Recruitment of cdk9 to the immediate-early viral transcriptosomes during human cytomegalovirus infection requires efficient binding to cyclin T1, a threshold level of IE2 86, and active transcription

Journal of Virology

Volumn 83, Issue 11, 2009, Pages 5904-5917

  Kapasi, Anokhi J ^a   Clark, Charles L ^a   Tran, Karen ^a   Spector, Deborah H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 9; CYCLIN T1; TRANSCRIPTOME; BRD4 PROTEIN, HUMAN; CCNT1 PROTEIN, HUMAN; CYCLINE; IE2 PROTEIN, CYTOMEGALOVIRUS; IMMEDIATE EARLY PROTEIN; NUCLEAR PROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; VIRUS RNA;

ARTICLE; BINDING SITE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; CELL CULTURE; CYTOMEGALOVIRUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM;

HUMAN HERPESVIRUS 5;

CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 9; CYCLINS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, VIRAL; HUMANS; IMMEDIATE-EARLY PROTEINS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RNA, VIRAL; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 66149116458     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02651-08     Document Type: Article

References (57)

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. Ahn, J.-H., E. R. Brignole III, and G. S. Hayward. 1998. Disruption of PML subnuclear domains by the acidic IE1 protein of human cytomegalovirus is mediated through interaction with PML and may modulate a RING finger-dependent cryptic transactivator function of PML. Mol. Cell. Biol. 18:4899-4913. (Pubitemid 28343073)
3. Ahn, J. H., and G. S. Hayward. 1997. The major immediate-early proteins IE1 and IE2 of human cytomegalovirus colocalize with and disrupt PML-associated nuclear bodies at very early times in infected permissive cells. J. Virol. 71:4599-4613. (Pubitemid 27204153)
4. Baek, M.-C., P. M. Krosky, A. Pearson, and D. M. Coen. 2004. Phosphorylation of the RNA polymerase II carboxyl-terminal domain in human cytomegalovirus-infected cells and in vitro by the viral UL97 protein kinase. Virology 324:184-193. (Pubitemid 38737410)
5. Bark-Jones, S. J., H. M. Webb, and M. J. West. 2006. EBV EBNA 2 stimulates CDK9-dependent transcription and RNA polymerase II phosphorylation on serine 5. Oncogene 25:1775-1785.
6. Baumli, S., G. Lolli, E. D. Lowe, S. Troiani, L. Rusconi, A. N. Bullock, J. E. Debreczeni, S. Knapp, and L. N. Johnson. 2008. The structure of P-TEFb (CDK9/cyclin T1), its complex with flavopiridol and regulation by phosphorylation. EMBO J. 27:1907-1918.
7. Baxter, M. K., M. G. McPhillips, K. Ozato, and A. A. McBride. 2005. The mitotic chromosome binding activity of the papillomavirus E2 protein correlates with interaction with the cellular chromosomal protein, Brd4. J. Virol. 79:4806-4818. (Pubitemid 40464231)
8. Bieniasz, P. D., T. A. Grdina, H. P. Bogerd, and B. R. Cullen. 1999. Recruitment of cyclin T1/P-TEFb to an HIV type 1 long terminal repeat promoter proximal RNA target is both necessary and sufficient for full activation of transcription. Proc. Natl. Acad. Sci. USA 96:7791-7796. (Pubitemid 29328360)
9. Borst, E. M., G. Hahn, U. H. Koszinowski, and M. Messerle. 1999. Cloning of the human cytomegalovirus (HCMV) genome as an infectious bacterial artificial chromosome in Escherichia coli: a new approach for construction of HCMV mutants. J. Virol. 73:8320-8329.
10. Brown, N. R., M. E. Noble, J. A. Endicott, E. F. Garman, S. Wakatsuki, E. Mitchell, B. Rasmussen, T. Hunt, and L. N. Johnson. 1995. The crystal structure of cyclin A. Structure 3:1235-1247. (Pubitemid 3001419)
11. Chang, P. C., and M. Li. 2008. Kaposi's sarcoma-associated herpesvirus K-cyclin interacts with Cdk9 and stimulates Cdk9-mediated phosphorylation of p53 tumor suppressor. J. Virol. 82:278-290.
12. Cho, W. K., M. Zhou, M. K. Jang, K. Huang, S. J. Jeong, K. Ozato, and J. N. Brady. 2007. Modulation of the Brd4/P-TEFb interaction by the human T-lymphotropic virus type 1 tax protein. J. Virol. 81:11179-11186. (Pubitemid 47536090)
13. De Azevedo, W. F., S. Leclerc, L. Meijer, L. Havlicek, M. Strnad, and S. H. Kim. 1997. Inhibition of cyclin-dependent kinases by purine analogues: crystal structure of human cdk2 complexed with roscovitine. Eur. J. Biochem. 243:518-526. (Pubitemid 27060442)
