An Essential Viral Transcription Activator Modulates Chromatin Dynamics

PLoS Pathogens

Volumn 12, Issue 8, 2016, Pages

  Gibeault, Rebecca L ^a   Conn, Kristen L ^a   Bildersheim, Michael D ^a   Schang, Luis M ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2B; HISTONE H4; VIRUS DNA; CHROMATIN; HERPES SIMPLEX VIRUS, TYPE 1 PROTEIN ICP4; HISTONE; IMMEDIATE EARLY PROTEIN;

ANIMAL CELL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE SILENCING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HERPES SIMPLEX VIRUS 1; HISTONE MODIFICATION; IMMUNOFLUORESCENCE TEST; NONHUMAN; NUCLEOSOME; TRANSCRIPTION REGULATION; TRANSIENT EXPRESSION; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS REPLICATION; ANIMAL; CELL LINE; CHLOROCEBUS AETHIOPS; CHROMATIN; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; HERPES SIMPLEX; HUMAN; METABOLISM; PATHOGENICITY; VERO CELL LINE; VIROLOGY;

ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; CHROMATIN; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, VIRAL; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HISTONES; HUMANS; IMMEDIATE-EARLY PROTEINS; TRANSCRIPTION, GENETIC; TRANSFECTION; VERO CELLS; VIRUS REPLICATION;

EID: 84984782759     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005842     Document Type: Article

References (76)

