Human cytomegalovirus UL29/28 protein interacts with components of the NuRD complex which promote accumulation of immediate-early RNA

PLoS Pathogens

Volumn 6, Issue 6, 2010, Pages

  Terhune, Scott S ^a,b   Moorman, Nathaniel J ^a   Cristea, Ileana M ^a,c   Savaryn, John Paul ^b   Cuevas Bennett, Christian ^a,d   Rout, Michael P ^c   Chait, Brian T ^c   Shenk, Thomas ^a  

^a PRINCETON UNIVERSITY   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE 1; PROTEIN PUL28; PROTEIN PUL29; RNA; SHORT HAIRPIN RNA; TRICHOSTATIN A; UNCLASSIFIED DRUG; VIRUS PROTEIN; AUTOANTIGEN; CHD4 PROTEIN, HUMAN; HDAC1 PROTEIN, HUMAN; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; IMMEDIATE EARLY PROTEIN; LUCIFERASE; MESSENGER RNA; MTA2 PROTEIN, HUMAN; REPRESSOR PROTEIN; RETINOBLASTOMA BINDING PROTEIN 4; VIRUS RNA;

ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; MASS SPECTROMETRY; NUCLEOSOME; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; VIRUS REPLICATION; CELL CULTURE; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DRUG ANTAGONISM; DRUG EFFECT; FIBROBLAST; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOPRECIPITATION; METABOLISM; PATHOGENICITY; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY; WESTERN BLOTTING;

HUMAN HERPESVIRUS 5;

AUTOANTIGENS; BLOTTING, WESTERN; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; IMMEDIATE-EARLY PROTEINS; IMMUNOPRECIPITATION; LUCIFERASES; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; RETINOBLASTOMA-BINDING PROTEIN 4; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, VIRAL; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 77954671476     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000965     Document Type: Article

References (82)

