Tat modifies the activity of CDK9 to phosphorylate serine 5 of the RNA polymerase II carboxyl-terminal domain during human immunodeficiency virus type 1 transcription

Molecular and Cellular Biology

Volumn 20, Issue 14, 2000, Pages 5077-5086

  Zhou, Meisheng ^c   Halanski, Matthew A ^c   Radonovich, Michael F ^c   Kashanchi, Fatah ^a,c   Peng, Junmin ^b,c   Price, David H ^b,c   Brady, John N ^c  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE II; TRANSACTIVATOR PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; DNA TEMPLATE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR AFFINITY; VIRUS TRANSCRIPTION;

BIOTIN; CYCLIN-DEPENDENT KINASE 9; CYCLIN-DEPENDENT KINASES; DICHLORORIBOFURANOSYLBENZIMIDAZOLE; ENZYME INHIBITORS; GENE PRODUCTS, TAT; HIV LONG TERMINAL REPEAT; HIV-1; HUMANS; PHOSPHORYLATION; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT PROTEINS; RNA POLYMERASE II; SERINE; SUBSTRATE SPECIFICITY; TEMPLATES, GENETIC; TRANSCRIPTION, GENETIC;

EID: 0033920260     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.14.5077-5086.2000     Document Type: Article

References (85)

1. Alonso, A., D. Derse, and B. M. Peterlin. 1992. Human chromosome 12 is required for optimal interactions between Tat and TAR of human immunodeficiency virus type 1 in rodent cells. J. Virol. 66:4617-4621.
2. Bieniasz, P. D., T. A. Grdina, H. P. Bogerd, and B. R. Cullen. 1998. Recruitment of a protein complex containing Tat and cyclin T1 to TAR governs the species specificity of HIV-1 Tat. EMBO J. 17:7056-7065.
3. 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.
4. Boris-Lawrie, K. A., J. N. Brady, and A. Kumar. 1992. Sequences within the R region of the long terminal repeat activate basal transcription from the HIV-1 promoter. Gene Expr. 2:215-230.
5. Chen, D., and Q. Zhou. 1999. Tat activates human immunodeficiency virus type 1 transcriptional elongation independent of TFIIH kinase. Mol. Cell. Biol. 19:2863-2871.
6. Chun, R. F., and K. T. Jeang. 1996. Requirements for RNA polymerase II carboxyl-terminal domain for activated transcription of human retroviruses human T-cell lymphotropic virus 1 and HIV-1. J. Biol. Chem. 271:27888-27894.
7. Cisek, L. J., and J. L. Corden. 1989. Phosphorylation of RNA polymerase by the murine homologue of the cell-cycle control protein cdc2. Nature 339: 679-684.
8. Cismowski, M. J., G. M. Laff, M. J. Solomon, and S. I. Reed. 1995. KIN28 encodes a C-terminal domain kinase that controls mRNA transcription in Saccharomyces cerevisiae but lacks cyclin-dependent kinase-activating kinase (CAK) activity. Mol. Cell. Biol. 15:2983-2992.
9. Cooper, K. F., M. J. Mallory, J. B. Smith, and R. Strich. 1997. Stress and developmental regulation of the yeast C-type cyclin Ume3p (Srb11p/Ssn8p). EMBO J. 16:4665-4675.
10. Cullen, B. R. 1986. Trans-activation of human immunodeficiency virus occurs via a bimodal mechanism. Cell 46:973-982.
11. Dahmus, M. E. 1996. Reversible phosphorylation of the C-terminal domain of RNA polymerase II. J. Biol. Chem. 271:19009-19012.
12. Dingwall, C., I. Ernberg, M. J. Gait, S. M. Green, S. Heaphy, J. Karn, A. D. Lowe, M. Singh, M. A. Skinner, and R. Valerio. 1989. Human immunodeficiency virus 1 Tat protein binds trans-activation-responsive region (TAR) RNA in vitro. Proc. Natl. Acad. Sci. USA 86:6925-6929.
