Inhibition of S-Phase Cyclin-Dependent Kinase Activity Blocks Expression of Epstein-Barr Virus Immediate-Early and Early Genes, Preventing Viral Lytic Replication

Journal of Virology

Volumn 78, Issue 1, 2004, Pages 104-115

  Kudoh, Ayumi ^a,b   Daikoku, Tohru ^a   Sugaya, Yutaka ^a   Isomura, Hiroki ^a   Fujita, Masatoshi ^c   Kiyono, Tohru ^c   Nishiyama, Yukihiro ^b   Tsurumi, Tatsuya ^a  

^a AICHI CANCER CENTER HOSPITAL   (Japan)

^b NATIONAL CANCER CENTER   (Japan)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLOHEXIMIDE; IMMEDIATE EARLY PROTEIN BZLF1; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; PURVALANOL A; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; EARLY GENE; ENZYME ACTIVITY; ENZYME INHIBITION; EPSTEIN BARR VIRUS; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMEDIATE EARLY GENE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; VIRUS GENE; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

CELL LINE; CYCLIN-DEPENDENT KINASES; ENZYME INHIBITORS; HELA CELLS; HERPESVIRUS 4, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; PURINES; S PHASE; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 0346365302     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.1.104-115.2004     Document Type: Article

References (68)

