CDK9 Autophosphorylation Regulates High-Affinity Binding of the Human Immunodeficiency Virus Type 1 Tat–P-TEFb Complex to TAR RNA

REFERENCES

• Bieniasz, P., Grdina, T. A., Bogerd, H. P., and Cullen, B. R.. 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
   PubMed Web of Science ®Google Scholar
• Bieniasz, P. D., Grdina, T. A., Bogerd, H. P., and Cullen, B. R.. 1999. Analysis of the effect of natural sequence variation in Tat and in cyclin T on the formation and RNA binding properties of Tat-cyclin T complexes. J. Virol. 73:5777–5786
   PubMedGoogle Scholar
• Bieniasz, P. D., Grdina, T. A., Bogerd, H. P., and Cullen, B. R.. 1999. Highly divergent lentiviral Tat proteins activate viral gene expression by a common mechanism. Mol. Cell. Biol. 19:4592–4599
   PubMedGoogle Scholar
• Bieniasz, P. D., Grdina, T. A., Bogerd, H. P., and Cullen, B. R.. 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
   PubMed Web of Science ®Google Scholar
• Buermeyer, A. B., Thompson, N. E., Strasheim, L. A., Burgess, R. R., and Farnham, P. J.. 1992. The HIP1 initiator element plays a role in determining the in vitro requirement of the dihydrofolate reductase gene promoter for the C-terminal domain of RNA polymerase II. Mol. Cell. Biol. 12:2250–2259
   PubMedGoogle Scholar
• Chen, D., Fong, Y., and Zhou, Q.. 1999. Specific interaction of Tat with the human but not rodent P-TEFb complex mediates the species-specific Tat activation of HIV-1 transcription. Proc. Natl. Acad. Sci. USA 96:2728–2733
   PubMed Web of Science ®Google Scholar
• Chen, D., and Zhou, Q.. 1999. Tat activates human immunodeficiency virus type 1 transcriptional elongation independent of TFIIH kinase. Mol. Cell. Biol. 19:2863–2871
   PubMed Web of Science ®Google Scholar
• Cujec, T. P., Okamoto, H., Fujinaga, K., Meyer, J., Chamberlin, H., Morgan, D. O., and Peterlin, B. M.. 1997. The HIV trans-activator Tat binds to the CDK-activating kinase (CAK) and activates the phosphorylation of the C-terminal domain of RNA polymerase II. Genes Dev. 11:2645–2657
   PubMed Web of Science ®Google Scholar
• Dahmus, M. E.. 1996. Reversible phosphorylation of the C-terminal domain of RNA polymerase II. J. Biol. Chem. 271:19009–19012
   PubMed Web of Science ®Google Scholar
• Douziech, M., Forget, D., Greenblatt, J., and Coulombe, B.. 1999. Topological localization of the carboxyl-terminal domain of RNA polymerase II in the initiation complex. J. Biol. Chem. 274:19868–19873
   PubMedGoogle Scholar
• Du, L., and Warren, S. L.. 1997. A functional interaction between the carboxy-terminal domain of RNA polymerase II and pre-mRNA splicing. J. Cell Biol. 136:5–18
   PubMed Web of Science ®Google Scholar
• Flores, O., Lee, G., Kessler, J., Miller, M., Schlief, W., Tomassini, J., and Hazuda, D.. 1999. Host-cell positive transcription elongation factor b kinase activity is essential and limiting for HIV1 type 1 replication. Proc. Natl. Acad. Sci. USA 96:7208–7213
   PubMed Web of Science ®Google Scholar
• Fu, T. J., Peng, J., Lee, G., Price, D. H., and Flores, O.. 1999. Cyclin K functions as a CDK9 regulatory subunit and participates in RNA polymerase II transcription. J. Biol. Chem. 274:34527–34530
   PubMed Web of Science ®Google Scholar
• Fujinaga, K., Taube, R., Wimmer, J., Cujec, T. P., and Peterlin, B. M.. 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
   PubMed Web of Science ®Google Scholar
