Previous Article | Next Article 
Mol Cell Biol, July 1998, p. 3668-3680, Vol. 18, No. 7
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Role of Histone H1 as an Architectural Determinant of Chromatin
Structure and as a Specific Repressor of Transcription on
Xenopus Oocyte 5S rRNA Genes
Takashi
Sera and
Alan P.
Wolffe*
Laboratory of Molecular Embryology, National
Institute of Child Health and Human Development, Bethesda, Maryland
20892-5431
Received 20 January 1998/Returned for modification 23 March
1998/Accepted 9 April 1998
We explore the role of histone H1 as a DNA sequence-dependent
architectural determinant of chromatin structure and of transcriptional activity in chromatin. The Xenopus laevis oocyte- and
somatic-type 5S rRNA genes are differentially transcribed in embryonic
chromosomes in vivo depending on the incorporation of somatic
histone H1 into chromatin. We establish that this effect can be
reconstructed at the level of a single nucleosome. H1
selectively represses oocyte-type 5S rRNA genes by directing the stable
positioning of a nucleosome such that transcription factors cannot bind
to the gene. This effect does not occur on the somatic-type genes. Histone H1 binds to the 5' end of the nucleosome core on the somatic 5S
rRNA gene, leaving key regulatory elements in the
promoter accessible, while histone H1 binds to the 3' end of the
nucleosome core on the oocyte 5S rRNA genes, specifically blocking
access to a key promoter element (the C box). TFIIIA can bind to the somatic 5S rRNA gene assembled into a nucleosome in the presence of H1.
Because H1 binds with equivalent affinities to nucleosomes containing
either gene, we establish that it is the sequence-selective assembly of
a specific repressive chromatin structure on the oocyte 5S rRNA genes
that accounts for differential transcriptional repression. Thus,
general components of chromatin can determine the assembly of specific
regulatory nucleoprotein complexes.
*
Corresponding author. Mailing address: Laboratory of
Molecular Embryology, National Institute of Child Health and Human
Development, NIH, Bldg. 18T, Rm. 106, Bethesda, MD 20892-5431. Phone:
(301) 402-2722. Fax: (301) 402-1323. E-mail:
awlme{at}helix.nih.gov.
Mol Cell Biol, July 1998, p. 3668-3680, Vol. 18, No. 7
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Yang, Z., Zheng, C., Hayes, J. J.
(2007). The Core Histone Tail Domains Contribute to Sequence-dependent Nucleosome Positioning. J. Biol. Chem.
282: 7930-7938
[Abstract]
[Full Text]
-
Konesky, K. L., Nyborg, J. K., Laybourn, P. J.
(2006). Tax Abolishes Histone H1 Repression of p300 Acetyltransferase Activity at the Human T-Cell Leukemia Virus Type 1 Promoter. J. Virol.
80: 10542-10553
[Abstract]
[Full Text]
-
Becker, M., Becker, A., Miyara, F., Han, Z., Kihara, M., Brown, D. T., Hager, G. L., Latham, K., Adashi, E. Y., Misteli, T.
(2005). Differential In Vivo Binding Dynamics of Somatic and Oocyte-specific Linker Histones in Oocytes and During ES Cell Nuclear Transfer. Mol. Biol. Cell
16: 3887-3895
[Abstract]
[Full Text]
-
Jason, L. J. M., Finn, R. M., Lindsey, G., Ausio, J.
(2005). Histone H2A Ubiquitination Does Not Preclude Histone H1 Binding, but It Facilitates Its Association with the Nucleosome. J. Biol. Chem.
280: 4975-4982
[Abstract]
[Full Text]
-
Chioda, M., Spada, F., Eskeland, R., Thompson, E. M.
(2004). Histone mRNAs Do Not Accumulate during S Phase of either Mitotic or Endoreduplicative Cycles in the Chordate Oikopleura dioica. Mol. Cell. Biol.
24: 5391-5403
[Abstract]
[Full Text]
-
Ghose, R., Malik, M., Huber, P. W.
(2004). Restricted Specificity of Xenopus TFIIIA for Transcription of Somatic 5S rRNA Genes. Mol. Cell. Biol.
24: 2467-2477
[Abstract]
[Full Text]
-
Ragab, A., Travers, A.
