Herpes simplex virus is equipped with RNA- and protein-based mechanisms to repress expression of ATRX, an effector of intrinsic immunity

Journal of Virology

Volumn 86, Issue 18, 2012, Pages 10093-10102

  Jurak, Igor ^a   Silverstein, Leah B ^a   Sharma, Mayuri ^a   Coen, Donald M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA THALASSEMIA MENTAL RETARDATION SYNDROME X LINKED PROTEIN; IMMEDIATE EARLY PROTEIN; IMMEDIATE EARLY PROTEIN ICP0; MESSENGER RNA; MICROORGANISM PROTEIN; MICRORNA; MICRORNA H1; MICRORNA H6; PROTEASOME INHIBITOR; UNCLASSIFIED DRUG; VIRUS PROTEIN;

3' UNTRANSLATED REGION; ALPHA THALASSEMIA MENTAL RETARDATION SYNDROME X LINKED GENE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOLYSIS; DOWN REGULATION; GENE DELETION; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 2; HUMAN; HUMAN CELL; IMMUNITY; INTRINSIC IMMUNITY; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR DOMAIN 10; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS; VIRUS GENE;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CELL LINE; CERCOPITHECUS AETHIOPS; DNA HELICASES; DOWN SYNDROME; HEK293 CELLS; HERPESVIRUS 1, HUMAN; HERPESVIRUS 2, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMEDIATE-EARLY PROTEINS; MICRORNAS; NUCLEAR PROTEINS; REPRESSOR PROTEINS; RNA, MESSENGER; RNA, VIRAL; SIMPLEXVIRUS; TRANSFECTION; UBIQUITIN-PROTEIN LIGASES; VERO CELLS; VIRAL PROTEINS;

HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 2; HUMAN HERPESVIRUS 5; SIMPLEXVIRUS;

EID: 84866177156     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00930-12     Document Type: Article

References (99)

1. Adler M, Tavalai N, Muller R, Stamminger T. 2011. Human cytomegalovirus immediate-early gene expression is restricted by the nuclear domain 10 component Sp100. J. Gen. Virol. 92:1532-1538.
2. Ahn JH, Brignole EJ III, Hayward GS. 1998. Disruption of PML subnuclear domains by the acidic IE1 protein of human cytomegalovirus is mediated through interaction with PML and may modulate a RING finger-dependent cryptic transactivator function of PML. Mol. Cell. Biol. 18:4899-4913.
3. Baek D, et al. 2008. The impact of microRNAs on protein output. Nature 455:64-71.
4. Barbato C, et al. 2009. Computational challenges in miRNA target predictions: to be or not to be a true target? J. Biomed. Biotechnol. 2009:803069.
5. Becker Y, Tavor E, Asher Y, Berkowitz C, Moyal M. 1993. Effect of herpes simplex virus type-1 UL41 gene on the stability of mRNA from the cellular genes: beta-actin, fibronectin, glucose transporter-1, and docking protein, and on virus intraperitoneal pathogenicity to newborn mice. Virus Genes 7:133-143.
6. Bieniasz PD. 2004. Intrinsic immunity: a front-line defense against viral attack. Nat. Immunol. 5:1109-1115.
7. Boutell C, Sadis S, Everett RD. 2002. Herpes simplex virus type 1 immediate-early protein ICP0 and its isolated RING finger domain act as ubiquitin E3 ligases in vitro. J. Virol. 76:841-850.
8. Cai WZ, Schaffer PA. 1989. Herpes simplex virus type 1 ICP0 plays a critical role in the de novo synthesis of infectious virus following transfection of viral DNA. J. Virol. 63:4579-4589.
9. Cantrell SR, Bresnahan WA. 2006. Human cytomegalovirus (HCMV) UL82 gene product (pp71) relieves hDaxx-mediated repression ofHCMV replication. J. Virol. 80:6188-6191.