1. Herrera FJ, Triezenberg SJ, VP16-dependent association of chromatin-modifying coactivators and underrepresentation of histones at immediate-early gene promoters during herpes simplex virus infection. J Virol. 2004;78:9689–9696. 15331701
2. Hill JM, Quenelle DC, Cardin RD, et al. Inhibition of LSD1 reduces herpesvirus infection, shedding, and recurrence by promoting epigenetic suppression of viral genomes. Sci Transl Med. 2014;6:265ra169. doi: 10.1126/scitranslmed.301064325473037
3. Liang Y, Vogel JL, Narayanan A, Peng H, Kristie TM, Inhibition of the histone demethylase LSD1 blocks alpha-herpesvirus lytic replication and reactivation from latency. Nat Med. 2009;15:1312–1317. doi: 10.1038/nm.205119855399
4. Liang Y, Quenelle D, Vogel JL, Mascaro C, Ortega A, Kristie TM, A novel selective LSD1/KDM1A inhibitor epigenetically blocks herpes simplex virus lytic replication and reactivation from latency. MBio. 2013;4:e00558–12. doi: 10.1128/mBio.00558-1223386436
5. Memedula S, Belmont AS, Sequential recruitment of HAT and SWI/SNF components to condensed chromatin by VP16. Curr Biol. 2003;13:241–246. 12573221
6. Everett RD, Trans activation of transcription by herpes virus products: requirement for two HSV-1 immediate-early polypeptides for maximum activity. EMBO J. 1984;3:3135–3141. 6098466
7. apRhys CM, Ciufo DM, O’Neill EA, Kelly TJ, Hayward GS, Overlapping octamer and TAATGARAT motifs in the VF65-response elements in herpes simplex virus immediate-early promoters represent independent binding sites for cellular nuclear factor III. J Virol. 1989;63:2798–2812. 2542590
8. Gerster T, Roeder RG, A herpesvirus trans-activating protein interacts with transcription factor OTF-1 and other cellular proteins. Proc Natl Acad Sci U S A. 1988;85:6347–6351. 2842768
9. Kristie TM, Roizman B, Host cell proteins bind to the cis-acting site required for virion-mediated induction of herpes simplex virus 1 alpha genes. Proc Natl Acad Sci U S A. 1987;84:71–75. 3025864
10. Narayanan A, Ruyechan WT, Kristie TM, The coactivator host cell factor-1 mediates Set1 and MLL1 H3K4 trimethylation at herpesvirus immediate early promoters for initiation of infection. Proc Natl Acad Sci U S A. 2007;104:10835–10840. 17578910
11. Xiao P, Capone JP, A cellular factor binds to the herpes simplex virus type 1 transactivator Vmw65 and is required for Vmw65-dependent protein-DNA complex assembly with Oct-1. Mol Cell Biol. 1990;10:4974–4977. 2167442
12. Zhou G, Te D, Roizman B, The CoREST/REST repressor is both necessary and inimical for expression of herpes simplex virus genes. MBio. 2011;2:e00313–10.
13. Resnick J, Boyd BA, Haffey ML, DNA binding by the herpes simplex virus type 1 ICP4 protein is necessary for efficient down regulation of the ICP0 promoter. J Virol. 1989;63:2497–2503. 2542567
14. Shepard AA, DeLuca NA, A second-site revertant of a defective herpes simplex virus ICP4 protein with restored regulatory activities and impaired DNA-binding properties. J Virol. 1991;65:787–795. 1846199
15. Wagner LM, DeLuca NA, Temporal association of herpes simplex virus ICP4 with cellular complexes functioning at multiple steps in PolII transcription. PLoS One. 2013;8:e78242. doi: 10.1371/journal.pone.007824224147125
16. Kalamvoki M, Roizman B, The histone acetyltransferase CLOCK is an essential component of the herpes simplex virus 1 transcriptome that includes TFIID, ICP4, ICP27, and ICP22. J Virol. 2011;85:9472–9477. doi: 10.1128/JVI.00876-1121734043
17. Lacasse JJ, Schang LM, During lytic infections, herpes simplex virus type 1 DNA is in complexes with the properties of unstable nucleosomes. J Virol. 2010;84:1920–1933. doi: 10.1128/JVI.01934-0920007274
18. Kimura H, Cook PR, Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J Cell Biol. 2001;153:1341–1353. 11425866
19. Lever MA, Th’ng JP, Sun X, Hendzel MJ, Rapid exchange of histone H1.1 on chromatin in living human cells. Nature. 2000;408:873–876. 11130728
20. Misteli T, Gunjan A, Hock R, Bustin M, Brown DT, Dynamic binding of histone H1 to chromatin in living cells. Nature. 2000;408:877–881. 11130729
21. Aygün O, Mehta S, Grewal SI, HDAC-mediated suppression of histone turnover promotes epigenetic stability of heterochromatin. Nat Struct Mol Biol. 2013;20:547–554. doi: 10.1038/nsmb.256523604080
22. Hieb AR, Gansen A, Böhm V, Langowski J, The conformational state of the nucleosome entry-exit site modulates TATA box-specific TBP binding. Nucleic Acids Res. 2014;42:7561–7576. doi: 10.1093/nar/gku42324829456
23. Kim J, Lee J, Lee TH, Lysine Acetylation Facilitates Spontaneous DNA Dynamics in the Nucleosome. J Phys Chem B. 2015;119:15001–15005. doi: 10.1021/acs.jpcb.5b0973426575591
24. Kuo MH, Brownell JE, Sobel RE, et al. Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines. Nature. 1996;383:269–272. 8805705