• Fujinaga, L., Cujec, T. P., Peng, J., Garriga, J., Price, D. H., Grana, X., and Peterlin, B. M.. 1998. The ability of positive transcription elongation factor B to transactivate human immunodeficiency virus transcription depends on a functional kinase domain, cyclin T1, and Tat. J. Virol. 72:7154–7159
   PubMed Web of Science ®Google Scholar
• Garber, M. E., and Jones, K. A.. 1999. HIV-1 Tat: coping with negative elongation factors. Curr. Opin. Immunol. 11:460–465
   PubMed Web of Science ®Google Scholar
• Garber, M. E., Wei, P., and Jones, K. A.. 1998. HIV-1 Tat interacts with Cyclin T1 to direct the P-TEFb complex to TAR RNA. Cold Spring Harbor Symp. Quant. Biol. 63:371–380
   PubMedGoogle Scholar
• Garber, M. E., Wei, P., KewalRamani, V. N., Mayall, T. P., Herrmann, C. H., Rice, A. P., Littman, D. R., and Jones, K. A.. 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
   PubMed Web of Science ®Google Scholar
• Garcia-Martinez, L. F., Mavankal, G., Neveu, J. M., Lane, W. S., Ivanov, D., and Gaynor, R. B.. 1997. Purification of a Tat-associated kinase reveals a TFIIH complex that modulates HIV-1 transcription. EMBO J. 16:2836–2850
   PubMed Web of Science ®Google Scholar
• Garriga, J., Mayol, X., and Graña, X.. 1996. The CDC2-related kinase PITALRE is the catalytic subunit of active multimeric protein complexes. Biochem. J. 319:293–298
   PubMedGoogle Scholar
• Gold, M. O., Yang, X., Herrmann, C. H., and Rice, A. P.. 1998. PITALRE, the catalytic subunit of TAK, is required for human immunodeficiency virus Tat trans-activation in vivo. J. Virol. 72:4448–4453
   PubMedGoogle Scholar
• Hartzog, G. A., Wada, T., Handa, H., and Winston, F.. 1998. Evidence that Spt4, Spt5, and Spt6 control transcription elongation by RNA polymerase II in Saccharomyces cerevisae. Genes Dev. 12:357–369
   PubMed Web of Science ®Google Scholar
• Herrmann, C. H., and Rice, A. P.. 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
   PubMed Web of Science ®Google Scholar
• Herrmann, C. H., and Rice, A. P.. 1993. Specific interaction of the human immunodeficiency virus Tat proteins with a cellular protein kinase. Virol. 197:601–68
   PubMed Web of Science ®Google Scholar
• Ho, C. K., and Shuman, S.. 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
   PubMed Web of Science ®Google Scholar
• Isel, C., and Karn, J.. 1999. Direct evidence that HIV-1 Tat stimulates RNA polymerase II carboxyl-terminal domain hyperphosphorylation during transcriptional elongation. J. Mol. Biol. 290:929–941
   PubMed Web of Science ®Google Scholar
• Ivanov, D., Kwak, Y. T., Nee, E., Guo, J., Garcia-Martinez, L., and Gaynor, R. B.. 1999. Cyclin T1 domains involved in complex formation with Tat and TAR RNA are critical for tat-activation. J. Mol. Biol. 288:41–56
   PubMedGoogle Scholar
• Jeffrey, P. D., Russo, A. A., Polyak, K., Gibbs, E., Hurwitz, J., Massague, J., and Pavletich, N. P.. 1995. Mechanism of CDK activation revealed by the structure of a cyclin A-CDK2 complex. Nature 376:313–320
   PubMed Web of Science ®Google Scholar
• Jones, K. A.. 1997. Taking a new TAK on Tat transactivation. Genes Dev. 11:2593–2599
   PubMedGoogle Scholar
• Karn, J.. 1999. Tackling Tat. J. Mol. Biol. 293:235–254
   PubMed Web of Science ®Google Scholar
• Keen, N. J., Churcher, M. J., and Karn, J.. 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
   PubMedGoogle Scholar
