Cyclin-dependent kinase activity controls the onset of the HCMV lytic cycle

PLoS Pathogens

Volumn 6, Issue 9, 2010, Pages

  Zydek, Martin ^a,b   Hagemeier, Christian ^a   Wiebusch, Lüder ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; PROTEIN P53; ROSCOVITINE; ANTINEOPLASTIC ANTIBIOTIC; DOXORUBICIN; IMMEDIATE EARLY PROTEIN;

ARTICLE; CANCER CELL; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; DNA REPLICATION; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENOTOXICITY; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IMMEDIATE EARLY GENE; LATENT VIRUS INFECTION; LOW DRUG DOSE; NONHUMAN; SIGNAL TRANSDUCTION; STRESS; TERATOCARCINOMA; CELL CYCLE; CYTOMEGALOVIRUS; DRUG ANTAGONISM; DRUG EFFECT; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PHYSIOLOGY; RADIATION EXPOSURE; ULTRAVIOLET RADIATION; VIROLOGY; VIRUS ACTIVATION; VIRUS LATENCY; VIRUS REPLICATION; WESTERN BLOTTING;

HUMAN HERPESVIRUS 5;

ANTIBIOTICS, ANTINEOPLASTIC; BLOTTING, WESTERN; CELL CYCLE; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DNA REPLICATION; DOXORUBICIN; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMEDIATE-EARLY PROTEINS; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS; VIRUS ACTIVATION; VIRUS LATENCY; VIRUS REPLICATION;

EID: 78149343945     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001096     Document Type: Article

References (68)

