Histone cross-talk connects protein phosphatase 1α (PP1α) and histone deacetylase (HDAC) pathways to regulate the functional transition of bromodomain-containing 4 (BRD4) for inducible gene expression

Journal of Biological Chemistry

Volumn 289, Issue 33, 2014, Pages 23154-23167

  Hu, Xiangming ^a   Lu, Xiaodong ^a   Liu, Runzhong ^a   Ai, Nanping ^a   Cao, Zhenhua ^a   Li, Yannan ^a   Liu, Jiangfang ^a   Yu, Bin ^a   Liu, Kai ^a   Wang, Huiping ^a   Zhou, Chao ^a   Wang, Yu ^a   Han, Aidong ^a   Ding, Feng ^a   Chen, Ruichuan ^a  

^a XIAMEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; AMINO ACIDS; CROSSTALK; ELONGATION; GENES; PHOSPHATASES; PHOSPHORYLATION; PROTEINS; SIGNALING;

FUNCTIONAL TRANSITIONS; HISTONE DEACETYLASES; INDUCIBLE GENE EXPRESSION; MULTIPLE CELLULAR PROCESS; POSITIVE TRANSCRIPTION; PROTEIN PHOSPHATASE; PROTEIN PHOSPHATASE-1; TRANSCRIPTION REGULATIONS;

TRANSCRIPTION;

BINDING PROTEIN; BROMODOMAIN CONTAINING 4; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE H3; HISTONE H4; LYSINE; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 1ALPHA; SERINE; UNCLASSIFIED DRUG; BRD4 PROTEIN, HUMAN; CHROMATIN; HISTONE; NUCLEAR PROTEIN; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; TRANSCRIPTION FACTOR;

ARTICLE; BINDING SITE; BRD4 GENE; CHROMATIN; CONTROLLED STUDY; DEACETYLATION; DEPHOSPHORYLATION; ENZYME REGULATION; GENE EXPRESSION; HDAC GENE; HISTONE ACETYLATION; HUMAN; HUMAN CELL; MOLECULAR BIOLOGY; MOLECULAR INTERACTION; MOUSE; NONHUMAN; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PP1ALPHA GENE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; STRESS; TRANSCRIPTION ELONGATION; ACETYLATION; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

ACETYLATION; CHROMATIN; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEK293 CELLS; HELA CELLS; HISTONE DEACETYLASES; HISTONES; HUMANS; NUCLEAR PROTEINS; PHOSPHORYLATION; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROTEIN PHOSPHATASE 1; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84905984517     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.570812     Document Type: Article

References (64)

