Histone deacetylase inhibitors (HDACis) that release the positive transcription elongation factor b (P-TEFb) from its inhibitory complex also activate HIV transcription

Journal of Biological Chemistry

Volumn 288, Issue 20, 2013, Pages 14400-14407

  Bartholomeeusen, Koen ^a   Fujinaga, Koh ^a   Xiang, Yanhui ^a,b   Peterlin, B Matija ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BRYOSTATIN 1; CELL LINES; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; INHIBITORY COMPLEX; MINIMAL EFFECTS; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PRIMARY CELLS;

ACETYLATION; CELL CULTURE; T-CELLS;

TRANSCRIPTION;

7SK SMALL NUCLEAR RIBONUCLEOPROTEIN; BRYOSTATIN 1; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; SMALL NUCLEAR RIBONUCLEOPROTEIN; SUBEROYLANILIDE HYDROXYAMIC ACID; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; CD4+ T LYMPHOCYTE; CHROMATIN; CONTROLLED STUDY; EPISOME; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TARGETING; TRANSCRIPTION INITIATION; VIRUS REACTIVATION;

7SK SNRNP; HEXIM1; HISTONE DEACETYLASE INHIBITORS; HISTONE MODIFICATION; HIV; HIV LATENCY; P-TEFB; TRANSCRIPTION ELONGATION FACTORS; TUBULIN;

CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; GENE EXPRESSION REGULATION, VIRAL; HELA CELLS; HISTONE DEACETYLASE INHIBITORS; HISTONES; HIV INFECTIONS; HIV-1; HUMANS; JURKAT CELLS; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; RNA-BINDING PROTEINS; TRANSCRIPTION, GENETIC; TUBULIN;

EID: 84877895204     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.464834     Document Type: Article

References (61)

