Acetylation of conserved lysines in the catalytic core of cyclin-dependent kinase 9 inhibits kinase activity and regulates transcription

Molecular and Cellular Biology

Volumn 28, Issue 7, 2008, Pages 2201-2212

  Sabò, Arianna ^a   Lusic, Marina ^b   Cereseto, Anna ^a   Giacca, Mauro ^a,b  

^a CNR   (Italy)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 9; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE GCN5; HISTONE ACETYLTRANSFERASE PCAF; LYSINE; PHOSPHOTRANSFERASE; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; RNA POLYMERASE II;

ACETYLATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME MODIFICATION; ENZYME REGULATION; EUKARYOTIC CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROVIRUS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ACETYLATION; ADENOSINE TRIPHOSPHATE; CATALYTIC DOMAIN; CELL COMPARTMENTATION; CELL LINE; CYCLIN-DEPENDENT KINASE 9; CYCLINS; DNA, VIRAL; HIV-1; HUMANS; LYSINE; MONOCYTES; PHOSPHORYLATION; PHOSPHOSERINE; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROVIRUSES; RECOMBINANT FUSION PROTEINS; RNA POLYMERASE II; TRANSCRIPTION, GENETIC; VIRUS LATENCY;

EUKARYOTA; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 41149145576     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01557-07     Document Type: Article

References (56)

