Multilayered chromatin analysis reveals E2f, Smad and Zfx as transcriptional regulators of histones

Nature Structural and Molecular Biology

Volumn 20, Issue 1, 2013, Pages 119-124

  Gokhman, David ^a   Livyatan, Ilana ^a   Sailaja, Badi Sri ^a   Melcer, Shai ^a   Meshorer, Eran ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

E1A ASSOCIATED P300 PROTEIN; SMAD PROTEIN; SMAD1 PROTEIN; SMAD2 PROTEIN; TRANCRIPTION FACTOR ZFX; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F4; TRANSCRIPTION FACTOR YY1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; EMBRYONIC STEM CELL; GENE EXPRESSION; GENETIC REGULATION; HISTONE MODIFICATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MICROARRAY; SEQUENCE ANALYSIS; TRANSCRIPTION REGULATION;

ANIMALS; BINDING SITES; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; E1A-ASSOCIATED P300 PROTEIN; E2F1 TRANSCRIPTION FACTOR; E2F4 TRANSCRIPTION FACTOR; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION; HISTONES; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRESSOR PROTEINS; SEQUENCE ANALYSIS, DNA; SMAD1 PROTEIN; SMAD2 PROTEIN; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; YY1 TRANSCRIPTION FACTOR;

EUKARYOTA;

EID: 84872050486     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2448     Document Type: Article

References (61)

