Visualization of positive transcription elongation factor b (P-TEFb) activation in living cells

Journal of Biological Chemistry

Volumn 290, Issue 3, 2015, Pages 1829-1836

  Fujinaga, Koh ^a   Luo, Zeping ^a   Schaufele, Fred ^a   Matija Peterlin, B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASSAYS; CELLS; CHEMICAL ACTIVATION; DISEASES; ELONGATION; ENZYME INHIBITION; FLUORESCENCE; TRANSCRIPTION; VISUALIZATION;

BIOCHEMICAL ASSAY; C-TERMINAL DOMAINS; EXPERIMENTAL SYSTEM; HISTONE DEACETYLASE INHIBITOR; NUCLEAR RIBONUCLEOPROTEIN; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; REGULATION OF TRANSCRIPTION; SUBEROYLANILIDE HYDROXAMIC ACIDS;

CYTOLOGY;

AZACITIDINE; BROMODOMAIN INHIBITOR; CYCLIN DEPENDENT KINASE 9; HEXAMETHYLENE BISACETAMIDE INDUCIBLE PROTEIN 1; HISTONE DEACETYLASE INHIBITOR; HYBRID PROTEIN; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROTEIN KINASE C; RNA POLYMERASE II; UNCLASSIFIED DRUG; VORINOSTAT; BACTERIAL PROTEIN; GLYCEROL; HYDROXAMIC ACID; PHOTOPROTEIN; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; SUPERNATANT; TRANSCRIPTION REGULATION; WESTERN BLOTTING; APOPTOSIS; CELL FREE SYSTEM; CHEMISTRY; FLUORESCENCE MICROSCOPY; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PLASMID; PROTEIN TERTIARY STRUCTURE; TIME;

APOPTOSIS; AZACITIDINE; BACTERIAL PROTEINS; CELL-FREE SYSTEM; GENETIC COMPLEMENTATION TEST; GLYCEROL; HEK293 CELLS; HELA CELLS; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; PLASMIDS; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROTEIN KINASE C; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOPROTEINS; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA-BINDING PROTEINS; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84921418379     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.605816     Document Type: Article

References (50)