1. Adams, P. D., and W. G. Kaelin, Jr. 1995. Transcriptional control by E2F. Semin. Cancer Biol. 6:99-108.
2. Adamson, A. L., and S. C. Kenney. 1998. Rescue of the Epstein-Barr virus BZLF1 mutant, Z(S186A), early gene activation defect by the BRLF1 gene product. Virology 251:187-197.
3. Borgne, A., and L. Meijer. 1996. Sequential dephosphorylation of p34(cdc2) on Thr-14 and Tyr-15 at the prophase/metaphase transition. J. Biol. Chem. 271:27847-27854.
4. Bresnahan, W. A., I. Boldogh, P. Chi, E. A. Thompson, and T. Albrecht. 1997. Inhibition of cellular Cdk2 activity blocks human cytomegalovirus replication. Virology 231:239-247.
5. Bresnahan, W. A., I. Boldogh, E. A. Thompson, and T. Albrecht. 1996. Human cytomegalovirus inhibits cellular DNA synthesis and arrests productively infected cells in late G1. Virology 224:150-160.
6. Cardoso, M. C., H. Leonhardt, and B. Nadal-Ginard. 1993. Reversal of terminal differentiation and control of DNA replication: cyclin A and Cdk2 specifically localize at subnuclear sites of DNA replication. Cell 74:979-992.
7. Cayrol, C., and E. K. Flemington. 1996. The Epstein-Barr virus bZIP transcription factor Zta causes G0/G1 cell cycle arrest through induction of cyclin-dependent kinase inhibitors. EMBO J. 15:2748-2759.
8. Chang, Y. N., D. L. Dong, G. S. Hayward, and S. D. Hayward. 1990. The Epstein-Barr virus Zta transactivator: a member of the bZIP family with unique DNA-binding specificity and a dimerization domain that lacks the characteristic heptad leucine zipper motif. J. Virol. 64:3358-3369.
9. Darr, C. D., A. Mauser, and S. Kenney. 2001. Epstein-Barr virus immediate-early protein BRLF1 induces the lytic form of viral replication through a mechanism involving phosphatidylinositol-3 kinase activation. J. Virol. 75:6135-6142.
10. Davido, D. J., D. A. Leib, and P. A. Schaffer. 2002. The cyclin-dependent kinase inhibitor roscovitine inhibits the transactivating activity and alters the posttranslational modification of herpes simplex virus type 1 ICP0. J. Virol. 76:1077-1088.
11. Decaussin, G., V. Leclerc, and T. Ooka. 1995. The lytic cycle of Epstein-Barr virus in the nonproducer Raji line can be rescued by the expression of a 135-kilodalton protein encoded by the BALF2 open reading frame, J. Virol. 69:7309-7314.
12. DePamphilis, M. L. (ed.). 1996. DNA replication in eukaryotic cells. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
13. 1/S transition. J. Virol. 71:1629-1634.
14. Dudley, D. T., L. Pang, S. J. Decker, A. J. Bridges, and A. R. Saltiel. 1995. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 92:7686-7689.
15. Farrell, P. J., G. J. Allan, F. Shanahan, K. H. Vousden, and T. Crook. 1991. p53 is frequently mutated in Burkitt's lymphoma cell lines. EMBO J. 10:2879-2887.
16. Fields, B. N., D. M. Knipe, P. M. Howley, and D. E. Griffin. 2002. Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
17. Fischer, P. M., and D. P. Lane. 2000. Inhibitors of cyclin-dependent kinases as anti-cancer therapeutics. Curr. Med. Chem. 7:1213-1245.
18. Fixman, E. D., G. S. Hayward, and S. D. Hayward. 1995. Replication of Epstein-Barr virus oriLyt: lack of a dedicated virally encoded origin-binding protein and dependence on Zta in cotransfection assays. J. Virol. 69:2998-3006.
19. Fujii, K., N. Yokoyama, T. Kiyono, K. Kuzushima, M. Homma, Y. Nishiyama, M. Fujita, and T. Tsurumi. 2000. The Epstein-Barr virus Pol catalytic subunit physically interacts with the BBLF4-BSLF1-BBLF2/3 complex. J. Virol. 74:2550-2557.
20. Gao, X., K. Ikuta, M. Tajima, and T. Sairenji. 2001. 12-O-tetradecanoyl-phorbol-13-acetate induces Epstein-Barr virus reactivation via NF-κB and AP-1 as regulated by protein kinase C and mitogen-activated protein kinase. Virology 286:91-99.
21. Gray, N., L. Detivaud, C. Doerig, and L. Meijer. 1999. ATP-site directed inhibitors of cyclin-dependent kinases. Curr. Med. Chem. 6:859-875.
22. Gray, N. S., L. Wodicka, A. M. Thunnissen, T. C. Norman, S. Kwon, F. H. Espinoza, D. O. Morgan, G. Barnes, S. LeClerc, L. Meijer, S. H. Kim, D. J. Lockhart, and P. G. Schultz. 1998. Exploiting chemical libraries, structure, and genomics in the search for kinase inhibitors. Science 281:533-538.
23. Hammerschmidt, W., and B. Sugden. 1988. Identification and characterization of oriLyt, a lytic origin of DNA replication of Epstein-Barr virus. Cell 55:427-433.
24. Harbour, J. W., and D. C. Dean. 2000. The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev. 14:2393-2409.
25. Jackson, P. K., S. Chevalier, M. Philippe, and M. W. Kirschner. 1995. Early events in DNA replication require cyclin E and are blocked by p21CIP1. J. Cell Biol. 130:755-769.