1. Mocarski E, Shenk T, Pass RF (2007) Cytomegaloviruses. Fields Virology: Lippincott Williams & Wilkins. pp 2702-2772.
2. Streblow DN, Dumortier J, Moses AV, Orloff SL, Nelson JA (2008) Mechanisms of cytomegalovirus-accelerated vascular disease: induction of paracrine factors that promote angiogenesis and wound healing. Curr Top Microbiol Immunol 325: 397-415.
3. Waller EC, Day E, Sissons JG, Wills MR (2008) Dynamics of T cell memory in human cytomegalovirus infection. Med Microbiol Immunol 197: 83-96.
4. Cinatl J, Jr., Nevels M, Paulus C, Michaelis M (2009) Activation of telomerase in glioma cells by human cytomegalovirus: another piece of the puzzle. J Natl Cancer Inst 101: 441-443.
5. Terhune SS, Schroer J, Shenk T (2004) RNAs are packaged into human cytomegalovirus virions in proportion to their intracellular concentration. J Virol 78: 10390-10398.
6. Bresnahan WA, Shenk T (2000) A subset of viral transcripts packaged within human cytomegalovirus particles. Science 288: 2373-2376.
7. Reeves MB, Davies AA, McSharry BP, Wilkinson GW, Sinclair JH (2007) Complex I binding by a virally encoded RNA regulates mitochondria-induced cell death. Science 316: 1345-1348.
8. Nitzsche A, Paulus C, Nevels M (2008) Temporal Dynamics of Cytomegalovirus Chromatin Assembly in Productively Infected Human Cells. J Virol.
9. Cuevas-Bennett C, Shenk T (2008) Dynamic Histone H3 Acetylation and Methylation at Human Cytomegalovirus Promoters during Replication in Fibroblasts. J Virol 82: 9525-9536.
10. Reeves M, Murphy J, Greaves R, Fairley J, Brehm A, et al. (2006) Autorepression of the human cytomegalovirus major immediate-early promot- er/enhancer at late times of infection is mediated by the recruitment of chromatin remodeling enzymes by IE86. J Virol 80: 9998-10009.
11. Ioudinkova E, Arcangeletti MC, Rynditch A, De Conto F, Motta F, et al. (2006) Control of human cytomegalovirus gene expression by differential histone modifications during lytic and latent infection of a monocytic cell line. Gene 384: 120-128.
12. Denslow SA, Wade PA (2007) The human Mi-2/NuRD complex and gene regulation. Oncogene 26: 5433-5438.
13. Lakowski B, Roelens I, Jacob S (2006) CoREST-like complexes regulate chromatin modification and neuronal gene expression. J Mol Neurosci 29: 227-239.
14. Silverstein RA, Ekwall K (2005) Sin3: a flexible regulator of global gene expression and genome stability. Curr Genet 47: 1-17.
15. Wang Y, Zhang H, Chen Y, Sun Y, Yang F, et al. (2009) LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138: 660-672.
16. Guschin D, Wade PA, Kikyo N, Wolffe AP (2000) ATP-Dependent histone octamer mobilization and histone deacetylation mediated by the Mi-2 chromatin remodeling complex. Biochemistry 39: 5238-5245.
17. Luo J, Su F, Chen D, Shiloh A, Gu W (2000) Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 408: 377-381.
18. Yoo YG, Kong G, Lee MO (2006) Metastasis-associated protein 1 enhances stability of hypoxia-inducible factor-1alpha protein by recruiting histone deacetylase 1. EMBO J 25: 1231-1241.
19. Park JJ, Kim YE, Pham HT, Kim ET, Chung YH, et al. (2007) Functional interaction of the human cytomegalovirus IE2 protein with histone deacetylase 2 in infected human fibroblasts. J Gen Virol 88: 3214-3223.
20. Kuntz-Simon G, Obert G (1995) Sodium valproate, an anticonvulsant drug, stimulates human cytomegalovirus replication. J Gen Virol 76 (Pt 6): 1409-1415.
21. Tang Q, Maul GG (2003) Mouse cytomegalovirus immediate-early protein 1 binds with host cell repressors to relieve suppressive effects on viral transcription and replication during lytic infection. J Virol 77: 1357-1367.
22. Saffert RT, Kalejta RF (2006) Inactivating a cellular intrinsic immune defense mediated by Daxx is the mechanism through which the human cytomegalovirus pp71 protein stimulates viral immediate-early gene expression. J Virol 80: 3863-3871.
23. Michaelis M, Suhan T, Reinisch A, Reisenauer A, Fleckenstein C, et al. (2005) Increased replication of human cytomegalovirus in retinal pigment epithelial cells by valproic acid depends on histone deacetylase inhibition. Invest Ophthalmol Vis Sci 46: 3451-3457.
24. Hummel M, Yan S, Li Z, Varghese TK, Abecassis M (2007) Transcriptional reactivation of murine cytomegalovirus ie gene expression by 5-aza-2'- deoxycytidine and trichostatin A in latently infected cells despite lack of methylation of the major immediate-early promoter. J Gen Virol 88: 1097-1102.
25. Woodhall DL, Groves IJ, Reeves MB, Wilkinson G, Sinclair JH (2006) Human Daxx-mediated repression of human cytomegalovirus gene expression correlates with a repressive chromatin structure around the major immediate early promoter. J Biol Chem 281: 37652-37660.
26. Nevels M, Paulus C, Shenk T (2004) Human cytomegalovirus immediate-early 1 protein facilitates viral replication by antagonizing histone deacetylation. Proc Natl Acad Sci U S A 101: 17234-17239.
