Human cytomegalovirus immediate-early protein 2 (IE2)-mediated activation of cyclin E is cell-cycle-independent and forces S-phase entry in IE2-arrested cells

Journal of General Virology

Volumn 84, Issue 1, 2003, Pages 51-60

  Wiebusch, Lüder ^a   Asmar, Jasmin ^a   Uecker, Ralf ^a   Hagemeier, Christian ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN E; IMMEDIATE EARLY PROTEIN; IMMEDIATE EARLY PROTEIN 2; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL STRAIN; CONTROLLED STUDY; EMBRYO; FIBROBLAST; GENE ACTIVATION; GENE EXPRESSION; GENE MUTATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; UPREGULATION; VIRUS INFECTION; WILD TYPE;

CELL CYCLE; CELL LINE; CELLS, CULTURED; CYCLIN E; CYTOMEGALOVIRUS; FIBROBLASTS; GENE EXPRESSION REGULATION, VIRAL; HUMANS; IMMEDIATE-EARLY PROTEINS; S PHASE; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSFECTION;

CYTOMEGALOVIRUS; DNA VIRUSES; HUMAN HERPESVIRUS 5;

EID: 0037231927     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.18702-0     Document Type: Review

References (50)

1. Adams, P. D., Lopez, P., Sellers, W. R. & Kaelin, W. G., Jr (1997). Fluorescence-activated cell sorting of transfected cells. Methods Enzymol 283, 59-72.
2. Bartek, J. & Lukas, J. (2001). Pathways governing G1/S transition and their response to DNA damage. FEBS Lett 490, 117-122.
3. Biron, K. K., Fyfe, J. A., Stanat, S. C., Leslie, L. K., Sorrell, J. B., Lambe, C. U. & Coen, D. M. (1986). A human cytomegalovirus mutant resistant to the nucleoside analog 9-([2-hydroxy-I-(hydroxymethyl)ethoxy]methyl) guanine (BW B759U) induces reduced levels of BW B759U triphosphate. Proc Natl Acad Sci U S A 83, 8769-8773.
4. Bresnahan, W. A., Boldogh, I., Thompson, E. A. & Albrecht, T. (1996). Human cytomegalovirus inhibits cellular DNA synthesis and arrests productively infected cells in late G1. Virology 224, 150-160.
5. Bresnahan, W. A., Boldogh, I., Chi, P., Thompson, E. A. & Albrecht, T. (1997a). Inhibition of cellular Cdk2 activity blocks human cytomegalovirus replication. Virology 231, 239-247.
6. Bresnahan, W. A., Thompson, E. A. & Albrecht, T. (1997b). Human cytomegalovirus infection results in altered Cdk2 subcellular localization. J Gen Virol 78, 1993-1997.
7. Bresnahan, W. A., Albrecht, T. & Thompson, E. A. (1998). The cyclin E promoter is activated by human cytomegalovirus 86-kDa immediate early protein. J Biol Chem 273, 22075-22082.
8. Castillo, J. P., Yurochko, A. D. & Kowalik, T. F. (2000). Role of human cytomegalovirus immediate-early proteins in cell growth control. J Virol 74, 8028-8037.
9. cip1 in cells productively infected with human cytomegalovirus. J Virol 75, 3613-3625.
10. DeGregori, J., Kowalik, T. & Nevins, J. R. (1995). Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatory genes. Mol Cell Biol 15, 4215-4224.
11. Dittmer, D. & Mocarski, E. S. (1997). Human cytomegalovirus infection inhibits G1/S transition. J Virol 71, 1629-1634.
12. Donnellan, R. & Chatty, R. (1999). Cyclin E in human cancers. FASEB J 13, 773-780.
13. Dulic, V., Lees, E. & Reed, S. I. (1992). Association of human cyclin E with a periodic G1-S phase protein kinase. Science 257, 1958-1961.
14. Ekholm, S. V., Zickert, P., Reed, S. I. & Zetterberg, A. (2001). Accumulation of cyclin E is not a prerequisite for passage through the restriction point. Mol Cell Biol 21, 3256-3265.
15. Fortunato, E. A., Sommer, M. H., Yoder, K. & Spector, D. H. (1997). Identification of domains within the human cytomegalovirus major immediate-early 86-kilodalton protein and the retinoblastoma protein required for physical and functional interaction with each other. J Virol 71, 8176-8185.
16. Fortunato, E. A., McElroy, A. K., Sanchez, I. & Spector, D. H. (2000). Exploitation of cellular signaling and regulatory pathways by human cytomegalovirus. Trends Microbiol 8, 111-119.
17. Gebert, S., Schmolke, S., Sorg, G., Floss, S., Plachter, B. & Stamminger, T. (1997). The UL84 protein of human cytomegalovirus acts as a transdominant inhibitor of immediate-early-mediated transactivation that is able to prevent viral replication. J Virol 71, 7048-7060.
18. Green, S., Issemann, I. & Sheer, E. (1988). A versatile in vivo and in vitro eukaryotic expression vector for protein engineering. Nucleic Acids Res 16, 369.
19. Gribaudo, G., Riera, L., Lembo, D. & 8 other authors (2000). Murine cytomegalovirus stimulates cellular thymidylate synthase gene expression in quiescent cells and requires the enzyme for replication. J Virol 74, 4979-4987.
20. Hagemeier, C., Caswell, R., Hayhurst, G., Sinclair, J. & Kouzarides, T. (1994). Functional interaction between the HCMV IE2 transactivator and the retinoblastoma protein. EMBO J 13, 2897-2903.
