This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Li, J.
Right arrow Articles by Wong, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Li, J.
Right arrow Articles by Wong, J.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, August 2002, p. 5688-5697, Vol. 22, No. 16
0270-7306/02/$04.00+0     DOI: 10.1128/MCB.22.16.5688-5697.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Involvement of Histone Methylation and Phosphorylation in Regulation of Transcription by Thyroid Hormone Receptor

Jiwen Li,1 Qiushi Lin,1 Ho-Geun Yoon,1 Zhi-Qing Huang,1 Brian D. Strahl,2 C. David Allis,2 and Jiemin Wong1*

Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas 77030,1 Department of Biochemistry and Molecular Genetics, University of Virginia Health System, Charlottesville, Virginia 22908-07332

Received 13 December 2001/ Returned for modification 5 February 2002/ Accepted 22 May 2002

Previous studies have established an important role of histone acetylation in transcriptional control by nuclear hormone receptors. With chromatin immunoprecipitation assays, we have now investigated whether histone methylation and phosphorylation are also involved in transcriptional regulation by thyroid hormone receptor (TR). We found that repression by unliganded TR is associated with a substantial increase in methylation of H3 lysine 9 (H3-K9) and a decrease in methylation of H3 lysine 4 (H3-K4), methylation of H3 arginine 17 (H3-R17), and a dual modification of phosphorylation of H3 serine 10 and acetylation of lysine 14 (pS10/acK14). On the other hand, transcriptional activation by liganded TR is coupled with a substantial decrease in both H3-K4 and H3-K9 methylation and a robust increase in H3-R17 methylation and the dual modification of pS10/acK14. Trichostatin A treatment results in not only histone hyperacetylation but also an increase in methylation of H3-K4, increase in dual modification of pS10/acK14, and reduction in methylation of H3-K9, revealing an extensive interplay between histone acetylation, methylation, and phosphorylation. In an effort to understand the underlying mechanism for an increase in H3-K9 methylation during repression by unliganded TR, we demonstrated that TR interacts in vitro with an H3-K9-specific histone methyltransferase (HMT), SUV39H1. Functional analysis indicates that SUV39H1 can facilitate repression by unliganded TR and in so doing requires its HMT activity. Together, our data uncover a novel role of H3-K9 methylation in repression by unliganded TR and provide strong evidence for the involvement of multiple distinct histone covalent modifications (acetylation, methylation, and phosphorylation) in transcriptional control by nuclear hormone receptors.

* Corresponding author. Mailing address: Department of Molecular and Cellular Biology, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030. Phone: (713) 798-6291. Fax: (713) 790-1275. E-mail: jwong{at}bcm.tmc.edu.

