ESET methylates UBF at K232/254 and regulates nucleolar heterochromatin plasticity and rDNA transcription

Nucleic Acids Research

Volumn 42, Issue 3, 2014, Pages 1628-1643

  Hwang, Yu Jin ^a   Han, Dohyun ^a   Kim, Ki Yoon ^a   Min, Sun Joon ^b   Kowall, Neil W ^c,d   Yang, Liu ^e,f   Lee, Junghee ^c,d   Kim, Youngsoo ^a   Ryu, Hoon ^b,c,d  

^a Seoul National University College of Medicine   (South Korea)

^b Korea Institute of Science and Technology   (South Korea)

^c VA BOSTON HEALTHCARE SYSTEM   (United States)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^f VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ETS RELATED GENE ASSOCIATED PROTEIN WITH SET PROTEIN; HISTONE METHYLTRANSFERASE; LYSINE; MUTANT PROTEIN; RIBOSOME DNA; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; UPSTREAM BINDING FACTOR;

ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN CONDENSATION; CONTROLLED STUDY; DNA MODIFICATION; EPIGENETICS; HETEROCHROMATIN; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN METHYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINE; CELL NUCLEOLUS; DNA, RIBOSOMAL; HETEROCHROMATIN; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; HUNTINGTON DISEASE; METHYLATION; MICE; MUTATION; POL1 TRANSCRIPTION INITIATION COMPLEX PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84896701163     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1041     Document Type: Article

References (42)