1. Contreras, X., Lenasi, T., and Peterlin, B. M. (2006) HIV latency: present knowledge, future directions. Future Virol. 1, 733-745
2. Eisele, E., and Siliciano, R. F. (2012) Redefining the viral reservoirs that prevent HIV-1 eradication. Immunity 37, 377-388
3. Richman, D. D., Margolis, D. M., Delaney, M., Greene, W. C., Hazuda, D., and Pomerantz, R. J. (2009) The challenge of finding a cure for HIV infection. Science 323, 1304-1307
4. Mbonye, U., and Karn, J. (2011) Control of HIV latency by epigenetic and nonepigenetic mechanisms. Curr. HIV Res. 9, 554-567
5. Xing, S., and Siliciano, R. F. (2012) Targeting HIV latency: pharmacologic strategies toward eradication. Drug Discov. Today pii, S1359-6446
6. Shan, L., Deng, K., Shroff, N. S., Durand, C. M., Rabi, S. A., Yang, H. C., Zhang, H., Margolick, J. B., Blankson, J. N., and Siliciano, R. F. (2012) Stimulation of HIV-1-specific cytolytic T lymphocytes facilitates elimination of latent viral reservoir after virus reactivation. Immunity 36, 491-501
7. 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
8. Peterlin, B. M., and Price, D. H. (2006) Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 23, 297-305 (Pubitemid 44128850)
9. Fujinaga, K., Irwin, D., Huang, Y., Taube, R., Kurosu, T., and Peterlin, B. M. (2004) Dynamics of human immunodeficiency virus transcription: P-TEFb phosphorylates RD and dissociates negative effectors from the transactivation response element. Mol. Cell. Biol. 24, 787-795 (Pubitemid 38057929)
10. Barboric, M., and Lenasi, T. (2010) Kick-sTARting HIV-1 transcription elongation by 7SK snRNP deporTATion. Nat. Struct. Mol. Biol. 17, 928-930
11. + T cells. J. Virol. 87, 1211-1220
12. + T cells and monocytes. Viruses 4, 1390-1409
13. + T lymphocytes. J. Virol. 86, 3244-3252
14. 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
15. He, N., and Zhou, Q. (2011) New insights into the control of HIV-1 transcription: when Tat meets the 7SK snRNP and super-elongation complex (SEC). J. Neuroimmune Pharmacol. 6, 260-268
16. Luo, Z., Lin, C., and Shilatifard, A. (2012) The super-elongation complex (SEC) family in transcriptional control. Nat. Rev. Mol. Cell Biol. 13, 543-547
17. Marshall, R. M., and Grana, X. (2006) Mechanisms controlling CDK9 activity. Front. Biosci. 11, 2598-2613 (Pubitemid 43806567)
18. 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
19. Schröder, S., Cho, S., Zeng, L., Zhang, Q., Kaehlcke, K., Mak, L., Lau, J., Bisgrove, D., Schnölzer, M., Verdin, E., Zhou, M. M., and Ott, M. (2012) Two-pronged binding with bromodomain-containing protein 4 liberates positive transcription elongation factor b from inactive ribonucleoprotein complexes. J. Biol. Chem. 287, 1090-1099
20. Takahashi, H., Parmely, T. J., Sato, S., Tomomori-Sato, C., Banks, C. A., Kong, S. E., Szutorisz, H., Swanson, S. K., Martin-Brown, S., Washburn, M. P., Florens, L., Seidel, C. W., Lin, C., Smith, E. R., Shilatifard, A., Conaway, R. C., and Conaway, J. W. (2011) Human mediator subunit MED26 functions as a docking site for transcription elongation factors. Cell 146, 92-104
21. Barboric, M., Yik, J. H., Czudnochowski, N., Yang, Z., Chen, R., Contreras, X., Geyer, M., Matija Peterlin, B., and Zhou, Q. (2007) Tat competes with HEXIM1 to increase the active pool of P-TEFb for HIV-1 transcription. Nucleic Acids Res. 35, 2003-2012 (Pubitemid 47061666)
22. Archin, N. M., Espeseth, A., Parker, D., Cheema, M., Hazuda, D., and Margolis, D. M. (2009) Expression of latent HIV induced by the potent HDAC inhibitor suberoylanilide hydroxamic acid. AIDS Res. Hum. Retroviruses 25, 207-212
23. Bartholomeeusen, K., Xiang, Y., Fujinaga, K., and Peterlin, B. M. (2012) Bromodomain and extra-terminal (BET) bromodomain inhibition activate transcription via transient release of positive transcription elongation factor b (P-TEFb) from 7SK small nuclear ribonucleoprotein. J. Biol. Chem. 287, 36609-36616
