-247.
36. Kutluay, S. B., S. L. DeVos, J. E. Klomp, and S. J. Triezenberg. 2009. Transcriptional coactivators are not required for herpes simplex virus type 1 immediate-early gene expression in vitro. J. Virol. 83:3436-3449.
37. Larschan, E., and F. Winston. 2001. The S. cerevisiae SAGA complex functions in vivo as a coactivator for transcriptional activation by Gal4. Genes Dev. 15:1946-1956. (Pubitemid 32738624)
38. Lee, C. K., Y. Shibata, B. Rao, B. D. Strahl, and J. D. Lieb. 2004. Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat. Genet. 36:900-905. (Pubitemid 39014111)
39. 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. (Pubitemid 11182549)
40. 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. (Pubitemid 20223299)
41. Li, B., M. Carey, and J. L. Workman. 2007. The role of chromatin during transcription. Cell 128:707-719. (Pubitemid 46273570)
42. Lin, Y. S., I. Ha, E. Maldonado, D. Reinberg, and M. R. Green. 1991. Binding of general transcription factor TFIIB to an acidic activating region. Nature 353:569-571. (Pubitemid 21912558)
43. Memedula, S., and A. S. Belmont. 2003. Sequential recruitment of HAT and SWI/SNF components to condensed chromatin by VP16. Curr. Biol. 13:241-246. (Pubitemid 36178303)
44. Mito, Y., J. G. Henikoff, and S. Henikoff. 2005. Genome-scale profiling of histone H3.3 replacement patterns. Nat. Genet. 37:1090-1097. (Pubitemid 41486661)
45. Morillon, A. 2006. Is histone loss a common feature of DNA metabolism regulation? Biochem. Cell Biol. 84:450-462. (Pubitemid 44703650)
46. 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)
47. Neely, K. E., A. H. Hassan, C. E. Brown, L. Howe, and J. L. Workman. 2002. Transcription activator interactions with multiple SWI/SNF subunits. Mol. Cell. Biol. 22:1615-1625. (Pubitemid 34176809)
48. Neely, K. E., A. H. Hassan, A. E. Wallberg, D. J. Steger, B. R. Cairns, A. P. Wright, and J. L. Workman. 1999. Activation domain-mediated targeting of the SWI/SNF complex to promoters stimulates transcription from nucleosome arrays. Mol. Cell 4:649-655.
49. 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 mouse trigeminal ganglia can be detected at early times after butyrate treatment. J. Virol. 81:13248-13253.
50. 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.
51. Ottosen, S., F. J. Herrera, J. R. Doroghazi, A. Hull, S. Mittal, W. S. Lane, and S. J. Triezenberg. 2006. Phosphorylation of the VP16 transcriptional activator protein during herpes simplex virus infection and mutational analysis of putative phosphorylation sites. Virology 345:468-481. (Pubitemid 43189905)
52. Pichyangkura, R. 1995. The effect of deletion mutations of the activation domain of VP16 upon herpes simplex virus type 1 lytic infection. Ph.D. dissertation. Michigan State University, East Lansing.
53. Pignatti, P. F., and E. Cassai. 1980. Analysis of herpes simplex virus nucleoprotein complexes extracted from infected cells. J. Virol. 36:816-828. (Pubitemid 11194321)
54. Placek, B. J., J. Huang, J. R. Kent, J. Dorsey, L. Rice, N. W. Fraser, and S. L. Berger. 2009. The histone variant H3.3 regulates gene expression during lytic infection with herpes simplex virus type 1. J. Virol. 83:1416-1421.
55. Reinke, H., and W. Horz. 2003. Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol. Cell 11:1599-1607.
56. Saha, A., J. Wittmeyer, and B. R. Cairns. 2006. Chromatin remodelling: the industrial revolution of DNA around histones. Nat. Rev. Mol. Cell Biol. 7:437-447. (Pubitemid 44050097)
57. Sarma, K., and D. Reinberg. 2005. Histone variants meet their match. Nat. Rev. Mol. Cell Biol. 6:139-149. (Pubitemid 40215809)
58. Schwabish, M. A., and K. Struhl. 2004. Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 24:10111-10117. (Pubitemid 39507851)
59. Stafford, G. A., and R. H. Morse. 2001. GCN5 dependence of chromatin remodeling and transcriptional activation by the GAL4 and VP16 activation domains in budding yeast. Mol. Cell. Biol. 21:4568-4578. (Pubitemid 32588240)
60. Tal-Singer, R., R. Pichyangkura, E. Chung, T. M. Lasner, B. P. Randazzo, J. Q. Trojanowski, N. W. Fraser, and S. J. Triezenberg. 1999. The transcriptional activation domain of VP16 is required for efficient infection and establishment of latency by HSV-1 in the murine peripheral and central nervous systems. Virology 259:20-33. (Pubitemid 29391752)
61. Triezenberg, S. J., R. C. Kingsbury, and S. L. McKnight. 1988. Functional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression. Genes Dev. 2:718-729.
62. Uhlmann, T., S. Boeing, M. Lehmbacher, and M. Meisterernst. 2007. The VP16 activation domain establishes an active mediator lacking CDK8 in vivo. J. Biol. Chem. 282:2163-2173. (Pubitemid 47076741)
63. Utley, R. T., K. Ikeda, P. A. Grant, J. Cote, D. J. Steger, A. Eberharter, S. John, and J. L. Workman. 1998. Transcriptional activators direct histone acetyltransferase complexes to nucleosomes. Nature 394:498-502. (Pubitemid 28373963)
64. 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. (Pubitemid 37063140)
65. Wang, L., S. R. Grossman, and E. Kieff. 2000. Epstein-Barr virus nuclear protein 2 interacts with p300, CBP, and PCAF histone acetyltransferases in activation of the LMP1 promoter. Proc. Natl. Acad. Sci. USA 97:430-435.
66. 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. (Pubitemid 41552866)
67. Wysocka, J., and W. Herr. 2003. The herpes simplex virus VP16-induced complex: the makings of a regulatory switch. Trends Biochem. Sci. 28:294-304. (Pubitemid 36776292)
68. Xiao, H., A. Pearson, B. Coulombe, R. Truant, S. Zhang, J. L. Regier, S. J. Triezenberg, D. Reinberg, O. Flores, C. J. Ingles, et al. 1994. Binding of basal transcription factor TFIIH to the acidic activation domains of VP16 and p53. Mol. Cell. Biol. 14:7013-7024. (Pubitemid 24299770)
69. Ye, X., B. Zerlanko, R. Zhang, N. Somaiah, M. Lipinski, P. Salomoni, and P. D. Adams. 2007. Definition of pRB- and p53-dependent and -independent steps in HIRA/ASF1a-mediated formation of senescence-associated heterochromatin foci. Mol. Cell. Biol. 27:2452-2465. (Pubitemid 46581338)