1. Mocarski ES, Shenk T, Pass RF (2007) Cytomegaloviruses. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE, eds. Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA. pp 2701-2772.
2. Meier JL, Stinski MF (2006) Major immediate-early enhancer and its gene products. In Cytomegaloviruses: Molecular Biology and Immunology ed. Reddehase M, ed. Norfolk: Caister Academic Press. pp 151-166.
3. Bego M, Maciejewski J, Khaiboullina S, Pari G, St Jeor S (2005) Characterization of an antisense transcript spanning the UL81-82 locus of human cytomegalovirus. J Virol 79: 11022-11034.
4. Kondo K, Xu J, Mocarski ES (1996) Human cytomegalovirus latent gene expression in granulocyte-macrophage progenitors in culture and in seropositive individuals. Proc Natl Acad Sci U S A 93: 11137-11142.
5. Petrucelli A, Rak M, Grainger L, Goodrum F (2009) Characterization of a novel Golgi apparatus-localized latency determinant encoded by human cytomegalovirus. J Virol 83: 5615-5629.
6. Jenkins C, Abendroth A, Slobedman B (2004) A novel viral transcript with homology to human interleukin-10 is expressed during latent human cytomegalovirus infection. J Virol 78: 1440-1447.
7. Keller MJ, Wu AW, Andrews JI, McGonagill PW, Tibesar EE, et al. (2007) Reversal of human cytomegalovirus major immediate-early enhancer/promoter silencing in quiescently infected cells via the cyclic AMP signaling pathway. J Virol 81: 6669-6681.
8. Yuan J, Liu X, Wu AW, McGonagill PW, Keller MJ, et al. (2009) Breaking human cytomegalovirus major immediate-early gene silence by vasoactive intestinal peptide stimulation of the protein kinase A-CREB-TORC2 signaling cascade in human pluripotent embryonal NTera2 cells. J Virol 83: 6391-6403.
9. Reeves MB, MacAry PA, Lehner PJ, Sissons JG, Sinclair JH (2005) Latency, chromatin remodeling, and reactivation of human cytomegalovirus in the dendritic cells of healthy carriers. Proc Natl Acad Sci U S A 102: 4140-4145.
10. Grillone LR, Lanz R (2001) Fomivirsen. Drugs Today (Barc) 37: 245-255.
11. Salvant BS, Fortunato EA, Spector DH (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.
12. Fortunato EA, Sanchez V, Yen JY, Spector DH (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.
13. Wiebusch L, Neuwirth A, Grabenhenrich L, Voigt S, Hagemeier C (2008) Cell cycle-independent expression of immediate-early gene 3 results in G1 and G2 arrest in murine cytomegalovirus-infected cells. J Virol 82: 10188-10198.
14. Nayak BK, Das GM (2002) Stabilization of p53 and transactivation of its target genes in response to replication blockade. Oncogene 21: 7226-7229.
15. Byun TS, Pacek M, Yee MC, Walter JC, Cimprich KA (2005) Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev 19: 1040-1052.
16. Levine AJ, Oren M (2009) The first 30 years of p53: growing ever more complex. Nat Rev Cancer 9: 749-758.
17. Wiebusch L, Hagemeier C (2010) P53 and p21 dependent premature APC/C-Cdh1 activation is part of the long term response to genotoxic stress. Oncogene 29: 3477-3489.
18. Brooks CL, Gu W (2006) p53 ubiquitination: Mdm2 and beyond. Mol Cell 21: 307-315.
19. Abbas T, Dutta A (2009) p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 9: 400-414.
20. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, et al. (1998) Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282: 1497-1501.
21. Rosenke K, Fortunato EA (2004) Bromodeoxyuridine-labeled viral particles as a tool for visualization of the immediate-early events of human cytomegalovirus infection. J Virol 78: 7818-7822.
22. Sanchez V, McElroy AK, Yen J, Tamrakar S, Clark CL, et al. (2004) Cyclin-dependent kinase activity is required at early times for accurate processing and accumulation of the human cytomegalovirus UL122-123 and UL37 immediate-early transcripts and at later times for virus production. J Virol 78: 11219-11232.
23. Tamrakar S, Kapasi AJ, Spector DH (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.
24. Kapasi AJ, Spector DH (2008) Inhibition of the cyclin-dependent kinases at the beginning of 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.
25. Savio M, Cerri M, Cazzalini O, Perucca P, Stivala LA, et al. (2006) Replication-dependent DNA damage response triggered by roscovitine induces an uncoupling of DNA replication proteins. Cell Cycle 5: 2153-2159.
26. Wesierska-Gadek J, Schmid G (2006) Dual action of the inhibitors of cyclin-dependent kinases: targeting of the cell-cycle progression and activation of wild-type p53 protein. Expert Opin Investig Drugs 15: 23-38.
27. Dosa R, Burian K, Gonczol E (2005) Human cytomegalovirus latency is associated with the state of differentiation of the host cells: an in vitro model in teratocarcinoma cells. Acta Microbiol Immunol Hung 52: 397-406.
28. Gonczol E, Andrews PW, Plotkin SA (1984) Cytomegalovirus replicates in differentiated but not in undifferentiated human embryonal carcinoma cells. Science 224: 159-161.
29. Andrews PW, Gonczol E, Plotkin SA, Dignazio M, Oosterhuis JW (1986) Differentiation of TERA-2 human embryonal carcinoma cells into neurons and HCMV permissive cells. Induction by agents other than retinoic acid. Differentiation 31: 119-126.
30. LaFemina R, Hayward GS (1986) Constitutive and retinoic acid-inducible expression of cytomegalovirus immediate-early genes in human teratocarcinoma cells. J Virol 58: 434-440.
31. Nelson JA, Groudine M (1986) Transcriptional regulation of the human cytomegalovirus major immediate-early gene is associated with induction of DNase I-hypersensitive sites. Mol Cell Biol 6: 452-461.
32. Sinclair J (2008) Human cytomegalovirus: Latency and reactivation in the myeloid lineage. J Clin Virol 41: 180-185.
33. Meier JL (2001) Reactivation of the human cytomegalovirus major immediate-early regulatory region and viral replication in embryonal NTera2 cells: role of trichostatin A, retinoic acid, and deletion of the 21-base-pair repeats and modulator. J Virol 75: 1581-1593.