10. Cardoso C, et al. 1998. Specific interaction between the XNP/ATR-X gene product and the SET domain of the human EZH2 protein. Hum. Mol. Genet. 7:679-684.
11. Carlson M, Laurent BC. 1994. The SNF/SWI family of global transcriptional activators. Curr. Opin. Cell Biol. 6:396-402.
12. Chelbi-Alix MK, de The H. 1999. Herpes virus induced proteasomedependent degradation of the nuclear bodies-associated PML and Sp100 proteins. Oncogene 18:935-941.
13. Chen D, Zhao M, Mundy GR. 2004. Bone morphogenetic proteins. Growth Factors 22:233-241.
14. Coen DM, Fleming HE, Jr, Leslie LK, Retondo MJ. 1985. Sensitivity of arabinosyladenine-resistant mutants of herpes simplex virus to other antiviral drugs and mapping of drug hypersensitivity mutations to the DNA polymerase locus. J. Virol. 53:477-488.
15. Cui C, et al. 2006. Prediction and identification of herpes simplex virus 1-encoded microRNAs. J. Virol. 80:5499-5508.
16. Derynck R, Miyazono K (ed). 2008. TGF-β and the TGF-β family. Cold Spring Harbor Laboratory Press, New York, NY.
17. Drane P, Ouararhni K, Depaux A, Shuaib M, Hamiche A. 2010. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev. 24:1253-1265.
18. Du T, Zhou G, Roizman B. 2011. HSV-1 gene expression from reactivated ganglia is disordered and concurrent with suppression of latencyassociated transcript and miRNAs. Proc. Natl. Acad. Sci. U. S. A. 108:18820-18824.
19. Everett RD, et al. 1998. The disruption of ND10 during herpes simplex virus infection correlates with the Vmw110- and proteasome-dependent loss of several PML isoforms. J. Virol. 72:6581-6591.
20. Everett RD, Maul GG. 1994. HSV-1 IE protein Vmw110 causes redistribution of PML. EMBO J. 13:5062-5069.
21. Everett RD, Murray J. 2005. ND10 components relocate to sites associated with herpes simplex virus type 1 nucleoprotein complexes during virus infection. J. Virol. 79:5078-5089.
22. Everett RD, Murray J, Orr A, Preston CM. 2007. Herpes simplex virus type 1 genomes are associated with ND10 nuclear substructures in quiescently infected human fibroblasts. J. Virol. 81:10991-11004.
23. Everett RD, Parada C, Gripon P, Sirma H, Orr A. 2008. Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J. Virol. 82:2661-2672.
24. Everett RD, et al. 2006. PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J. Virol. 80:7995-8005.
25. Everett RD, Sourvinos G, Orr A. 2003. Recruitment of herpes simplex virus type 1 transcriptional regulatory protein ICP4 into foci juxtaposed to ND10 in live, infected cells. J. Virol. 77:3680-3689.
26. Friedman RC, Farh KK, Burge CB, Bartel DP. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19:92-105.
27. Gibbons RJ, et al. 1997. Mutations in transcriptional regulator ATRX establish the functional significance of a PHD-like domain. Nat. Genet. 17:146-148.
28. Goldberg AD, et al. 2010. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140:678-691.
29. Grimson A, et al. 2007. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 27:91-105.
30. Guo H, Ingolia NT, Weissman JS, Bartel DP. 2010. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466:835-840.
31. Heaphy CM, et al. 2011. Altered telomeres in tumors with ATRX and DAXX mutations. Science 333:425.
32. Hogan BL. 1996. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10:1580-1594.
33. Hwang J, Kalejta RF. 2007. Proteasome-dependent, ubiquitin-independent degradation of Daxx by the viral pp71 protein in human cytomegalovirusinfected cells. Virology 367:334-338.
