Human and rodent transcription elongation factor P-TEFb: Interactions with human immunodeficiency virus type 1 Tat and carboxy-terminal domain substrate

Journal of Virology

Volumn 73, Issue 7, 1999, Pages 5448-5458

  Ramanathan, Y ^a   Reza, Syed M ^a   Young, Tara M ^a   Mathews, Michael B ^a   Pe'ery, Tsafi ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL EXTRACT; CYCLIN T1; CYCLINE; ELONGATION FACTOR; MAGNESIUM ION; POSITIVE TRANSCRIPTION ELONGATION FACTOR BETA; PROTEIN KINASE; SERINE; THREONINE; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; ZINC ION;

AMINO ACID ANALYSIS; ANIMAL CELL; ARTICLE; CHROMOSOME 12; COMPLEX FORMATION; ENZYME BINDING; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; ENZYME PURIFICATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOPRECIPITATION; MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SPECIES DIFFERENCE; TRANSACTIVATION; TRANSCRIPTION REGULATION;

EID: 0032991426     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.7.5448-5458.1999     Document Type: Article

References (80)

1. Akoulitchev, S., T. P. Makela, R. A. Weinberg, and D. Reinberg. 1995. Requirement for TFIIH kinase activity in transcription by RNA polymerase II. Nature (London) 377:557-560.
2. Alonso, A., T. P. Cujec, and B. M. Peterlin. 1994. Effects of human chromosome 12 on interactions between Tat and TAR of human immunodeficiency virus type 1. J. Virol. 68:6505-6513.
3. 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.
4. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1991. Current protocols in molecular biology, 2nd ed., vol. 1. John Wiley & Sons, New York, N.Y.
5. Braddock, M., A. M. Thorburn, A. J. Kingsman, and S. M. Kingsman. 1991. Blocking of Tat-dependent HIV-1 RNA modification by an inhibitor of RNA polymerase II processivity. Nature (London) 350:439-441.
6. Carroll, R., B. M. Peterlin, and D. Derse. 1992. Inhibition of human immunodeficiency virus type 1 Tat activity by coexpression of heterologous trans activators. J. Virol. 66:2000-2007.
7. 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 I and HIV-1. J. Biol. Chem. 271:27888-27894.
8. Cujec, T. P., H. Cho, E. Maldonado, J. Meyer, D. Reinberg, and B. M. Peterlin. 1997. The human immunodeficiency virus transactivator Tat interacts with the RNA polymerase II holoenzyme. Mol. Cell. Biol. 17:1817-1823.
9. Cujec, T. P., H. Okamoto, K. Fujinaga, J. Meyer, H. Chamberlin, D. O. Morgan, and B. M. Peterlin. 1997. The HIV transactivator TAT binds to the CDK-activating kinase and activates the phosphorylation of the carboxy-terminal domain of RNA polymerase II. Genes Dev. 11:2645-2657.
10. Dahmus, M. E. 1996. Phosphorylation of mammalian RNA polymerase II. Methods Enzymol. 273:185-193.
11. Dahmus, M. E. 1996. Reversible phosphorylation of the C-terminal domain of RNA polymerase II. J. Biol. Chem. 271:19009-19012.
12. Dahmus, M. E. 1994. The role of multisite phosphorylation in the regulation of RNA polymerase II activity. Prog. Nucleic Acid Res. Mol. Biol. 48:143-179.
13. Dahmus, M. E., A. Shilatifard, J. W. Conaway, and R. C. Conaway. 1995. Phosphorylation of the C-terminal domain of RNA polymerase II. Biochim. Biophys. Acta 1261:171-182.
14. De Luca, A., V. Esposito, A. Baldi, P. P. Claudio, Y. Fu, M. Caputi, M. M. Pisano, F. Baldi, and A. Giordano. 1997. CDC2-related kinase PITALRE phosphorylates pRb exclusively on serine and is widely expressed in human tissues. J. Cell. Physiol. 172:265-273.
15. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
16. Dignam, J. D., P. L. Martin, B. S. Shastry, and R. G. Roeder. 1983. Eukaryotic gene transcription with purified components. Methods Enzymol. 101: 582-598.
17. Dingwall, C., I. Ernberg, M. J. Gait, S. M. Green, S. Hearphy, 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.
18. Dvir, A., S. Tan, J. W. Conaway, and R. C. Conaway. 1997. Promoter escape by RNA polymerase II. Formation of an escape-competent transcriptional intermediate is a prerequisite for exit of polymerase from the promoter. J. Biol. Chem. 272:28175-28178.
19. Echetebu, C. O., H. Rhim, C. H. Herrmann, and A. P. Rice. 1994. Construction and characterization of a potent HIV-2 Tat transdominant mutant protein. J. Acquired Immune Defic. Syndr. 7:655-664.
20. Fisher, R. P., P. Jin, H. M. Chamberlin, and D. O. Morgan. 1995. Alternative mechanisms of CAK assembly require an assembly factor or an activating kinase. Cell 83:47-57.
21. Fisher, R. P., and D. O. Morgan. 1994. A novel cyclin associates with MO15/CDK7 to form the CDK-activating kinase. Cell 78:713-724.