34. Murphy JC, Fischle W, Verdin E, Sinclair JH (2002) Control of cytomegalovirus lytic gene expression by histone acetylation. Embo J 21: 1112-1120.
35. Kalaszczynska I, Geng Y, Iino T, Mizuno S, Choi Y, et al. (2009) Cyclin A is redundant in fibroblasts but essential in hematopoietic and embryonic stem cells. Cell 138: 352-365.
36. Welm AL, Timchenko NA, Ono Y, Sorimachi H, Radomska HS, et al. (2002) C/EBPalpha is required for proteolytic cleavage of cyclin A by calpain 3 in myeloid precursor cells. J Biol Chem 277: 33848-33856.
37. Baldassarre G, Boccia A, Bruni P, Sandomenico C, Barone MV, et al. (2000) Retinoic acid induces neuronal differentiation of embryonal carcinoma cells by reducing proteasome-dependent proteolysis of the cyclin-dependent inhibitor p27. Cell Growth Differ 11: 517-526.
38. 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.
39. 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.
40. Rechter S, Scott GM, Eickhoff J, Zielke K, Auerochs S, et al. (2009) Cyclin-dependent Kinases Phosphorylate the Cytomegalovirus RNA Export Protein pUL69 and Modulate Its Nuclear Localization and Activity. J Biol Chem 284: 8605-8613.
41. Sanchez V, Spector DH (2006) Cyclin-dependent kinase activity is required for efficient expression and posttranslational modification of human cytomegalovirus proteins and for production of extracellular particles. J Virol 80: 5886-5896.
42. Sanchez V, Mahr JA, Orazio NI, Spector DH (2007) Nuclear export of the human cytomegalovirus tegument protein pp65 requires cyclin-dependent kinase activity and the Crm1 exporter. J Virol 81: 11730-11736.
43. Bresnahan WA, Boldogh I, Chi P, Thompson EA, Albrecht T (1997) Inhibition of cellular Cdk2 activity blocks human cytomegalovirus replication. Virology 231: 239-247.
44. Hertel L, Chou S, Mocarski ES (2007) Viral and cell cycle-regulated kinases in cytomegalovirus-induced pseudomitosis and replication. PLoS Pathog 3: e6.
45. Marschall M, Stamminger T (2009) Molecular targets for antiviral therapy of cytomegalovirus infections. Future Microbiol 4: 731-742.
46. Schang LM, St Vincent MR, Lacasse JJ (2006) Five years of progress on cyclin-dependent kinases and other cellular proteins as potential targets for antiviral drugs. Antivir Chem Chemother 17: 293-320.
47. Harper JW, Elledge SJ, Keyomarsi K, Dynlacht B, Tsai LH, et al. (1995) Inhibition of cyclin-dependent kinases by p21. Mol Biol Cell 6: 387-400.
48. Wesierska-Gadek J, Krystof V (2009) Selective cyclin-dependent kinase inhibitors discriminating between cell cycle and transcriptional kinases: future reality or utopia? Ann N Y Acad Sci 1171: 228-241.
49. Yam CH, Fung TK, Poon RY (2002) Cyclin A in cell cycle control and cancer. Cell Mol Life Sci 59: 1317-1326.
50. Jault FM, Jault JM, Ruchti F, Fortunato EA, Clark C, et al. (1995) Cytomegalovirus infection induces high levels of cyclins, phosphorylated Rb, and p53, leading to cell cycle arrest. J Virol 69: 6697-6704.
51. Shlapobersky M, Sanders R, Clark C, Spector DH (2006) Repression of HMGA2 gene expression by human cytomegalovirus involves the IE2 86-kilodalton protein and is necessary for efficient viral replication and inhibition of cyclin A transcription. J Virol 80: 9951-9961.
52. Wiebusch L, Hagemeier C (2001) The human cytomegalovirus immediate early 2 protein dissociates cellular DNA synthesis from cyclin-dependent kinase activation. Embo J 20: 1086-1098.
53. Hsu CY, Mechali F, Bonne-Andrea C (2007) Nucleocytoplasmic shuttling of bovine papillomavirus E1 helicase downregulates viral DNA replication in S phase. J Virol 81: 384-394.
54. Maddika S, Panigrahi S, Wiechec E, Wesselborg S, Fischer U, et al. (2009) Unscheduled Akt-triggered activation of cyclin-dependent kinase 2 as a key effector mechanism of apoptin's anticancer toxicity. Mol Cell Biol 29: 1235-1248.
55. Kalejta RF (2008) Functions of human cytomegalovirus tegument proteins prior to immediate early gene expression. Curr Top Microbiol Immunol 325: 101-115.
56. 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.
57. Munger J, Yu D, Shenk T (2006) UL26-deficient human cytomegalovirus produces virions with hypophosphorylated pp28 tegument protein that is unstable within newly infected cells. J Virol 80: 3541-3548.
58. Stamminger T, Gstaiger M, Weinzierl K, Lorz K, Winkler M, et al. (2002) Open reading frame UL26 of human cytomegalovirus encodes a novel tegument protein that contains a strong transcriptional activation domain. J Virol 76: 4836-4847.
59. 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.
60. Schierling K, Stamminger T, Mertens T, Winkler M (2004) Human cytomegalovirus tegument proteins ppUL82 (pp71) and ppUL35 interact and cooperatively activate the major immediate-early enhancer. J Virol 78: 9512-9523.
61. Schierling K, Buser C, Mertens T, Winkler M (2005) Human cytomegalovirus tegument protein ppUL35 is important for viral replication and particle formation. J Virol 79: 3084-3096.
62. Bechtel JT, Shenk T (2002) Human cytomegalovirus UL47 tegument protein functions after entry and before immediate-early gene expression. J Virol 76: 1043-1050.
63. Wang SK, Duh CY, Wu CW (2004) Human cytomegalovirus UL76 encodes a novel virion-associated protein that is able to inhibit viral replication. J Virol 78: 9750-9762.
64. Daksis JI, Preston CM (1992) Herpes simplex virus immediate early gene expression in the absence of transinduction by Vmw65 varies during the cell cycle. Virology 189: 196-202.
65. Staib F, Robles AI, Varticovski L, Wang XW, Zeeberg BR, et al. (2005) The p53 tumor suppressor network is a key responder to microenvironmental components of chronic inflammatory stress. Cancer Res 65: 10255-10264.
66. Mallette FA, Ferbeyre G (2007) The DNA damage signaling pathway connects oncogenic stress to cellular senescence. Cell Cycle 6: 1831-1836.
67. Soderberg-Naucler C (2008) HCMV microinfections in inflammatory diseases and cancer. J Clin Virol 41: 218-223.
68. 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.