Molecular and Cellular Biology, August 2002, p. 5688-5697, Vol. 22, No. 16
0022-538X/02/$04.00+0     DOI: 10.1128/MCB.22.16.5688-5697.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Wu, S. C., Zhang, Y. (2009). Minireview: Role of Protein Methylation and Demethylation in Nuclear Hormone Signaling. Mol. Endocrinol. 23: 1323-1334 [Abstract] [Full Text]  
  • Umezawa, R., Yamada, M., Horiguchi, K., Ishii, S., Hashimoto, K., Okada, S., Satoh, T., Mori, M. (2009). Aberrant Histone Modifications at the Thyrotropin-Releasing Hormone Gene in Resistance to Thyroid Hormone: Analysis of F455S Mutant Thyroid Hormone Receptor. Endocrinology 150: 3425-3432 [Abstract] [Full Text]  
  • Matsuda, H., Paul, B. D., Choi, C. Y., Hasebe, T., Shi, Y.-B. (2009). Novel Functions of Protein Arginine Methyltransferase 1 in Thyroid Hormone Receptor-Mediated Transcription and in the Regulation of Metamorphic Rate in Xenopus laevis. Mol. Cell. Biol. 29: 745-757 [Abstract] [Full Text]  
  • Chinenov, Y., Sacta, M. A., Cruz, A. R., Rogatsky, I. (2008). GRIP1-associated SET-domain methyltransferase in glucocorticoid receptor target gene expression. Proc. Natl. Acad. Sci. USA 105: 20185-20190 [Abstract] [Full Text]  
  • Nguyen, P., Bar-Sela, G., Sun, L., Bisht, K. S., Cui, H., Kohn, E., Feinberg, A. P., Gius, D. (2008). BAT3 and SET1A Form a Complex with CTCFL/BORIS To Modulate H3K4 Histone Dimethylation and Gene Expression. Mol. Cell. Biol. 28: 6720-6729 [Abstract] [Full Text]  
  • Sun, L., Huang, L., Nguyen, P., Bisht, K. S., Bar-Sela, G., Ho, A. S., Bradbury, C. M., Yu, W., Cui, H., Lee, S., Trepel, J. B., Feinberg, A. P., Gius, D. (2008). DNA Methyltransferase 1 and 3B Activate BAG-1 Expression via Recruitment of CTCFL/BORIS and Modulation of Promoter Histone Methylation. Cancer Res. 68: 2726-2735 [Abstract] [Full Text]  
  • Eberlin, A., Grauffel, C., Oulad-Abdelghani, M., Robert, F., Torres-Padilla, M.-E., Lambrot, R., Spehner, D., Ponce-Perez, L., Wurtz, J.-M., Stote, R. H., Kimmins, S., Schultz, P., Dejaegere, A., Tora, L. (2008). Histone H3 Tails Containing Dimethylated Lysine and Adjacent Phosphorylated Serine Modifications Adopt a Specific Conformation during Mitosis and Meiosis. Mol. Cell. Biol. 28: 1739-1754 [Abstract] [Full Text]  
  • Witcher, M., Pettersson, F., Dupere-Richer, D., Padovani, A., Summers-Deluca, L., Baldwin, A. S., Miller, W. H. Jr (2008). Retinoic acid modulates chromatin to potentiate tumor necrosis factor alpha signaling on the DIF2 promoter. Nucleic Acids Res 36: 435-443 [Abstract] [Full Text]  
  • Gordon, M., Holt, D. G., Panigrahi, A., Wilhelm, B. T., Erdjument-Bromage, H., Tempst, P., Bahler, J., Cairns, B. R. (2007). Genome-Wide Dynamics of SAPHIRE, an Essential Complex for Gene Activation and Chromatin Boundaries. Mol. Cell. Biol. 27: 4058-4069 [Abstract] [Full Text]  
  • Matsuda, H., Paul, B. D., Choi, C. Y., Shi, Y.-B. (2007). Contrasting Effects of Two Alternative Splicing Forms of Coactivator-Associated Arginine Methyltransferase 1 on Thyroid Hormone Receptor-Mediated Transcription in Xenopus laevis. Mol. Endocrinol. 21: 1082-1094 [Abstract] [Full Text]  
  • Fava, G., Ueno, Y., Glaser, S., Francis, H., DeMorrow, S., Marucci, L., Marzioni, M., Benedetti, A., Venter, J., Vaculin, B., Vaculin, S., Alpini, G. (2007). Thyroid hormone inhibits biliary growth in bile duct-ligated rats by PLC/IP3/Ca2+-dependent downregulation of SRC/ERK1/2. Am. J. Physiol. Cell Physiol. 292: C1467-C1475 [Abstract] [Full Text]  
  • Wagner, S., Weber, S., Kleinschmidt, M. A., Nagata, K., Bauer, U.-M. (2006). SET-mediated Promoter Hypoacetylation Is a Prerequisite for Coactivation of the Estrogen-responsive pS2 Gene by PRMT1. J. Biol. Chem. 281: 27242-27250 [Abstract] [Full Text]  
  • Stewart, M. D., Sommerville, J., Wong, J. (2006). Dynamic Regulation of Histone Modifications in Xenopus Oocytes through Histone Exchange.. Mol. Cell. Biol. 26: 6890-6901 [Abstract] [Full Text]  
  • Nygard, M., Becker, N., Demeneix, B., Pettersson, K., Bondesson, M. (2006). Thyroid hormone-mediated negative transcriptional regulation of Necdin expression.. J Mol Endocrinol 36: 517-530 [Abstract] [Full Text]  
  • Liu, Y., Xia, X., Fondell, J. D., Yen, P. M. (2006). Thyroid Hormone-Regulated Target Genes Have Distinct Patterns of Coactivator Recruitment and Histone Acetylation. Mol. Endocrinol. 20: 483-490 [Abstract] [Full Text]  
  • Conde, I., Paniagua, R., Zamora, J., Blanquez, M. J., Fraile, B., Ruiz, A., Arenas, M. I. (2006). Influence of thyroid hormone receptors on breast cancer cell proliferation. Ann Oncol 17: 60-64 [Abstract] [Full Text]  