34. Ishov AM, et al. 1999. PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J. Cell Biol. 147:221-234.
35. Jones CA, Taylor TJ, Knipe DM. 2000. Biological properties of herpes simplex virus 2 replication-defective mutant strains in a murine nasal infection model. Virology 278:137-150.
36. Jurak I, Brune W. 2006. Induction of apoptosis limits cytomegalovirus cross-species infection. EMBO J. 25:2634-2642.
37. Jurak I, Griffiths A, Coen DM. 2011. Mammalian alphaherpesvirus miRNAs. Biochim. Biophys. Acta 1809:641-653.
38. Jurak I, et al. 2010. Numerous conserved and divergent microRNAs expressed by herpes simplex viruses 1 and 2. J. Virol. 84:4659-4672.
39. Kamil JP, Coen DM. 2007. Human cytomegalovirus protein kinase UL97 forms a complex with the tegument phosphoprotein pp65. J. Virol. 81:10659-10668.
40. Kim JY, Mandarino A, Chao MV, Mohr I, Wilson AC. 2012. Transient reversal of episome silencing precedes VP16-dependent transcription during reactivation of latent HSV-1 in neurons. PLoS Pathog. 8:e1002540. doi:10.1371/journal.ppat.1002540.
41. Korioth F, Maul GG, Plachter B, Stamminger T, Frey J. 1996. The nuclear domain 10 (ND10) is disrupted by the human cytomegalovirus gene product IE1. Exp. Cell Res. 229:155-158.
42. Kramer MF, et al. 2011. Herpes simplex virus 1 microRNAs expressed abundantly during latent infection are not essential for latency in mouse trigeminal ganglia. Virology 417:239-247.
43. Krikorian CR, Read GS. 1991. In vitro mRNA degradation system to study the virion host shutoff function of herpes simplex virus. J. Virol. 65:112-122.
44. Kummer M, et al. 2007. Herpes simplex virus type 1 induces CD83 degradation in mature dendritic cells with immediate-early kinetics via the cellular proteasome. J. Virol. 81:6326-6338.
45. Lau NC, Lim LP, Weinstein EG, Bartel DP. 2001. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294:858-862.
46. Lee HR, et al. 2004. Ability of the human cytomegalovirus IE1 protein to modulate sumoylation of PML correlates with its functional activities in transcriptional regulation and infectivity in cultured fibroblast cells. J. Virol. 78:6527-6542.
47. Lewis BP, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15-20
48. Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD. 2010. 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. 107:14075-14080.
49. Lomonte P, Sullivan KF, Everett RD. 2001. Degradation of nucleosomeassociated centromeric histone H3-like protein CENP-A induced by herpes simplex virus type 1 protein ICP0. J. Biol. Chem. 276:5829-5835.
50. Lukashchuk V, Everett RD. 2010. Regulation of ICP0-null mutant herpes simplex virus type 1 infection by ND10 components ATRX and hDaxx. J. Virol. 84:4026-4040.
51. Lukashchuk V, McFarlane S, Everett RD, Preston CM. 2008. Human cytomegalovirus protein pp71 displaces the chromatin-associated factor ATRX from nuclear domain 10 at early stages of infection. J. Virol. 82:12543-12554.
52. Machado RD, et al. 2006. Mutations of the TGF-beta type II receptor BMPR2 in pulmonary arterial hypertension. Hum. Mutat. 27:121-132.
53. Maul GG, Everett RD. 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.
54. Maul GG, Guldner HH, Spivack JG. 1993. Modification of discrete nuclear domains induced by herpes simplex virus type 1 immediate early gene 1 product (ICP0). J. Gen. Virol. 74:2679-2690.
55. McDowell TL, et al. 1999. Localization of a putative transcriptional regulator (ATRX) at pericentromeric heterochromatin and the short arms of acrocentric chromosomes. Proc. Natl. Acad. Sci. U. S. A. 96:13983-13988.
56. Morrell NW. 2010. Role of bone morphogenetic protein receptors in the development of pulmonary arterial hypertension. Adv. Exp. Med. Biol. 661:251-264.
