Proteasome subunits relocalize during human cytomegalovirus infection, and proteasome activity is necessary for efficient viral gene transcription

Journal of Virology

Volumn 84, Issue 6, 2010, Pages 3079-3093

  Tran, Karen ^a   Mahr, Jeffrey A ^a   Spector, Deborah H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME;

ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; DNA REPLICATION; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RNA TRANSCRIPTION; VIRUS GENE;

CELLS, CULTURED; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DNA REPLICATION; DNA, VIRAL; FIBROBLASTS; GENES, VIRAL; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SUBUNITS; TRANSCRIPTION, GENETIC; VIRUS REPLICATION;

HUMAN HERPESVIRUS 5;

EID: 77649093465     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02236-09     Document Type: Article

References (63)

1. Ahn, J.-H., W.-J. Jang, and G. S. Hayward. 1999. The human cytomegalovirus IE2 and UL112-113 proteins accumulate in viral DNA replication compartments that initiate from the periphery of promyelocytic leukemia protein-associated nuclear bodies (PODs or ND10). J. Virol. 73:10458- 10471.
2. Bajorek, M., and M. H. Glickman. 2004. Keepers at the final gates: regulatory complexes and gating of the proteasome channel. Cell. Mol. Life Sci. 61:1579-1588.
3. Banks, L., D. Pim, and M. Thomas. 2003. Viruses and the 26S proteasome: hacking into destruction. Trends Biochem. Sci. 28:452-459.
4. Biswas, N., V. Sanchez, and D. H. Spector. 2003. Human cytomegalovirus infection leads to accumulation of geminin and inhibition of the licensing of cellular DNA replication. J. Virol. 77:2369-2376.
5. Blanchette, P., and P. E. Branton. 2009. Manipulation of the ubiquitin-proteasome pathway by small DNA tumor viruses. Virology 384:317-323.
6. Burch, A. D., and S. K. Weller. 2005. Herpes simplex virus type 1 DNA polymerase requires the mammalian chaperone hsp90 for proper localization to the nucleus. J. Virol. 79:10740-10749.
7. Burch, A. D., and S. K. Weller. 2004. Nuclear sequestration of cellular chaperone and proteasomal machinery during herpes simplex virus type 1 infection. J. Virol. 78:7175-7185.
8. Cantrell, S. R., and W. A. Bresnahan. 2005. Interaction between the human cytomegalovirus UL82 gene product (pp71) and hDaxx regulates immediateearly gene expression and viral replication. J. Virol. 79:7792-7802.
9. Collins, G. A., and W. P. Tansey. 2006. The proteasome: a utility tool for transcription? Curr. Opin. Genet. Dev. 16:197-202.
10. Dai-Ju, J. Q., L. Li, L. A. Johnson, and R. M. Sandri-Goldin. 2006. ICP27 interacts with the C-terminal domain of RNA polymerase II and facilitates its recruitment to herpes simplex virus 1 transcription sites, where it undergoes proteasomal degradation during infection. J. Virol. 80:3567-3581.
11. Demartino, G. N., and T. G. Gillette. 2007. Proteasomes: machines for all reasons. Cell 129:659-662.
12. Dittmer, D., and E. S. Mocarski. 1997. Human cytomegalovirus infection inhibits G1/S transition. J. Virol. 71:1629-1634.
13. Ezhkova, E., and W. P. Tansey. 2004. Proteasomal ATPases link ubiquitylation of histone H2B to methylation of histone H3. Mol. Cell 13:435-442.
14. Finley, D. 2009. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78:477-513.
15. Fortunato, E. A., V. Sanchez, J. Y. Yen, and D. H. Spector. 2002. Infection of cells with human cytomegalovirus during S phase results in a blockade to immediate-early gene expression that can be overcome by inhibition of the proteasome. J. Virol. 76:5369-5379.
16. Fortunato, E. A., and D. H. Spector. 1998. p53 and RPA are sequestered in viral replication centers in the nuclei of cells infected with human cytomegalovirus. J. Virol. 72:2033-2039.
17. Fraser, K. A., and S. A. Rice. 2005. Herpes simplex virus type 1 infection leads to loss of serine-2 phosphorylation on the carboxyl-terminal domain of RNA polymerase II. J. Virol. 79:11323-11334.
18. Gao, G., and H. Luo. 2006. The ubiquitin-proteasome pathway in viral infections. Can. J. Physiol. Pharmacol. 84:5-14.
19. Glickman, M. H., and A. Ciechanover. 2002. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82:373-428.