(2003). HMG-D and histone H1 alter the local accessibility of nucleosomal DNA. Nucleic Acids Res
31: 7083-7089
[Abstract]
[Full Text]
-
Ramachandran, A., Omar, M., Cheslock, P., Schnitzler, G. R.
(2003). Linker Histone H1 Modulates Nucleosome Remodeling by Human SWI/SNF. J. Biol. Chem.
278: 48590-48601
[Abstract]
[Full Text]
-
Rastelli, L., Robinson, K., Xu, Y., Majumder, S.
(2001). Reconstitution of Enhancer Function in Paternal Pronuclei of One-Cell Mouse Embryos. Mol. Cell. Biol.
21: 5531-5540
[Abstract]
[Full Text]
-
Gui, C.-Y., Dean, A.
(2001). Acetylation of a Specific Promoter Nucleosome Accompanies Activation of the {varepsilon}-Globin Gene by {beta}-Globin Locus Control Region HS2. Mol. Cell. Biol.
21: 1155-1163
[Abstract]
[Full Text]
-
ZLATANOVA, J., CAIAFA, P., VAN HOLDE, K.
(2000). Linker histone binding and displacement: versatile mechanism for transcriptional regulation. FASEB J.
14: 1697-1704
[Abstract]
[Full Text]
-
Vassetzky, Y., Hair, A., Méchali, M.
(2000). Rearrangement of chromatin domains during development in Xenopus. Genes Dev.
14: 1541-1552
[Abstract]
[Full Text]
-
Vitolo, J. M., Thiriet, C., Hayes, J. J.
(2000). The H3-H4 N-Terminal Tail Domains Are the Primary Mediators of Transcription Factor IIIA Access to 5S DNA within a Nucleosome. Mol. Cell. Biol.
20: 2167-2175
[Abstract]
[Full Text]
-
Adenot, P., Campion, E, Legouy, E, Allis, C., Dimitrov, S, Renard, J, Thompson, E.
(2000). Somatic linker histone H1 is present throughout mouse embryogenesis and is not replaced by variant H1 degrees. J. Cell Sci.
113: 2897-2907
[Abstract]
-
Barra, J. L., Rhounim, L., Rossignol, J.-L., Faugeron, G.
(2000). Histone H1 Is Dispensable for Methylation-Associated Gene Silencing in Ascobolus immersus and Essential for Long Life Span. Mol. Cell. Biol.
20: 61-69
[Abstract]
[Full Text]
-
Bonnefoy, E., Bandu, M.-T., Doly, J.
(1999). Specific Binding of High-Mobility-Group I (HMGI) Protein and Histone H1 to the Upstream AT-Rich Region of the Murine Beta Interferon Promoter: HMGI Protein Acts as a Potential Antirepressor of the Promoter. Mol. Cell. Biol.
19: 2803-2816
[Abstract]
[Full Text]
-
Stünkel, W., Bernard, H.-U.
(1999). The Chromatin Structure of the Long Control Region of Human Papillomavirus Type 16 Represses Viral Oncoprotein Expression. J. Virol.
73: 1918-1930
[Abstract]
[Full Text]
-
An, W., van Holde, K., Zlatanova, J.
(1998). The Non-histone Chromatin Protein HMG1 Protects Linker DNA on the Side Opposite to That Protected by Linker Histones. J. Biol. Chem.
273: 26289-26291
[Abstract]
[Full Text]
-
Zhang, L., Spratt, S. K., Liu, Q., Johnstone, B., Qi, H., Raschke, E. E., Jamieson, A. C., Rebar, E. J., Wolffe, A. P., Case, C. C.
(2000). Synthetic Zinc Finger Transcription Factor Action at an Endogenous Chromosomal Site. ACTIVATION OF THE HUMAN ERYTHROPOIETIN GENE. J. Biol. Chem.
275: 33850-33860
[Abstract]
[Full Text]
-
Banks, G. C., Deterding, L. J., Tomer, K. B., Archer, T. K.
(2001). Hormone-mediated Dephosphorylation of Specific Histone H1 Isoforms. J. Biol. Chem.
276: 36467-36473
[Abstract]
[Full Text]