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Science 293 (5531): 853-857

Copyright © 2001 by the American Association for the Advancement of Science

Methylation of Histone H4 at Arginine 3 Facilitating Transcriptional Activation by Nuclear Hormone Receptor

Hengbin Wang,1 Zhi-Qing Huang,2 Li Xia,1 Qin Feng,1 Hediye Erdjument-Bromage,3 Brian D. Strahl,4 Scott D. Briggs,4 C. David Allis,4 Jiemin Wong,2 Paul Tempst,3 Yi Zhang1*

Acetylation of core histone tails plays a fundamental role in transcription regulation. In addition to acetylation, other posttranslational modifications, such as phosphorylation and methylation, occur in core histone tails. Here, we report the purification, molecular identification, and functional characterization of a histone H4-specific methyltransferase PRMT1, a protein arginine methyltransferase. PRMT1 specifically methylates arginine 3 (Arg 3) of H4 in vitro and in vivo. Methylation of Arg 3 by PRMT1 facilitates subsequent acetylation of H4 tails by p300. However, acetylation of H4 inhibits its methylation by PRMT1. Most important, a mutation in the S-adenosyl-L-methionine-binding site of PRMT1 substantially crippled its nuclear receptor coactivator activity. Our finding reveals Arg 3 of H4 as a novel methylation site by PRMT1 and indicates that Arg 3 methylation plays an important role in transcriptional regulation.

1 Department of Biochemistry and Biophysics, Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7295, USA.
2 Department of Molecular and Cellular Biology, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
3 Molecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10021, USA.
4 Department of Biochemistry and Molecular Genetics, University of Virginia Health Science Center, Charlottesville, VA 22908, USA.
*   To whom correspondence should be addressed. E-mail: yi_zhang{at}med.unc.edu


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Histone H4 Hyperacetylation Precludes Histone H4 Lysine 20 Trimethylation.
B. Sarg, W. Helliger, H. Talasz, E. Koutzamani, and H. H. Lindner (2004)
J. Biol. Chem. 279, 53458-53464
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Hepatitis Delta Virus Antigen Is Methylated at Arginine Residues, and Methylation Regulates Subcellular Localization and RNA Replication.
Y.-J. Li, M. R. Stallcup, and M. M. C. Lai (2004)
J. Virol. 78, 13325-13334
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Arginine Methylation of Scaffold Attachment Factor A by Heterogeneous Nuclear Ribonucleoprotein Particle-associated PRMT1.
F. Herrmann, M. Bossert, A. Schwander, E. Akgun, and F. O. Fackelmayer (2004)
J. Biol. Chem. 279, 48774-48779
   Abstract »    Full Text »    PDF »
Human SWI/SNF-Associated PRMT5 Methylates Histone H3 Arginine 8 and Negatively Regulates Expression of ST7 and NM23 Tumor Suppressor Genes.
S. Pal, S. N. Vishwanath, H. Erdjument-Bromage, P. Tempst, and S. Sif (2004)
Mol. Cell. Biol. 24, 9630-9645
   Abstract »    Full Text »    PDF »
Human PAD4 Regulates Histone Arginine Methylation Levels via Demethylimination.
Y. Wang, J. Wysocka, J. Sayegh, Y.-H. Lee, J. R. Perlin, L. Leonelli, L. S. Sonbuchner, C. H. McDonald, R. G. Cook, Y. Dou, et al. (2004)
Science 306, 279-283
   Abstract »    Full Text »    PDF »
Epigenetics and cancer.
A. H. Lund and M. van Lohuizen (2004)
Genes & Dev. 18, 2315-2335
   Abstract »    Full Text »    PDF »
Transcriptional complexes engaged by apo-estrogen receptor-{alpha} isoforms have divergent outcomes.
R. Metivier, G. Penot, R. P. Carmouche, M. R. Hubner, G. Reid, S. Denger, D. Manu, H. Brand, M. Kos, V. Benes, et al. (2004)
EMBO J. 23, 3653-3666
   Abstract »    Full Text »    PDF »
Dynamic alterations of specific histone modifications during early murine development.
O. F. Sarmento, L. C. Digilio, Y. Wang, J. Perlin, J. C. Herr, C. D. Allis, and S. A. Coonrod (2004)
J. Cell Sci. 117, 4449-4459
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A Histone Methyltransferase Is Required for Maximal Response to Female Sex Hormones.
T. Carling, K.-C. Kim, X.-H. Yang, J. Gu, X.-K. Zhang, and S. Huang (2004)
Mol. Cell. Biol. 24, 7032-7042
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Cluster Analysis of Mass Spectrometry Data Reveals a Novel Component of SAGA.
D. W. Powell, C. M. Weaver, J. L. Jennings, K. J. McAfee, Y. He, P. A. Weil, and A. J. Link (2004)
Mol. Cell. Biol. 24, 7249-7259
   Abstract »    Full Text »    PDF »
Small Molecule Regulators of Protein Arginine Methyltransferases.
D. Cheng, N. Yadav, R. W. King, M. S. Swanson, E. J. Weinstein, and M. T. Bedford (2004)
J. Biol. Chem. 279, 23892-23899
   Abstract »    Full Text »    PDF »
Mechanistic Relationship between Androgen Receptor Polyglutamine Tract Truncation and Androgen-dependent Transcriptional Hyperactivity in Prostate Cancer Cells.
Q. Wang, T. S. Udayakumar, T. S. Vasaitis, A. M. Brodie, and J. D. Fondell (2004)
J. Biol. Chem. 279, 17319-17328
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Transcription Factors and Nuclear Receptors Interact with the SWI/SNF Complex through the BAF60c Subunit.
M.-B. Debril, L. Gelman, E. Fayard, J.-S. Annicotte, S. Rocchi, and J. Auwerx (2004)
J. Biol. Chem. 279, 16677-16686
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Lessons from the Genome Sequence of Neurospora crassa: Tracing the Path from Genomic Blueprint to Multicellular Organism.
K. A. Borkovich, L. A. Alex, O. Yarden, M. Freitag, G. E. Turner, N. D. Read, S. Seiler, D. Bell-Pedersen, J. Paietta, N. Plesofsky, et al. (2004)
Microbiol. Mol. Biol. Rev. 68, 1-108
   Abstract »    Full Text »    PDF »
Linking Covalent Histone Modifications to Epigenetics: The Rigidity and Plasticity of the Marks.
Y. WANG, J. WYSOCKA, J.R. PERLIN, L. LEONELLI, C.D. ALLIS, and S.A. COONROD (2004)
Cold Spring Harb Symp Quant Biol 69, 161-170
   Abstract »    PDF »

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