1. Peterlin, B. M. (2010) Transcription elongation takes central stage: the P-TEFb connection. Cell Cycle 9, 2933-2934
2. Price, D. H. (2008) Poised polymerases: on your mark . . . get set . . . go! Mol. Cell 30, 7-10
3. Zhou, Q., and Yik, J. H. (2006) The Yin and Yang of P-TEFb regulation: implications for human immunodeficiency virus gene expression and global control of cell growth and differentiation. Microbiol. Mol. Biol. Rev. 70, 646-659
4. Brès, V., Yoh, S. M., and Jones, K. A. (2008) The multi-tasking P-TEFb complex. Curr. Opin. Cell Biol. 20, 334-340
5. Ott, M., Geyer, M., and Zhou, Q. (2011) The control of HIV transcription: keeping RNA polymerase II on track. Cell Host Microbe 10, 426-435
6. He, N., Liu, M., Hsu, J., Xue, Y., Chou, S., Burlingame, A., Krogan, N. J., Alber, T., and Zhou, Q. (2010) HIV-1 Tat and host AFF4 recruit two transcription elongation factors into a bifunctional complex for coordinated activation of HIV-1 transcription. Mol. Cell 38, 428-438
7. Yik, J. H., Chen, R., Nishimura, R., Jennings, J. L., Link, A. J., and Zhou, Q. (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
8. Michels, A. A., Nguyen, V. T., Fraldi, A., Labas, V., Edwards, M., Bonnet, F., Lania, L., and Bensaude, O. (2003) MAQ1 and 7SK RNA interact with CDK9/cyclin T complexes in a transcription-dependent manner. Mol. Cell. Biol. 23, 4859-4869
9. Krueger, B. J., Jeronimo, C., Roy, B. B., Bouchard, A., Barrandon, C., Byers, S. A., Searcey, C. E., Cooper, J. J., Bensaude, O., Cohen, E. A., Coulombe, B., and Price, D. H. (2008) LARP7 is a stable component of the 7SK snRNP while P-TEFb, HEXIM1 and hnRNP A1 are reversibly associated. Nucleic Acids Res. 36, 2219-2229
10. Peterlin, B. M., Brogie, J. E., and Price, D. H. (2012) 7SK snRNA: a noncoding RNA that plays a major role in regulating eukaryotic transcription. Wiley Interdiscip. Rev. RNA 3, 92-103
11. Bartholomeeusen, K., Xiang, Y., Fujinaga, K., and Peterlin, B. M. (2012) BET bromodomain inhibition activates transcription via a transient release of P-TEFb from 7SK snRNP. J. Biol. Chem. 287, 36609-36616
12. Taube, R., Lin, X., Irwin, D., Fujinaga, K., and Peterlin, B. M. (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
13. Peterlin, B. M., and Price, D. H. (2006) Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 23, 297-305
14. Bartholomeeusen, K., Fujinaga, K., Xiang, Y., and Peterlin, B. M. (2013) HDAC inhibitors that release positive transcription elongation factor b (P-TEFb) from its inhibitory complex also activate HIV transcription. J. Biol. Chem. 288, 14400-14407
15. Kim, Y. K., Mbonye, U., Hokello, J., and Karn, J. (2011) T-cell receptor signaling enhances transcriptional elongation from latent HIV proviruses by activating P-TEFb through an ERK-dependent pathway. J. Mol. Biol. 410, 896-916
16. Biglione, S., Byers, S. A., Price, J. P., Nguyen, V. T., Bensaude, O., Price, D. H., and Maury, W. (2007) Inhibition of HIV-1 replication by P-TEFb inhibitors DRB, seliciclib, and flavopiridol correlates with release of free P-TEFb from the large, inactive form of the complex. Retrovirology 4, 47
17. Michels, A. A., Fraldi, A., Li, Q., Adamson, T. E., Bonnet, F., Nguyen, V. T., Sedore, S. C., Price, J. P., Price, D. H., Lania, L., and Bensaude, O. (2004) Binding of the 7SK snRNA turns the HEXIM1 protein into a P-TEFb (CDK9/cyclin T) inhibitor. EMBO J. 23, 2608-2619
18. Nguyen, V. T., Kiss, T., Michels, A. A., and Bensaude, O. (2001) 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature 414, 322-325
19. Yang, Z., Zhu, Q., Luo, K., and Zhou, Q. (2001) The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 414, 317-322
20. Kerppola, T. K. (2009) Visualization of molecular interactions using bimolecular fluorescence complementation analysis: characteristics of protein fragment complementation. Chem. Soc. Rev. 38, 2876-2886
21. Fanara, P., Hodel, M. R., Corbett, A. H., and Hodel, A. E. (2000) Quantitative analysis of nuclear localization signal (NLS)-importin α interaction through fluorescence depolarization. Evidence for auto-inhibitory regulation of NLS binding. J. Biol. Chem. 275, 21218-21223
22. Fujinaga, K., Irwin, D., Geyer, M., and Peterlin, B. M. (2002) Optimized chimeras between kinase-inactive mutant Cdk9 and truncated cyclin T1 proteins efficiently inhibit Tat transactivation and human immunodeficiency virus gene expression. J. Virol. 76, 10873-10881
23. Robida, A. M., and Kerppola, T. K. (2009) Bimolecular fluorescence complementation analysis of inducible protein interactions: effects of factors affecting protein folding on fluorescent protein fragment association. J. Mol. Biol. 394, 391-409
24. Fujinaga, K., Luo, Z., and Peterlin, B. M. (2014) Genetic analysis of the structure and function of 7SK small nuclear ribonucleoprotein (snRNP) in cells. J. Biol. Chem. 289, 21181-21190
25. 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
26. Aune, G. J., Takagi, K., Sordet, O., Guirouilh-Barbat, J., Antony, S., Bohr, V. A., and Pommier, Y. (2008) Von Hippel-Lindau-coupled and transcription-coupled nucleotide excision repair-dependent degradation of RNA polymerase II in response to trabectedin. Clin. Cancer Res. 14, 6449-6455
27. He, N., Pezda, A. C., and Zhou, Q. (2006) Modulation of a P-TEFb functional equilibrium for the global control of cell growth and differentiation. Mol. Cell. Biol. 26, 7068-7076