25. Daujat S, Weiss T, Mohn F, et al. H3K64 trimethylation marks heterochromatin and is dynamically remodeled during developmental reprogramming. Nat Struct Mol Biol. 2009;16:777–781. doi: 10.1038/nsmb.162919561610
26. Jack AP, Bussemer S, Hahn M, et al. H3K56me3 is a novel, conserved heterochromatic mark that largely but not completely overlaps with H3K9me3 in both regulation and localization. PLoS One. 2013;8:e51765. doi: 10.1371/journal.pone.005176523451023
27. Litt MD, Simpson M, Gaszner M, Allis CD, Felsenfeld G, Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus. Science. 2001;293:2453–2455. 11498546
28. Santos-Rosa H, Schneider R, Bannister AJ, et al. Active genes are tri-methylated at K4 of histone H3. Nature. 2002;419:407–411. 12353038
29. Zheng Y, Tipton JD, Thomas PM, Kelleher NL, Sweet SM, Site-specific human histone H3 methylation stability: fast K4me3 turnover. Proteomics. 2014;14:2190–2199. doi: 10.1002/pmic.20140006024826939
30. Jin C, Felsenfeld G, Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev. 2007;21:1519–1529. 17575053
31. Ahmad K, Henikoff S, The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell. 2002;9:1191–1200. 12086617
32. Elsässer SJ, Huang H, Lewis PW, Chin JW, Allis CD, Patel DJ, DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature. 2012;491:560–565. doi: 10.1038/nature1160823075851
33. Goldberg AD, Banaszynski LA, Noh KM, et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell. 2010;140:678–691. doi: 10.1016/j.cell.2010.01.00320211137
34. Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD, Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc Natl Acad Sci U S A. 2010;107:14075–14080. doi: 10.1073/pnas.100885010720651253
35. Ray-Gallet D, Quivy JP, Scamps C, Martini EM, Lipinski M, Almouzni G, HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol Cell. 2002;9:1091–1100. 12049744
36. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y, Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell. 2004;116:51–61. 14718166
37. McKittrick E, Gafken PR, Ahmad K, Henikoff S, Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc Natl Acad Sci U S A. 2004;101:1525–1530. 14732680
38. Conn KL, Hendzel MJ, Schang LM, Linker histones are mobilized during infection with herpes simplex virus type 1. J Virol. 2008;82:8629–8646. doi: 10.1128/JVI.00616-0818579611
39. Conn KL, Hendzel MJ, Schang LM, Core histones H2B and H4 are mobilized during infection with herpes simplex virus 1. J Virol. 2011;85:13234–13252. doi: 10.1128/JVI.06038-1121994445
40. Conn KL, Hendzel MJ, Schang LM, The differential mobilization of histones H3.1 and H3.3 by herpes simplex virus 1 relates histone dynamics to the assembly of viral chromatin. PLoS Pathog. 2013;9:e1003695. doi: 10.1371/journal.ppat.100369524130491
41. DeLuca NA, Schaffer PA, Physical and functional domains of the herpes simplex virus transcriptional regulatory protein ICP4. J Virol. 1988;62:732–743. 2828668
42. Th’ng JP, Sung R, Ye M, Hendzel MJ, H1 family histones in the nucleus. Control of binding and localization by the C-terminal domain. J Biol Chem. 2005;280:27809–27814. 15911621
43. Mossman KL, Smiley JR, 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. 1999;73:9726–9733. 10559282
44. Smith CA, Schaffer PA, Mutants defective in herpes simplex virus type 2 ICP4: isolation and preliminary characterization. J Virol. 1987;61:1092–1097. 3029403
45. Placek BJ, Huang J, Kent JR, et al. The histone variant H3.3 regulates gene expression during lytic infection with herpes simplex virus type 1. J Virol. 2009;83:1416–1421. doi: 10.1128/JVI.01276-0819004946
46. Conn KL, Schang LM, Chromatin dynamics during lytic infection with herpes simplex virus 1. Viruses. 2013;5:1758–1786. doi: 10.3390/v507175823863878
47. Knipe DM, Nuclear sensing of viral DNA, epigenetic regulation of herpes simplex virus infection, and innate immunity. Virology. 2015;479–480:153–159. doi: 10.1016/j.virol.2015.02.00925742715
48. Kristie TM, Dynamic modulation of HSV chromatin drives initiation of infection and provides targets for epigenetic therapies. Virology. 2015;479–480:555–561. doi: 10.1016/j.virol.2015.01.02625702087
49. Bloom DC, Giordani NV, Kwiatkowski DL, Epigenetic regulation of latent HSV-1 gene expression. Biochim Biophys Acta. 2010;1799:246–256. doi: 10.1016/j.bbagrm.2009.12.00120045093
50. Knipe DM, Lieberman PM, Jung JU, et al. Snapshots: chromatin control of viral infection. Virology. 2013;435:141–156. doi: 10.1016/j.virol.2012.09.02323217624
51. Lieberman PM, Keeping it quiet: chromatin control of gammaherpesvirus latency. Nat Rev Microbiol. 2013;11:863–875. doi: 10.1038/nrmicro313524192651
