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Science 299 (5603): 112-114

Copyright © 2003 by the American Association for the Advancement of Science

Modulation of ATP-Dependent Chromatin-Remodeling Complexes by Inositol Polyphosphates

Xuetong Shen,* Hua Xiao, Ryan Ranallo, Wei-Hua Wu, Carl Wudagger

Eukaryotes use adenosine triphosphate (ATP)-dependent chromatin-remodeling complexes to regulate gene expression. Here, we show that inositol polyphosphates can modulate the activities of several chromatin-remodeling complexes in vitro. Inositol hexakisphosphate (IP6) inhibits nucleosome mobilization by NURF, ISW2, and INO80 complexes. In contrast, nucleosome mobilization by the yeast SWI/SNF complex is stimulated by inositol tetrakisphosphate (IP4) and inositol pentakisphosphate (IP5). We demonstrate that mutations in genes encoding inositol polyphosphate kinases that produce IP4, IP5, and IP6 impair transcription in vivo. These results provide a link between inositol polyphosphates, chromatin remodeling, and gene expression.

Laboratory of Molecular Cell Biology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892-4255, USA.
*   Present address: Department of Carcinogenesis, University of Texas MD Anderson Cancer Center, Science Park Research Division, Smithville, TX 78957, USA.

dagger    To whom correspondence should be addressed. E-mail: carlwu{at}helix.nih.gov



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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
PTEN M-CBR3, a Versatile and Selective Regulator of Inositol 1,3,4,5,6-Pentakisphosphate (Ins(1,3,4,5,6)P5): EVIDENCE FOR Ins(1,3,4,5,6)P5 AS A PROLIFERATIVE SIGNAL.
E. A. Orchiston, D. Bennett, N. R. Leslie, R. G. Clarke, L. Winward, C. P. Downes, and S. T. Safrany (2004)
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   Abstract »    Full Text »    PDF »
Nuclear lipids: key signaling effectors in the nervous system and other tissues.
R. W. Ledeen and G. Wu (2004)
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   Abstract »    Full Text »    PDF »
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A. Zewail, M. W. Xie, Y. Xing, L. Lin, P. F. Zhang, W. Zou, J. P. Saxe, and J. Huang (2003)
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   Abstract »    Full Text »    PDF »
Regulation of Chromatin Remodeling by Inositol Polyphosphates.
D. J. Steger, E. S. Haswell, A. L. Miller, S. R. Wente, and E. K. O'Shea (2003)
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   Abstract »    Full Text »    PDF »

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