24. 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 (Pubitemid 350085610)
25. + T cell model without inducing global T cell activation. J. Virol. 85, 6060-6064
26. Ying, H., Zhang, Y., Lin, S., Han, Y., and Zhu, H. Z. (2010) Histone deacetylase inhibitor Scriptaid reactivates latent HIV-1 promoter by inducing histone modification in in vitro latency cell lines. Int. J. Mol. Med. 26, 265-272
27. 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
28. Blazek, D., Kohoutek, J., Bartholomeeusen, K., Johansen, E., Hulinkova, P., Luo, Z., Cimermancic, P., Ule, J., and Peterlin, B. M. (2011) The cyclin K/Cdk12 complex maintains genomic stability via regulation of expression of DNA damage response genes. Genes Dev. 25, 2158-2172
29. Banerjee, C., Archin, N., Michaels, D., Belkina, A. C., Denis, G. V., Bradner, J., Sebastiani, P., Margolis, D. M., and Montano, M. (2012) BET bromodomain inhibition as a novel strategy for reactivation of HIV-1. J. Leukoc. Biol. 92, 1147-1154
30. Boehm, D., Calvanese, V., Dar, R. D., Xing, S., Schroeder, S., Martins, L., Aull, K., Li, P. C., Planelles, V., Bradner, J. E., Zhou, M. M., Siliciano, R. F., Weinberger, L., Verdin, E., and Ott, M. (2013) BET bromodomain-targeting compounds reactivate HIV from latency via a Tat-independent mechanism. Cell Cycle 12, 452-462
31. Choudhary, S. K., Archin, N. M., and Margolis, D. M. (2008) Hexamethylbisacetamide and disruption of human immunodeficiency virus type 1 latency in CD4+ T cells. J. Infect. Dis. 197, 1162-1170 (Pubitemid 351590052)
32. Gallastegui, E., Marshall, B., Vidal, D., Sanchez-Duffhues, G., Collado, J. A., Alvarez-Fernández, C., Luque, N., Terme, J. M., Gatell, J. M., Sánchez-Palomino, S., Muñoz, E., Mestres, J., Verdin, E., and Jordan, A. (2012) Combination of biological screening in a cellular model of viral latency and virtual screening identifies novel compounds that reactivate HIV-1. J. Virol. 86, 3795-3808
33. Li, Z., Guo, J., Wu, Y., and Zhou, Q. (2013) The BET bromodomain inhibitor JQ1 activates HIV latency through antagonizing Brd4 inhibition of Tat-transactivation. Nucleic Acids Res. 41, 277-287
34. Shishido, T., Wolschendorf, F., Duverger, A., Wagner, F., Kappes, J., Jones, J., and Kutsch, O. (2012) Selected drugs with reported secondary cell-differentiating capacity prime latent HIV-1 infection for reactivation. J. Virol. 86, 9055-9069
35. Ying, H., Zhang, Y., Zhou, X., Qu, X., Wang, P., Liu, S., Lu, D., and Zhu, H. (2012) Selective histone deacetylase inhibitor M344 intervenes in HIV-1 latency through increasing histone acetylation and activation of NF-κB. PLoS One 7, e48832
36. Bradner, J. E., West, N., Grachan, M. L., Greenberg, E. F., Haggarty, S. J., Warnow, T., and Mazitschek, R. (2010) Chemical phylogenetics of histone deacetylases. Nat. Chem. Biol. 6, 238-243
37. Heltweg, B., Dequiedt, F., Marshall, B. L., Brauch, C., Yoshida, M., Nishino, N., Verdin, E., and Jung, M. (2004) Subtype selective substrates for histone deacetylases. J. Med. Chem. 47, 5235-5243 (Pubitemid 39314921)
38. Butler, K. V., Kalin, J., Brochier, C., Vistoli, G., Langley, B., and Kozikowski, A. P. (2010) Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A. J. Am. Chem. Soc. 132, 10842-10846
39. Leonard, J., Parrott, C., Buckler-White, A. J., Turner, W., Ross, E. K., Martin, M. A., and Rabson, A. B. (1989) The NF-βB binding sites in the human immunodeficiency virus type 1 long terminal repeat are not required for virus infectivity. J. Virol. 63, 4919-4924 (Pubitemid 19257879)
40. 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
41. Žumer, K., Low, A. K., Jiang, H., Saksela, K., and Peterlin, B. M. (2012) Unmodified histone H3K4 and DNA-dependent protein kinase recruit autoimmune regulator to target genes. Mol. Cell. Biol. 32, 1354-1362
