Intrinsic cellular defense mechanisms targeting human cytomegalovirus

Virus Research

Volumn 157, Issue 2, 2011, Pages 128-133

  Tavalai, Nina ^a   Stamminger, Thomas ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Antiviral defense; ATRX; HCMV; HDaxx; Intrinsic immunity; Nuclear domain 10; PML; PML nuclear bodies; Sp100

Indexed keywords

CD34 ANTIBODY; INTRINSIC FACTOR; METHYLTRANSFERASE; SMALL INTERFERING RNA; VIRUS DNA;

ARTICLE; CELL FUSION; CELL METABOLISM; CELL NUCLEUS INCLUSION BODY; CYTOMEGALOVIRUS; DEFENSE MECHANISM; GENE EXPRESSION; HERPES VIRUS; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; MACROMOLECULE; MENTAL RETARDATION MALFORMATION SYNDROME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SUMOYLATION; VIROGENESIS; VIRUS GENE; VIRUS REPLICATION;

CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; GENE EXPRESSION REGULATION, VIRAL; HUMANS; IMMEDIATE-EARLY PROTEINS; IMMUNITY, INNATE; NUCLEAR PROTEINS; VIRAL PROTEINS; VIRUS LATENCY; VIRUS REPLICATION;

CYTOMEGALOVIRUS; HUMAN HERPESVIRUS 5;

EID: 79955028629     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2010.10.002     Document Type: Article

References (71)