1. Lafontaine, D.L. and Tollervey, D. (2001) The function and synthesis of ribosomes. Nat. Rev. Mol. Cell Biol., 2, 514-520.
2. McStay, B. and Grummt, I. (2008) The epigenetics of rRNA genes: from molecular to chromosome biology. Annu. Rev. Cell Dev. Biol., 24, 131-157.
3. Chen, D., Belmont, A.S. and Huang, S. (2004) Upstream binding factor association induces large-scale chromatin decondensation. Proc. Natl Acad. Sci. USA, 101, 15106-15111.
4. Mais, C., Wright, J.E., Prieto, J.L., Raggett, S.L. and McStay, B. (2005) UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machinery. Genes Dev., 19, 50-64.
5. OMahony, D.J. and Rothblum, L.I. (1991) Identification of two forms of the RNA polymerase I transcription factor UBF. Proc. Natl Acad. Sci. USA, 88, 3180-3184.
6. Hirschler-Laszkiewicz, I., Cavanaugh, A., Hu, Q., Catania, J., Avantaggiati, M.L. and Rothblum, L.I. (2001) The role of acetylation in rDNA transcription. Nucleic Acids Res., 29, 4114-4124.
7. Stefanovsky, V.Y. and Moss, T. (2008) The splice variants of UBF differentially regulate RNA polymerase I transcription elongation in response to ERK phosphorylation. Nucleic Acids Res., 36, 5093-5101.
8. Hannan, R.D., Stefanovsky, V., Taylor, L., Moss, T. and Rothblum, L.I. (1996) Overexpression of the transcription factor UBF1 is sufficient to increase ribosomal DNA transcription in neonatal cardiomyocytes: implications for cardiac hypertrophy. Proc. Natl Acad. Sci. USA, 93, 8750-8755.
9. Birch, J.L. and Zomerdijk, J.C. (2008) Structure and function of ribosomal RNA gene chromatin. Biochem. Soc. Trans., 36, 619-624.
10. Sanij, E., Poortinga, G., Sharkey, K., Hung, S., Holloway, T.P., Quin, J., Robb, E., Wong, L.H., Stefanovsky, V., Moss, T. et al. (2008) UBF levels determine the number of active ribosomal RNA genes in mammals. J. Cell Biol., 183, 1259-1274.
11. Meraner, J., Lechner, M., Loidl, A., Goralik-Schramel, M., Voit, R., Grummt, I. and Loidl, P. (2006) Acetylation of UBF changes during the cell cycle and regulates the interaction of UBF with RNA polymerase I. Nucleic Acids Res., 34, 1798-1806.
12. Lin, C.H., Platt, M.D., Ficarro, S.B., Hoofnagle, M.H., Shabanowitz, J., Comai, L., Hunt, D.F. and Owens, G.K. (2007) Mass spectrometric identification of phophorylation sites of rRNA transcription factor upstream binding factor. Am. J. Physiol. Cell Physiol., 292, 1617-1624.
13. Pelletier, G., Stefanovsky, V.Y., Faubladier, M., Hirschler-Laszkiewicz, I., Savard, J., Rlthblum, L.I., Côté , J. and Moss, T. (2000) Competitive recruitment of CBP and Rb-HDAC regulates UBF acetylation and ribosomal transcription. Mol. Cell, 6, 1059-1066.
14. Steffan, J.S., Bodai, L., Pallos, J., Poelman, M., McCampbell, A., Apostol, B.L., Kazantsev, A., Schmidt, E., Zhu, Y.Z., Greenwald, M. et al. (2001) Histone deacetylase inhibitors arrest polyglutaminedependent neurodegeneration in Drosophila. Nature, 413, 739-743.
15. Nucifora, F.C., Sasaki, M., Peters, M.F., Huang, H., Cooper, J.K., Yamada, M., Takahashi, H., Tsuji, S., Troncoso, J., Dawson, V.L. et al. (2001) Interference by huntingtin and atrophin-1 with CBPmediated transcription leading to cellular toxicity. Science, 291, 2423-2428.
16. Steffan, J.S., Kazantsev, A., Spasic-Boskovic, O., Greenwald, M., Zhu, Y.Z., Gohler, H., Wanker, E.E., Bates, G.P., Housman, D.E. and Thompson, L.M. (2000) The Huntingtons disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc. Natl Acad. Sci. USA, 97, 6763-6768.
17. Zoqhbi, H.Y. and Orr, H.T. (2000) Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci., 23, 271-247.
18. McCampbell, A. and Fischbeck, K.H. (2001) Polyglutamine and CBP: fatal attraction? Nat. Med., 7, 528-530.
19. Lee, J., Hwang, Y.J., Boo, J.H., Han, D., Kwon, O.K., Todorova, K., Kowall, N.W., Kim, Y. and Ryu, H. (2011) Dysregulation of upstream binding factor-1 acetylation at K352 is linked to impaired ribosomal DNA transcription in Huntingtons disease. Cell Death Differ., 18, 1726-1735.
20. Sadri-Vakili, G. and Cha, J.H. (2006) Mechanisms of disease: Histone modifications in Huntingtons disease. Nat. Clin. Pract. Neurol., 2, 330-338.
21. Hake, S.B., Xiao, A. and Allis, C.D. (2004) Linking the epigenetic language of covalent histone modifications to cancer. Br. J. Cancer, 90, 761-769.
22. Wu, R., Terry, A.V., Singh, P.B. and Gilbert, D.M. (2005) Differential subnuclear localization and replication timing of histone H3 lysine 9 methylation states. Mol. Biol. Cell, 16, 2872-2881.