1. Core, L. J., and Lis, J. T. (2008) Transcription regulation through promoter-proximal pausing of RNA polymerase II. Science 319, 1791-1792 (Pubitemid 351451556)
2. Price, D. H. (2008) Poised polymerases: on your mark.get set.go!. Mol. Cell 30, 7-10
3. Fujita, T., and Schlegel, W. (2010) Promoter-proximal pausing of RNA polymerase II: an opportunity to regulate gene transcription. J. Recept. Signal Transduct. Res. 30, 31-42
4. Nechaev, S., and Adelman, K. (2011) Pol II waiting in the starting gates: regulating the transition from transcription initiation into productive elongation. Biochim. Biophys. Acta 1809, 34-45
5. Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R., and Young, R. A. (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88 (Pubitemid 47031323)
6. Muse, G. W., Gilchrist, D. A., Nechaev, S., Shah, R., Parker, J. S., Grissom, S. F., Zeitlinger, J., and Adelman, K. (2007) RNA polymerase is poised for activation across the genome. Nat. Genet. 39, 1507-1511 (Pubitemid 350191341)
7. Zeitlinger, J., Stark, A., Kellis, M., Hong, J. W., Nechaev, S., Adelman, K., Levine, M., and Young, R. A. (2007) RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat. Genet. 39, 1512-1516 (Pubitemid 350191345)
8. Core, L. J., Waterfall, J. J., and Lis, J. T. (2008) Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322, 1845-1848
9. Koch, F., Jourquin, F., Ferrier, P., and Andrau, J. C. (2008) Genome-wide RNA polymerase II: not genes only!. Trends Biochem. Sci. 33, 265-273
10. Peterlin, B. M. (2010) Transcription elongation takes central stage: the P-TEFb connection. Cell Cycle 9, 2933-2934
11. Lenasi, T., and Barboric, M. (2010) P-TEFb stimulates transcription elongation and pre-mRNA splicing through multilateral mechanisms. RNA Biol. 7, 145-150
12. 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 (Pubitemid 44484688)
13. Diribarne, G., and Bensaude, O. (2009) 7SK RNA, a non-coding RNA regulating P-TEFb, a general transcription factor. RNA Biol. 6, 122-128
14. Chen, R., Liu, M., Li, H., Xue, Y., Ramey, W. N., He, N., Ai, N., Luo, H., Zhu, Y., Zhou, N., and Zhou, Q. (2008) PP2B and PP1α cooperatively disrupt 7SK snRNP to release P-TEFb for transcription in response to Ca2+ signaling. Genes Dev. 22, 1356-1368 (Pubitemid 351717526)
15. Jang, M. K., Mochizuki, K., Zhou, M., Jeong, H. S., Brady, J. N., and Ozato, K. (2005) The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Mol. Cell 19, 523-534 (Pubitemid 41140009)
16. Yang, Z., Yik, J. H., Chen, R., He, N., Jang, M. K., Ozato, K., and Zhou, Q. (2005) Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol. Cell 19, 535-545 (Pubitemid 41140010)
17. Chiang, C. M. (2009) Brd4 engagement from chromatin targeting to transcriptional regulation: selective contact with acetylated histone H3 and H4. F1000 Biol. Rep. 1, 98
18. Dey, A., Chitsaz, F., Abbasi, A., Misteli, T., and Ozato, K. (2003) The double bromodomain protein Brd4 binds to acetylated chromatin during interphase and mitosis. Proc. Natl. Acad. Sci. U.S.A. 100, 8758-8763 (Pubitemid 36899172)
19. Dey, A., Ellenberg, J., Farina, A., Coleman, A. E., Maruyama, T., Sciortino, S., Lippincott-Schwartz, J., and Ozato, K. (2000) A bromodomain protein, MCAP, associates with mitotic chromosomes and affects G2-to-M transition. Mol. Cell. Biol. 20, 6537-6549 (Pubitemid 30650239)
20. Filippakopoulos, P., Picaud, S., Mangos, M., Keates, T., Lambert, J. P., Barsyte-Lovejoy, D., Felletar, I., Volkmer, R., Müller, S., Pawson, T., Gingras, A. C., Arrowsmith, C. H., and Knapp, S. (2012) Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 149, 214-231
21. Mochizuki, K., Nishiyama, A., Jang, M. K., Dey, A., Ghosh, A., Tamura, T., Natsume, H., Yao, H., and Ozato, K. (2008) The bromodomain protein Brd4 stimulates G1 gene transcription and promotes progression to S phase. J. Biol. Chem. 283, 9040-9048
22. 1 gene expression and cell cycle progression. Mol. Cell. Biol. 28, 967-976
