Inhibition of human cytomegalovirus immediate-early gene expression by cyclin A2-dependent kinase activity

Journal of Virology

Volumn 86, Issue 17, 2012, Pages 9369-9383

  Oduro, Jennifer D ^a,b   Uecker, Ralf ^a   Hagemeier, Christian ^a   Wiebusch, Lüder ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A2; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYCLIN E; CYCLIN E1; CYCLIN E2; IMMEDIATE EARLY PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENE LOCUS; GENE REPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; HUMAN TISSUE; IMMEDIATE EARLY 1 GENE; IMMEDIATE EARLY 2 GENE; IMMEDIATE EARLY GENE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA PROCESSING; UL37 GENE; UPREGULATION; VIRUS REPLICATION;

ANIMALS; CDC2 PROTEIN KINASE; CELL CYCLE; CELL LINE, TUMOR; CYCLIN A2; CYCLIN-DEPENDENT KINASE 2; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DOWN-REGULATION; GENE EXPRESSION REGULATION, VIRAL; HUMANS; IMMEDIATE-EARLY PROTEINS; MICE; TRANS-ACTIVATORS;

HUMAN HERPESVIRUS 5; MURINAE;

EID: 84866148817     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.07181-11     Document Type: Article

References (81)

1. Adair R, Liebisch GW, Colberg-Poley AM. 2003. Complex alternative processing of human cytomegalovirus UL37 pre-mRNA. J. Gen. Virol. 84:3353-3358.
2. Ahn K, et al. 1996. Human cytomegalovirus inhibits antigen presentation by a sequential multistep process. Proc. Natl. Acad. Sci. U. S. A. 93:10990-10995.
3. Arlt H, Lang D, Gebert S, Stamminger T. 1994. Identification of binding sites for the 86-kilodalton IE2 protein of human cytomegalovirus within an IE2-responsive viral early promoter. J. Virol. 68:4117-4125.
4. Bain M, Sinclair J. 2007. The S phase of the cell cycle and its perturbation by human cytomegalovirus. Rev. Med. Virol. 17:423-434.
5. Biswas N, Sanchez V, Spector DH. 2003. Human cytomegalovirus infection leads to accumulation of geminin and inhibition of the licensing of cellular DNA replication. J. Virol. 77:2369-2376.
6. Blanchard JM. 2000. Cyclin A2 transcriptional regulation: modulation of cell cycle control at the G1/S transition by peripheral cues. Biochem. Pharmacol. 60:1179-1184.
7. Bresnahan WA, Albrecht T, Thompson EA. 1998. The cyclin E promoter is activated by human cytomegalovirus 86-kDa immediate early protein. J. Biol. Chem. 273:22075-22082.
8. Castillo JP, et al. 2005. Human cytomegalovirus IE1-72 activates ataxia telangiectasia mutated kinase and a p53/p21-mediated growth arrest response. J. Virol. 79:11467-11475.
9. Chevillotte M, et al. 2009. Major tegument protein pp65 of human cytomegalovirus is required for the incorporation of pUL69 and pUL97 into the virus particle and for viral growth in macrophages. J. Virol. 83:2480-2490.
10. Child SJ, Hakki M, De Niro KL, Geballe AP. 2004. Evasion of cellular antiviral responses by human cytomegalovirus TRS1 and IRS1. J. Virol. 78:197-205.
11. Dittmer D, Mocarski ES. 1997. Human cytomegalovirus infection inhibits G1/S transition. J. Virol. 71:1629-1634.
12. 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.
13. Fehr AR, Yu D. 2011. Human cytomegalovirus early protein pUL21a promotes efficient viral DNA synthesis and the late accumulation of immediate-early transcripts. J. Virol. 85:663-674.
14. 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.
15. Gatherer D, et al. 2011. High-resolution human cytomegalovirus transcriptome. Proc. Natl. Acad. Sci. U. S. A. 108:19755-19760.