23. Ryu, H., Lee, J., Hagerty, S.W., Soh, B.Y., McAlpin, S.E., Cormier, K.A., Smith, K.M. and Ferrante, R.J. (2006) ESET/ SETDB1 gene expression and histone H3 (K9) trimethylation in Huntingtons disease. Proc. Natl Acad. Sci. USA, 103, 19176-19181.
24. Yang, L., Xia, L., Wu, D.Y., Wang, H., Chansky, H.A., Schubach, W.H., Hickstein, D.D. and Zhang, Y. (2002) Molecular cloning of ESET, a novel histone H3-specific methyltransferase that interacts with ERG transcription factor. Oncogene, 21, 148-152.
25. Feng, W., Yonezawa, M., Jenuwein, T. and Grummt, I. (2010) PHF8 activates transcription of rRNA genes through H3K4me3 binding and H3K9me1/2 demethylation. Nat. Struct. Mol. Biol., 17, 445-450.
26. Ghoshal, K., Majumder, S., Datta, J., Motiwala, T., Bai, S., Sharma, S.M., Frankel, W. and Jacob, S.T. (2004) Role of human ribosomal RNA (rRNA) promoter methylation and of methyl-CpG-binding protein MBD2 in the suppression of rRNA gene expression. J. Biol. Chem., 279, 6783-6793.
27. Schultz, D.C., Ayyanathan, K., Negorev, D., Maul, G.G. and Rauscher, F.J. 3rd (2002) SETDB1: a novel KAP-1-Associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev., 16, 919-932.
28. Rea, S., Eisenhaber, F., OCarroll, D., Strahl, B.D., Sun, Z.W., Schmid, M., Opravil, S., Mechtler, K., Ponting, C.P., Allis, C.D. et al. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature, 406, 593-599.
29. Trettel, F., Rigamonti, D., Hilditch-Maguire, P., Wheeler, V.C., Sharp, A.H., Persichetti, F., Cattaneo, E. and MacDonald, M.E. (2000) Dominant phenotypes produced by the HD mutation in STHdh (Q111) striatal cell. Hum. Mol. Genet., 9, 2799-2809.
30. Lee, J., Hagerty, S., Cormier, K.A., Kim, J., Kung, A.L., Ferrante, R.J. and Ryu, H. (2008) Monoallele deletion of CBP leads to pericentromeric heterochromatin condensation through ESET expression and histone H3 (K9) methylation. Hum. Mol. Genet., 17, 1774-1782.
31. Lee, J., Hong, Y.K., Jeon, G.S., Hwang, Y.J., Kim, K.Y., Seong, K.H., Jung, M.K., Picketts, D.J., Kowall, N.W., Cho, K.S. et al. (2012) ATRX induction by mutant huntingtin via Cdx2 modulates heterochromatin condensation and pathology in Huntingtons disease. Cell Death Differ., 19, 1109-1116.
32. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J.V. and Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc., 1, 2856-2860.
33. Han, D., Moon, S., Kim, Y., Ho, W.K., Kang, Y., Jun, H. and Kim, Y. (2012) Comprehensive phosphoproteome analysis of INS-1 pancreatic beta-cells using various digestion strategies coupled with liquid chromatography-tandem mass spectrometry. J. Proteome Res., 11, 2206-2223.
34. Ryu, H., Lee, J., Olofssson, B.A., Mwidau, A., Dedeoglu, A., Escudero, M., Flemington, E., Azizkhan-Clifford, J., Ferrante, R.J. and RatanR, R. (2003) Histone deacetylase inhibitors prevent oxidative neuronal death independent of expanded polyglutamine repeats via an Sp1-dependent pathway. Proc. Natl Acad. Sci. USA, 100, 4281-4286.
35. Ryu, H., Lee, J., Zaman, K., Kubilis, J., Ferrante, R.J., Ross, B.D., Neve, R. and Ratan, R.R. (2003) Sp1 and Sp3 are oxidative stressinducible, anti-death transcription factors in cortical neurons. J. Neurosci., 23, 3597-3606.
36. Ryu, H., Smith, K., Camelo, S.I., Carreras, I., Lee, J., Iglesias, A.H., Dangond, F., Cormier, K.A., Cudkowicz, M.E., Brown, R.H. Jr et al. (2005) Sodium phenylbutyrate prolongs survival and regulates expression of anti-Apoptotic genes in transgenic amyotrophic lateral sclerosis mice. J. Neurochem., 93, 1087-1098.
37. Casafont, I., Bengoechea, R., Navascué s, J., Pena, E., Berciano, M.T. and Lafarga, M. (2007) The giant fibrillar center: a nucleolar structure enriched in upstream binding factor (UBF) that appears in transcriptionally more active sensory ganglia neurons. J. Struct. Biol., 159, 451-461.
38. Dalal, Y., Wang, H., Lindsay, S. and Henikoff, S. (2007) Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol., 5, e218.
39. Dimitriadis, E.K., Weber, C., Gill, R.K., Diekmann, S. and Dalal, Y. (2010) Tetrameric organization of vertebrate centromeric nucleosomes. Proc. Natl Acad. Sci. USA, 107, 20317-20322.
40. Santos-Rosa, H., Schneider, R., Bannister, A.J., Sherriff, J., Bernstein, B.E., Emre, N.C., Schreiber, S.L., Mellor, J. and Kouzarides, T. (2002) Active genes are tri-methylated at K4 of histone H3. Nature, 419, 407-411.
41. Vonsattel, J.P. and DiFiglia, M. (1998) Huntington disease. J. Neuropathol. Exp. Neurol., 57, 369-384.
42. Chen, D., Belmont, A.S. and Huang, S. (2004) Upstream binding factor association induces large-scale chromatin decondensation. Proc. Natl Acad. Sci. USA, 101, 15106-15111.