1. Zhao, J. Coordination of DNA synthesis and histone gene expression during normal cell cycle progression and after DNA damage. Cell Cycle 3, 695-697 (2004).
2. Meeks-Wagner, D. & Hartwell, L. H. Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission. Cell 44, 43-52 (1986).
3. Ye, X. et al. Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol. Cell 11, 341-351 (2003).
4. Marzluff, W. F. & Duronio, R. J. Histone mRNA expression: multiple levels of cell cycle regulation and important developmental consequences. Curr. Opin. Cell Biol. 14, 692-699 (2002).
5. Osley, M. A. The regulation of histone synthesis in the cell cycle. Annu. Rev. Biochem. 60, 827-861 (1991).
6. Jaeger, S., Barends, S., Giege, R., Eriani, G. & Martin, F. Expression of metazoan replication-dependent histone genes. Biochimie 87, 827-834 (2005).
7. DeLisle, A. J., Graves, R. A., Marzluff, W. F. & Johnson, L. F. Regulation of histone mRNA production and stability in serum-stimulated mouse 3T6 fibroblasts. Mol. Cell Biol. 3, 1920-1929 (1983).
8. Heintz, N., Sive, H. L. & Roeder, R. G. Regulation of human histone gene expression: kinetics of accumulation and changes in the rate of synthesis and in the half-lives of individual histone mRNAs during the HeLa cell cycle. Mol. Cell Biol. 3, 539-550 (1983).
9. Segil, N., Roberts, S. B. & Heintz, N. Mitotic phosphorylation of the Oct-1 homeodomain and regulation of Oct-1 DNA binding activity. Science 254, 1814-1816 (1991).
10. Fletcher, C., Heintz, N. & Roeder, R. G. Purification and characterization of OTF-1, a transcription factor regulating cell cycle expression of a human histone H2b gene. Cell 51, 773-781 (1987).
11. Mitra, P. et al. Identification of HiNF-P, a key activator of cell cycle-controlled histone H4 genes at the onset of S phase. Mol. Cell Biol. 23, 8110-8123 (2003).
12. Zhao, J. et al. NPAT links cyclin E-Cdk2 to the regulation of replication-dependent histone gene transcription. Genes Dev. 14, 2283-2297 (2000).
13. Artishevsky, A., Wooden, S., Sharma, A., Resendez, E. Jr. & Lee, A. S. Cell-cycle regulatory sequences in a hamster histone promoter and their interactions with cellular factors. Nature 328, 823-827 (1987).
14. Wu, F. & Lee, A. S. Identification of AP-2 as an interactive target of Rb and a regulator of the G1/S control element of the hamster histone H3. 2 promoter. Nucleic Acids Res. 26, 4837-4845 (1998).
15. Wu, F. & Lee, A. S. YY1 as a regulator of replication-dependent hamster histone H3. 2 promoter and an interactive partner of AP-2. J. Biol. Chem. 276, 28-34 (2001).
16. Last, T. J., van Wijnen, A. J., Birnbaum, M. J., Stein, G. S. & Stein, J. L. Multiple interactions of the transcription factor YY1 with human histone H4 gene regulatory elements. J. Cell. Biochem. 72, 507-516 (1999).
17. La Bella, F., Gallinari, P., McKinney, J. & Heintz, N. Histone H1 subtype-specific consensus elements mediate cell cycle-regulated transcription in vitro. Genes Dev. 3, 1982-1990 (1989).
18. Yagi, H. et al. Regulation of the mouse histone H2A. X gene promoter by the transcription factor E2F and CCAAT binding protein. J. Biol. Chem. 270, 18759-18765 (1995).
19. Nelson, D. M. et al. Coupling of DNA synthesis and histone synthesis in S phase independent of cyclin/cdk2 activity. Mol. Cell Biol. 22, 7459-7472 (2002).
20. Mitra, P., Vaughan, P. S., Stein, J. L., Stein, G. S. & van Wijnen, A. J. Purification and functional analysis of a novel leucine-zipper/nucleotide- fold protein, BZAP45, stimulating cell cycle regulated histone H4 gene transcription. Biochemistry 40, 10693-10699 (2001).
21. Isogai, Y., Keles, S., Prestel, M., Hochheimer, A. & Tjian, R. Transcription of histone gene cluster by differential core-promoter factors. Genes Dev. 21, 2936-2949 (2007).
22. He, H., Yu, F. X., Sun, C. & Luo, Y. CBP/p300 and SIRT1 are involved in transcriptional regulation of S-phase specific histone genes. PLoS ONE 6, e22088 (2011).
23. DeRan, M., Pulvino, M., Greene, E., Su, C. & Zhao, J. Transcriptional activation of histone genes requires NPAT-dependent recruitment of TRRAP-Tip60 complex to histone promoters during the G1/S phase transition. Mol. Cell Biol. 28, 435-447 (2008).
24. Marti, A., Wirbelauer, C., Scheffner, M. & Krek, W. Interaction between ubiquitin-protein ligase SCFSKP2 and E2F-1 underlies the regulation of E2F-1 degradation. Nat. Cell Biol. 1, 14-19 (1999).
25. Oswald, F., Dobner, T. & Lipp, M. The E2F transcription factor activates a replication-dependent human H2A gene in early S phase of the cell cycle. Mol. Cell Biol. 16, 1889-1895 (1996).
26. Rabinovich, A., Jin, V. X., Rabinovich, R., Xu, X. & Farnham, P. J. E2F in vivo binding specificity: comparison of consensus versus nonconsensus binding sites. Genome Res. 18, 1763-1777 (2008).
27. Seyedin, S. M., Cole, R. D. & Kistler, W. S. H1 histones from mammalian testes. The widespread occurrence of H1t. Exp. Cell Res. 136, 399-405 (1981).
28. Yang, L., Duff, M. O., Graveley, B. R., Carmichael, G. G. & Chen, L. L. Genomewide characterization of non-polyadenylated RNAs. Genome Biol. 12, R16 (2011).