16. Geley S, et al. 2001. Anaphase-promoting complex/cyclosomedependent proteolysis of human cyclin A starts at the beginning of mitosis and is not subject to the spindle assembly checkpoint. J. Cell Biol. 153:137-148.
17. Gibbs E, Pan ZQ, Niu H, Hurwitz J. 1996. Studies on the in vitro phosphorylation of HSSB-p34 and -p107 by cyclin-dependent kinases. Cyclinsubstrate interactions dictate the efficiency of phosphorylation. J. Biol. Chem. 271:22847-22854.
18. Goldmacher VS, et al. 1999. A cytomegalovirus-encoded mitochondrialocalized inhibitor of apoptosis structurally unrelated to Bcl-2. Proc. Natl. Acad. Sci. U. S. A. 96:12536-12541.
19. Gopinathan L, Ratnacaram CK, Kaldis P. 2011. Established and novel Cdk/cyclin complexes regulating the cell cycle and development. Results Probl. Cell Differ. 53:365-389.
20. Greaves RF, Mocarski ES. 1998. Defective growth correlates with reduced accumulation of a viral DNA replication protein after low-multiplicity infection by a human cytomegalovirus ie1 mutant. J. Virol. 72:366-379.
21. Grey F, et al. 2010. A viral microRNA down-regulates multiple cell cycle genes through mRNA 5'UTRs. PLoS Pathog. 6:e1000967. doi:10.1371/journal.ppat.1000967.
22. Hamirally S, et al. 2009. Viral mimicry of Cdc2/cyclin-dependent kinase 1 mediates disruption of nuclear lamina during human cytomegalovirus nuclear egress. PLoS Pathog. 5:e1000275. doi:10.1371/journal.ppat.1000275.
23. Hume AJ, et al. 2008. Phosphorylation of retinoblastoma protein by viral protein with cyclin-dependent kinase function. Science 320:797-799.
24. Hwang HC, Clurman BE. 2005. Cyclin E in normal and neoplastic cell cycles. Oncogene 24:2776-2786.
25. Hwang J, Kalejta RF. 2011. In vivo analysis of protein sumoylation induced by a viral protein: detection of HCMV pp71-induced Daxx sumoylation. Methods 55:160-165.
26. Jabs DA, Griffiths PD. 2002. Fomivirsen for the treatment of cytomegalovirus retinitis. Am. J. Ophthalmol. 133:552-556.
27. Jackman M, Kubota Y, den Elzen N, Hagting A, Pines J. 2002. Cyclin A and cyclin E-Cdk complexes shuttle between the nucleus and the cytoplasm. Mol. Biol. Cell 13:1030-1045.
28. Jault FM, et al. 1995. Cytomegalovirus infection induces high levels of cyclins, phosphorylated Rb, and p53, leading to cell cycle arrest. J. Virol. 69:6697-6704.
29. 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.
30. Jenkins C, Garcia W, Abendroth A, Slobedman B. 2008. Expression of a human cytomegalovirus latency-associated homolog of interleukin-10 during the productive phase of infection. Virology 370:285-294.
31. Jones TR, et al. 1996. Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc. Natl. Acad. Sci. U. S. A. 93:11327-11333.
32. Kalaszczynska I, et al. 2009. Cyclin A is redundant in fibroblasts but essential in hematopoietic and embryonic stem cells. Cell 138:352-365.
33. Kalejta RF, Bechtel JT, Shenk T. 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.
34. Kim YE, et al. 2011. Human cytomegalovirus infection causes degradation of Sp100 proteins that suppress viral gene expression. J. Virol. 85:11928-11937.
35. Klopocki E, et al. 2007. Complex inheritance pattern resembling autosomal recessive inheritance involving a microdeletion in thrombocytopenia-absent radius syndrome. Am. J. Hum. Genet. 80:232-240.
36. Knudsen KE, Fribourg AF, Strobeck MW, Blanchard JM, Knudsen ES. 1999. Cyclin A is a functional target of retinoblastoma tumor suppressor protein-mediated cell cycle arrest. J. Biol. Chem. 274:27632-27641.
37. Kobayashi H, et al. 1992. Identification of the domains in cyclin A required for binding to, and activation of, p34cdc2 and p32cdk2 protein kinase subunits. Mol. Biol. Cell 3:1279-1294.