13. Drapkin, R., and D. Reinberg. 1994. The multifunctional TFIIH complex and transcriptional control. Trends Biochem. Sci. 19:504-508.
14. Feaver, W. J., O. Gileadi, Y. Li, and R. D. Kornberg. 1991. CTD kinase associated with yeast RNA polymerase II initiation factor b. Cell 67:1223-1230.
15. Feaver, W. J., J. Q. Svejstrup, N. L. Henry, and R. D. Kornberg. 1994. Relationship of CDK-activating kinase and RNA polymerase II CTD kinase TFIIH/TFIIK. Cell 79:1103-1109.
16. Fujinaga, K., R. Taube, J. Wimmer, T. P. Cujec, and B. M. Peterlin. 1999. Interactions between human cyclin T, Tat, and the transactivation response element (TAR) are disrupted by a cysteine to tyrosine substitution found in mouse cyclin T. Proc. Natl. Acad. Sci. USA 96:1285-1290.
17. Garber, M. E., P. Wei, V. N. KewalRamani, T. P. Mayall, C. H. Herrmann, A. P. Rice, D. R. Littman, and K. A. Jones. 1998. The interaction between HIV-1 Tat and human cyclin T1 requires zinc and a critical cysteine residue that is not conserved in the murine CycT1 protein. Genes Dev. 12:3512-3527.
18. Grana, X., A. De Luca, N. Sang, Y. Fu, P. P. Claudio, J. Rosenblatt, D. O. Morgan, and A. Giordano. 1994. PITALRE, a nuclear CDC2-related protein kinase that phosphorylates the retinoblastoma protein in vitro. Proc. Natl. Acad. Sci. USA 91:3834-3838.
19. Harper, J. W., and S. J. Elledge. 1998. The role of Cdk7 in CAK function, a retro-retrospective. Genes Dev. 12:285-289.
20. Hengartner, C. J., V. E. Myer, S. M. Liao, C. J. Wilson, S. S. Koh, and R. A. Young. 1998. Temporal regulation of RNA polymerase II by Srb10 and Kin28 cyclin-dependent kinases. Mol. Cell 2:43-53.
21. Hetrmann, C. H., and A. P. Rice. 1993. Specific interaction of the human immunodeficiency virus Tat proteins with a cellular protein kinase. Virology 197:601-608.
22. Herrmann, C. H., and A. P. Rice. 1995. Lentivirus Tat proteins specifically associate with a cellular protein kinase, TAK, that hyperphosphorylates the carboxyl-terminal domain of the large subunit of RNA polymerase II: candidate for a Tat cofactor. J. Virol. 69:1612-1620.
23. Ho, C. K., and S. Shuman. 1999. Distinct roles for CTD Ser-2 and Ser-5 phosphorylation in the recruitment and allosteric activation of mammalian mRNA capping enzyme. Mol. Cell 3:405-411.
24. Joeijmakers, J. H., J. M. Egly, and W. Vermeulen. 1996. TFIIH: a key component in multiple DNA transactions. Curr. Opin. Genet. Dev. 6:26-33.
25. 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.
26. Ivanov, D., Y. T. Kwak, E. Nee, J. Guo, L. F. Garcia-Martinez, 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.
27. Jones, K. A. 1997. Taking a new TAK on tat transactivation. Genes Dev. 11:2593-2599.
28. Kao, S. Y., A. F. Calman, P. A. Luciw, and B. M. Peterlin. 1987. Anti-termination of transcription within the long terminal repeat of HIV-1 by tat gene product. Nature 330:489-493.
29. Keen, N. J., M. J. Churcher, and J. Karn. 1997. Transfer of Tat and release of TAR RNA during the activation of the human immunodeficiency virus type-1 transcription elongation complex. EMBO J. 16:5260-5272.