28. Contreras, X., Barboric, M., Lenasi, T., and Peterlin, B. M. (2007) HMBA releases P-TEFb from HEXIM1 and 7SK snRNA via PI3K/Akt and activates HIV transcription. PLoS Pathog. 3, 1459-1469
29. Contreras, X., Schweneker, M., Chen, C. S., McCune, J. M., Deeks, S. G., Martin, J., and Peterlin, B. M. (2009) Suberoylanilide hydroxamic acid reactivates HIV from latently infected cells. J. Biol. Chem. 284, 6782-6789
30. Napolitano, G., Licciardo, P., Carbone, R., Majello, B., and Lania, L. (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
31. Izeddin, I., Récamier, V., Bosanac, L., Cissé, II, Boudarene, L., Dugast-Darzacq, C., Proux, F., Bénichou, O., Voituriez, R., Bensaude, O., Dahan, M., and Darzacq, X. (2014) Single-molecule tracking in live cells reveals distinct target-search strategies of transcription factors in the nucleus. eLife 3, e02230
32. Fujinaga, K., Barboric, M., Li, Q., Luo, Z., Price, D. H., and Peterlin, B. M. (2012) PKC phosphorylates HEXIM1 and regulates P-TEFb activity. Nucleic Acids Res. 40, 9160-9170
33. Christman, J. K. (2002) 5-Azacytidine and 5-aza-2′-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene 21, 5483-5495
34. Fernandez, G., and Zeichner, S. L. (2010) Cell line-dependent variability in HIV activation employing DNMT inhibitors. Virol. J. 7, 266
35. Kauder, S. E., Bosque, A., Lindqvist, A., Planelles, V., and Verdin, E. (2009) Epigenetic regulation of HIV-1 latency by cytosine methylation. PLoS Pathog. 5, e1000495
36. Jeeninga, R. E., Westerhout, E. M., van Gerven, M. L., and Berkhout, B. (2008) HIV-1 latency in actively dividing human T cell lines. Retrovirology 5, 37
37. Liu, P., Xiang, Y., Fujinaga, K., Bartholomeeusen, K., Nilson, K. A., Price, D. H., and Peterlin, B. M. (2014) Release of positive transcription elongation factor b (P-TEFb) from 7SK small nuclear ribonucleoprotein (snRNP) activates hexamethylene bisacetamide-inducible protein (HEXIM1) transcription. J. Biol. Chem. 289, 9918-9925
38. Hu, C. D., Grinberg, A. V., and Kerppola, T. K. (2006) Visualization of protein interactions in living cells using bimolecular fluorescence complementation (BiFC) analysis. Curr. Protoc. Cell Biol. Chapter 21, Unit 21.3
39. Hsin, J. P., Xiang, K., and Manley, J. L. (2014) Function and control of RNA polymerase II C-terminal domain phosphorylation in vertebrate transcription and RNA processing. Mol. Cell. Biol. 34, 2488-2498
40. Czudnochowski, N., Bösken, C. A., and Geyer, M. (2012) Serine-7 but not serine-5 phosphorylation primes RNA polymerase II CTD for P-TEFb recognition. Nat. Commun. 3, 842
41. Cho, S., Schroeder, S., and Ott, M. (2010) CYCLINg through transcription: posttranslational modifications of P-TEFb regulate transcription elongation. Cell Cycle 9, 1697-1705
42. Ramakrishnan, R., Chiang, K., Liu, H., Budhiraja, S., Donahue, H., and Rice, A. P. (2012) Making a short story long: regulation of P-TEFb and HIV-1 transcriptional elongation in CD4+ T lymphocytes and macrophages. Biology 1, 94-115
43. Cheng, Y., Jin, Z., Agarwal, R., Ma, K., Yang, J., Ibrahim, S., Olaru, A. V., David, S., Ashktorab, H., Smoot, D. T., Duncan, M. D., Hutcheon, D. F., Abraham, J. M., Meltzer, S. J., and Mori, Y. (2012) LARP7 is a potential tumor suppressor gene in gastric cancer. Lab. Invest. 92, 1013-1019
44. Alazami, A. M., Al-Owain, M., Alzahrani, F., Shuaib, T., Al-Shamrani, H., Al-Falki, Y. H., Al-Qahtani, S. M., Alsheddi, T., Colak, D., and Alkuraya, F. S. (2012) Loss of function mutation in LARP7, chaperone of 7SK ncRNA, causes a syndrome of facial dysmorphism, intellectual disability, and primordial dwarfism. Hum. Mutat. 33, 1429-1434
45. Biewenga, P., Buist, M. R., Moerland, P. D., Ver Loren van Themaat, E., van Kampen, A. H., ten Kate, F. J., and Baas, F. (2008) Gene expression in early stage cervical cancer. Gynecol. Oncol. 108, 520-526
46. Dai, Q., Luan, G., Deng, L., Lei, T., Kang, H., Song, X., Zhang, Y., Xiao, Z. X., and Li, Q. (2014) Primordial dwarfism gene maintains Lin28 expression to safeguard embryonic stem cells from premature differentiation. Cell Rep. 7, 735-746
47. Wittmann, B. M., Fujinaga, K., Deng, H., Ogba, N., and Montano, M. M. (2005) The breast cell growth inhibitor, estrogen down regulated gene 1, modulates a novel functional interaction between estrogen receptor α and transcriptional elongation factor cyclin T1. Oncogene 24, 5576-5588
48. Castelo-Branco, G., Amaral, P. P., Engström, P. G., Robson, S. C., Marques, S. C., Bertone, P., and Kouzarides, T. (2013) The non-coding snRNA 7SK controls transcriptional termination, poising, and bidirectionality in embryonic stem cells. Genome Biol. 14, R98
49. Okamura, D., Maeda, I., Taniguchi, H., Tokitake, Y., Ikeda, M., Ozato, K., Mise, N., Abe, K., Noce, T., Izpisua Belmonte, J. C., and Matsui, Y. (2012) Cell cycle gene-specific control of transcription has a critical role in proliferation of primordial germ cells. Genes Dev. 26, 2477-2482
50. Dawson, M. A., Prinjha, R. K., Dittmann, A., Giotopoulos, G., Bantscheff, M., Chan, W. I., Robson, S. C., Chung, C. W., Hopf, C., Savitski, M. M., Huthmacher, C., Gudgin, E., Lugo, D., Beinke, S., Chapman, T. D., Roberts, E. J., Soden, P. E., Auger, K. R., Mirguet, O., Doehner, K., Delwel, R., Burnett, A. K., Jeffrey, P., Drewes, G., Lee, K., Huntly, B. J., and Kouzarides, T. (2011) Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature 478, 529-533