57. Nachmani D, Stern-Ginossar N, Sarid R, Mandelboim O. 2009. Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe 5:376-385.
58. Negorev D, Maul GG. 2001. Cellular proteins localized at and interacting within ND10/PML nuclear bodies/PODs suggest functions of a nuclear depot. Oncogene 20:7234-7242.
59. Negorev DG, Vladimirova OV, Ivanov A, Rauscher F III, Maul GG. 2006. Differential role of Sp100 isoforms in interferon-mediated repression of herpes simplex virus type 1 immediate-early protein expression. J. Virol. 80:8019-8029.
60. Pan D, Coen DM. 2012. Quantification and analysis of thymidine kinase expression from acyclovir-resistant g-string insertion and deletion mutants in herpes simplex virus-infected cells. J. Virol. 86:4518-4526.
61. Parkinson J, Everett RD. 2000. Alphaherpesvirus proteins related to herpes simplex virus type 1 ICP0 affect cellular structures and proteins. J. Virol. 74:10006-10017.
62. Parkinson J, Lees-Miller SP, Everett RD. 1999. Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA-dependent protein kinase. J. Virol. 73:650-657.
63. Picketts DJ, et al. 1996. ATRX encodes a novel member of the SNF2 family of proteins: mutations point to a common mechanism underlying the ATR-X syndrome. Hum. Mol. Genet. 5:1899-1907.
64. Preston CM, Nicholl MJ. 2006. Role of the cellular protein hDaxx in human cytomegalovirus immediate-early gene expression. J. Gen. Virol. 87:1113-1121.
65. Rajewsky N. 2006. microRNA target predictions in animals. Nat. Genet. 38(Suppl):S8-S13.
66. Ratnakumar K, et al. 2012. ATRX-mediated chromatin association of histone variant macroH2A1 regulates alpha-globin expression. Genes Dev. 26:433-438.
67. Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R. 2004. Fast and effective prediction of microRNA/target duplexes. RNA 10:1507-1517.
68. Sacks WR, Schaffer PA. 1987. Deletion mutants in the gene encoding the herpes simplex virus type 1 immediate-early protein ICP0 exhibit impaired growth in cell culture. J. Virol. 61:829-839.
69. Saffert RT, Kalejta RF. 2007. Human cytomegalovirus gene expression is silenced by Daxx-mediated intrinsic immune defense in model latent infections established in vitro. J. Virol. 81:9109-9120.
70. 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.
71. Selbach M, et al. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455:58-63.
72. Sethupathy P, Megraw M, Hatzigeorgiou AG. 2006. A guide through present computational approaches for the identification of mammalian microRNA targets. Nat. Methods 3:881-886.
73. Skalsky RL, Cullen BR. 2010. Viruses, microRNAs, and host interactions. Annu. Rev. Microbiol. 64:123-141.
74. Smiley JR. 2004. Herpes simplex virus virion host shutoff protein: immune evasion mediated by a viral RNase? J. Virol. 78:1063-1068.
75. Sorenson CM, Hart PA, Ross J. 1991. Analysis of herpes simplex virusinduced mRNA destabilizing activity using an in vitro mRNA decay system. Nucleic Acids Res. 19:4459-4465.
76. Stern-Ginossar N, et al. 2007. Host immune system gene targeting by a viral miRNA. Science 317:376-381.
77. Stow ND, Stow EC. 1986. Isolation and characterization of a herpes simplex virus type 1 mutant containing a deletion within the gene encoding the immediate early polypeptide Vmw110. J. Gen. Virol. 67:2571-2585.
78. Strelow LI, Leib DA. 1995. Role of the virion host shutoff (vhs) of herpes simplex virus type 1 in latency and pathogenesis. J. Virol. 69:6779-6786.