27. Paulus C, Krauss S, Nevels M (2006) A human cytomegalovirus antagonist of type I IFN-dependent signal transducer and activator of transcription signaling. Proc Natl Acad Sci U S A 103: 3840-3845.
28. Taylor TJ, Knipe DM (2004) Proteomics of herpes simplex virus replication compartments: association of cellular DNA replication, repair, recombination, and chromatin remodeling proteins with ICP8. J Virol 78: 5856-5866.
29. Lomonte P, Thomas J, Texier P, Caron C, Khochbin S, et al. (2004) Functional interaction between class II histone deacetylases and ICP0 of herpes simplex virus type 1. J Virol 78: 6744-6757.
30. 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.
31. Radkov SA, Touitou R, Brehm A, Rowe M, West M, et al. (1999) Epstein-Barr virus nuclear antigen 3C interacts with histone deacetylase to repress transcription. J Virol 73: 5688-5697.
32. Knight JS, Lan K, Subramanian C, Robertson ES (2003) Epstein-Barr virus nuclear antigen 3C recruits histone deacetylase activity and associates with the corepressors mSin3A and NCoR in human B-cell lines. J Virol 77: 4261-4272.
33. Brehm A, Nielsen SJ, Miska EA, McCance DJ, Reid JL, et al. (1999) The E7 oncoprotein associates with Mi2 and histone deacetylase activity to promote cell growth. EMBO J 18: 2449-2458.
34. Longworth MS, Laimins LA (2004) The binding of histone deacetylases and the integrity of zinc finger-like motifs of the E7 protein are essential for the life cycle of human papillomavirus type 31. J Virol 78: 3533-3541.
35. Longworth MS, Wilson R, Laimins LA (2005) HPV31 E7 facilitates replication by activating E2F2 transcription through its interaction with HDACs. EMBO J 24: 1821-1830.
36. Moorman NJ, Cristea IM, Terhune SS, Rout MP, Chait BT, et al. (2008) Human cytomegalovirus protein UL38 inhibits host cell stress responses by antagonizing the tuberous sclerosis protein complex. Cell Host Microbe 3: 253-262.
37. Terhune S, Torigoi E, Moorman N, Silva M, Qian Z, et al. (2007) Human cytomegalovirus UL38 protein blocks apoptosis. J Virol 81: 3109-3123.
38. Xuan B, Qian Z, Torigoi E, Yu D (2009) Human cytomegalovirus protein pUL38 induces ATF4 expression, inhibits persistent JNK phosphorylation, and suppresses endoplasmic reticulum stress-induced cell death. J Virol 83: 3463-3474.
39. Yu D, Silva MC, Shenk T (2003) Functional map of human cytomegalovirus AD169 defined by global mutational analysis. Proc Natl Acad Sci U S A 100: 12396-12401.
40. Dunn W, Chou C, Li H, Hai R, Patterson D, et al. (2003) Functional profiling of a human cytomegalovirus genome. Proc Natl Acad Sci U S A 100: 14223-14228.
41. Mitchell DP, Savaryn JP, Moorman NJ, Shenk T, Terhune SS (2009) Human cytomegalovirus UL28 and UL29 open reading frames encode a spliced mRNA and stimulate accumulation of immediate-early RNAs. J Virol 83: 10187-10197.
42. Romanowski MJ, Shenk T (1997) Characterization of the human cytomegalo- virus irs1 and trs1 genes: a second immediate-early transcription unit within irs1 whose product antagonizes transcriptional activation. J Virol 71: 1485-1496.
43. Bresnahan WA, Hultman GE, Shenk T (2000) Replication of wild-type and mutant human cytomegalovirus in life-extended human diploid fibroblasts. J Virol 74: 10816-10818.
44. Kinsella TM, Nolan GP (1996) Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum Gene Ther 7: 1405-1413.
45. Yu D, Smith GA, Enquist LW, Shenk T (2002) Construction of a self-excisable bacterial artificial chromosome containing the human cytomegalovirus genome and mutagenesis of the diploid TRL/IRL13 gene. J Virol 76: 2316-2328.
46. Cristea IM, Carroll JW, Rout MP, Rice CM, Chait BT, et al. (2006) Tracking and elucidating alphavirus-host protein interactions. J Biol Chem 281: 30269-30278.
47. Cristea IM, Williams R, Chait BT, Rout MP (2005) Fluorescent proteins as proteomic probes. Mol Cell Proteomics 4: 1933-1941.
48. Krutchinsky AN, Zhang W, Chait BT (2000) Rapidly switchable matrix-assisted laser desorption/ionization and electrospray quadrupole-time-of-flight mass spectrometry for protein identification. J Am Soc Mass Spectrom 11: 493-504.
49. Krutchinsky AN, Kalkum M, Chait BT (2001) Automatic identification of proteins with a MALDI-quadrupole ion trap mass spectrometer. Anal Chem 73: 5066-5077.
50. Luo Y, Li T, Yu F, Kramer T, Cristea IM (2009) Resolving the Composition of Protein Complexes Using a MALDI LTQ Orbitrap. J Am Soc Mass Spectrom.
51. Zhu H, Shen Y, Shenk T (1995) Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J Virol 69: 7960-7970.
52. Feng X, Schroer J, Yu D, Shenk T (2006) Human cytomegalovirus pUS24 is a virion protein that functions very early in the replication cycle. J Virol 80: 8371-8378.
53. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, et al. (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267.
54. Naldini L, Blomer U, Gage FH, Trono D, Verma IM (1996) Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci U S A 93: 11382-11388.
55. Lu F, Zhou J, Wiedmer A, Madden K, Yuan Y, et al. (2003) Chromatin remodeling of the Kaposi's sarcoma-associated herpesvirus ORF50 promoter correlates with reactivation from latency. J Virol 77: 11425-11435.