1. Ahn J.H., Hayward G.S. The major immediate-early proteins IE1 and IE2 of human cytomegalovirus colocalize with and disrupt PML-associated nuclear bodies at very early times in infected permissive cells. J. Virol. 1997, 71:4599-4613.
2. Ahn J.H., Brignole E.J., Hayward G.S. 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. 1998, 18:4899-4913.
3. Bernardi R., Pandolfi P.P. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat. Rev. Mol. Cell Biol. 2007.
4. Bernardi R., Papa A., Pandolfi P.P. Regulation of apoptosis by PML and the PML-NBs. Oncogene 2008, 27:6299-6312.
5. Bieniasz P.D. Intrinsic immunity: a front-line defense against viral attack. Nat. Immunol. 2004, 5:1109-1115.
6. Bischof O., Kirsh O., Pearson M., Itahana K., Pelicci P.G., Dejean A. Deconstructing PML-induced premature senescence. EMBO J. 2002, 21:3358-3369.
7. Boutell C., Orr A., Everett R.D. PML residue lysine 160 is required for the degradation of PML induced by herpes simplex virus type 1 regulatory protein ICP0. J. Virol. 2003, 77:8686-8694.
8. Cantrell S.R., Bresnahan W.A. Interaction between the human cytomegalovirus UL82 gene product (pp71) and hDaxx regulates immediate-early gene expression and viral replication. J. Virol. 2005, 79:7792-7802.
9. Cantrell S.R., Bresnahan W.A. Human cytomegalovirus (HCMV) UL82 gene product (pp71) relieves hDaxx-mediated repression of HCMV replication. J. Virol. 2006, 80:6188-6191.
10. Carbone R., Botrugno O.A., Ronzoni S., Insinga A., Di C.L., Pelicci P.G., Minucci S. Recruitment of the histone methyltransferase SUV39H1 and its role in the oncogenic properties of the leukemia-associated PML-retinoic acid receptor fusion protein. Mol. Cell Biol. 2006, 26:1288-1296.
11. Dellaire G., Bazett-Jones D.P. PML nuclear bodies: dynamic sensors of DNA damage and cellular stress. Bioessays 2004, 26:963-977.
12. Di C.L., Raker V.A., Corsaro M., Fazi F., Fanelli M., Faretta M., Fuks F., Lo C.F., Kouzarides T., Nervi C., Minucci S., Pelicci P.G. Methyltransferase recruitment and DNA hypermethylation of target promoters by an oncogenic transcription factor. Science 2002, 295:1079-1082.
13. Dimitropoulou P., Caswell R., McSharry B.P., Greaves R.F., Spandidos D.A., Wilkinson G.W., Sourvinos G. Differential relocation and stability of PML-body components during productive human cytomegalovirus infection: detailed characterization by live-cell imaging. Eur. J. Cell Biol. 2010, 89:757-768.
14. Everett R.D., Chelbi-Alix M.K. PML and PML nuclear bodies: implications in antiviral defence. Biochimie 2007, 89:819-830.
15. Goila-Gaur R., Strebel K. HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology 2008, 5:51.
16. Groves I.J., Sinclair J.H. Knockdown of hDaxx in normally non-permissive undifferentiated cells does not permit human cytomegalovirus immediate-early gene expression. J. Gen. Virol. 2007, 88:2935-2940.
17. Groves I.J., Reeves M.B., Sinclair J.H. 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. 2009, 90:2364-2374.
18. Hofmann H., Sindre H., Stamminger T. Functional interaction between the pp71 protein of human cytomegalovirus and the PML-interacting protein human Daxx. J. Virol. 2002, 76:5769-5783.
19. Hwang J., Kalejta R.F. Proteasome-dependent, ubiquitin-independent degradation of Daxx by the viral pp71 protein in human cytomegalovirus-infected cells. Virology 2007, 367:334-338.
20. Hwang J., Kalejta R.F. Human cytomegalovirus protein pp71 induces Daxx SUMOylation. J. Virol. 2009, 83:6591-6598.
21. Ishov A.M., Maul G.G. The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. J. Cell Biol. 1996, 134:815-826.
22. Ishov A.M., Stenberg R.M., Maul G.G. Human cytomegalovirus immediate early interaction with host nuclear structures: definition of an immediate transcript environment. J. Cell Biol. 1997, 138:5-16.
23. Ishov A.M., Sotnikov A.G., Negorev D., Vladimirova O.V., Neff N., Kamitani T., Yeh E.T.H., Strauss J.F., Maul G.G. 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. 1999, 147:221-233.
24. Ishov A.M., Vladimirova O.V., Maul G.G. Daxx-mediated accumulation of human cytomegalovirus tegument protein pp71 at ND10 facilitates initiation of viral infection at these nuclear domains. J. Virol. 2002, 76:7705-7712.
25. Kang H., Kim E.T., Lee H.R., Park J.J., Go Y.Y., Choi C.Y., Ahn J.H. Inhibition of SUMO-independent PML oligomerization by the human cytomegalovirus IE1 protein. J. Gen. Virol. 2006, 87:2181-2190.