1. 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.
2. Bourachot, B., M. Yaniv, and C. Muchardt. 2003. Growth inhibition by the mammalian SWI-SNF subunit Brm is regulated by acetylation. EMBO J. 22:6505-6515.
3. Caillaud, A., A. Prakash, E. Smith, A. Masumi, A. G. Hovanessian, D. E. Levy, and I. Marie. 2002. Acetylation of interferon regulatory factor-7 by p300/CREB-binding protein (CBP)-associated factor (PCAF) impairs its DNA binding. J. Biol. Chem. 277:49417-49421.
4. Candau, R., P. A. Moore, L. Wang, N. Barlev, C. Y. Ying, C. A. Rosen, and S. L. Berger. 1996. Identification of human proteins functionally conserved with the yeast putative adaptors ADA2 and GCN5. Mol. Cell. Biol. 16:593-602.
5. Chao, S. H., and D. H. Price. 2001. Flavopiridol inactivates P-TEFb and blocks most RNA polymerase II transcription in vivo. J. Biol. Chem. 276:31793-31799.
6. Col, E., C. Caron, D. Seigneurin-Berny, J. Gracia, A. Favier, and S. Khochbin. 2001. The histone acetyltransferase, hGCN5, interacts with and acetylates the HIV transactivator, Tat. J. Biol. Chem. 276:28179-28184.
7. De Bondt, H. L., J. Rosenblatt, J. Jancarik, H. D. Jones, D. O. Morgan, and S. H. Kim. 1993. Crystal structure of cyclin-dependent kinase 2. Nature 363:595-602.
8. Fogal, V., M. Gostissa, P. Sandy, P. Zacchi, T. Sternsdorf, K. Jensen, P. P. Pandolfi, H. Will, C. Schneider, and G. Del Sal. 2000. Regulation of p53 activity in nuclear bodies by a specific PML isoform. EMBO J. 19:6185-6195.
9. Folks, T. M., J. Justement, A. Kinter, C. A. Dinarello, and A. S. Fauci. 1987. Cytokine-induced expression of HIV- in a chronically infected promonocyte cell line. Science 238:800-802.
10. Fong, Y. W., and Q. Zhou. 2000. Relief of two built-in autoinhibitoiy mechanisms in P-TEFb is required for assembly of a multicomponent transcription elongation complex at the human immunodeficiency virus type 1 promoter. Mol. Cell. Biol. 20:5897-5907.
11. Fu, J., H. G. Yoon, J. Qin, and J. Wong. 2007. Regulation of P-TEFb elongation complex activity by CDK9 acetylation. Mol. Cell. Biol. 27:4641-4651.
12. Fujinaga, K., T. P. Cujec, J. Peng, J. Garriga, D. H. Price, X. Grana, and B. M. Peterlin. 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.
13. Fukuoka, M., H. Daitoku, M. Hatta, H. Matsuzaki, S. Umemura, and A. Fukamizu. 2003. Negative regulation of forkhead transcription factor AFX (Foxo4) by CBP-induced acetylation. Int. J. Mol. Med. 12:503-508.
14. Garriga, J., J. Peng, M. Parreno, D. H. Price, E. E. Henderson, and X. Grana. 1998. Upregulation of cyclin T1/CDK9 complexes during T cell activation. Oncogene 17:3093-3102.
15. Gibbs, C. S., and M. J. Zoller. 1991. Rational scanning mutagenesis of a protein kinase identifies functional regions involved in catalysis and substrate interactions. J. Biol. Chem. 266:8923-8931.
16. Greene, W. C., and B. M. Peterlin. 2002. Charting HIV's remarkable voyage through the cell: basic science as a passport to future therapy. Nat. Med. 8:673-680.
17. Hallows, W. C., S. Lee, and J. M. Denu. 2006. Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc. Natl. Acad. Sci. USA 103:10230-10235.
18. Hanks, S. K., and T. Hunter. 1995. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9:576-596.
19. Kiernan, R., V. Bres, R. W. Ng, M. P. Coudart, S. El Messaoudi, C. Sardet, D. Y. Jin, S. Emiliani, and M. Benkirane. 2003. Post-activation turn-off of NF-kappa B-dependent transcription is regulated by acetylation of p65. J. Biol. Chem. 278:2758-2766.
20. Kiernan, R. E., S. Emiliani, K. Nakayama, A. Castro, J. C. Labbe, T. Lorca, K. Nakayama, and M. Benkirane. 2001. Interaction between cyclin T1 and SCF(SKP2) targets CDK9 for ubiquitination and degradation by the proteasome. Mol. Cell. Biol. 21:7956-7970.
21. Kiernan, R. E., C. Vanhulle, L. Schiltz, E. Adam, H. Xiao, F. Maudoux, C. Calomme, A. Burny, Y. Nakatani, K. T. Jeang, M. Benkirane, and C. Van Lint. 1999. HIV-1 Tat transcriptional activity is regulated by acetylation. EMBO J. 18:6106-6118.
22. Lerin, C., J. T. Rodgers, D. E. Kalume, S. H. Kim, A. Pandey, and P. Puigserver. 2006. GCN5 acetyltransferase complex controls glucose metabolism through transcriptional repression of PGC-1alpha. Cell Metab. 3:429-438.
23. Lusic, M., A. Marcello, A. Cereseto, and M. Giacca. 2003. Regulation of HIV-1 gene expression by histone acetylation and factor recruitment at the LTR promoter. EMBO J. 22:6550-6561.
24. Madhusudan, E. A. Trafny, N. H. Xuong, J. A. Adams, L. F. Ten Eyck, S. S. Taylor, and J. M. Sowadski. 1994. cAMP-dependent protein kinase: crystallographic insights into substrate recognition and phosphotransfer. Protein Sci. 3:176-187.
25. 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.
26. Marcello, A., A. Ferrari, V. Pellegrini, G. Pegoraro, M. Lusic, F. Beltram, and M. Giacca. 2003. Recruitment of human cyclin T1 to nuclear bodies through direct interaction with the PML protein. EMBO J. 22:2156-2166.