14. de Falco, G., and A. Giordano. 1998. CDK9 (PITALRE): a multifunctional cdc2-related kinase. J. Cell Physiol. 177:501-506. (Pubitemid 28541575)
15. Durand, L. O., S. J. Advani, A. P. Poon, and B. Roizman. 2005. The carboxyl-terminal domain of RNA polymerase II is phosphorylated by a complex containing cdk9 and infected-cell protein 22 of herpes simplex virus 1. J. Virol. 79:6757-6762. (Pubitemid 40677307)
16. Durand, L. O., and B. Roizman. 2008. Role of cdk9 in the optimization of expression of the genes regulated by ICP22 of herpes simplex virus 1. J. Virol. 82:10591-10599. (Pubitemid 352691193)
17. Fortunato, E. A., A. K. McElroy, V. Sanchez, and D. H. Spector. 2000. Exploitation of cellular signaling and regulatory pathways by human cytomegalovirus. Trends Microbiol. 8:111-119. (Pubitemid 30155486)
18. Gold, M. O., X. Yang, C. H. Herrmann, and A. P. Rice. 1998. PITALRE, the catalytic subunit of TAK, is required for human immunodeficiency virus Tat transactivation in vivo. J. Virol. 72:4448-4453. (Pubitemid 28188755)
19. Hagemeier, C., S. Walker, R. Caswell, T. Kouzarides, and J. Sinclair. 1992. The human cytomegalovirus 80-kilodalton but not the 72-kilodalton immediate-early protein transactivates heterologous promoters in a TATA box-dependent mechanism and interacts directly with TFIID. J. Virol. 66:4452-4456.
20. Hahn, G., M. Jarosch, J. B. Wang, C. Berbes, and M. A. McVoy. 2003. Tn7-mediated introduction of DNA sequences into bacmid-cloned cytomegalovirus genomes for rapid recombinant virus construction. J. Virol. Methods 107:185-194.
21. Herrmann, C. H., and M. A. Mancini. 2001. The CDK9 and cyclin T subunits of TAK/P-TEFb localize to splicing factor-rich nuclear speckle regions. J. Cell Sci. 114:1491-1503. (Pubitemid 32427836)
22. Isel, C., and J. Karn. 1999. Direct evidence that HIV-1 Tat stimulates RNA polymerase II carboxyl-terminal domain hyperphosphorylation during transcriptional elongation. J. Mol. Biol. 290:929-941. (Pubitemid 29371730)
23. 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. (Pubitemid 26278209)
24. 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. (Pubitemid 27337448)
25. Ivanov, D., Y. T. Kwak, E. Nee, J. Guo, L. F. García- Martínez, and R. B. Gaynor. 1999. Cyclin T1 domains involved in complex formation with Tat and TAR RNA are critical for tat-activation. J. Mol. Biol. 288:41-56. (Pubitemid 29201503)
26. Jang, M. K., K. Mochizuki, M. Zhou, H. S. Jeong, J. N. Brady, and K. Ozato. 2005. The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Mol. Cell 19:523-534.
27. 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. (Pubitemid 350309154)
28. Li, Q., J. P. Price, S. A. Byers, D. Cheng, J. Peng, and D. H. Price. 2005. Analysis of the large inactive P-TEFb complex indicates that it contains one 7SK molecule, a dimer of HEXIM1 or HEXIM2, and two P-TEFb molecules containing Cdk9 phosphorylated at threonine 186. J. Biol. Chem. 280:28819-28826. (Pubitemid 41105784)
29. Majello, B., and G. Napolitano. 2001. Control of RNA polymerase II activity by dedicated CTD kinases and phosphatases. Front. Biosci. 6:D1358-D1368.
30. Majello, B., G. Napolitano, A. Giordano, and L. Lania. 1999. Transcriptional regulation by targeted recruitment of cyclin-dependent CDK9 kinase in vivo. Oncogene 18:4598-4605. (Pubitemid 29405891)
31. Mancebo, H. S., G. Lee, J. Flygare, J. Tomassini, P. Luu, Y. Zhu, J. Peng, C. Blau, D. Hazuda, D. Price, and O. Flores. 1997. P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev. 11:2633-2644. (Pubitemid 27452387)
32. McPhillips, M. G., J. G. Oliveira, J. E. Spindler, R. Mitra, and A. A. McBride. 2006. Brd4 is required for E2-mediated transcriptional activation but not genome partitioning of all papillomaviruses. J. Virol. 80:9530-9543. (Pubitemid 44435629)
33. Meinhart, A., T. Kamenski, S. Hoeppner, S. Baumli, and P. Cramer. 2005. A structural perspective of CTD function. Genes Dev. 15:1401-1415. (Pubitemid 41003005)
34. 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. Lippincott Williams & Wilkins, Philadelphia, PA.
35. Morello, C. S., L. D. Cranmer, and D. H. Spector. 1999. In vivo replication, latency, and immunogenicity of murine cytomegalovirus mutants with deletions in the M83 and M84 genes, the putative homologs of human cytomegalovirus pp65 (UL83). J. Virol. 73:7678-7693.