23. Dey, A., Nishiyama, A., Karpova, T., McNally, J., and Ozato, K. (2009) Brd4 marks select genes on mitotic chromatin and directs postmitotic transcription. Mol. Biol. Cell 20, 4899-4909
24. 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
25. Devaiah, B. N., and Singer, D. S. (2013) Two faces of BRD4: mitotic bookmark and transcriptional lynchpin. Transcription 4, 13-17
26. Voigt, P., and Reinberg, D. (2011) BRD4 jump-starts transcription after mitotic silencing. Genome Biol. 12, 133
27. + T cells. J. Biol. Chem. 287, 43137-43155
28. Wang, R., Li, Q., Helfer, C. M., Jiao, J., and You, J. (2012) Bromodomain protein Brd4 associated with acetylated chromatin is important for maintenance of higher-order chromatin structure. J. Biol. Chem. 287, 10738-10752
29. You, J., Croyle, J. L., Nishimura, A., Ozato, K., and Howley, P. M. (2004) Interaction of the bovine papillomavirus E2 protein with Brd4 tethers the viral DNA to host mitotic chromosomes. Cell 117, 349-360 (Pubitemid 38534541)
30. Bisgrove, D. A., Mahmoudi, T., Henklein, P., and Verdin, E. (2007) Conserved P-TEFb-interacting domain of BRD4 inhibits HIV transcription. Proc. Natl. Acad. Sci. U.S.A. 104, 13690-13695 (Pubitemid 350003382)
31. 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
32. Zippo, A., Serafini, R., Rocchigiani, M., Pennacchini, S., Krepelova, A., and Oliviero, S. (2009) Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138, 1122-1136
33. Hargreaves, D. C., Horng, T., and Medzhitov, R. (2009) Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 138, 129-145
34. Karn, J. (2013) A new BET on the control of HIV latency. Cell Cycle 12, 545-546
35. Zhou, M., Huang, K., Jung, K. J., Cho, W. K., Klase, Z., Kashanchi, F., Pise-Masison, C. A., and Brady, J. N. (2009) Bromodomain protein Brd4 regulates human immunodeficiency virus transcription through phosphorylation of CDK9 at threonine 29. J. Virol. 83, 1036-1044
36. Zhang, G., Liu, R., Zhong, Y., Plotnikov, A. N., Zhang, W., Zeng, L., Rusinova, E., Gerona-Nevarro, G., Moshkina, N., Joshua, J., Chuang, P. Y., Ohlmeyer, M., He, J. C., and Zhou, M. M. (2012) Down-regulation of NF-κB transcriptional activity in HIV-associated kidney disease by BRD4 inhibition. J. Biol. Chem. 287, 28840-28851
37. Huang, B., Yang, X. D., Zhou, M. M., Ozato, K., and Chen, L. F. (2009) Brd4 coactivates transcriptional activation of NF-κB via specific binding to acetylated RelA. Mol. Cell. Biol. 29, 1375-1387
38. Anand, P., Brown, J. D., Lin, C. Y., Qi, J., Zhang, R., Artero, P. C., Alaiti, M. A., Bullard, J., Alazem, K., Margulies, K. B., Cappola, T. P., Lemieux, M., Plutzky, J., Bradner, J. E., and Haldar, S. M. (2013) BET bromodomains mediate transcriptional pause release in heart failure. Cell 154, 569-582
39. Spiltoir, J. I., Stratton, M. S., Cavasin, M. A., Demos-Davies, K., Reid, B. G., Qi, J., Bradner, J. E., and McKinsey, T. A. (2013) BET acetyl-lysine binding proteins control pathological cardiac hypertrophy. J. Mol. Cell. Cardiol. 63, 175-179
40. Zuber, J., Shi, J., Wang, E., Rappaport, A. R., Herrmann, H., Sison, E. A., Magoon, D., Qi, J., Blatt, K., Wunderlich, M., Taylor, M. J., Johns, C., Chicas, A., Mulloy, J. C., Kogan, S. C., Brown, P., Valent, P., Bradner, J. E., Lowe, S. W., and Vakoc, C. R. (2011) RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia. Nature 478, 524-528
41. Blobel, G. A., Kalota, A., Sanchez, P. V., and Carroll, M. (2011) Short hairpin RNA screen reveals bromodomain proteins as novel targets in acute myeloid leukemia. Cancer Cell 20, 287-288
42. Delmore, J. E., Issa, G. C., Lemieux, M. E., Rahl, P. B., Shi, J., Jacobs, H. M., Kastritis, E., Gilpatrick, T., Paranal, R. M., Qi, J., Chesi, M., Schinzel, A. C., McKeown, M. R., Heffernan, T. P., Vakoc, C. R., Bergsagel, P. L., Ghobrial, I. M., Richardson, P. G., Young, R. A., Hahn, W. C., Anderson, K. C., Kung, A. L., Bradner, J. E., and Mitsiades, C. S. (2011) BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 146, 904-917
43. 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
