Epigenetic repression of herpes simplex virus infection by the nucleosome remodeler CHD3

mBio

Volumn 5, Issue 1, 2014, Pages

  Arbuckle, Jesse H ^a   Kristie, Thomas M ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMODOMAIN HELICASE DNA BINDING PROTEIN; DNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; CONTROLLED STUDY; EPIGENETIC REPRESSION; FIBROBLAST; GENE EXPRESSION; HELA CELL; HERPES SIMPLEX; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; IMMEDIATE EARLY GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS GENOME; WESTERN BLOTTING;

CELL LINE; DNA HELICASES; EPIGENETIC REPRESSION; GENE EXPRESSION REGULATION, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; SIMPLEXVIRUS; VIRUS REPLICATION;

EID: 84903365431     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01027-13     Document Type: Article

References (52)

1. Roizman B, Knipe DM, Whitley RJ. 2013. Herpes simplex viruses. In Knipe DM, Howley PM (ed), Fields virology, 6th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Whitley R, Kimberlin DW, Prober CG. 2007. Pathogenesis and disease. In Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K (ed), Human herpesviruses biology, therapy, and immunoprophylaxis. Cambridge University Press, New York, NY.
3. Kristie TM. 2007. Early events pre-initiation of alphaherpesvirus viral gene expression, p 112-127. In Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K (ed), Human herpesviruses biology, therapy, and immunoprophylaxis. Cambridge University Press, New York, NY.
4. Bryant KF, Colgrove RC, Knipe DM. 2011. Cellular SNF2H chromatinremodeling factor promotes herpes simplex virus 1 immediate-early gene expression and replication. mBio 2(1):e00330-00310. http://dx.doi.org/ 10.1128/mBio.00330-10.
5. Cliffe AR, Knipe DM. 2008. Herpes simplex virus ICP0 promotes both histone removal and acetylation on viral DNA during lytic infection. J. Virol. 82:12030-12038.
6. Conn KL, Schang LM. 2013. Chromatin dynamics during lytic infection with herpes simplex virus 1. Viruses 5:1758-1786.
7. Gu H, Liang Y, Mandel G, Roizman B. 2005. Components of the REST/CoREST/histone deacetylase repressor complex are disrupted, modified, and translocated in HSV-1-infected cells. Proc. Natl. Acad. Sci. U. S. A. 102:7571-7576.
8. Gu H, Roizman B. 2007. Herpes simplex virus-infected cell protein 0 blocks the silencing of viralDNAby dissociating histone deacetylases from the CoREST-REST complex. Proc. Natl. Acad. Sci. U. S. A. 104: 17134-17139.
9. Huang J, Kent JR, Placek B, Whelan KA, Hollow CM, Zeng PY, Fraser NW, Berger SL. 2006. Trimethylation of histone H3 lysine 4 by Set1 in the lytic infection of human herpes simplex virus 1. J. Virol. 80:5740-5746.
10. Kalamvoki M, Roizman B. 2010. Circadian CLOCK histone acetyl transferase localizes at ND10 nuclear bodies and enables herpes simplex virus gene expression. Proc. Natl. Acad. Sci. U. S. A. 107:17721-17726.
11. Kent JR, Zeng PY, Atanasiu D, Gardner J, Fraser NW, Berger SL. 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.
12. Knipe DM, Cliffe A. 2008. Chromatin control of herpes simplex virus lytic and latent infection. Nat. Rev. Microbiol. 6:211-221.
13. Kristie TM, Liang Y, Vogel JL. 2010. Control of alpha-herpesvirus IE gene expression by HCF-1 coupled chromatin modification activities. Biochim. Biophys. Acta 1799:257-265.
14. Lacasse JJ, Schang LM. 2010. During lytic infections, herpes simplex virus type 1 DNA is in complexes with the properties of unstable nucleosomes. J. Virol. 84:1920-1933.
15. Lacasse JJ, Schang LM. 2012. Herpes simplex virus 1 DNA is in unstable nucleosomes throughout the lytic infection cycle, and the instability of the nucleosomes is independent of DNA replication. J. Virol. 86: 11287-11300.