56. 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.
57. Zhang Y, Jones C (2001) The bovine herpesvirus 1 immediate-early protein (bICP0) associates with histone deacetylase 1 to activate transcription. J Virol 75: 9571-9578.
58. Glozak MA, Seto E (2007) Histone deacetylases and cancer. Oncogene 26: 5420-5432.
59. Wolf DG, Courcelle CT, Prichard MN, Mocarski ES (2001) Distinct and separate roles for herpesvirus-conserved UL97 kinase in cytomegalovirus DNA synthesis and encapsidation. Proc Natl Acad Sci U S A 98: 1895-1900.
60. Krosky PM, Baek MC, Coen DM (2003) The human cytomegalovirus UL97 protein kinase, an antiviral drug target, is required at the stage of nuclear egress. J Virol 77: 905-914.
61. Mitchell DP, Savaryn JP, Moorman NJ, Shenk T, Terhune SS (2009) Human cytomegalovirus UL28 and UL29 open reading frames encode a spliced mRNA and stimulate accumulation of immediate-early RNAs. J Virol.
62. Moorman NJ, Sharon-Friling R, Shenk T, Cristea IM (2009) A targeted spatial- temporal proteomic approach implicates multiple cellular trafficking pathways in human cytomegalovirus virion maturation. Mol Cell Proteomics.
63. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, et al. (2004) Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 86: 3993-4003.
64. Nevels M, Brune W, Shenk T (2004) SUMOylation of the human cytomegalovirus 72-kilodalton IE1 protein facilitates expression of the 86- kilodalton IE2 protein and promotes viral replication. J Virol 78: 7803-7812.
65. Groves I, Reeves M, Sinclair J (2009) Lytic infection of permissive cells with human cytomegalovirus is regulated by an intrinsic ''pre-immediate early'' repression of viral gene expression mediated by histone post-translational modification. J Gen Virol.
66. Guo W, Shan B, Klingsberg RC, Qin X, Lasky JA (2009) Abrogation of TGF- beta1-induced fibroblast-myofibroblast differentiation by histone deacetylase inhibition. Am J Physiol Lung Cell Mol Physiol 297: L864-870.
67. Pegoraro G, Kubben N, Wickert U, Gohler H, Hoffmann K, et al. (2009) Ageing-related chromatin defects through loss of the NURD complex. Nat Cell Biol 11: 1261-1267.
68. Ramirez-Carrozzi VR, Nazarian AA, Li CC, Gore SL, Sridharan R, et al. (2006) Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response. Genes Dev 20: 282-296.
69. DeMeritt IB, Milford LE, Yurochko AD (2004) Activation of the NF-kappaB pathway in human cytomegalovirus-infected cells is necessary for efficient transactivation of the major immediate-early promoter. J Virol 78: 4498-4507.
70. Netterwald J, Yang S, Wang W, Ghanny S, Cody M, et al. (2005) Two gamma interferon-activated site-like elements in the human cytomegalovirus major immediate-early promoter/enhancer are important for viral replication. J Virol 79: 5035-5046.
71. Walters MS, Erazo A, Kinchington PR, Silverstein S (2009) Histone Deacetylase 1 and 2 are Phosphorylated at Novel Sites During Varicella Zoster Virus Infection. J Virol.
72. Miccio A, Wang Y, Hong W, Gregory GD, Wang H, et al. NuRD mediates activating and repressive functions of GATA-1 and FOG-1 during blood development. EMBO J 29: 442-456.
73. Lee SB, Ou DS, Lee CF, Juan LJ (2009) Gene-specific transcriptional activation mediated by the p150 subunit of the chromatin assembly factor 1. J Biol Chem 284: 14040-14049.
74. Takami Y, Ono T, Fukagawa T, Shibahara K, Nakayama T (2007) Essential role of chromatin assembly factor-1-mediated rapid nucleosome assembly for DNA replication and cell division in vertebrate cells. Mol Biol Cell 18: 129-141.
75. Kitagawa H, Fujiki R, Yoshimura K, Mezaki Y, Uematsu Y, et al. (2003) The chromatin-remodeling complex WINAC targets a nuclear receptor to promoters and is impaired in Williams syndrome. Cell 113: 905-917.
76. Fujita N, Jaye DL, Kajita M, Geigerman C, Moreno CS, et al. (2003) MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 113: 207-219.
77. Zhang H, Singh RR, Talukder AH, Kumar R (2006) Metastatic tumor antigen 3 is a direct corepressor of the Wnt4 pathway. Genes Dev 20: 2943-2948.
78. Molli PR, Singh RR, Lee SW, Kumar R (2008) MTA1-mediated transcriptional repression of BRCA1 tumor suppressor gene. Oncogene 27: 1971-1980.
79. Browne EP, Wing B, Coleman D, Shenk T (2001) Altered cellular mRNA levels in human cytomegalovirus-infected fibroblasts: viral block to the accumulation of antiviral mRNAs. J Virol 75: 12319-12330.
80. Casavant NC, Luo MH, Rosenke K, Winegardner T, Zurawska A, et al. (2006) Potential role for p53 in the permissive life cycle of human cytomegalovirus. J Virol 80: 8390-8401.
81. Hannemann H, Rosenke K, O'Dowd JM, Fortunato EA (2009) The presence of p53 influences the expression of multiple human cytomegalovirus genes at early times postinfection. J Virol 83: 4316-4325.
82. Lu Z, Hu X, Li Y, Zheng L, Zhou Y, et al. (2004) Human papillomavirus 16 E6 oncoprotein interferences with insulin signaling pathway by binding to tuberin. J Biol Chem 279: 35664-35670.