30. Koleske, A. J., and R. A. Young. 1994. An RNA polymerase II holoenzyme responsive to activators. Nature 368:466-469.
31. Kuchin, S., P. Yeghiayan, and M. Carlson. 1995. Cyclin-dependent protein kinase and cyclin homologs SSN3 and SSN8 contribute to transcriptional control in yeast. Proc. Natl. Acad. Sci. USA 92:4006-4010.
32. Kwak, Y. T., D. Ivanov, J. Guo, E. Nee, and R. B. Gaynor. 1999. Role of the human and murine cyclin T proteins in regulating HIV-1 tat-activation. J. Mol. Biol. 288:57-69.
33. Laspia, M. F., A. P. Rice, and M. B. Mathews. 1990. Synergy between HIV-1 Tat and adenovirus E1A is principally due to stabilization of transcriptional elongation. Genes Dev. 4:2397-2408.
34. Leclerc, V., J. P. Tassan, P. H. O'Farrell, E. A. Nigg, and P. Leopold. 1996. Drosophila Cdk8, a kinase partner of cyclin C that interacts with the large subunit of RNA polymerase II. Mol. Biol. Cell 7:505-513.
35. Lee, J. M., and A. L. Greenleaf. 1991. CTD kinase large subunit is encoded by CTK1, a gene required for normal growth of Saccharomyces cerevisiae. Gene Expr. 1:149-167.
36. Liao, S. M., J. Zhang, D. A. Jeffery, A. J. Koleske, C. M. Thompson, D. M. Chao, M. Viljoen, H. J. van Vuuren, and R. A. Young. 1995. A kinase-cyclin pair in the RNA polymerase II holoenzyme. Nature 374:193-196.
37. Lu, H., L. Zawel, L. Fisher, J. M. Egly, and D. Reinberg. 1992. Human general transcription factor IIH phosphorylates the C-terminal domain of RNA polymerase II. Nature 358:641-645.
38. Madore, S. J., and B. R. Cullen. 1993. Genetic analysis of the cofactor requirement for human immunodeficiency virus type 1 Tat function. J. Virol. 67:3703-3711.
39. 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.
40. Marshall, N. F., J. Peng, Z. Xie, and D. H. Price. 1996. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J. Biol. Chem. 271:27176-27183.
41. Marshall, N. F., and D. H. Price. 1995. Purification of P-TEFb, a transcription factor required for the transition into productive elongation. J. Biol. Chem. 270:12335-12338.
42. Morgan, D. O. 1995. Principles of CDK regulation. Nature 374:131-134.
43. Morgan, D. O., R. P. Fisher, F. H. Espinoza, A. Farrell, J. Nourse, H. Chamberlin, and P. Jin. 1998. Control of eukaryotic cell cycle progression by phosphorylation of cyclin-dependent kinases. Cancer J. Sci. Am. 4(Suppl. 1):S77-S83.
44. Okamoto, H., C. T. Sheline, J. L. Corden, K. A. Jones, and B. M. Peterlin. 1996. Trans-activation by human immunodeficiency virus Tat protein requires the C-terminal domain of RNA polymerase II. Proc. Natl. Acad. Sci. USA 93:11575-11579.
45. Orphanides, G., T. Lagrange, and D. Reinberg. 1996. The general transcription factors of RNA polymerase II. Genes Dev. 10:2657-2683.
46. Parada, C. A., and R. G. Roeder. 1996. Enhanced processivity of RNA polymerase II triggered by Tat-induced phosphorylation of its carboxy-terminal domain. Nature 384:375-378.
47. Parada, C. A., and R. G. Roeder. 1999. A novel RNA polymerase II-containing complex potentiates Tat-enhanced HIV-1 transcription. EMBO J. 18:3688-3701.
48. Patturajan, M., N. K. Conrad, D. B. Bregman, and J. L. Corden. 1999. Yeast carboxyl-terminal domain kinase I positively and negatively regulates RNA polymerase II carboxyl-terminal domain phosphorylation. J. Biol. Chem. 274:27823-27828.