22. Frankel, A. D., D. S. Bredt, and C. O. Pabo. 1988. Tat protein from human immunodeficiency virus forms a metal-linked dimer. Science 240:70-73.
23. Garda-Martínez, L. F., G. Mavankal, J. M. Neveu, W. S. Lane, D. Ivanov, and R. B. Gaynor. 1997. Purification of a Tat-associated kinase reveals a TFIIH complex that modulates HIV-1 transcription. EMBO J. 16:2836-2850.
24. Garriga, J., X. Mayol, and X. Graña. 1996. The CDC2-related kinase PITALRE is the catalytic subunit of active multimeric protein complexes. Biochem. J. 319:293-298.
25. Garriga, J., E. Segura, X. Mayol, C. Grubmeyer, and X. Graña. 1996. Phosphorylation site specificity of the CDC2-related kinase PITALRE. Biochem. J. 320:983-989.
26. Gaynor, R. B. 1995. Regulation of HIV-1 gene expression by the transactivator protein Tat. Curr. Top. Microbiol. Immunol. 193:51-77.
27. Gebara, M. M., M. H. Sayre, and J. L. Corden. 1997. Phosphorylation of the carboxy-terminal repeat domain in RNA polymerase II by cyclin-dependent kinases is sufficient to inhibit transcription. J. Cell. Biochem. 64:390-402.
28. Graeble, M. A., M. J. Churcher, A. D. Lowe, M. J. Gait, and J. Karn. 1993. Human immunodeficiency virus type 1 transactivator protein, tat, stimulates transcriptional read-through of distal terminator sequences in vitro. Proc. Natl. Acad. Sci. USA 90:6184-6188.
29. Graña, X., A. DeLuca, 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.
30. Greenberg, M. E., D. A. Ostapenko, and M. B. Mathews. 1997. Potentiation of human immunodeficiency virus type 1 Tat by human cellular proteins. J. Virol. 71:7140-7144.
31. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N. Y.
32. Harper, J. W., and S. J. Elledge. 1998. The role of Cdk7 in CAK function, a retro-retrospective. Genes Dev. 12:285-289.
33. Hart, C. E., C. Y. Ou, J. C. Galphin, J. Moore, L. T. Bacheler, J. J. Wasmuth, S. R. Petteway, Jr., and G. Schochetman. 1989. Human chromosome 12 is required for elevated HIV-1 expression in human-hamster hybrid cells. Science 246:488-491.
34. Herrmann, C. H., M. O. Gold, and A. P. Rice. 1996. Viral transactivators specifically target distinct cellular protein kinases that phosphorylate the RNA polymerase II C-terminal domain. Nucleic Acids Res. 24:501-508.
35. 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.
36. Herrmann, 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.
37. Hirose, Y., and J. L. Manley. 1998. RNA polymerase II is an essential mRNA polyadenylation factor. Nature (London) 395:93-96.
38. Hottiger, M. O., and G. J. Nabel. 1998. Interaction of human immunodeficiency virus type 1 Tat with the transcriptional coactivators p300 and CREB binding protein. J. Virol. 72:8252-8256.
39. Ippolito, J. A., and T. A. Steitz. 1998. A 1.3-A resolution crystal structure of the HIV-1 trans-activation response region RNA stem reveals a metal ion-dependent bulge conformation. Proc. Natl. Acad. Sci. USA 95:9819-9824.
40. Jakobi, R., and J. A. Traugh. 1995. Site-directed mutagenesis and structure/ function studies of casein kinase II correlate stimulation of activity by the beta subunit with changes in conformation and ATP/GTP utilization. Eur. J. Biochem. 230:1111-1117.
41. Jeang, K. T., B. Berkhout, and B. Dropulic. 1993. Effects of integration and replication on transcription of the HIV-1 long terminal repeat. J. Biol. Chem. 268:24940-24949.
42. Kao, S. Y., A. F. Caiman, 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 (London) 330:489-493.
43. Kashanchi, F., G. Pira, M. F. Radonovich, J. F. Duval, A. Fattaey, C. M. Chian, R. G. Reeder, and J. N. Bradj. 1994. Direct interaction of human TFIID with the HIV-1 transactivator Tat. Nature (London) 367:295-299.
44. Kato, H., H. Sumimoto, P. Pognonec, C-H. Chen, C. A. Rosen, and R. G. Roeder. 1992. HIV-1 tat acts as a processivity factor in vitro in conjunction with cellular elongation factors. Genes Dev. 6:655-666.
45. Kessler, M., and M. B. Mathews. 1992. Premature termination and processing of human immunodeficiency virus type 1-promoted transcripts. J. Virol. 66:4488-4496.
46. Laspia, M. F., A. P. Rice, and M. B. Mathews. 1989. HIV-1 Tat protein increases transcriptional initiation and stabilizes elongation. Cell 59:283-292.
47. 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.
48. Makela, T. P., J. D. Parvin, J. Kim, L. J. Huber, P. A. Sharp, and R. A. Weinberg. 1995. A kinase-deficient transcription factor TFIIH is functional in basal and activated transcription. Proc. Natl. Acad. Sci. USA 92:5174-5178.