21. Heider, J. A., Bresnahan, W. A. & Shenk, T. E. (2002). Construction of a rationally designed human cytomegalovirus variant encoding a temperature-sensitive immediate-early 2 protein. Proc Natl Acad Sci U S A 99, 3141-3146.
22. Hughes, T. A. & Cook, P. R. (1996). Mimosine arrests the cell cycle after cells enter S-phase. Exp Cell Res 222, 275-280.
23. Jault, F. M., Jault, J.-M., Ruchti, F., Fortunato, E. A., Clark, C., Corbeil, J., Richman, D. D. & Spector, D. H. (1995). Cytomegalovirus infection induces high levels of cyclins, phosphorylated Rb and p53, leading to cell cycle arrest. J Virol 69, 6697-6704.
24. Jiang, H., Chou, H. S. & Zhu, L. (1998). Requirement of cyclin E-Cdk2 inhibition in p16(INK4a)-mediated growth suppression. Mol Cell Biol 18, 5284-5290.
25. Kalejta, R. F. & Shenk, T. (2002). Manipulation of the cell cycle by human cytomegalovirus. Front Biosci 7, D295-306.
26. Koff, A., Giordano, A., Desai, D. & 7 other authors (1992). Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science 257, 1689-1694.
27. Kronschnabl, M., Marschall, M. & Stamminger, T. (2002). Efficient and tightly regulated expression systems for the human cytomegalovirus major transactivator protein IE2p86 in permissive cells. Virus Res 83, 89-102.
28. Krude, T. (1999). Mimosine arrests proliferating human cells before onset of DNA replication in a dose-dependent manner. Exp Cell Res 247, 148-159.
29. 1 cyclin-dependent kinase activity in the induction of S phase. Proc Natl Acad Sci U S A 96, 6626-6631.
30. 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.
31. Lukac, D. M., Harel, N. Y., Tanese, N. & Alwine, J. C. (1997). TAF-like functions of human cytomegalovirus immediate-early proteins. J Virol 71, 7227-7239.
32. Lukas, J., Herzinger, T., Hansen, K., Moroni, M. C., Resnitzky, D., Helin, K., Reed, S. I. & Bartek, J. (1997). Cyclin E-induced S phase without activation of the pRb/E2F pathway. Genes & Dev 11, 1479-1492.
33. McElroy, A. K., Dwarakanath, R. S. & Spector, D. H. (2000). Dysregulation of cyclin E gene expression in human cytomegalovirus-infected cells requires viral early gene expression and is associated with changes in the Rb-related protein p130. J Virol 74, 4192-4206.
34. 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.
35. Murphy, E. A., Streblow, D. N., Nelson, J. A. & Stinski, M. F. (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.
36. Resnitzky, D., Gossen, M., Bujard, H. & Reed, S. I. (1994). Acceleration of the G1/S phase transition by expression of cyclins D1 and E with an inducible system. Mol Cell Biol 14, 1669-1679.
37. Rodriguez, A., Armstrong, M., Dwyer, D. & Flemington, E. (1999). Genetic dissection of cell growth arrest functions mediated by the Epstein-Barr virus lytic gene product, Zta. J Virol 73, 9029-9038.
38. Salvant, B. S., Fortunato, E. A. & Spector, D. H. (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.
39. Sauer, K. & Lehner, C. F. (1995). The role of cyclin E in the regulation of entry into S phase. Prog Cell Cycle Res 1, 125-139.
40. Shen, Y., Zhu, H. & Shenk, T. (1997). Human cytomagalovirus IE1 and IE2 proteins are mutagenic and mediate "hit-and-run" oncogenic transformation in cooperation with the adenovirus E1A proteins. Proc Natl Acad Sci U S A 94, 3341-3345.
41. 1 into early S phase in terminally differentiated cells. J Gen Virol 81, 1553-1565.
42. Song, Y. J. & Stinski, M. F. (2002). Effect of the human cytomegalovirus IE86 protein on expression of E2F-responsive genes: a DNA microarray analysis. Proc Natl Acad Sci U S A 99, 2836-2841.
43. Speir, E., Modali, R., Huang, E-S., Leon, M. B., Shawl, F., Finkel, T. & Epstein, S. E. (1994). Potential role of human cytomegalovirus and p53 interaction in coronary restenosis. Science 265, 391-394.
44. Spruck, C. H., Won, K. A. & Reed, S. I. (1999). Deregulated cyclin E induces chromosome instability. Nature 401, 297-300.
45. Strohmaier, H., Spruck, C. H., Kaiser, P., Won, K. A., Sangfelt, O. & Reed, S. I. (2001). Human F-box protein hCdc4 targets cyclin E for proteolysis and is mutated in a breast cancer cell line. Nature 413, 316-322.
46. Wade, M., Kowalik, T. F., Mudryj, M., Huang, E. S. & Azizkhan, J. C. (1992). E2F mediates dihydrofolate reductase promoter activation and multiprotein complex formation in human cytomegalovirus infection. Mol Cell Biol 12, 4364-4374.
47. 1. J Virol 73, 9274-9283.
48. 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.
49. Yu, Y. & Alwine, J. C. (2002). Human cytomegalovirus major immediate-early proteins and simian virus 40 large T antigen can inhibit apoptosis through activation of the phosphatidylinositide 3′-OH kinase pathway and the cellular kinase Akt. J Virol 76, 3731-3738.
50. Zhu, H., Shen, Y. & Shenk, T. (1995). Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J Virol 69, 7960-7970.