• Keen, N. J., Gait, M. J., and Karn, J.. 1996. Human immunodeficiency virus type-1 Tat is an integral component of the activated transcription-elongation complex. Proc. Natl. Acad. Sci. USA 93:2505–2510
   PubMedGoogle Scholar
• Kiernan, R. E., Vanhulle, C., Schiltz, L., Adam, E., Xiao, H., Maudoux, F., Calomme, C., Burny, A., Nakatani, Y., Jeang, K. T., Benkirane, M., and Van Lint, C.. 1999. HIV-1 Tat transcriptional activity is regulated by acetylation. EMBO J. 18:6106–6118
   PubMed Web of Science ®Google Scholar
• Kwak, Y. T., Ivanov, D., Guo, J., Nee, E., and Gaynor, R. B.. 1999. Role of the human and murine cyclin T proteins in regulating HIV-1 tat-activation. J. Mol. Biol. 288:57–69
   PubMedGoogle Scholar
• Mancebo, H. S., Lee, G., Flygare, J., Tomassini, J., Luu, P., Zhu, Y., Blau, C., Hazuda, D., Price, D., and Flores, O.. 1997. P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev. 11:2633–2644
   PubMed Web of Science ®Google Scholar
• Marshall, N. F., Peng, J., Xie, Z., and Price, D. H.. 1996. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J. Biol. Chem. 271:27176–27183
   PubMed Web of Science ®Google Scholar
• Ott, M., Schnolzer, M., Garnica, J., Fischle, W., Emiliani, S., Rackwitz, H. R., and Verdin, E.. 1999. Acetylation of the HIV-1 Tat protein by p300 is important for its transcriptional activity. Curr. Biol. 9:1489–1492
   PubMed Web of Science ®Google Scholar
• Palangat, M., Meier, T. I., Keene, R. G., and Landick, R.. 1998. Transcriptional pausing at +62 of the HIV-1 nascent RNA modulates formation of the TAR RNA structure. Mol. Cell 1:1033–1042
   PubMed Web of Science ®Google Scholar
• Parada, C. A., and Roeder, R. G.. 1996. Enhanced processivity of RNA polymerase II triggered by Tat-induced phosphorylation of its carboxy-terminal domain. Nature 384:375–378
   PubMed Web of Science ®Google Scholar
• Peng, J., Zhu, Y., Milton, J. T., and Price, D. H.. 1998. Identification of multiple cyclin subunits of human P-TEFb. Genes Dev. 12:755–762
   PubMed Web of Science ®Google Scholar
• Peterson, S. R., Dvir, A., Anderson, C. W., and Dynan, W. S.. 1992. DNA binding provides a signal for phosphorylation of the RNA polymerase II heptapeptide repeats. Genes Dev. 6:426–438
   PubMedGoogle Scholar
• Ping, Y. H., and Rana, T. M.. 1999. Tat-associated kinase (P-TEFb): a component of transcription preinitiation and elongation complexes. J. Biol. Chem. 274:7399–7404
   PubMed Web of Science ®Google Scholar
• Ramanathan, Y., Reza, S. M., Young, T. M., Mathews, M. B., and Pe'ery, T.. 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
   PubMed Web of Science ®Google Scholar
• Russo, A. A., Jeffrey, P. D., and Pavletich, N. P.. 1996. Structural basis of cyclin-dependent kinase activation by phosphorylation. Nat. Struct. Biol. 3:696–700
   PubMedGoogle Scholar
• Taube, R., Fujinaga, K., Irwin, D., Wimmer, J., Geyer, M., and Peterlin, B. M.. 2000. Interactions between equine cyclin T1, Tat, and TAR are disrupted by a leucine-to-valine substitution fopund in human cyclin T1. J. Virol. 74:892–898
   PubMedGoogle Scholar
• Thompson, N. E., Aronson, D. B., and Burgess, R. R.. 1990. Purification of eukaryotic RNA polymerase II by immunoaffinity chromatography: elution of active enzyme with protein stabilizing agents from a polyol-responsive monoclonal antibody. J. Biol. Chem. 265:7069–7077
   PubMedGoogle Scholar