16. Liang Y, Vogel JL, Arbuckle JH, Rai G, Jadhav A, Simeonov A, Maloney DJ, Kristie TM. 2013. Targeting the JMJD2 histone demethylases to epigenetically control herpesvirus infection and reactivation from latency. Sci. Transl. Med. 5: 167ra165.
17. Liang Y, Vogel JL, Narayanan A, Peng H, Kristie TM. 2009. Inhibition of the histone demethylase LSD1 blocks alpha-herpesvirus lytic replication and reactivation from latency. Nat. Med. 15:1312-1317.
18. Narayanan A, Ruyechan WT, Kristie TM. 2007. 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. 104:10835-10840.
19. Peng H, Nogueira ML, Vogel JL, Kristie TM. 2010. Transcriptional coactivator HCF-1 couples the histone chaperone Asf1b to HSV-1 DNA replication components. Proc. Natl. Acad. Sci. U. S. A. 107:2461-2466.
20. Poon AP, Gu H, Roizman B. 2006. ICP0 and the US3 protein kinase of herpes simplex virus 1 independently block histone deacetylation to enable gene expression. Proc. Natl. Acad. Sci. U. S. A. 103:9993-9998.
21. Silva L, Cliffe A, Chang L, Knipe DM. 2008. Role for A-type lamins in herpesviral DNA targeting and heterochromatin modulation. PLoS Pathog. 4:e1000071. http://dx.doi.org/10.1371/journal.ppat.1000071.
22. Pignatti PF, Cassai E. 1980. Analysis of herpes simplex virus nucleoprotein complexes extracted from infected cells. J. Virol. 36:816-828.
23. Amelio AL, Giordani NV, Kubat NJ, O'Neil JE, Bloom DC. 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.
24. Bloom DC, Giordani NV, Kwiatkowski DL. 2010. Epigenetic regulation of latent HSV-1 gene expression. Biochim. Biophys. Acta 1799:246-256.
25. Cliffe AR, Garber DA, Knipe DM. 2009. Transcription of the herpes simplex virus latency-associated transcript promotes the formation of facultative heterochromatin on lytic promoters. J. Virol. 83:8182-8190.
26. Creech CC, Neumann DM. 2010. Changes to euchromatin on LAT and ICP4 following reactivation are more prevalent in an efficiently reactivating strain of HSV-1. PLoS One 5:e15416. http://dx.doi.org/10.1371/ journal.pone.0015416.
27. Giordani NV, Neumann DM, Kwiatkowski DL, Bhattacharjee PS, McAnany PK, Hill JM, Bloom DC. 2008. During herpes simplex virus type 1 infection of rabbits, the ability to express the latency-associated transcript increases latent-phase transcription of lytic genes. J. Virol. 82:6056-6060.
28. Kwiatkowski DL, Thompson HW, Bloom DC. 2009. The polycomb group protein Bmi1 binds to the herpes simplex virus 1 latent genome and maintains repressive histone marks during latency. J. Virol. 83: 8173-8181.
29. Neumann DM, Bhattacharjee PS, Giordani NV, Bloom DC, Hill JM. 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.
30. Wang QY, Zhou C, Johnson KE, Colgrove RC, Coen DM, Knipe DM. 2005. Herpesviral latency-associated transcript gene promotes assembly of heterochromatin on viral lytic-gene promoters in latent infection. Proc. Natl. Acad. Sci. U. S. A. 102:16055-16059.
31. Cliffe AR, Coen DM, Knipe DM. 2013. Kinetics of facultative heterochromatin and polycomb group protein association with the herpes simplex viral genome during establishment of latent infection. mBio 4(1): e00590-12. http://dx.doi.org/10.1128/mBio.00590-12.
32. Liang Y, Quenelle D, Vogel JL, Mascaro C, Ortega A, Kristie TM. 2013. A novel selective LSD1/KDM1A inhibitor epigenetically blocks herpes simplex virus lytic replication and reactivation from latency. mBio 4(1): e00558-00512. http://dx.doi.org/10.1128/mBio.00558-12.
33. Hall JA, Georgel PT. 2007. CHD proteins: a diverse family with strong ties. Biochem. Cell Biol. 85:463-476.
34. Marfella CG, Imbalzano AN. 2007. The Chd family of chromatin remodelers. Mutat. Res. 618:30-40.
35. Murawska M, Brehm A. 2011. CHD chromatin remodelers and the transcription cycle. Transcription 2:244-253.