42. Zhu, J., Gaiha, G. D., John, S. P., Pertel, T., Chin, C. R., Gao, G., Qu, H., Walker, B. D., Elledge, S. J., and Brass, A. L. (2012) Reactivation of latent HIV-1 by inhibition of BRD4. Cell Rep. 2, 807-816
43. 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 (Pubitemid 44477686)
44. Felber, B. K., and Pavlakis, G. N. (1988) A quantitative bioassay for HIV-1 based on trans-activation. Science 239, 184-187
45. + T cells. Blood 113, 58-65
46. Lassen, K. G., Hebbeler, A. M., Bhattacharyya, D., Lobritz, M. A., and Greene, W. C. (2012) A flexible model of HIV-1 latency permitting evaluation of many primary CD4 T-cell reservoirs. PLoS One 7, e30176
47. + T cells. Retrovirology 3, 66
48. Mehla, R., Bivalkar-Mehla, S., Zhang, R., Handy, I., Albrecht, H., Giri, S., Nagarkatti, P., Nagarkatti, M., and Chauhan, A. (2010) Bryostatin modulates latent HIV-1 infection via PKC and AMPK signaling but inhibits acute infection in a receptor-independent manner. PLoS One 5, e11160
49. Wender, P. A., Baryza, J. L., Brenner, S. E., DeChristopher, B. A., Loy, B. A., Schrier, A. J., and Verma, V. A. (2011) Design, synthesis, and evaluation of potent bryostatin analogs that modulate PKC translocation selectivity. Proc. Natl. Acad. Sci. U.S.A. 108, 6721-6726
50. Williams, S. A., Chen, L. F., Kwon, H., Ruiz-Jarabo, C. M., Verdin, E., and Greene, W. C. (2006) NF-κB p50 promotes HIV latency through HDAC recruitment and repression of transcriptional initiation. EMBO J. 25, 139-149 (Pubitemid 43077303)
51. Gryder, B. E., Sodji, Q. H., and Oyelere, A. K. (2012) Targeted cancer therapy: giving histone deacetylase inhibitors all they need to succeed. Future Med. Chem. 4, 505-524
52. Friedman, J., Cho, W. K., Chu, C. K., Keedy, K. S., Archin, N. M., Margolis, D. M., and Karn, J. (2011) Epigenetic silencing of HIV-1 by the histone H3 lysine 27 methyltransferase enhancer of Zeste 2. J. Virol. 85, 9078-9089
53. Sahu, G. K., and Cloyd, M. W. (2011) Latent HIV in primary T lymphocytes is unresponsive to histone deacetylase inhibitors. Virol. J. 8, 400
54. + cells is due to epigenetic transcriptional silencing and P-TEFb restriction. J. Virol. 84, 6425-6437
55. Hoque, M., Shamanna, R. A., Guan, D., Pe'ery, T., and Mathews, M. B. (2011) HIV-1 replication and latency are regulated by translational control of cyclin T1. J. Mol. Biol. 410, 917-932
56. Archin, N. M., Keedy, K. S., Espeseth, A., Dang, H., Hazuda, D. J., and Margolis, D. M. (2009) Expression of latent human immunodeficiency type 1 is induced by novel and selective histone deacetylase inhibitors. AIDS 23, 1799-1806
57. Huber, K., Doyon, G., Plaks, J., Fyne, E., Mellors, J. W., and Sluis-Cremer, N. (2011) Inhibitors of histone deacetylases: correlation between isoform specificity and reactivation of HIV type 1 (HIV-1) from latently infected cells. J. Biol. Chem. 286, 22211-22218
58. Keedy, K. S., Archin, N. M., Gates, A. T., Espeseth, A., Hazuda, D. J., and Margolis, D. M. (2009) A limited group of class I histone deacetylases acts to repress human immunodeficiency virus type 1 expression. J. Virol. 83, 4749-4756
59. Cho, S., Schroeder, S., Kaehlcke, K., Kwon, H. S., Pedal, A., Herker, E., Schnoelzer, M., and Ott, M. (2009) Acetylation of cyclin T1 regulates the equilibrium between active and inactive P-TEFb in cells. EMBO J. 28, 1407-1417
60. Ai, N., Hu, X., Ding, F., Yu, B., Wang, H., Lu, X., Zhang, K., Li, Y., Han, A., Lin, W., Liu, R., and Chen, R. (2011) Signal-induced Brd4 release from chromatin is essential for its role transition from chromatin targeting to transcriptional regulation. Nucleic Acids Res. 39, 9592-9604
61. Zhao, R., Nakamura, T., Fu, Y., Lazar, Z., and Spector, D. L. (2011) Gene bookmarking accelerates the kinetics of post-mitotic transcriptional reactivation. Nat. Cell Biol. 13, 1295-1304