27. Marcello, A., M. Lusic, G. Pegoraro, V. Pellegrini, F. Beltram, and M. Giacca. 2004. Nuclear organization and the control of HIV-1 transcription. Gene 326:1-11.
28. Marzio, G., M. Tyagi, M. I. Gutierrez, and M. Giacca. 1998. HIV-1 Tat transactivator recruits p300 and CREB-binding protein histone acetyltransferases to the viral promoter. Proc. Natl. Acad. Sci. USA 95:13519-13524.
29. Meinhart, A., T. Kamenski, S. Hoeppner, S. Baumli, and P. Cramer. 2005. A structural perspective of CTD function. Genes Dev. 19:1401-1415.
30. Mendez, J., and B. Stillman. 2000. Chromatin association of human origin recognition complex, Cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20:8602-8612.
31. Michels, A. A., V. T. Nguyen, A. Fraldi, V. Labas, M. Edwards, F. Bonnet, L. Lania, and O. Bensaude. 2003. MAQ1 and 7SK RNA interact with CDK9/cyclin T complexes in a transcription-dependent manner. Mol. Cell. Biol. 23:4859-4869.
32. Mukherjee, S., G. Keitany, Y. Li, Y. Wang, H. L. Ball, E. J. Goldsmith, and K. Orth. 2006. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312:1211-1214.
33. Munshi, N., T. Agalioti, S. Lomvardas, M. Merika, G. Chen, and D. Thanos. 2001. Coordination of a transcriptional switch by HMGI(Y) acetylation. Science 293:1133-1136.
34. 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.
35. Nguyen, V. T., T. Kiss, A. A. Michels, and O. Bensaude. 2001. 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature 414:322-325.
36. Paulson, M., C. Press, E. Smith, N. Tanese, and D. E. Levy. 2002. IFN-stimulated transcription through a TBP-free acetyltransferase complex escapes viral shutoft. Nat. Cell Biol. 4:140-147.
37. Peterlin, B. M., and D. H. Price. 2006. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 23:297-305.
38. Price, D. H. 2000. P-TEFb, a cyclin-dependent kinase controlling elongation by RNA polymerase 11. Mol. Cell. Biol. 20:2629-2634.
39. Sano, M., M. Abdellatif, H. Oh, M. Xie, L. Bagella, A. Giordano, L. H. Michael, F. J. DeMayo, and M. D. Schneider. 2002. Activation and function of cyclin T-Cdk9 (positive transcription elongation factor-b) in cardiac muscle-cell hypertrophy. Nat. Med. 8:1310-1317.
40. Schwer, B., J. Bunkenborg, R. O. Verdin, J. S. Andersen, and E. Verdin. 2006. Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc. Natl. Acad. Sci. USA 103:10224-10229.
41. Shim, E. Y., A. K. Walker, Y. Shi, and T. K. Blackwell. 2002. CDK-9/cyclin T (P-TEFb) is required in two postinitiation pathways for transcription in the C. elegans embryo. Genes Dev. 16:2135-2146.
42. Starai, V. J., I. Celic, R. N. Cole, J. D. Boeke, and J. C. Escalante-Semerena. 2002. Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science 298:2390-2392.
43. Taube, R., X. Lin, D. Irwin, K. Fujinaga, and B. M. Peterlin. 2002. Interaction between P-TEFb and the C-terminal domain of RNA polymerase II activates transcriptional elongation from sites upstream or downstream of target genes. Mol. Cell. Biol. 22:321-331.
44. Thompson, P. R., D. Wang, L. Wang, M. Fulco, N. Pediconi, D. Zhang, W. An, Q. Ge, R. G. Roeder, J. Wong, M. Levrero, V. Sartorelli, R. J. Cotter, and P. A. Cole. 2004. Regulation of the p300 HAT domain via a novel activation loop. Nat. Struct. Mol. Biol. 11:308-315.
45. Todorovic, V., S. Giadrossi, C. Pelizon, R. Mendoza-Maldonado, H. Masai, and M. Giacca. 2005. Human origins of DNA replication selected from a library of nascent DNA. Mol. Cell 19:567-575.
46. von Mikecz, A., S. Zhang, M. Montminy, E. M. Tan, and P. Hemmerich. 2000. CREB-binding protein (CBP)/p300 and RNA polymerase II colocalize in transcriptionally active domains in the nucleus. J. Cell Biol. 150:265-273.
47. 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.
48. 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 promonocyte cell lines. Proc. Natl. Acad. Sci. USA 94:12331-12336.
49. Yang, X. J. 2004. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res. 32:959-976.
50. 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.
51. Yang, Z., Q. Zhu, K. Luo, and Q. Zhou. 2001. The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 414:317-322.
52. Yik, J. H., R. Chen, R. Nishimura, J. L. Jennings, A. J. Link, and Q. Zhou. 2003. Inhibition of P-TEFb (CDK9/cyclin T) kinase and RNA polymerase II transcription by the coordinated actions of HEXIM1 and 7SK snRNA. Mol. Cell 12:971-982.
53. Zhou, M., M. A. Halanski, M. F. Radonovich, F. Kashanchi, J. Peng, D. H. Price, and J. N. Brady. 2000. Tat modifies the activity of CDK9 to phosphoiylate serine 5 of the RNA polymerase II carboxyl-terminal domain during human immunodeficiency virus type 1 transcription. Mol. Cell. Biol. 20:5077-5086.
54. 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.
55. 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.
56. Zoller, M. J., N. C. Nelson, and S. S. Taylor. 1981. Affinity labeling of cAMP-dependent protein kinase with p-fluorosulfonylbenzoyl adenosine. Covalent modification of lysine 71. J. Biol. Chem. 256:10837-10842.