36. Müller, S., and A. Dejean. 1999. Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption. J. Virol. 73:5137-5143. (Pubitemid 29246776)
37. Napolitano, G., P. Licciardo, R. Carbone, B. Majello, and L. Lania. 2002. CDK9 has the intrinsic property to shuttle between nucleus and cytoplasm, and enhanced expression of cyclin T1 promotes its nuclear localization. J. Cell. Physiol. 192:209-215. (Pubitemid 34747789)
38. Palermo, R. D., H. M. Webb, A. Gunnell, and M. J. West. 2008. Regulation of transcription by the Epstein-Barr virus nuclear antigen EBNA 2. Biochem. Soc. Trans. 36:625-628.
39. Park, J. J., Y. E. Kim, H. T. Pham, E. T. Kim, Y. H. Chung, and J. H. Ahn. 2007. Functional interaction of the human cytomegalovirus IE2 protein with histone deacetylase 2 in infected human fibroblasts. J. Gen. Virol. 88:3214-3223. (Pubitemid 350201830)
40. Prelich, G. 2002. RNA polymerase II carboxy-terminal domain kinases: emerging clues to their function. Eukaryot. Cell 1:153-162.
41. 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. (Pubitemid 28188671)
42. Sanchez, V., C. L. Clark, J. Y. Yen, R. Dwarakanath, and D. H. Spector. 2002. Viable human cytomegalovirus recombinant virus with an internal deletion of the IE2 86 gene affects late stages of viral replication. J. Virol. 76:2973-2989. (Pubitemid 34184882)
43. Sanchez, V., A. K. McElroy, J. Yen, S. Tamrakar, C. L. Clark, R. A. Schwartz, and D. H. Spector. 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. (Pubitemid 39299661)
44. Shin, K. J., E. A. Wall, J. R. Zavzavadjian, L. A. Santat, J. Liu, J. I. Hwang, R. Rebres, T. Roach, W. Seaman, M. I. Simon, and I. D. Fraser. 2006. A single lentiviral vector platform for microRNA-based conditional RNA interference and coordinated transgene expression. Proc. Natl. Acad. Sci. USA 103:13759-13764. (Pubitemid 44413981)
45. Shlapobersky, M., R. Sanders, C. Clark, and D. H. Spector. 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. (Pubitemid 44522589)
46. Sommer, M. H., A. L. Scully, and D. H. Spector. 1994. Transactivation by the human cytomegalovirus IE2 86 kilodalton protein requires a domain that binds to both the TATA box-binding protein and the retinoblastoma protein. J. Virol. 68:6223-6231. (Pubitemid 24294872)
47. Sourvinos, G., N. Tavalai, A. Berndt, D. A. Spandidos, and T. Stamminger. 2007. Recruitment of human cytomegalovirus immediate-early 2 protein onto parental viral genomes in association with ND10 in live-infected cells. J. Virol. 81:10123-10136. (Pubitemid 350067716)
48. 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.
49. 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. (Pubitemid 43032330)
50. Wei, P., M. E. Garber, S. M. Fang, W. H. Fischer, and K. A. Jones. 1998. A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 92:451-462. (Pubitemid 28101109)
51. Wilkinson, G. W., C. Kelly, J. H. Sinclair, and C. Rickards. 1998. Disruption of PML-associated nuclear bodies mediated by the human cytomegalovirus major immediate early gene product. J. Gen. Virol. 79:1233-1245. (Pubitemid 28203865)
52. Yang, Z., J. H. Yik, R. Chen, N. He, M. K. Jang, K. Ozato, and Q. Zhou. 2005. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol. Cell 19:535-545.
53. You, J., J. L. Croyle, A. Nishimura, K. Ozato, and P. M. Howley. 2004. Interaction of the bovine papillomavirus E2 protein with Brd4 tethers the viral DNA to host mitotic chromosomes. Cell 117:349-360. (Pubitemid 38534541)
54. You, J., V. Srinivasan, G. V. Denis, W. J. Harrington, Jr., M. E. Ballestas, K. M. Kaye, and P. M. Howley. 2006. Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen interacts with bromodomain protein Brd4 on host mitotic chromosomes. J. Virol. 80:8909-8919. (Pubitemid 44359965)
55. Zhou, M., H. Lu, H. Park, J. Wilson-Chiru, R. Linton, and J. N. Brady. 2006. Tax interacts with P-TEFb in a novel manner to stimulate human T-lymphotropic virus type 1 transcription. J. Virol. 80:4781-4791.
56. Zhou, Q., D. Chen, E. Pierstorff, and K. Luo. 1998. Transcription elongation factor P-TEFb mediates Tat activation of HIV-1 transcription at multiple stages. EMBO J. 17:3681-3691. (Pubitemid 28327386)
57. Zhu, Y., T. Pe'ery, J. Peng, Y. Ramanathan, N. Marshall, T. Marshall, B. Amendt, M. B. Mathews, and D. H. Price. 1997. Transcription elongation factor P-TEFb is required for HIV-1 tat transactivation in vitro. Genes Dev. 11:2622-2632.