26. Jault, F. M., J. M. Jault, F. Ruchti, E. A. Fortunato, C. Clark, J. Corbeil, D. D. Richman, and D. H. Spector. 1995. Cytomegalovirus infection induces high levels of cyclins, phosphorylated Rb, and p53, leading to cell cycle arrest. J. Virol. 69:6697-6704.
27. Kato, J. 1999. Induction of S phase by G1 regulatory factors. Front. Biosci. 4:D787-D792.
28. Kawaguchi, Y., K. Kato, M. Tanaka, M. Kanamori, Y. Nishiyama, and Y. Yamanashi. 2003, Conserved protein kinases encoded by herpesviruses and cellular protein kinase cdc2 target the same phosphorylation site in eukaryotic elongation factor 1δ. J. Virol. 77:2359-2368.
29. Krude, T., M. Jackman, J. Pines, and R. A. Laskey. 1997. Cyclin/Cdk-dependent initiation of DNA replication in a human cell-free system. Cell 88:109-119.
30. Kudoh, A., M. Fujita, T. Kiyono, K. Kuzushima, Y. Sugaya, S, Izuta, Y. Nishiyama, and T. Tsurumi. 2003. Reactivation of lytic replication from B cells latently infected with Epstein-Barr virus occurs with high S-phase cyclin-dependent kinase activity while inhibiting cellular DNA replication. J. Virol. 77:851-861.
31. Lam, L. T., O. K. Pickeral, A. C. Peng, A. Rosenwald, E. M. Hurt, J. M. Giltnane, L. M. Averett, H. Zhao, R. E. Davis, M. Sathyamoorthy, L. M. Wahl, E. D. Harris, J. A. Mikovits, A. P. Monks, M. G. Hollingshead, E. A. Sausville, and L. M. Staudt. 2001. Genomic-scale measurement of mRNA turnover and the mechanisms of action of the anti-cancer drug flavopiridol. Genome Biol. 2: research0041.1-0041.11. [Online.]
32. Laux, G., U. K. Freese, R. Fischer, A. Polack, E. Kofler, and G. W. Bornkamm. 1988. TPA-inducible Epstein-Barr virus genes in Raji cells and their regulation. Virology 162:503-507.
33. Liu, C., N. D. Sista, and J. S. Pagano. 1996. Activation of the Epstein-Barr virus DNA polymerase promoter by the BRLF1 immediate-early protein is mediated through USF and E2F. J. Virol. 70:2545-2555.
34. 1, to S. J. Virol., 70:8850-8857.
35. Mauser, A., E. Holley-Guthrie, A. Zanation, W. Yarborough, W. Kaufmann, A. Klingelhutz, W. T. Seaman, and S. Kenney. 2002. The Epstein-Barr virus immediate-early protein BZLF1 induces expression of E2F-1 and other proteins involved in cell cycle progression in primary keratinocytes and gastric carcinoma cells. J. Virol. 76:12543-12552.
36. Meijer, L., A. Borgne, O. Mulner, J. P. Chong, J. J. Blow, N. Inagaki, M. Inagaki, J. G. Delcros, and J. P. Moulinoux. 1997. Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur. J. Biochem. 243:527-536.
37. Meijer, L., S. Leclerc, and M. Leost. 1999. Properties and potential-applications of chemical inhibitors of cyclin-dependent kinases. Pharmacol. Ther. 82:279-284.
38. Nelson, P. J., I. H. Gelman, and P. E. Klotman. 2001. Suppression of HIV-1 expression by inhibitors of cyclin-dependent kinases promotes differentiation of infected podocytes. J. Am. Soc. Nephrol. 12:2827-2831.
39. Nevins, J. R. 1992. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science 258:424-429.
40. Nicolas, M., V. V. Noe, and C. J. Ciudad. 2003. Transcriptional regulation of the human SP1 gene promoter by SP-family members, NF-Y and E2F. Biochem. J. 371:265-275.
41. Quinlivan, E. B., E. A. Holley-Guthrie, M. Norris, D. Gutsch, S. L. Bachenheimer, and S. C. Kenney. 1993. Direct BRLF1 binding is required for cooperative BZLF1/BRLF1 activation of the Epstein-Barr virus early promoter, BMRF1. Nucleic Acids Res. 21:1999-2007.
42. Ragoczy, T., and G. Miller. 2001. Autostimulation of the Epstein-Barr virus BRLF1 promoter is mediated through consensus Sp1 and Sp3 binding sites. J. Virol. 75:5240-5251.
43. Rodriguez, A., E. J. Jung, Q. Yin, C. Cayrol, and E. K. Flemington. 2001. Role of c-myc regulation in Zta-mediated induction of the cyclin-dependent kinase inhibitors p21 and p27 and cell growth arrest. Virology 284:159-169.
44. 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.
45. Schang, L. M. 2002. Cyclin-dependent kinases as cellular targets for antiviral drugs. J. Antimicrob. Chemother. 50:779-792.
46. Schang, L. M., A. Bantly, M. Knockaert, F. Shaheen, L. Meijer, M. H. Malim, N. S. Gray, and P. A. Schaffer. 2002. Pharmacological cyclin-dependent kinase inhibitors inhibit replication of wild-type and drug-resistant strains of herpes simplex virus and human immunodeficiency virus type 1 by targeting cellular, not viral, proteins. J. Virol. 76:7874-7882.
47. Schang, L. M., J. Phillips, and P. A. Schaffer. 1998. Requirement for cellular cyclin-dependent kinases in herpes simplex virus replication and transcription. J. Virol. 72:5626-5637.
48. Schang, L. M., A. Rosenberg, and P. A. Schaffer. 2000. Roscovitine, a specific inhibitor of cellular cyclin-dependent kinases, inhibits herpes simplex virus DNA synthesis in the presence of viral early proteins. J. Virol. 74:2107-2120.