36. Alfonso R, Lutz T, Rodriguez A, Chavez JP, Rodriguez P, Gutierrez S, Nieto A. 2011. CHD6 chromatin remodeler is a negative modulator of influenza virus replication that relocates to inactive chromatin upon infection. Cell. Microbiol. 13:1894-1906.
37. Hu Y, Liu D, Zhong X, Zhang C, Zhang Q, Zhou DX. 2012. CHD3 protein recognizes and regulates methylated histone H3 lysines 4 and 27 over a subset of targets in the rice genome. Proc. Natl. Acad. Sci. U. S. A. 109:5773-5778.
38. Zhang H, Bishop B, Ringenberg W, Muir WM, Ogas J. 2012. The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27. Plant Physiol. 159:418-432.
39. Bolderson E, Savage KI, Mahen R, Pisupati V, Graham ME, Richard DJ, Robinson PJ, Venkitaraman AR, Khanna KK. 2012. Kruppel-associated box (KRAB)-associated co-repressor (KAP-1) ser-473 phosphorylation regulates heterochromatin protein 1β (HP1-β) mobilization and DNA repair in heterochromatin. J. Biol. Chem. 287:28122-28131.
40. Garvin AJ, Densham RM, Blair-Reid SA, Pratt KM, Stone HR, Weekes D, Lawrence KJ, Morris JR. 2013. The deSUMOylase SENP7 promotes chromatin relaxation for homologous recombinationDNArepair. EMBO Rep. 14:975-983.
41. Goodarzi AA, Kurka T, Jeggo PA. 2011. KAP-1 phosphorylation regulatesCHD3nucleosome remodeling during theDNAdouble-strand break response. Nat. Struct. Mol. Biol. 18:831-839.
42. Ivanov AV, Peng H, Yurchenko V, Yap KL, Negorev DG, Schultz DC, Psulkowski E, Fredericks WJ, White DE, Maul GG, Sadofsky MJ, Zhou MM, Rauscher FJ III. 2007. PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol. Cell 28:823-837.
43. Kunert N, Wagner E, Murawska M, Klinker H, Kremmer E, Brehm A. 2009. DMEC: a novel mi-2 chromatin remodelling complex involved in transcriptional repression. EMBO J. 28:533-544.
44. Ryan RF, Schultz DC, Ayyanathan K, Singh PB, Friedman JR, Fredericks WJ, Rauscher FJ, III. 1999. KAP-1 corepressor protein interacts and colocalizes with heterochromatic and euchromatic HP1 proteins: a potential role for Kruppel-associated box-zinc finger proteins in heterochromatin-mediated gene silencing. Mol. Cell. Biol. 19:4366-4378.
45. Tong JK, Hassig CA, Schnitzler GR, Kingston RE, Schreiber SL. 1998. Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 395:917-921.
46. Simon JM, Giresi PG, Davis IJ, Lieb JD. 2012. Using formaldehydeassisted isolation of regulatory elements (FAIRE) to isolate active regulatory DNA. Nat. Protoc. 7:256-267.
47. Song L, Zhang Z, Grasfeder LL, Boyle AP, Giresi PG, Lee BK, Sheffield NC, Gräf S, Huss M, Keefe D, Liu Z, London D, McDaniell RM, Shibata Y, Showers KA, Simon JM, Vales T, Wang T, Winter D, Zhang Z, Clarke ND, Birney E, Iyer VR, Crawford GE, Lieb JD, Furey TS. 2011. Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res. 21:1757-1767.
48. Giresi PG, Kim J, McDaniell RM, Iyer VR, Lieb JD. 2007. FAIRE (formaldehyde-assisted isolation of regulatory elements) isolates active regulatory elements from human chromatin. Genome Res. 17:877-885.
49. Hennig BP, Bendrin K, Zhou Y, Fischer T. 2012. Chd1 chromatin remodelers maintain nucleosome organization and repress cryptic transcription. EMBO Rep. 13:997-1003.
50. Jae Yoo E, Kyu Jang Y, Ae Lee M, Bjerling P, Bum Kim J, Ekwall K, Hyun Seong R, Dai Park S. 2002. Hrp3, a chromodomain helicase/ ATPase DNA binding protein, is required for heterochromatin silencing in fission yeast. Biochem. Biophys. Res. Commun. 295:970-974.
51. Lusser A, Urwin DL, Kadonaga JT. 2005. Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat. Struct. Mol. Biol. 12: 160-166.
52. Smolle M, Venkatesh S, Gogol MM, Li H, Zhang Y, Florens L, Washburn MP, Workman JL. 2012. Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat. Struct. Mol. Biol. 19:884-892.