Human cytomegalovirus protein pp71 displaces the chromatin-associated factor ATRX from nuclear domain 10 at early stages of infection

Journal of Virology

Volumn 82, Issue 24, 2008, Pages 12543-12554

  Lukashchuk, Vera ^a   McFarlane, Steven ^a   Everett, Roger D ^a   Preston, Chris M ^a  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PROTEIN HDAXX; PROTEIN PP71; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS VECTOR;

ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS; GENE EXPRESSION; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; VIRUS INFECTION; VIRUS REPLICATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE; CELL NUCLEUS; CHROMATIN; CYTOMEGALOVIRUS; DNA HELICASES; GENE DELETION; GENE EXPRESSION REGULATION; HUMANS; NUCLEAR PROTEINS; TIME FACTORS; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 5;

EID: 57349108706     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01215-08     Document Type: Article

References (62)

1. Ahn, J. H., and G. S. Hayward. 2000. Disruption of PML-associated nuclear bodies by IE1 correlates with efficient early stages of viral gene expression and DNA replication in human cytomegalovirus infection. Virology 274:39-55.
2. Ahn, J.-H., and G. S. Hayward. 1997. 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. 71:4599-4613.
3. Argentaro, A., J.-C. Yang, L. Chapman, M. S. Kowalczyk, R. J. Gibbons, D. R. HIggs, D. Neuhaus, and D. Rhodes. 2007. Structural consequences of disease-causing mutations in the ATRX-DNMT3L (ADD) domain of the chromatin-associated protein ATRX. Proc. Natl. Acad. Sci. USA 104:11939-11944.
4. Baldick, C. J., A. Marchini, C. E. Patterson, and T. Shenk. 1997. Human cytomegalovirus tegument protein pp71 (ppUL82) enhances the infectivity of viral DNA and accelerates the infectious cycle. J. Virol. 71:4400-4408.
5. Baumann, C., A. Schmidtmann, K. Muegge, and R. De La Fuente. 2008. Association of ATRX with pericentric heterochromatin and the Y chromosome of neonatal mouse spermatogonia. BMC Mol. Biol. 9:29.
6. Berube, N. G., J. Healy, C. F. Medina, S. Wu, T. Hodgson, M. Jagla, and D. J. Picketts. 2007. Patient mutations alter ATRX targeting to PML nuclear bodies. Eur. J. Hum. Genet. 16:192-201.
7. Bresnahan, W. A., and T. E. Shenk. 2000. UL82 virion protein activates expression of immediate early viral genes in human cytomegalovirus-infected cells. Proc. Natl. Acad. Sci. USA 97:14506- 14511.
8. Cantrell, S. R., and W. A. Bresnahan. 2006. Human cytomegalovirus (HCMV) UL82 gene product (pp71) relieves hDaxx-mediated repression of HCMV replication. J. Virol. 80:6188-6191.
9. Cantrell, S. R., and W. A. Bresnahan. 2005. Interaction between the human cytomegalovirus UL82 gene product (pp71) and hDaxx regulates immediate-early gene expression and viral replication. J. Virol. 79:7792-7802.
10. Chau, N. H., C. D. Vanson, and J. A. Kerry. 1999. Transcriptional regulation of the human cytomegalovirus US11 early gene. J. Virol. 73:863-870.
11. Dolan, A., C. Cunningham, R. D. Hector, A. F. Hassan-Walker, L. Lee, C. Addison, D. J. Dargan, D. J. McGeoch, D. Gatherer, V. C. Emery, P. D. Griffiths, C. Sinzger, B. P. McSharry, G. W. G. Wilkinson, and A. J. Davison. 2004. Genetic content of wild-type human cytomegalovirus. J. Gen. Virol. 85:1301-1312.
12. Everett, R. D. 2001. DNA viruses and viral proteins that interact with PML nuclear bodies. Oncogene 20:7266-7273.
13. Everett, R. D. 2006. Interactions between DNA viruses, ND10 and the DNA damage response. Cell Microbiol. 8:365-374.
14. Everett, R. D., W. C. Earnshaw, J. Findlay, and P. Lomonte. 1999. Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110. EMBO J. 18:1526-1538.
15. Everett, R. D., and J. Murray. 2005. ND10 components relocate to sites associated with herpes simplex virus type 1 nucleoprotein complexes during virus infection. J. Virol. 79:5078-5089.
16. Everett, R. D., J. Murray, A. Orr, and C. M. Preston. 2007. Herpes simplex virus type 1 genomes are associated with ND10 nuclear substructures in quiescently infected human fibroblasts. J. Virol. 81:10991-11004.
17. Everett, R. D., C. Parada, P. Gripon, H. Sirma, and A. Orr. 2008. Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J. Virol. 82:2661-2672.