49. Patturajan, M., R. J. Schulte, B. M. Sefton, R. Berezney, M. Vincent, O. Bensaude, S. L. Warren, and J. L. Corden. 1998. Growth-related changes in phosphorylation of yeast RNA polymerase II. J. Biol. Chem. 273:4689-4694.
50. Payne, J. M., and M. E. Dahmus. 1993. Partial purification and characterization of two distinct protein kinases that differentially phosphorylate the carboxyl-terminal domain of RNA polymerase subunit IIa. J. Biol. Chem. 268:80-87.
51. Peng, J., Y. Zhu, J. T. Milton, and D. H. Price. 1998. Identification of multiple cyclin subunits of human P-TEFb. Genes Dev. 12:755-762.
52. Ping, Y. H., and T. M. Rana. 1999. Tat-associated kinase (P-TEFb): a component of transcription preinitiation and elongation complexes. J. Biol. Chem. 274:7399-7404.
53. Poon, R. Y., K. Yamashita, M. Howell, M. A. Ershler, A. Belyavsky, and T. Hunt. 1994. Cell cycle regulation of the p34cdc2/p33cdk2-activating kinase p40MO15. J. Cell Sci. 107:2789-2799.
54. Price, D. H. 2000. P-TEFb, a cyclin-dependent kinase controlling elongation by RNA polymerase II. Mol. Cell. Biol. 20:2629-2634.
55. Ramanathan, Y., S. M. Reza, T. M. Young, M. B. Mathews, and T. Pe'ery. 1999. Human and rodent transcription elongation factor P-TEFb: interactions with human immunodeficiency virus type 1 Tat and carboxy-terminal domain substrate. J. Virol. 73:5448-5458.
56. Rickert, P., W. Seghezzi, F. Shanahan, H. Cho, and E. Lees. 1996. Cyclin C/CDK8 is a novel CTD kinase associated with RNA polymerase II. Oncogene 12:2631-2640.
57. Rossignol, M., I. Kolb-Cheynel, and J. M. Egly. 1997. Substrate specificity of the cdk-activating kinase (CAK) is altered upon association with TFIIH. EMBO J. 16:1628-1637.
58. Roy, R., J. P. Adamczewski, T. Seroz, W. Vermeulen, J. P. Tassan, L. Schaeffer, E. A. Nigg, J. H. Hoeijmakers, and J. M. Egly. 1994. The MO15 cell cycle kinase is associated with the TFIIH transcription-DNA repair factor. Cell 79:1093-1101.
59. Selby, M. J., and B. M. Peterlin. 1990. Trans-activation by HIV-1 Tat via a heterologous RNA binding protein. Cell 62:769-776.
60. Serizawa, H., R. C. Conaway, and J. W. Conaway. 1992. A carboxyl-terminal-domain kinase associated with RNA polymerase II transcription factor delta from rat liver. Proc. Natl. Acad. Sci. USA 89:7476-7480.
61. Serizawa, H., T. P. Makela, J. W. Conaway, R. C. Conaway, R. A. Weinberg, and R. A. Young. 1995. Association of Cdk-activating kinase subunits with transcription factor TFIIH. Nature 374:280-282.
62. Shiekhattar, R., F. Mermelstein, R. P. Fisher, R. Drapkin, B. Dynlacht, H. C. Wessling, D. O. Morgan, and D. Reinberg. 1995 Cdk-activating kinase complex is a component of human transcription factor TFIIH. Nature 374: 283-287.
63. Sterner, D. E., J. M. Lee, S. E. Hardin, and A. L. Greenleaf. 1995. The yeast carboxyl-terminal repeat domain kinase CTDK-I is a divergent cyclin-cyclin-dependent kinase complex. Mol. Cell. Biol. 15:5716-5724.
64. Strich, R., M. R. Slater, and R. E. Esposito. 1989. Identification of negative regulatory genes that govern the expression of early meiotic genes in yeast. Proc. Natl. Acad. Sci. USA 86:10018-10022.
65. Sun, X., Y. Zhang, H. Cho, P. Rickert, E. Lees, W. Lane, and D. Reinberg. 1998. NAT, a human complex containing Srb polypeptides that functions as a negative regulator of activated transcription. Mol. Cell 2:213-222.