79. Taddeo B, Roizman B. 2006. The virion host shutoff protein (UL41) of herpes simplex virus 1 is an endoribonuclease with a substrate specificity similar to that of RNase A. J. Virol. 80:9341-9345.
80. Takane K, Kanai A. 2011. Vertebrate virus-encoded microRNAs and their sequence conservation. Jpn. J. Infect. Dis. 64:357-366.
81. Tang J, et al. 2004. A novel transcription regulatory complex containing death domain-associated protein and the ATR-X syndrome protein. J. Biol. Chem. 279:20369-20377.
82. Tang S, Bertke AS, Patel A, Margolis TP, Krause PR. 2011. Herpes simplex virus 2 microRNA miR-H6 is a novel latency-associated transcript-associated microRNA, but reduction of its expression does not influence the establishment of viral latency or the recurrence phenotype. J. Virol. 85:4501-4509.
83. Tang S, et al. 2008. An acutely and latently expressed herpes simplex virus 2 viral microRNA inhibits expression of ICP34.5, a viral neurovirulence factor. Proc. Natl. Acad. Sci. U. S. A. 105:10931-10936.
84. Tang S, Patel A, Krause PR. 2009. Novel less-abundant viral microRNAs encoded by herpes simplex virus 2 latency-associated transcript and their roles in regulating ICP34.5 and ICP0 mRNAs. J. Virol. 83:1433-1442.
85. Tavalai N, Adler M, Scherer M, Riedl Y, Stamminger T. 2011. Evidence for a dual antiviral role of the major nuclear domain 10 component Sp100 during the immediate-early and late phases of the human cytomegalovirus replication cycle. J. Virol. 85:9447-9458.
86. Tavalai N, Papior P, Rechter S, Leis M, Stamminger T. 2006. Evidence for a role of the cellular ND10 protein PML in mediating intrinsic immunity against human cytomegalovirus infections. J. Virol. 80:8006-8018.
87. Tavalai N, Papior P, Rechter S, Stamminger T. 2008. Nuclear domain 10 components promyelocytic leukemia protein and hDaxx independently contribute to an intrinsic antiviral defense against human cytomegalovirus infection. J. Virol. 82:126-137.
88. Tavalai N, Stamminger T. 2008. New insights into the role of the subnuclear structure ND10 for viral infection. Biochim. Biophys. Acta 1783: 2207-2221.
89. Thomson JR, et al. 2000. Sporadic primary pulmonary hypertension is associated with germline mutations of the gene encoding BMPR-II, a receptor member of the TGF-beta family. J. Med. Genet. 37:741-745.
90. Tischer BK, von Einem J, Kaufer B, Osterrieder N. 2006. Two-step red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. Biotechniques 40:191-197.
91. Umbach JL, et al. 2008. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454:780-783.
92. Umbach JL, Nagel MA, Cohrs RJ, Gilden DH, Cullen BR. 2009. Analysis of human alphaherpesvirus microRNA expression in latently infected human trigeminal ganglia. J. Virol. 83:10677-10683.
93. Umbach JL, et al. 2010. Identification of viral microRNAs expressed in human sacral ganglia latently infected with herpes simplex virus 2. J. Virol. 84:1189-1192.
94. Villard L, et al. 1997. Determination of the genomic structure of the XNP/ATRX gene encoding a potential zinc finger helicase. Genomics 43:149-155.
95. Wong LH, et al. 2010. ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res. 20:351-360.
96. 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.
97. Xue Y, et al. 2003. The ATRX syndrome protein forms a chromatinremodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. Proc. Natl. Acad. Sci. U. S. A. 100:10635-10640.
98. Yan N, Chen ZJ. 2012. Intrinsic antiviral immunity. Nat. Immunol. 13:214-222.
99. Yao Y, et al. 2007. Marek's disease virus type 2 (MDV-2)-encoded microRNAs show no sequence conservation with those encoded by MDV-1. J. Virol. 81:7164-7170.