20. Hegde, A. N., and S. C. Upadhya. 2006. Proteasome and transcription: a destroyer goes into construction. Bioessays 28:235-239.
21. Hirsch, C., and H. Ploegh. 2000. Intracellular targeting of the proteasome. Trends Cell Biol. 10:268-272.
22. 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.
23. Hwang, J., 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.
24. Ishov, A. M., and G. G. Maul. 1996. The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. J. Cell Biol. 134:815-826.
25. 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.
26. 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.
27. Kalejta, R. F., J. T. Bechtel, and T. Shenk. 2003. Human cytomegalovirus pp71 stimulates cell cycle progression by inducing the proteasome-dependent degradation of the retinoblastoma family of tumor suppressors. Mol. Cell. Biol. 23:1885-1895.
28. Kalejta, R. F., and T. Shenk. 2003. Proteasome-dependent, ubiquitin-independent degradation of the Rb family of tumor suppressors by the human cytomegalovirus pp71 protein. Proc. Natl. Acad. Sci. U. S. A. 100:3263-3268.
29. Kaneko, T., J. Hamazaki, S.-I. Iemura, K. Sasaki, K. Furuyama, T. Natsume, K. Tanaka, and S. Murata. 2009. Assembly pathway of the mammalian proteasome base subcomplex is mediated by multiple specific chaperones. Cell 137:914-925.
30. Kapasi, A. J., and D. H. Spector. 2008. Inhibition of the cyclin-dependent kinases at the beginning of the human cytomegalovirus infection specifically alters the levels and localization of the RNA polymerase II carboxyl-terminal domain kinases cdk9 and cdk7 at the viral transcriptosome. J. Virol. 82:394-407.
31. Kaspari, M., N. Tavalai, T. Stamminger, A. Zimmermann, R. Schilf, and E. Bogner. 2008. Proteasome inhibitor MG132 blocks viral DNA replication and assembly of human cytomegalovirus. FEBS Lett. 582:666-672.
32. Kinyamu, H. K., W. N. Jefferson, and T. K. Archer. 2008. Intersection of nuclear receptors and the proteasome on the epigenetic landscape. Environ. Mol. Mutagen. 49:83-95.
33. Lassot, I., D. Latreille, E. Rousset, M. Sourisseau, L. K. Linares, C. Chable-Bessia, O. Coux, M. Benkirane, and R. E. Kiernan. 2007. The proteasome regulates HIV-1 transcription by both proteolytic and nonproteolytic mechanisms. Mol. Cell 25:369-383.
34. Lee, D., E. Ezhkova, B. Li, S. G. Pattenden, W. P. Tansey, and J. L. Workman. 2005. The proteasome regulatory particle alters the SAGA coactivator to enhance its interactions with transcriptional activators. Cell 123:423-436.
35. Li, L., L. A. Johnson, J. Q. Dai-Ju, and R. M. Sandri-Goldin. 2008. Hsc70 focus formation at the periphery of HSV-1 transcription sites requires ICP27. PLoS One 3:e1491.
36. Livingston, C. M., N. A. Deluca, D. E. Wilkinson, and S. K. Weller. 2008. Oligomerization of ICP4 and rearrangement of heat shock proteins may be important for herpes simplex virus type 1 prereplicative site formation. J. Virol. 82:6324-6336.
37. Livingston, C. M., M. F. Ifrim, A. E. Cowan, and S. K. Weller. 2009. Virusi-nduced chaperone-enriched (VICE) domains function as nuclear protein quality control centers during HSV-1 infection. PLoS Pathog. 5:e1000619.
38. Luo, M. H., K. Rosenke, K. Czornak, and E. A. Fortunato. 2007. Human cytomegalovirus disrupts both ataxia telangiectasia mutated protein (ATM)-and ATM-Rad3-related kinase-mediated DNA damage responses during lytic infection. J. Virol. 81:1934-1950.
39. 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.
40. Mittenberg, A., T. Moiseeva, and N. Barlev. 2008. Role of proteasomes in transcription and their regulation by covalent modifications. Front. Biosci. 13:7184.
41. Mocarski, E. S., T. Shenk, and R. F. Pass. 2007. Cytomegaloviruses, p. 2701-2772. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 5th ed., vol. 2. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia, PA.
42. Nelbock, P., P. J. Dillon, A. Perkins, and C. A. Rosen. 1990. A cDNA for a protein that interacts with the human immunodeficiency virus tat transactivator. Science 248:1650-1653.
43. Ohana, B., P. A. Moore, S. M. Ruben, C. D. Southgate, M. R. Green, and C. A. Rosen. 1993. The type 1 human immunodeficiency virus Tat binding protein is a transcriptional activator belonging to an additional family of evolutionary conserved genes. Proc. Natl. Acad. Sci. U. S. A. 90:138-142.