66. Surosky, R. T., R. Strich, and R. E. Esposito. 1994. The yeast UME5 gene regulates the stability of meiotic mRNAs in response to glucose. Mol. Cell. Biol. 14:3446-3458.
67. Tassan, J. P., S. J. Schultz, J. Bartek, and E. A. Nigg. 1994. Cell cycle analysis of the activity, subcellular localization, and subunit composition of human CAK (CDK-activating kinase). J. Cell Biol. 127:467-478.
68. Taube, R., K. Fujinaga, J. Wimmer, M. Barboric, and B. M. Peterlin. 1999. Tat transactivation: a model for the regulation of eukaryotic transcriptional elongation. Virology 264:245-253.
69. Thompson, N. E., T. H. Steinberg, D. B. Aronson, and R. R. Burgess. 1989. Inhibition of in vivo and in vitro transcription by monoclonal antibodies prepared against wheat germ RNA polymerase II that react with the heptapeptide repeat of eukaryotic RNA polymerase II. J. Biol. Chem. 264: 11511-11520.
70. Tiley, L. S., S. J. Madore, M. H. Malim, and B. R. Cullen. 1992. The VP16 transcription activation domain is functional when targeted to a promoter-proximal RNA sequence. Genes Dev. 6:2077-2087.
71. Trigon, S., H. Serizawa, J. W. Conaway, R. C. Conaway, S. P. Jackson, and M. Morange. 1998. Characterization of the residues phosphorylated in vitro by different C-terminal domain kinases. J. Biol. Chem. 273:6769-6775.
72. Valay, J. G., M. Simon, M. F. Dubois, O. Bensaude, C. Facca, and G. Faye. 1995. The KIN28 gene is required both for RNA polymerase II mediated transcription and phosphorylation of the Rpblp CTD. J. Mol. Biol. 249:535-544.
73. Valay, J. G., M. Simon, and G. Faye. 1993. The kin28 protein kinase is associated with a cyclin in Saccharomyces cerevisiae. J. Mol. Biol. 234:307-310.
74. Wahi, M., and A. D. Johnson. 1995. Identification of genes required for alpha 2 repression in Saccharomyces cerevisiae. Genetics 140:79-90.
75. Weeks, K. M., C. Ampe, S. C. Schultz, T. A. Steitz, and D. M. Crothers. 1990. Fragments of the HIV-1 Tat protein specifically bind TAR RNA. Science 249:1281-1285.
76. 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.
77. West, M. L., and J. L. Corden. 1995. Construction and analysis of yeast RNA polymerase II CTD deletion and substitution mutations. Genetics 140:1223-1233.
78. Wright, C. M., B. K. Felber, H. Paskalis, and G. N. Pavlakis. 1986. Expression and characterization of the transactivator of HTLV-III/LAV virus. Science 234:988-992.
79. Yang, X., C. H. Herrmann, and A. P. Rice. 1996. The human immunodeficiency virus Tat proteins specifically associate with TAK in vivo and require the carboxyl-terminal domain of RNA polymerase II for function. J. Virol. 70:4576-4584.
80. Yankulov, K., and D. Bentley. 1998. Transcriptional control: Tat cofactors and transcriptional elongation. Curr. Biol. 8:R447-R449.
81. Yankulov, K. Y., and D. L. Bentley. 1997. Regulation of CDK7 substrate specificity by MAT1 and TFIIH. EMBO J. 16:1638-1646.
82. Yuryev, A., and J. L. Corden. 1996. Suppression analysis reveals a functional difference between the serines in positions two and five in the consensus sequence of the C-terminal domain of yeast RNA polymerase II. Genetics 143:661-671.
83. Zawel, L., K. P. Kumar, and D. Reinberg. 1995. Recycling of the general transcription factors during RNA polymerase II transcription. Genes Dev. 9:1479-1490.
84. 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.
85. 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.