29. Levine, B. J., Liu, T. J., Marzluff, W. F. & Skoultchi, A. I. Differential expression of individual members of the histone multigene family due to sequences in the 5′ and 3′ regions of the genes. Mol. Cell Biol. 8, 1887-1895 (1988).
30. Fan, Y. et al. Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell 123, 1199-1212 (2005).
31. Stead, E. et al. Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A/E and E2F activities. Oncogene 21, 8320-8333 (2002).
32. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
33. van Wijnen, A. J. et al. CDP/cut is the DNA-binding subunit of histone gene transcription factor HiNF-D: a mechanism for gene regulation at the G1/S phase cell cycle transition point independent of transcription factor E2F. Proc. Natl. Acad. Sci. USA 93, 11516-11521 (1996).
34. Bieda, M., Xu, X., Singer, M. A., Green, R. & Farnham, P. J. Unbiased location analysis of E2F1-binding sites suggests a widespread role for E2F1 in the human genome. Genome Res. 16, 595-605 (2006).
35. Antonio Giordano, A. G. & Soprano, K. J. Cell Cycle Inhibitors in Cancer Therapy: Current Strategies, (Humana Press inc., Totowa, New Jersey, 2003).
36. Cao, A. R. et al. Genome-wide analysis of transcription factor E2F1 mutant proteins reveals that N-and C-terminal protein interaction domains do not participate in targeting E2F1 to the human genome. J. Biol. Chem. 286, 11985-11996 (2011).
37. Heckmann, S. et al. The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana. Plant J. 68, 646-656 (2011).
38. Holmes, W. F. et al. Coordinate control and selective expression of the full complement of replication-dependent histone H4 genes in normal and cancer cells. J. Biol. Chem. 280, 37400-37407 (2005).
39. Andrechek, E. R., Mori, S., Rempel, R. E., Chang, J. T. & Nevins, J. R. Patterns of cell signaling pathway activation that characterize mammary development. Development 135, 2403-2413 (2008).
40. Xu, X. et al. A comprehensive ChIP-chip analysis of E2F1, E2F4, and E2F6 in normal and tumor cells reveals interchangeable roles of E2F family members. Genome Res. 17, 1550-1561 (2007).
41. Gaubatz, S. et al. E2F4 and E2F5 play an essential role in pocket protein-mediated G1 control. Mol. Cell 6, 729-735 (2000).
42. Takimoto, T. et al. Smad2 and Smad3 are redundantly essential for the TGF-beta-mediated regulation of regulatory T plasticity and Th1 development. J. Immunol. 185, 842-855 (2010).
43. Galvin, K. E., Travis, E. D., Yee, D., Magnuson, T. & Vivian, J. L. Nodal signaling regulates the bone morphogenic protein pluripotency pathway in mouse embryonic stem cells. J. Biol. Chem. 285, 19747-19756 (2010).
44. Galan-Caridad, J. M. et al. Zfx controls the self-renewal of embryonic and hematopoietic stem cells. Cell 129, 345-357 (2007).
45. Lee, J. S. et al. Relief of YY1 transcriptional repression by adenovirus E1A is mediated by E1A-associated protein p300. Genes Dev. 9, 1188-1198 (1995).
46. Schlisio, S., Halperin, T., Vidal, M. & Nevins, J. R. Interaction of YY1 with E2Fs, mediated by RYBP, provides a mechanism for specificity of E2F function. EMBO J. 21, 5775-5786 (2002).
47. Marzluff, W. F., Wagner, E. J. & Duronio, R. J. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat. Rev. Genet. 9, 843-854 (2008).
48. Heldin, C. H., Miyazono, K. & ten Dijke, P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471 (1997).
49. Ten Dijke, P., Miyazono, K. & Heldin, C. H. Signaling inputs converge on nuclear effectors in TGF-beta signaling. Trends Biochem. Sci. 25, 64-70 (2000).
50. Pucéat, M. TGFbeta in the differentiation of embryonic stem cells. Cardiovasc. Res. 74, 256-261 (2007).
51. Wu, H. & Zhang, Y. Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev. 25, 2436-2452 (2011).
52. Kagey, M. H. et al. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467, 430-435 (2010).
53. Chen, H. Z., Tsai, S. Y. & Leone, G. Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat. Rev. Cancer 9, 785-797 (2009).
54. Nikpour, P., Emadi-Baygi, M., Mohammad-Hashem, F., Maracy, M. R. & Haghjooy-Javanmard, S. Differential expression of ZFX gene in gastric cancer. J. Biosci. 37, 85-90 (2012).
55. Nicholson, S., Whitehouse, H., Naidoo, K. & Byers, R. J. Yin Yang 1 in human cancer. Crit. Rev. Oncog. 16, 245-260 (2011).
56. Fiorentino, F. P. & Giordano, A. The tumor suppressor role of CTCF. J. Cell Physiol. 227, 479-492 (2012).
57. The ENCODE Project Consortium. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 9, e1001046 (2011).
58. Chen, L., Wu, G. & Ji, H. hmChIP: a database and web server for exploring publicly available human and mouse ChIP-seq and ChIP-chip data. Bioinformatics 27, 1447-1448 (2011).
59. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
60. Sailaja, B. S., Takizawa, T. & Meshorer, E. Chromatin immunoprecipitation in mouse hippocampal cells and tissues. Methods Mol. Biol. 809, 353-364 (2012).
61. Chen, X. et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133, 1106-1117 (2008).