38. Liu Z, Winkler M, Biegalke B. 2009. Human cytomegalovirus: host immune modulation by the viral US3 gene. Int. J. Biochem. Cell Biol. 41:503-506.
39. Lu M, Shenk T. 1996. Human cytomegalovirus infection inhibits cell cycle progression at multiple points, including the transition from G1 to S. J. Virol. 70:8850-8857.
40. Machida YJ, Dutta A. 2007. The APC/C inhibitor, Emi1, is essential for prevention of rereplication. Genes Dev. 21:184-194.
41. Marchini A, Liu H, Zhu H. 2001. Human cytomegalovirus with IE-2 (UL122) deleted fails to express early lytic genes. J. Virol. 75:1870-1878.
42. Marshall EE, Bierle CJ, Brune W, Geballe AP. 2009. Essential role for either TRS1 or IRS1 in human cytomegalovirus replication. J. Virol. 83:4112-4120.
43. McCormick AL, Roback L, Livingston-Rosanoff D, St Clair C. 2010. The human cytomegalovirus UL36 gene controls caspase-dependent and -independent cell death programs activated by infection of monocytes differentiating to macrophages. J. Virol. 84:5108-5123.
44. McCormick AL, Roback L, Mocarski ES. 2008. HtrA2/Omi terminates cytomegalovirus infection and is controlled by the viral mitochondrial inhibitor of apoptosis (vMIA). PLoS Pathog. 4:e1000063. doi:10.1371/journal.ppat.1000063.
45. Merrick KA, et al. 2008. Distinct activation pathways confer cyclinbinding specificity on Cdk1 and Cdk2 in human cells. Mol. Cell 32:662-672.
46. Merrick KA, et al. 2011. Switching Cdk2 on or off with small molecules to reveal requirements in human cell proliferation. Mol. Cell 42:624-636.
47. Moroy T, Geisen C. 2004. Cyclin E. Int. J. Biochem. Cell Biol. 36:1424-1439.
48. Murphy EA, Streblow DN, Nelson JA, Stinski MF. 2000. The human cytomegalovirus IE86 protein can block cell cycle progression after inducing transition into the S phase of permissive cells. J. Virol. 74:7108-7118.
49. Nevels M, Brune W, Shenk T. 2004. SUMOylation of the human cytomegalovirus 72-kilodalton IE1 protein facilitates expression of the 86-kilodalton IE2 protein and promotes viral replication. J. Virol. 78:7803-7812.
50. Nevels M, Paulus C, Shenk T. 2004. Human cytomegalovirus immediate-early 1 protein facilitates viral replication by antagonizing histone deacetylation. Proc. Natl. Acad. Sci. U. S. A. 101:17234-17239.
51. Paulus C, Krauss S, Nevels M. 2006. A human cytomegalovirus antagonist of type I IFN-dependent signal transducer and activator of transcription signaling. Proc. Natl. Acad. Sci. U. S. A. 103:3840-3845.
52. Reeves M, Woodhall D, Compton T, Sinclair J. 2010. Human cytomegalovirus IE72 protein interacts with the transcriptional repressor hDaxx to regulate LUNA gene expression during lytic infection. J. Virol. 84:7185-7194.
53. Rodems SM, Clark CL, Spector DH. 1998. Separate DNA elements containing ATF/CREB and IE86 binding sites differentially regulate the human cytomegalovirus UL112-113 promoter at early and late times in the infection. J. Virol. 72:2697-2707.
54. 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.
55. 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.
56. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning-a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
57. Sanchez V, 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.
58. Sanchez V, Spector DH. 2008. Subversion of cell cycle regulatory pathways. Curr. Top. Microbiol. Immunol. 325:243-262.
59. Schulze A, et al. 1995. Cell cycle regulation of the cyclin A gene promoter is mediated by a variant E2F site. Proc. Natl. Acad. Sci. U. S. A. 92:11264-11268.