26. Kaspari M., Tavalai N., Stamminger T., Zimmermann A., Schilf R., Bogner E. Proteasome inhibitor MG132 blocks viral DNA replication and assembly of human cytomegalovirus. FEBS Lett. 2008, 582:666-672.
27. Korioth F., Maul G.G., Plachter B., Stamminger T., Frey J. The nuclear domain 10 (ND10) is disrupted by the human cytomegalovirus gene product IE1. Exp. Cell Res. 1996, 229:155-158.
28. Lallemand-Breitenbach V., de The H. PML nuclear bodies. Cold Spring Harb. Perspect. Biol. 2010, 2:a000661.
29. Lallemand-Breitenbach V., Zhu J., Puvion F., Koken M., Honore N., Doubeikovsky A., Duprez E., Pandolfi P.P., Puvion E., Freemont P., de T.H. Role of promyelocytic leukemia (PML) sumolation in nuclear body formation, 11S proteasome recruitment, and As2O3-induced PML or PML/retinoic acid receptor alpha degradation. J. Exp. Med. 2001, 193:1361-1371.
30. Lavau C., Marchio A., Fagioli M., Jansen J., Falini B., Lebon P., Grosveld F., Pandolfi P.P., Pelicci P.G., Dejean A. The acute promyelocytic leukaemia-associated PML gene is induced by interferon. Oncogene 1995, 11:871-876.
31. Lee H.R., Kim D.J., Lee J.M., Choi C.Y., Ahn B.Y., Hayward G.S., Ahn J.H. 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. 2004, 78:6527-6542.
32. Lukashchuk V., McFarlane S., Everett R.D., Preston C.M. Human cytomegalovirus protein pp71 displaces the chromatin-associated factor ATRX from nuclear domain 10 at early stages of infection. J. Virol. 2008, 82:12543-12554.
33. Mangeat B., Turelli P., Caron G., Friedli M., Perrin L., Trono D. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 2003, 424:99-103.
34. Marshall K.R., Rowley K.V., Rinaldi A., Nicholson I.P., Ishov A.M., Maul G.G., Preston C.M. Activity and intracellular localization of the human cytomegalovirus protein pp71. J. Gen. Virol. 2002, 83:1601-1612.
35. Maul G.G. Nuclear domain 10, the site of DNA virus transcription and replication. Bioessays 1998, 20:660-667.
36. Maul G.G., Yu E., Ishov A.M., Epstein A.L. Nuclear domain 10 (ND10) associated proteins are also present in nuclear bodies and redistribute to hundreds of nuclear sites after stress. J. Cell Biochem. 1995, 59:498-513.
37. Muller S., Dejean A. Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption. J. Virol. 1999, 73:5137-5143.
38. Penkert R.R., Kalejta R.F. Nuclear localization of tegument-delivered pp71 in human cytomegalovirus infected cells is facilitated by one or more factor present in terminally differentiated fibroblasts. J. Virol. 2010.
39. Preston C.M., Nicholl M.J. Role of the cellular protein hDaxx in human cytomegalovirus immediate-early gene expression. J. Gen. Virol. 2006, 87:1113-1121.
40. Reeves M.B., Sinclair J.H. Analysis of latent viral gene expression in natural and experimental latency models of human cytomegalovirus and its correlation with histone modifications at a latent promoter. J. Gen. Virol. 2010, 91:599-604.
41. Reeves M.B., MacAry P.A., Lehner P.J., Sissons J.G., Sinclair J.H. Latency, chromatin remodeling, and reactivation of human cytomegalovirus in the dendritic cells of healthy carriers. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:4140-4145.
42. Reeves M., Woodhall D., Compton T., Sinclair J. Human cytomegalovirus IE72 protein interacts with the transcriptional repressor hDaxx to regulate LUNA gene expression during lytic infection. J. Virol. 2010, 84:7185-7194.
43. Roy C.R., Mocarski E.S. Pathogen subversion of cell-intrinsic innate immunity. Nat. Immunol. 2007, 8:1179-1187.
44. Saffert R.T., Kalejta R.F. 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. 2006, 80:3863-3871.
45. Saffert R.T., Kalejta R.F. Human cytomegalovirus gene expression is silenced by Daxx-mediated intrinsic immune defense in model latent infections established in vitro. J. Virol. 2007, 81:9109-9120.
46. Saffert R.T., Penkert R.R., Kalejta R.F. Cellular and viral control over the initial events of human cytomegalovirus experimental latency in CD34+ cells. J. Virol. 2010, 84:5594-5604.
47. Sakuma R., Mael A.A., Ikeda Y. Alpha interferon enhances TRIM5alpha-mediated antiviral activities in human and rhesus monkey cells. J. Virol. 2007, 81:10201-10206.
48. Salomoni P., Pandolfi P.P. The role of PML in tumor suppression. Cell 2002, 108:165-170.
49. Salsman J., Zimmerman N., Chen T., Domagala M., Frappier L. Genome-wide screen of three herpesviruses for protein subcellular localization and alteration of PML nuclear bodies. PLoS Pathog. 2008, 4:e1000100.