18. Everett, R. D., S. Rechter, P. Papior, N. Tavalai, T. Stamminger, and A. Orr. 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.
19. Gibbons, R. J., D. J. Picketts, and D. R. Higgs. 1995. Mutations in a putative global transcriptional regulator cause X-linked mental retardation with α-thalassemia (ATR-X syndrome). Cell 80:837-845.
20. Hensel, G. M., H. H. Meyer, I. Buchmann, D. Pommerehne, S. Schmolke, B. Plachter, K. Radsak, and H. F. Kern. 1996. Intracellular localization and expression of the human cytomegalovirus matrix phosphoprotein pp71 (ppUL82): evidence for its translocation into the nucleus. J. Gen. Virol. 77:3087-3097.
21. Hofmann, H., H. Sindre, and T. Stamminger. 2002. Functional interaction between the pp71 protein of human cytomegalovirus and the PML-interacting protein human Daxx. J. Virol. 76:5769-5783.
22. Hollenbach, A. D., C. J. McPherson, E. J. Mientjes, R. Lyengar, and G. Grosveld. 2002. Daxx and histone deacetylase II associate with chromatin through an interaction with core histones and the chromatin-associated protein Dek. J. Cell Sci. 115:3319-3330.
23. Homer, E. G., A. Rinaldi, M. J. Nicholl, and C. M. Preston. 1999. Activation of herpesvirus gene expression by the human cytomegalovirus protein pp71. J. Virol. 73:8512-8518.
24. Hwang, J. W., and R. F. Kalejta. 2007. Proteasome-dependent, ubiquitin-independent degradation of Daxx by the viral pp71 protein in human cytomegalovirus-infected cells. Virology 367:334-338.
25. Ishov, A. M., A. G. Sotnikov, D. Negerov, O. V. Vladimirova, N. Neff, T. Kamitani, E. T. Yeh, J. F. Strauss III, and G. G. Maul. 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. 138:221-234.
26. Ishov, A. M., R. M. Stenberg, and G. G. Maul. 1997. Human cytomegalovirus immediate early interaction with host nuclear structures: definition of an immediate transcript environment. J. Cell Biol. 138:5-16.
27. Ishov, A. M., O. V. Vladimirova, and G. G. Maul. 2002. Daxx-mediated accumulation of human cytomegalovirus tegument protein pp71 at ND10 facilitates initiation of viral infection at these nuclear domains. J. Virol. 76:7705-7712.
28. Ishov, A. M., O. V. Vladimirova, and G. G. Maul. 2004. Heterochromatin and ND10 are cell-cycle regulated and phosphorylation-dependent alternate nuclear sites of the transcription repressor Daxx and SWI/SNF protein ATRX. J. Cell Sci. 117:3807-3820.
29. Kelly, C., R. van Driel, and G. W. G. Wilkinson. 1995. Disruption of PML-associated nuclear bodies during human cytomegalovirus infection. J. Gen. Virol. 76:2887-2893.
30. Korioth, F., G. G. Maul, B. Plachter, T. Stamminger, and J. Frey. 1996. The nuclear domain 10 (ND10) is disrupted by the human cytomegalovirus gene product IE1. Exp. Cell Res. 229:155-158.
31. Lee, H.-R., D.-J. Kim, J.-M. Lee, C. Y. Choi, B.-Y. Ahn, G. S. Hayward, and J.-H. Ahn. 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.
32. Li, H., C. Lieo, J. Zhu, X. Wu, J. O'Neill, E.-J. Park, and J. D. Chen. 2000. Sequestration and inhibition of Daxx-mediated transcriptional repression by PML. Mol. Cell. Biol. 20:1784-1796.
33. Li, R., H. Pei, D. K. Watson, and T. S. Papas. 2000. EAP1/Daxx interacts with ETS1 and represses transcriptional activation of ETS1 target genes. Oncogene 19:745-753.
34. Liu, B., and M. F. Stinski. 1992. Human cytomegalovirus contains a tegument protein that enhances transcription from promoters with upstream ATF and AP-1 cis-acting elements. J. Virol. 66:4434-4444.
35. Marshall, K. R., K. V. Rowley, A. Rinaldi, I. P. Nicholson, A. M. Ishov, G. G. Maul, and C. M. Preston. 2002. Activity and intracellular localization of the human cytomegalovirus protein pp71. J. Gen. Virol. 83:1601-1612.
36. Maul, G. G. 1998. Nuclear domain 10, the site of DNA virus transcription and replication. Bioessays 26:660-667.
37. Maul, G. G., and D. Negerov. 2008. Differences between mouse and human cytomegalovirus interactions with their respective hosts at immediate early times of the replication cycle. Med. Microbiol. Immunol. 197:241-248.
38. Michaelson, J. S. 2000. The Daxx enigma. Apoptosis 5:217-220.
39. Michaelson, J. S., and P. Leder. 2003. RNAi reveals anti-apoptotic and transcriptionally repressive activities of DAXX. J. Cell Sci. 116:345-352.
40. Murphy, J. C., W. Fischle, E. Verdin, and J. H. Sinclair. 2002. Control of cytomegalovirus lytic gene expression by histone acetylation. EMBO J. 21:1112-1120.