44. Penfold, M. E., and E. S. Mocarski. 1997. Formation of cytomegalovirus DNA replication compartments defined by localization of viral proteins and DNA synthesis. Virology 239:46-61.
45. Pickart, C. M., and R. E. Cohen. 2004. Proteasomes and their kin: proteases in the machine age. Nat. Rev. Mol. Cell Biol. 5:177-187.
46. Prösch, S., C. Priemer, C. Höflich, C. Liebenthaf, N. Babel, D. H. Krüger, and H.-D. Volk. 2003. Proteasome inhibitors: a novel tool to suppress human cytomegalovirus replication and virus-induced immune modulation. Antivir. Ther. (London) 8:555-567.
47. Rasti, M., R. J. A. Grand, A. F. Yousef, M. Shuen, J. S. Mymryk, P. H. Gallimore, and A. S. Turnell. 2006. Roles for APIS and the 20S proteasome in adenovirus E1A-dependent transcription. EMBO J. 25:2710-2722.
48. Rechsteiner, M., and C. P. Hill. 2005. Mobilizing the proteolytic machine: cell biological roles of proteasome activators and inhibitors. Trends Cell Biol. 15:27-33.
49. Reed, S. H., and T. G. Gillette. 2007. Nucleotide excision repair and the ubiquitin proteasome pathway: do all roads lead to Rome? DNA Repair (Amsterdam) 6:149-156.
50. Sadanari, H., J. Tanaka, Z. Li, R. Yamada, K. Matsubara, and T. Murayama. 2009. Proteasome inhibitor differentially regulates expression of the major immediate early genes of human cytomegalovirus in human central nervous system-derived cell lines. Virus Res. 142:68-77.
51. Saffert, R. T., and R. F. Kalejta. 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.
52. Salvant, B. S., E. A. Fortunato, and D. H. Spector. 1998. Cell cycle dysregulation by human cytomegalovirus: influence of the cell cycle phase at the time of infection and effects on cyclin transcription. J. Virol. 72:3729-3741.
53. Sanchez, V., A. K. McElroy, and D. H. Spector. 2003. Mechanisms governing maintenance of cdk1/cyclin B1 kinase activity in cells infected with human cytomegalovirus. J. Virol. 77:13214-13224.
54. Shackelford, J., and J. S. Pagano. 2005. Targeting of host-cell ubiquitin pathways by viruses. Essays Biochem. 41:139-156.
55. Shibuya, H., K. Irie, J. Ninomiya-Tsuji, M. Goebl, T. Taniguchi, and K. Matsumoto. 1992. A new human gene encoding a positive modulator of HIV Tat-mediated transactivation. Nature 357:700-702.
56. Tamashiro, J. C., L. J. Hock, and D. H. Spector. 1982. Construction of a cloned library of the EcoRI fragments from the human cytomegalovirus genome (strain AD169). J. Virol. 42:547-557.
57. Tamrakar, S., A. J. Kapasi, and D. H. Spector. 2005. Human cytomegalovirus infection induces specific hyperphosphorylation of the carboxyl-terminal domain of the large subunit of RNA polymerase II that is associated with changes in the abundance, activity, and localization of cdk9 and cdk7. J. Virol. 79:15477-15493.
58. Tortorella, D., B. Gewurz, D. Schust, M. Furman, and H. Ploegh. 2000. Down-regulation of MHC class I antigen presentation by HCMV; lessons for tumor immunology. Immunol. Invest. 29:97-100.
59. Tran, K., J. A. Mahr, J. Choi, J. G. Teodoro, M. R. Green, and D. H. Spector. 2008. Accumulation of substrates of the anaphase-promoting complex (APC) during human cytomegalovirus infection is associated with the phosphorylation of Cdh1 and the dissociation and relocalization of the APC subunits. J. Virol. 82:529-537.
60. White, E. A., C. L. Clark, V. Sanchez, and D. H. Spector. 2004. Small internal deletions in the human cytomegalovirus IE2 gene result in nonviable recombinant viruses with differential defects in viral gene expression. J. Virol. 78:1817-1830.
61. Wiebusch, L., M. Bach, R. Uecker, and C. Hagemeier. 2005. Human cytomegalovirus inactivates the G0/G1-APC/C ubiquitin ligase by Cdh1 dissociation. Cell Cycle 4:1435-1439.
62. Wiebusch, L., R. Uecker, and C. Hagemeier. 2003. Human cytomegalovirus prevents replication licensing by inhibiting MCM loading onto chromatin. EMBO Rep. 4:42-46.
63. Wing, B. A., and E. S. Huang. 1995. Analysis and mapping of a family of 3′-coterminal transcripts containing coding sequences for human cytomegalovirus open reading frames UL93 through UL99. J. Virol. 69:1521-1531.