52. Lu X, Triezenberg SJ, Chromatin assembly on herpes simplex virus genomes during lytic infection. Biochim Biophys Acta. 2010;1799:217–222. doi: 10.1016/j.bbagrm.2009.08.00419682614
53. Roizman B, The checkpoints of viral gene expression in productive and latent infection: the role of the HDAC/CoREST/LSD1/REST repressor complex. J Virol. 2011;85:7474–7482. doi: 10.1128/JVI.00180-1121450817
54. Almer A, Rudolph H, Hinnen A, Hörz W, Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J. 1986;5:2689–2696. 3536481
55. Dion MF, Kaplan T, Kim M, Buratowski S, Friedman N, Rando OJ, Dynamics of replication-independent histone turnover in budding yeast. Science. 2007;315:1405–1408. 17347438
56. Mao C, Brown CR, Griesenbeck J, Boeger H, Occlusion of regulatory sequences by promoter nucleosomes in vivo. PLoS One. 2011;6:e17521. doi: 10.1371/journal.pone.001752121408617
57. Ferenczy MW, DeLuca NA, Epigenetic modulation of gene expression from quiescent herpes simplex virus genomes. J Virol. 2009;83:8514–8524. doi: 10.1128/JVI.00785-0919535445
58. Cliffe AR, Knipe DM, Herpes simplex virus ICP0 promotes both histone removal and acetylation on viral DNA during lytic infection. J Virol. 2008;82:12030–12038. doi: 10.1128/JVI.01575-0818842720
59. Monier K, Armas JC, Etteldorf S, Ghazal P, Sullivan KF, Annexation of the interchromosomal space during viral infection. Nat Cell Biol. 2000;2:661–665. 10980708
60. Tolstorukov MY, Goldman JA, Gilbert C, Ogryzko V, Kingston RE, Park PJ, Histone variant H2A.Bbd is associated with active transcription and mRNA processing in human cells. Mol Cell. 2012;47:596–607. doi: 10.1016/j.molcel.2012.06.01122795134
61. Bowerman S, Wereszczynski J, Effects of MacroH2A and H2A.Z on Nucleosome Dynamics as Elucidated by Molecular Dynamics Simulations. Biophys J. 2016;110:327–337. doi: 10.1016/j.bpj.2015.12.01526789756
62. Chakravarthy S, Luger K, The histone variant macro-H2A preferentially forms “hybrid nucleosomes”. J Biol Chem. 2006;281:25522–25531. 16803903
63. Zalckvar E, Paulus C, Tillo D, et al. Nucleosome maps of the human cytomegalovirus genome reveal a temporal switch in chromatin organization linked to a major IE protein. Proc Natl Acad Sci U S A. 2013;110:13126–13131. doi: 10.1073/pnas.130554811023878222
64. Tsai K, Chan L, Gibeault R, et al. Viral reprogramming of the Daxx histone H3.3 chaperone during early Epstein-Barr virus infection. J Virol. 2014;88:14350–14363. doi: 10.1128/JVI.01895-1425275136
65. Dyson PJ, Farrell PJ, Chromatin structure of Epstein-Barr virus. J Gen Virol. 1985;66:1931–1940. 2993484
66. Muggeridge MI, Fraser NW, Chromosomal organization of the herpes simplex virus genome during acute infection of the mouse central nervous system. J Virol. 1986;59:764–767. 3016340
67. Nitzsche A, Paulus C, Nevels M, Temporal dynamics of cytomegalovirus chromatin assembly in productively infected human cells. J Virol. 2008;82:11167–11180. doi: 10.1128/JVI.01218-0818786996
68. Coleman HM, Connor V, Cheng ZS, Grey F, Preston CM, Efstathiou S, Histone modifications associated with herpes simplex virus type 1 genomes during quiescence and following ICP0-mediated de-repression. J Gen Virol. 2008;89:68–77. 18089730
69. Murata T, Kondo Y, Sugimoto A, et al. Epigenetic histone modification of Epstein-Barr virus BZLF1 promoter during latency and reactivation in Raji cells. J Virol. 2012;86:4752–4761. doi: 10.1128/JVI.06768-1122357272
70. Nitzsche A, Steinhäusser C, Mücke K, Paulus C, Nevels M, Histone H3 lysine 4 methylation marks postreplicative human cytomegalovirus chromatin. J Virol. 2012;86:9817–9827. doi: 10.1128/JVI.00581-1222761369
71. Arvey A, Tempera I, Lieberman PM, Interpreting the Epstein-Barr Virus (EBV) epigenome using high-throughput data. Viruses. 2013;5:1042–1054. doi: 10.3390/v504104223549386
72. Oh J, Sanders IF, Chen EZ, et al. Genome wide nucleosome mapping for HSV-1 shows nucleosomes are deposited at preferred positions during lytic infection. PLoS One. 2015;10:e0117471. doi: 10.1371/journal.pone.011747125710170
73. Costanzo F, Campadelli-Fiume G, Foa-Tomasi L, Cassai E, Evidence that herpes simplex virus DNA is transcribed by cellular RNA polymerase B. J Virol. 1977;21:996–1001. 191658
74. Abrisch RG, Eidem TM, Yakovchuk P, Kugel JF, Goodrich JA, Infection by Herpes Simplex Virus 1 Causes Near-Complete Loss of RNA Polymerase II Occupancy on the Host Cell Genome. J Virol. 2016;90:2503–2513.
75. Smith KO, Relationship between the envelope and the infectivity of herpes simplex virus. Proc Soc Exp Biol Med. 1964;115:814–816. 14155835
76. DeLuca NA, Schaffer PA, Activation of immediate-early, early, and late promoters by temperature-sensitive and wild-type forms of herpes simplex virus type 1 protein ICP4. Mol Cell Biol. 1985;5:1997–2008. 3018543