44. Segura, M. F., Fontanals-Cirera, B., Gaziel-Sovran, A., Guijarro, M. V., Hanniford, D., Zhang, G., González-Gomez, P., Morante, M., Jubierre, L., Zhang, W., Darvishian, F., Ohlmeyer, M., Osman, I., Zhou, M. M., and Hernando, E. (2013) BRD4 sustains melanoma proliferation and represents a new target for epigenetic therapy. Cancer Res. 73, 6264-6276
45. Rodriguez, R. M., Huidobro, C., Urdinguio, R. G., Mangas, C., Soldevilla, B., Domínguez, G., Bonilla, F., Fernandez, A. F., and Fraga, M. F. (2012) Aberrant epigenetic regulation of bromodomain Brd4 in human colon cancer. J. Mol. Med. 90, 587-595
46. Alsarraj, J., and Hunter, K. W. (2012) Bromodomain-containing protein 4: a dynamic regulator of breast cancer metastasis through modulation of the extracellular matrix. Int. J. Breast Cancer 2012, 670632
47. Wang, H., Zhou, N., Ding, F., Li, Z., Chen, R., Han, A., and Liu, R. (2011) An efficient approach for site-directed mutagenesis using central overlapping primers. Anal. Biochem. 418, 304-306
48. Chen, R., Liu, M., Zhang, K., and Zhou, Q. (2011) Isolation and functional characterization of P-TEFb-associated factors that control general and HIV-1 transcriptional elongation. Methods 53, 85-90
49. 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 (Pubitemid 37352789)
50. Nowak, S. J., and Corces, V. G. (2004) Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. Trends Genet. 20, 214-220 (Pubitemid 38369193)
51. Haberland, M., Montgomery, R. L., and Olson, E. N. (2009) The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nature Rev. Genet. 10, 32-42
52. Beckers, T., Burkhardt, C., Wieland, H., Gimmnich, P., Ciossek, T., Maier, T., and Sanders, K. (2007) Distinct pharmacological properties of second generation HDAC inhibitors with the benzamide or hydroxamate head group. Int. J. Cancer 121, 1138-1148 (Pubitemid 47101654)
53. Shi, Y. (2009) Serine/threonine phosphatases: mechanism through structure. Cell 139, 468-484
54. 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
55. Heroes, E., Lesage, B., Görnemann, J., Beullens, M., Van Meervelt, L., and Bollen, M. (2013) The PP1 binding code: a molecular-lego strategy that governs specificity. FEBS J. 280, 584-595
56. He, S., Khan, D. H., Winter, S., Seiser, C., and Davie, J. R. (2013) Dynamic distribution of HDAC1 and HDAC2 during mitosis: association with F-actin. J. Cell. Physiol. 228, 1525-1535
57. Banerjee, T., and Chakravarti, D. (2011) A peek into the complex realm of histone phosphorylation. Mol. Cell. Biol. 31, 4858-4873
58. Rossetto, D., Avvakumov, N., and Côté, J. (2012) Histone phosphorylation: a chromatin modification involved in diverse nuclear events. Epigenetics 7, 1098-1108
59. Sawicka, A., and Seiser, C. (2012) Histone H3 phosphorylation: a versatile chromatin modification for different occasions. Biochimie 94, 2193-2201
60. Mahadevan, L. C., Willis, A. C., and Barratt, M. J. (1991) Rapid histone H3 phosphorylation in response to growth factors, phorbol esters, okadaic acid, and protein synthesis inhibitors. Cell 65, 775-783 (Pubitemid 121001309)
61. Chadee, D. N., Hendzel, M. J., Tylipski, C. P., Allis, C. D., Bazett-Jones, D. P., Wright, J. A., and Davie, J. R. (1999) Increased Ser-10 phosphorylation of histone H3 in mitogen-stimulated and oncogene-transformed mouse fibroblasts. J. Biol. Chem. 274, 24914-24920
62. Nowak, S. J., Pai, C. Y., and Corces, V. G. (2003) Protein phosphatase 2A activity affects histone H3 phosphorylation and transcription in Drosophila melanogaster. Mol. Cell. Biol. 23, 6129-6138 (Pubitemid 37013091)
63. Wang, W., Yao, X., Huang, Y., Hu, X., Liu, R., Hou, D., Chen, R., and Wang, G. (2013) Mediator MED23 regulates basal transcription in vivo via an interaction with P-TEFb. Transcription 4, 39-51
64. Kanazawa, S., Soucek, L., Evan, G., Okamoto, T., and Peterlin, B. M. (2003) c-Myc recruits P-TEFb for transcription, cellular proliferation and apoptosis. Oncogene 22, 5707-5711 (Pubitemid 37102708)