49. Schang, L. M., A. Rosenberg, and P. A. Schaffer. 1999. Transcription of herpes simplex virus immediate-early and early genes is inhibited by roscovitine, an inhibitor specific for cellular cyclin-dependent kinases. J. Virol. 73:2161-2172.
50. Schepers, A., D. Pich, and W. Hammerschmidt. 1996. Activation of oriLyt, the lytic origin of DNA replication of Epstein-Barr virus, by BZLF1. Virology 220:367-376.
51. Sielecki, T. M., J. F. Boylan, P. A. Benfield, and G. L. Trainor. 2000. Cyclin-dependent kinase inhibitors: useful targets in cell cycle regulation. J. Med. Chem. 43:1-18.
52. Suzuki, S., K. Tamai, and S. Yoshida. 2002. Enzyme-linked immunosorbent assay for distinct cyclin-dependent kinase activities using phosphorylation-site-specific anti-pRB monoclonal antibodies. Anal. Biochem. 301:65-74.
53. Swenson, J. J., A. E. Mauser, W. K. Kaufmann, and S. C. Kenney. 1999. The Epstein-Barr virus protein BRLF1 activates S phase entry through E2F1 induction. J. Virol. 73:6540-6550.
54. Toullec, D., P. Pianetti, H. Coste, P. Bellevergue, T. Grand-Perret, M. Ajakane, V. Baudet, P. Boissin, E. Boursier, F. Loriolle, et al. 1991. The bisin-dolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266:15771-15781.
55. Tsurumi, T. 1993. Purification and characterization of the DNA-binding activity of the Epstein-Barr virus DNA polymerase accessory protein BMRF1 gene products, as expressed in insect cells by using the baculovirus system. J. Virol. 67:1681-1687.
56. Tsurumi, T., T. Daikoku, R. Kurachi, and Y. Nishiyama. 1993. Functional interaction between Epstein-Barr virus DNA polymerase catalytic subunit and its accessory subunit in vitro. J. Virol. 67:7648-7653.
57. Tsurumi, T., T. Daikoku, and Y. Nishiyama. 1994. Further characterization of the interaction between the Epstein-Barr virus DNA polymerase catalytic subunit and its accessory subunit with regard to the 3′-to-5′ exonucleolytic activity and stability of initiation complex at primer terminus. J. Virol. 68:3354-3363.
58. Tsurumi, T., J. Kishore, N. Yokoyama, M. Fujita, T. Daikoku, H. Yamada, Y. Yamashita, and Y. Nishiyama. 1998. Overexpression, purification and helix-destabilizing properties of Epstein-Barr virus ssDNA-binding protein. J. Gen. Virol. 79:1257-1264.
59. Tsurumi, T., A. Kobayashi, K. Tamai, T. Daikoku, R. Kurachi, and Y. Nishiyama. 1993. Functional expression and characterization of the Epstein-Barr virus DNA polymerase catalytic subunit. J. Virol. 67:4651-4658.
60. Tsurumi, T., A. Kobayashi, K. Tamai, H. Yamada, T. Daikoku, Y. Yamashita, and Y. Nishiyama. 1996. Epstein-Barr virus single-stranded DNA-binding protein: purification, characterization, and action on DNA synthesis by the viral DNA polymerase. Virology 222:352-364.
61. Tsurumi, T., H. Yamada, T. Daikoku, Y. Yamashita, and Y. Nishiyama. 1997. Strand displacement associated DNA synthesis catalyzed by the Epstein-Barr virus DNA polymerase. Biochem. Biophys. Res. Commun. 238:33-38.
62. Villerbu, N., A. M. Gaben, G. Redeuilh, and J. Mester. 2002. Cellular effects of purvalanol A: a specific inhibitor of cyclin-dependent kinase activities. Int. J. Cancer 97:761-769.
63. Wang, D., C. de la Fuente, L. Deng, L. Wang, I. Zilberman, C. Eadie, M. Healey, D. Stein, T. Denny, L. E. Harrison, L. Meijer, and F. Kashanchi. 2001. Inhibition of human immunodeficiency virus type 1 transcription by chemical cyclin-dependent kinase inhibitors. J. Virol. 75:7266-7279.
64. Wang, L., L. Deng, K. Wu, C. de la Fuente, D. Wang, K. Kehn, A. Maddukuri, S. Baylor, F. Santiago, E. Agbottah, S. Trigon, M. Morange, R. Mahieux, and F. Kashanchi. 2002. Inhibition of HTLV-1 transcription by cyclin dependent kinase inhibitors. Mol. Cell. Biochem. 237:137-153.
65. Wiebusch, L., and C. Hagemeier. 2001. The human cytomegalovirus immediate early 2 protein dissociates cellular DNA synthesis from cyclin-dependent kinase activation. EMBO J. 20:1086-1098.
66. Yates, J. L., and N. Guan. 1991. Epstein-Barr virus-derived plasmids replicate only once per cell cycle and are not amplified after entry into cells. J. Virol. 65:483-488.
67. Yokoyama, N., K. Fujii, M. Hirata, K. Tamai, T. Kiyono, K. Kuzushima, Y. Nishiyama, M. Fujita, and T. Tsurumi. 1999. Assembly of the Epstein Barr virus BBLF4, BSLF1 and BBLF2/3 proteins and their interactive properties. J. Gen. Virol. 80:2879-2887.
68. Zhang, Q., Y. Hong, D. Dorsky, E. Holley-Guthrie, S. Zalani, N. A. Elshiekh, A. Kiehl, T. Le, and S. Kenney. 1996. Functional and physical interactions between the Epstein-Barr virus (EBV) proteins BZLF1 and BMRF1: effects on EBV transcription and lytic replication. J. Virol. 70:5131-5142.