60. Shin J, et al. 2006. A short isoform of human cytomegalovirus US3 functions as a dominant negative inhibitor of the full-length form. J. Virol. 80:5397-5404.
61. 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.
62. Skaletskaya A, et al. 2001. A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc. Natl. Acad. Sci. U. S. A. 98:7829-7834.
63. Su Y, Adair R, Davis CN, DiFronzo NL, Colberg-Poley AM. 2003. Convergence of RNA cis elements and cellular polyadenylation factors in the regulation of human cytomegalovirus UL37 exon 1 unspliced RNA production. J. Virol. 77:12729-12741.
64. 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.
65. Tenney DJ, Santomenna LD, Goudie KB, Colberg-Poley AM. 1993. The human cytomegalovirus US3 immediate-early protein lacking the putative transmembrane domain regulates gene expression. Nucleic Acids Res. 21:2931-2937.
66. Trang P, Liu F. 2004. RNase P ribozyme as an antiviral agent against human cytomegalovirus. Methods Mol. Biol. 252:437-450.
67. van Zeijl M, Fairhurst J, Baum EZ, Sun L, Jones TR. 1997. The human cytomegalovirus UL97 protein is phosphorylated and a component of virions. Virology 231:72-80.
68. Vaziri C, et al. 2003. A p53-dependent checkpoint pathway prevents rereplication. Mol. Cell 11:997-1008.
69. Wheeler LW, Lents NH, Baldassare JJ. 2008. Cyclin A-CDK activity during G1 phase impairs MCM chromatin loading and inhibits DNA synthesis in mammalian cells. Cell Cycle 7:2179-2188.
70. White EA, Spector DH. 2007. Early viral gene expression and function, p 264-294. In Arvin A, et al. (ed), Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, United Kingdom.
71. Wiebusch L, Bach M, Uecker R, Hagemeier C. 2005. Human cytomegalovirus inactivates the G0/G1-APC/C ubiquitin ligase by Cdh1 dissociation. Cell Cycle 4:1435-1439.
72. Wiebusch L, Hagemeier C. 2001. The human cytomegalovirus immediate early 2 protein dissociates cellular DNA synthesis from cyclindependent kinase activation. EMBO J. 20:1086-1098.
73. 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.
74. Wiebusch L, Truss M, Hagemeier C. 2004. Inhibition of human cytomegalovirus replication by small interfering RNAs. J. Gen. Virol. 85:179-184.
75. Wiebusch L, Uecker R, Hagemeier C. 2003. Human cytomegalovirus prevents replication licensing by inhibiting MCM loading onto chromatin. EMBO Rep. 4:42-46.
76. Wolf DG, Honigman A, Lazarovits J, Tavor E, Panet A. 1998. Characterization of the human cytomegalovirus UL97 gene product as a virionassociated protein kinase. Arch. Virol. 143:1223-1232.
77. Xu Y, Cei SA, Rodriguez Huete A, Colletti KS, Pari GS. 2004. Human cytomegalovirus DNA replication requires transcriptional activation via an IE2- and UL84-responsive bidirectional promoter element within ori-Lyt. J. Virol. 78:11664-11677.
78. Yam CH, Fung TK, Poon RY. 2002. Cyclin A in cell cycle control and cancer. Cell Mol. Life Sci. 59:1317-1326.
79. Zhu H, Cong JP, Yu D, Bresnahan WA, Shenk TE. 2002. Inhibition of cyclooxygenase 2 blocks human cytomegalovirus replication. Proc. Natl. Acad. Sci. U. S. A. 99:3932-3937.
80. Zydek M, Hagemeier C, Wiebusch L. 2010. Cyclin-dependent kinase activity controls the onset of the HCMV lytic cycle. PLoS Pathog. 6:e1001096. doi:10.1371/journal.ppat.1001096.
81. Zydek M, et al. 2011. General blockade of human cytomegalovirus immediate-earlymRNAexpression in the S/G2 phase by a nuclear, Daxx- and PML-independent mechanism. J. Gen. Virol. 92:2757-2769.