• Thompson, N. E., and Burgess, R. R.. 1996. Immunoaffinity purification of RNA polymerase II and transcription factors using polyol-responsive monoclonal antibodies. Methods Enzymol. 274:513–526
   PubMedGoogle Scholar
• Van Der Geer, P., Luo, K., Sefton, B. M., and Hunter, T.. 1993. Phosphopeptide mapping and phosphoamino acid analysis on cellulose thin-layer plates Protein phosphorylation. Hardie, D. G. 31–60 Oxford University Press, Oxford, England
   Google Scholar
• Verhoef, K., Tijms, M., and Berkhout, B.. 1997. Optimal Tat-mediated activation of the HIV-1 LTR promoter requires a full-length TAR RNA hairpin. Nucleic Acids Res. 25:496–502
   PubMed Web of Science ®Google Scholar
• Wada, T., Takagi, T., Yamaguchi, Y., Ferdous, A., Imai, T., Hirose, S., Sugimoto, S., Yano, K., Hartzog, G. A., Winston, F., Buratowski, S., and Handa, H.. 1998. DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev. 12:343–356
   PubMed Web of Science ®Google Scholar
• Wada, T., Takagi, T., Yamaguchi, Y., Watanabe, D., and Handa, H.. 1998. Evidence that P-TEFb alleviates the negative effect of DSIF on RNA polymerase II-dependent transcription in vitro. EMBO J. 17:7395–7403
   PubMed Web of Science ®Google Scholar
• Wei, P., Garber, M. E., Fang, S.-M., Fischer, W. H., and Jones, K. A.. 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
   PubMed Web of Science ®Google Scholar
• Wimmer, J., Fujinaga, K., Taube, R., Cujec, T. P., Zhu, Y., Peng, J., Price, D. H., and Peterlin, B. M.. 1999. Interactions between Tat and TAR and human immunodeficiency virus replication are facilitated by human cyclin T1 but not cyclins T2a or T2b. Virology 255:182–189
   PubMed Web of Science ®Google Scholar
• Wu-Baer, F., Lane, W. S., and Gaynor, R. B.. 1998. Role of the human homolog of the yeast transcription factor SPT5 in HIV-1 Tat-activation. J. Mol. Biol. 277:179–197
   PubMed Web of Science ®Google Scholar
• Yamaguchi, Y., Takagi, T., Wada, T., Yano, K., Furuya, A., Sugimoto, S., Hasegawa, J., and Handa, H.. 1999. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 97:41–51
   PubMed Web of Science ®Google Scholar
• Yamaguchi, Y., Wada, T., and Handa, H.. 1998. Interplay between positive and negative elongation factors: drawing a new view of DRB. Genes Cells 3:9–15
   PubMedGoogle Scholar
• Yamaguchi, Y., Wada, T., Watanabe, D., Takagi, T., Hasegawa, J., and Handa, H.. 1999. Structure and function of the human transcription elongation factor DSIF. J. Biol. Chem. 274:8085–8092
   PubMed Web of Science ®Google Scholar
• Yang, X., Gold, M. O., Tang, D. N., Lewis, D. E., Aguilar-Cordova, E., Rice, A. P., and Herrmann, C. H.. 1997. TAK, an HIV Tat-associated kinase, is a member of the cyclin-dependent family of protein kinases and is induced by activation of peripheral blood lymphocytes and differentiation of promonocytic cell lines. Proc. Natl. Acad. Sci. USA 94:12331–12336
   PubMed Web of Science ®Google Scholar
• Zhou, Q., Chen, D., Pierstorff, E., and Luo, K.. 1998. Transcription elongation factor P-TEFb mediates Tat activation of HIV-1 transcription at multiple stages. EMBO J. 17:3681–3691
   PubMed Web of Science ®Google Scholar
• Zhu, Y., Pe'ery, T., Peng, J., Ramanathan, Y., Marshall, N., Marshall, T., Amendt, B., Mathews, M. B., and Price, D. H.. 1997. Transcription elongation factor P-TEFb is required for HIV-1 Tat transactivation in vitro. Genes Dev. 11:2622–2632
   PubMed Web of Science ®Google Scholar