49. 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.
50. Marciniak, R. A., B. J. Calnan, A. D. Frankel, and P. A. Sharp. 1990. HIV-1 Tat protein trans-activates transcription in vitro. Cell 63:791-802.
51. Marciniak, R. A., and P. A. Sharp. 1991. HIV-1 Tat protein promotes formation of more-processive elongation complexes. EMBO J. 10:4189-4196.
52. Marshall, N. F., J. Peng, Z. Xie, and D. H. Price. 1996. Control of RNA polymerase II elongation potential by a novel carboxl-terminal domain kinase. J. Biol. Chem. 271:27176-27183.
53. Marshall, N. F., and D. H. Price. 1992. Control of formation of two distinct classes of RNA polymerase II elongation complexes. Mol. Cell. Biol. 12: 2078-2090.
54. 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.
55. McCracken, S., N. Fong, K. Yankulov, S. Ballantyne, G. Pan, J. Greenblatt, S. D. Patterson, M. Wickens, and D. L. Bentley. 1997. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature (London) 385:357-361.
56. Modesti, N., J. Garcia, C. Debouck, M. Peterlin, and R. Gaynor. 1991. Trans-dominant Tat mutants with alterations in the basic domain inhibit HIV-1 gene expression. New Biol. 3:759-768.
57. Mortillaro, M. J., B. J. Blencowe, X. Wei, H. Nakayasu, L. Du, S. L. Warren, P. A. Sharp, and R. Berezney. 1996. A hyperphosphorylated form of the large subunit of RNA polymerase II is associated with splicing complexes and the nuclear matrix. Proc. Natl. Acad. Sci. USA 93:8253-8257.
58. Newstein, M., E. J. Stanbridge, G. Casey, and P. R. Shank. 1990. Human chromosome 12 encodes a species-specific factor which increases human immunodeficiency virus type 1 Tat-mediated transactivation in rodent cells. J. Virol. 64:4565-4567.
59. Nonet, M., D. Sweetser, and R. A. Young. 1987. Functional redundancy and structural polymorphism in the large subunit of RNA polymerase II. Cell 50:909-915.
60. O'Brien, T., S. Hardin, A. Greenleaf, and J. T. Lis. 1994. Phosphorylation of RNA polymerase II C-terminal domain and transcriptional elongation. Nature (London) 370:75-77.
61. 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.
62. Orphanides, G., T. Lagrange, and D. Reinberg. 1996. The general transcription factors of RNA polymerase II. Genes Dev. 10:2657-2683.
63. Orsini, M. J., and C. M. Debouck. 1996. Inhibition of human immunodeficiency virus type 1 and type 2 Tat function by transdominant Tat protein localized to both the nucleus and cytoplasm. J. Virol. 70:8055-8063.
64. 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 (London) 384:375-378.
65. Patturajan, M., R. J. Schulte, B. M. Setton, 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.
66. Peng, J., N. F. Marshall, and D. H. Price. 1998. Identification of a cyclin subunit required for the function of Drosophila P-TEFb. J. Biol. Chem. 273:13855-13860.
67. 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.
68. Rhim, H., C. O. Echetebu, C. H. Herrmann, and A. P. Rice. 1994. Wild-type and mutant HIV-1 and HIV-2 Tat proteins expressed in Escherichia coli as fusions with glutathione S-transferase. J. Acquired Immune Defic. Syndr. 7:1116-1121.
69. Rice, A. P., and F. Carlotti. 1990. Structural analysis of wild-type and mutant human immunodeficiency virus type 1 Tat proteins. J. Virol. 64:6018-6026.
70. Serizawa, H., J. W. Conaway, and R. C. Conaway. 1993. Phosphorylation of C-terminal domain of RNA polymerase II is not required in basal transcription. Nature (London) 363:371-374.
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. Weeks, K. M., C. Ampe, S. Schultz, T. Steite, and D. M. Crothers. 1990. Fragments of the HIV-1 Tat protein specifically bind TAR RNA. Science 249:1281-1285.
73. 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.
74. Yang, X., M. O. Gold, D. N. Tang, D. E. Lewis, E. Aguilar-Cordova, A. P. Rice, and C. H. Herrmann. 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.
75. 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. 79:4576-4584.
76. Yankulov, K. Y., and D. L. Bentley. 1997. Regulation of CDK7 substrate specificity by MAT1 and TFIIH. EMBO J. 16:1638-1646.
77. Zhang, J., J. L. Corden, A. Shilatifard, J. W. Conaway, and R. C. Conaway. 1991. Identification of phosphorylation sites in the repetitive carboxyl-terminal domain of the mouse RNA polymerase II largest subunit. J. Biol. Chem. 266:2290-2296.
78. 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.
79. Zhou, Q., and P. A. Sharp. 1996. Tat-SF1: cofactor for stimulation of transcriptional elongation by HIV-1 Tat. Science 274:605-610.
80. 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.