50. Schierling K., Stamminger T., Mertens T., Winkler M. Human cytomegalovirus tegument proteins ppUL82 (pp71) and ppUL35 interact and cooperatively activate the major immediate-early enhancer. J. Virol. 2004, 78:9512-9523.
51. Seeler J.S., Marchio A., Sitterlin D., Transy C., Dejean A. Interaction of SP100 with HP1 proteins: a link between the promyelocytic leukemia-associated nuclear bodies and the chromatin compartment. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:7316-7321.
52. Shen T.H., Lin H.K., Scaglioni P.P., Yung T.M., Pandolfi P.P. The mechanisms of PML-nuclear body formation. Mol. Cell 2006, 24:331-339.
53. Sinclair J. Chromatin structure regulates human cytomegalovirus gene expression during latency, reactivation and lytic infection. Biochim. Biophys. Acta 2010, 1799:286-295.
54. Stinski M.F., Meier J.L. Immediate-early viral gene regulation and function. Human Herpesviruses-Biology, Therapy and Immunoprophylaxis 2007, 241-263. Cambridge University Press, Cambridge, UK. A. Armin, G. Campadelli-Fiume, E. Mocarski, P.S. Moore, B. Roizman, R. Whitley, K. Yamanishi (Eds.).
55. Stremlau M., Owens C.M., Perron M.J., Kiessling M., Autissier P., Sodroski J. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 2004, 427:848-853.
56. Takahashi Y., Lallemand-Breitenbach V., Zhu J., de T.H. PML nuclear bodies and apoptosis. Oncogene 2004, 23:2819-2824.
57. Takeuchi H., Matano T. Host factors involved in resistance to retroviral infection. Microbiol. Immunol. 2008, 52:318-325.
58. Tanaka Y., Marusawa H., Seno H., Matsumoto Y., Ueda Y., Kodama Y., Endo Y., Yamauchi J., Matsumoto T., Takaori-Kondo A., Ikai I., Chiba T. Anti-viral protein APOBEC3G is induced by interferon-alpha stimulation in human hepatocytes. Biochem. Biophys. Res. Commun. 2006, 341:314-319.
59. Tavalai N., Stamminger T. New insights into the role of the subnuclear structure ND10 for viral infection. Biochim. Biophys. Acta 2008, 1783:2207-2221.
60. Tavalai N., Stamminger T. Interplay between herpesvirus infection and host defense by PML nuclear bodies. Viruses 2009, 1:1240-1264.
61. Tavalai N., Papior P., Rechter S., Leis M., Stamminger T. Evidence for a role of the cellular ND10 protein PML in mediating intrinsic immunity against human cytomegalovirus infections. J. Virol. 2006, 80:8006-8018.
62. Tavalai N., Papior P., Rechter S., Stamminger T. Nuclear domain 10 components promyelocytic leukemia protein and hDaxx independently contribute to an intrinsic antiviral defense against human cytomegalovirus infection. J. Virol. 2008, 82:126-137.
63. Torok D., Ching R.W., Bazett-Jones D.P. PML nuclear bodies as sites of epigenetic regulation. Front. Biosci. 2009, 14:1325-1336.
64. Van Damme E., Laukens K., Dang T.H., Van Ostade X. A manually curated network of the PML nuclear body interactome reveals an important role for PML-NBs in SUMOylation dynamics. Int. J. Biol. Sci. 2010, 6:51-67.
65. Wilcox K.W., Sheriff S., Isaac A., Taylor J.L. SP100B is a repressor of gene expression. J. Cell Biochem. 2005, 95:352-365.
66. Wilkinson G.W., Kelly C., Sinclair J.H., Rickards C. Disruption of PML-associated nuclear bodies mediated by the human cytomegalovirus major immediate early gene product. J. Gen. Virol. 1998, 79(Pt 5):1233-1245.
67. Woodhall D.L., Groves I.J., Reeves M.B., Wilkinson G., Sinclair J.H. Human Daxx-mediated repression of human cytomegalovirus gene expression correlates with a repressive chromatin structure around the major immediate early promoter. J. Biol. Chem. 2006, 281:37652-37660.
68. Wu W.S., Vallian S., Seto E., Yang W.M., Edmondson D., Roth S., Chang K.S. The growth suppressor PML represses transcription by functionally and physically interacting with histone deacetylases. Mol. Cell Biol. 2001, 21:2259-2268.
69. Xu Y., Ahn J.H., Cheng M., apRhys C.M., Chiou C.J., Zong J., Matunis M.J., Hayward G.S. Proteasome-independent disruption of PML oncogenic domains (PODs), but not covalent modification by SUMO-1, is required for human cytomegalovirus immediate-early protein IE1 to inhibit PML-mediated transcriptional repression. J. Virol. 2001, 75:10683-10695.
70. Zhong S., Muller S., Ronchetti S., Freemont P.S., Dejean A., Pandolfi P.P. Role of SUMO-1-modified PML in nuclear body formation. Blood 2000, 95:2748-2753.
71. Zhong S., Salomoni P., Pandolfi P.P. The transcriptional role of PML and the nuclear body. Nat. Cell Biol. 2000, 2:E85-E90.