41. Nan, X., J. Hou, A. Maclean, J. Nasir, M. J. Lafuente, X. Shu, S. Kriaucionis, and A. Bird. 2007. Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation. Proc. Natl. Acad. Sci. USA 104:2709-2714.
42. Nevels, M., C. Paulus, and T. Shenk. 2004. Human cytomegalovirus immediate-early 1 protein facilitates viral replication by antagonizing histone deacetylation. Proc. Natl. Acad. Sci. USA 101:17234-17239.
43. Pluta, A. F., W. C. Earnshaw, and I. G. Goldberg. 1998. Interphase-specific association of intrinsic centromere protein CENP-C with HDaxx, a death domain-binding protein implicated in Fas-mediated cell death. J. Cell Sci. 111:2029-2041.
44. Preston, C. M., and M. J. Nicholl. 2005. Human cytomegalovirus tegument protein pp71 directs long-term gene expression from quiescent herpes simplex virus genomes. J. Virol. 79:525-535.
45. Preston, C. M., and M. J. Nicholl. 2006. Role of the cellular protein hDaxx in human cytomegalovirus immediate-early gene expression. J. Gen. Virol. 87:1113-1121.
46. Reeves, M. B., P. A. MacAry, P. J. Lehner, J. P. G. Sissons, and J. H. Sinclair. 2005. Latency, chromatin remodeling, and reactivation of human cytomegalovirus in the dendritic cells of healthy carriers. Proc. Natl. Acad. Sci. USA 102:4140-4145.
47. Ritchie, K., C. Seah, J. Moulin, F. Isaac, and N. G. Berube. 2008. Loss of ATRX leads to chromosome cohesion and congressional defects. J. Cell Biol. 180:315-324.
48. Rosenke, K., and E. A. Fortunato. 2004. Bromodeoxyuridine-labeled viral particles as a tool for visualization of the immediate-early events of human cytomegalovirus infection. J. Virol. 78:7818-7822.
49. Saffert, R. T., and R. F. Kalejta. 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.
50. Saffert, R. T., and R. F. Kalejta. 2006. Inactivating a cellular intrinsic 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.
51. Salomoni, P., and A. F. Khelifi. 2006. Daxx: death or survival protein? Trends Cell Biol. 16:97-104.
52. Stuurman, N., A. de Graaf, A. Floore, A. Josso, B. Humbel, L. de Jong, and R. van Driel. 1992. A monoclonal antibody recognizing nuclear matrixassociated nuclear bodies. J. Cell Sci. 101:773-784.
53. Talbot, P., and J. P. Almeida. 1977. Human cytomegalovirus: purification of enveloped virions and dense bodies. J. Gen. Virol. 36:345-349.
54. Tang, J., S. Wu, H. Liu, R. Stratt, O. G. Barak, R. Shiekhatter, D. J. Picketts, and X. Yang. 2004. A novel transcription regulatory complex containing death domain-associated protein and the ATR-X syndrome protein. J. Biol. Chem. 279:20369-20377.
55. Tavalai, N., P. Papior, S. Rechter, M. Leis, and T. Stamminger. 2006. Evidence for a role of the cellular ND10 protein PML in mediating intrinsic immunity against human cytomegalovirus infections. J. Virol. 80:8006-8018.
56. Tavalai, N., P. Papior, S. Rechter, and T. Stamminger. 2008. Nuclear domain 10 components promyelocytic leukaemia protein and hDaxx independently contribute to an intrinsic antiviral defense against human cytomegalovirus infection. J. Virol. 82:126-137.
57. Torii, S., D. A. Egan, R. A. Evans, and J. C. Reed. 1999. Human Daxx regulates Fas-induced apoptosis from nuclear PML oncogenic domains (PODs). EMBO J. 18:6037-6049.
58. Wilkinson, G. W., C. Kelly, J. H. Sinclair, and C. Rickards. 1998. Disruption of PML-associated nuclear bodies mediated by the human cytomegalovirus major immediate early gene product. J. Gen. Virol. 79:1233-1245.
59. Woodhall, D. L., I. J. Groves, M. B. Reeves, G. W. Wilkinson, and J. H. Sinclair. 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.
60. Wright, E., M. Bain, L. Teague, J. Murphy, and J. Sinclair. 2005. Ets-2 repressor factor recruits histone deacetylase to silence human cytomegalovirus immediate-early gene expression in non-permissive cells. J. Gen. Virol. 86:535-544.
61. Xu, Y., J.-H. Ahn, M. Cheng, C. M. apRhys, C.-J. Chiou, J. Zong, M. J. Matunis, and G. S. Hayward. 2001. 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. 75:10683-10695.
62. Xue, Y., R. Gibbons, Z. Yan, D. Yang, T. L. McDowell, S. Sechi, J. Qin, S. Zhou, D. Higgs, and W. Wang. 2003. The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. Proc. Natl. Acad. Sci. USA 100:10635-10640.