  • Zhang, Y., Fatima, N., Dufau, M. L. (2005). Coordinated Changes in DNA Methylation and Histone Modifications Regulate Silencing/Derepression of Luteinizing Hormone Receptor Gene Transcription. Mol. Cell. Biol. 25: 7929-7939 [Abstract] [Full Text]  
  • Akbarian, S., Ruehl, M. G., Bliven, E., Luiz, L. A., Peranelli, A. C., Baker, S. P., Roberts, R. C., Bunney, W. E. Jr, Conley, R. C., Jones, E. G., Tamminga, C. A., Guo, Y. (2005). Chromatin Alterations Associated With Down-regulated Metabolic Gene Expression in the Prefrontal Cortex of Subjects With Schizophrenia. Arch Gen Psychiatry 62: 829-840 [Abstract] [Full Text]  
  • Kinyamu, H K, Chen, J, Archer, T K (2005). Linking the ubiquitin-proteasome pathway to chromatin remodeling/modification by nuclear receptors. J Mol Endocrinol 34: 281-297 [Abstract] [Full Text]  
  • Stewart, M. D., Li, J., Wong, J. (2005). Relationship between Histone H3 Lysine 9 Methylation, Transcription Repression, and Heterochromatin Protein 1 Recruitment. Mol. Cell. Biol. 25: 2525-2538 [Abstract] [Full Text]  
  • Lee, D. Y., Teyssier, C., Strahl, B. D., Stallcup, M. R. (2005). Role of Protein Methylation in Regulation of Transcription. Endocr. Rev. 26: 147-170 [Abstract] [Full Text]  
  • Yoon, H.-G., Choi, Y., Cole, P. A., Wong, J. (2005). Reading and Function of a Histone Code Involved in Targeting Corepressor Complexes for Repression. Mol. Cell. Biol. 25: 324-335 [Abstract] [Full Text]  
  • Sarg, B., Helliger, W., Talasz, H., Koutzamani, E., Lindner, H. H. (2004). Histone H4 Hyperacetylation Precludes Histone H4 Lysine 20 Trimethylation. J. Biol. Chem. 279: 53458-53464 [Abstract] [Full Text]  
  • Li, Y.-J., Stallcup, M. R., Lai, M. M. C. (2004). Hepatitis Delta Virus Antigen Is Methylated at Arginine Residues, and Methylation Regulates Subcellular Localization and RNA Replication. J. Virol. 78: 13325-13334 [Abstract] [Full Text]  
  • Jallow, Z., Jacobi, U. G., Weeks, D. L., Dawid, I. B., Veenstra, G. J. C. (2004). Specialized and redundant roles of TBP and a vertebrate-specific TBP paralog in embryonic gene regulation in Xenopus. Proc. Natl. Acad. Sci. USA 101: 13525-13530 [Abstract] [Full Text]  
  • Powell, D. W., Weaver, C. M., Jennings, J. L., McAfee, K. J., He, Y., Weil, P. A., Link, A. J. (2004). Cluster Analysis of Mass Spectrometry Data Reveals a Novel Component of SAGA. Mol. Cell. Biol. 24: 7249-7259 [Abstract] [Full Text]  
  • Nishio, H., Walsh, M. J. (2004). CCAAT displacement protein/cut homolog recruits G9a histone lysine methyltransferase to repress transcription. Proc. Natl. Acad. Sci. USA 101: 11257-11262 [Abstract] [Full Text]  
  • Ma, Z., Shah, R. C., Chang, M. J., Benveniste, E. N. (2004). Coordination of Cell Signaling, Chromatin Remodeling, Histone Modifications, and Regulator Recruitment in Human Matrix Metalloproteinase 9 Gene Transcription. Mol. Cell. Biol. 24: 5496-5509 [Abstract] [Full Text]  
  • Szabo, P. E., Pfeifer, G. P., Mann, J. R. (2004). Parent-of-Origin-Specific Binding of Nuclear Hormone Receptor Complexes in the H19-Igf2 Imprinting Control Region. Mol. Cell. Biol. 24: 4858-4868 [Abstract] [Full Text]  
  • Kim, J., Jia, L., Tilley, W. D., Coetzee, G. A. (2003). Dynamic methylation of histone H3 at lysine 4 in transcriptional regulation by the androgen receptor. Nucleic Acids Res 31: 6741-6747 [Abstract] [Full Text]  
  • De Bosscher, K., Vanden Berghe, W., Haegeman, G. (2003). The Interplay between the Glucocorticoid Receptor and Nuclear Factor-{kappa}B or Activator Protein-1: Molecular Mechanisms for Gene Repression. Endocr. Rev. 24: 488-522 [Abstract] [Full Text]  
  • Fujii, S., Luo, R. Z., Yuan, J., Kadota, M., Oshimura, M., Dent, S. R., Kondo, Y., Issa, J.-P. J., Bast, R. C. Jr, Yu, Y. (2003). Reactivation of the silenced and imprinted alleles of ARHI is associated with increased histone H3 acetylation and decreased histone H3 lysine 9 methylation. Hum Mol Genet 12: 1791-1800 [Abstract] [Full Text]  
  • Kostrouchova, M., Kostrouch, Z., Saudek, V., Piatigorsky, J., Rall, J. E. (2003). BIR-1, a Caenorhabditis elegans homologue of Survivin, regulates transcription and development. Proc. Natl. Acad. Sci. USA 100: 5240-5245 [Abstract] [Full Text]  
  • Labrador, M., Corces, V. G. (2003). Phosphorylation of histone H3 during transcriptional activation depends on promoter structure. Genes Dev. 17: 43-48 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»