Previous Article | Next Article 
Molecular and Cellular Biology, December 2004, p. 10111-10117, Vol. 24, No. 23
0270-7306/04/$08.00+0 DOI: 10.1128/MCB.24.23.10111-10117.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.
Evidence for Eviction and Rapid Deposition of Histones upon Transcriptional Elongation by RNA Polymerase II
Marc A. Schwabish and
Kevin Struhl*
Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, Massachusetts
Received 1 June 2004/
Returned for modification 27 July 2004/
Accepted 26 August 2004
Biochemical experiments indicate that transcriptional elongation by RNA polymerase II (Pol II) is inhibited by nucleosomes and hence requires chromatin-modifying activities. Here, we examine the fate of histones upon passage of elongating Pol II in vivo. Histone density throughout the entire Saccharomyces cerevisiae GAL10 coding region is inversely correlated with Pol II association and transcriptional activity, suggesting that the elongating Pol II machinery efficiently evicts core histones from the DNA. Furthermore, new histones appear to be deposited onto DNA less than 1 min after passage of Pol II. Transcription-dependent deposition of histones requires the FACT complex that travels with elongating Pol II. Our results suggest that Pol II transcription generates a highly dynamic equilibrium of histone eviction and histone deposition and that there is significant histone exchange throughout most of the yeast genome within a single cell cycle.
* Corresponding author. Mailing address: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115. Phone: (617) 432-2104. Fax: (617) 432-2529. E-mail:
kevin{at}hms.harvard.edu.
Molecular and Cellular Biology, December 2004, p. 10111-10117, Vol. 24, No. 23
0022-538X/04/$08.00+0 DOI: 10.1128/MCB.24.23.10111-10117.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Ginsburg, D. S., Govind, C. K., Hinnebusch, A. G.
(2009). NuA4 Lysine Acetyltransferase Esa1 Is Targeted to Coding Regions and Stimulates Transcription Elongation with Gcn5. Mol. Cell. Biol.
29: 6473-6487
[Abstract]
[Full Text]
-
Li, C., Wu, K., Fu, G., Li, Y., Zhong, Y., Lin, X., Zhou, Y., Tian, L., Huang, S.
(2009). Regulation of oleosin expression in developing peanut (Arachis hypogaea L.) embryos through nucleosome loss and histone modifications. J Exp Bot
60: 4371-4382
[Abstract]
[Full Text]
-
Klopf, E., Paskova, L., Sole, C., Mas, G., Petryshyn, A., Posas, F., Wintersberger, U., Ammerer, G., Schuller, C.
(2009). Cooperation between the INO80 Complex and Histone Chaperones Determines Adaptation of Stress Gene Transcription in the Yeast Saccharomyces cerevisiae. Mol. Cell. Biol.
29: 4994-5007
[Abstract]
[Full Text]
-
Egloff, S., Al-Rawaf, H., O'Reilly, D., Murphy, S.
(2009). Chromatin Structure Is Implicated in "Late" Elongation Checkpoints on the U2 snRNA and {beta}-Actin Genes. Mol. Cell. Biol.
29: 4002-4013
[Abstract]
[Full Text]
-
Kutluay, S. B., Triezenberg, S. J.
(2009). Regulation of Histone Deposition on the Herpes Simplex Virus Type 1 Genome during Lytic Infection. J. Virol.
83: 5835-5845
[Abstract]
[Full Text]
-
Kutluay, S. B., DeVos, S. L., Klomp, J. E., Triezenberg, S. J.
(2009). Transcriptional Coactivators Are Not Required for Herpes Simplex Virus Type 1 Immediate-Early Gene Expression In Vitro. J. Virol.
83: 3436-3449
[Abstract]
[Full Text]
-
Nagata, M., Ito, T., Arimitsu, N., Koyama, H., Sekimizu, K.
(2009). Transcription arrest relief by S-II/TFIIS during gene expression in erythroblast differentiation. GENES CELLS
14: 371-380
[Abstract]
[Full Text]
-
Fan, X., Lamarre-Vincent, N., Wang, Q., Struhl, K.
(2008). Extensive chromatin fragmentation improves enrichment of protein binding sites in chromatin immunoprecipitation experiments. Nucleic Acids Res
36: e125-e125
[Abstract]
[Full Text]
-
Espinosa, J. M.
(2008). Histone H2B ubiquitination: the cancer connection. Genes Dev.
22: 2743-2749
[Abstract]
[Full Text]
-
Kim, J.-M., To, T. K., Ishida, J., Morosawa, T., Kawashima, M., Matsui, A., Toyoda, T., Kimura, H., Shinozaki, K., Seki, M.
(2008). Alterations of Lysine Modifications on the Histone H3 N-Tail under Drought Stress Conditions in Arabidopsis thaliana. Plant Cell Physiol
49: 1580-1588
[Abstract]
[Full Text]
-
Schafer, G., McEvoy, C. R. E., Patterton, H.-G.
(2008). The Saccharomyces cerevisiae linker histone Hho1p is essential for chromatin compaction in stationary phase and is displaced by transcription. Proc. Natl. Acad. Sci. USA
105: 14838-14843
[Abstract]
[Full Text]
-
Xie, F., Orr-Weaver, T. L.
(2008). Isolation of a Drosophila amplification origin developmentally activated by transcription. Proc. Natl. Acad. Sci. USA
105: 9651-9656
[Abstract]
[Full Text]
-
Flanagin, S., Nelson, J. D., Castner, D. G., Denisenko, O., Bomsztyk, K.
(2008). Microplate-based chromatin immunoprecipitation method, Matrix ChIP: a platform to study signaling of complex genomic events. Nucleic Acids Res
36: e17-e17
[Abstract]
[Full Text]
-
D'Alessio, A. C., Weaver, I. C. G., Szyf, M.
(2007). Acetylation-Induced Transcription Is Required for Active DNA Demethylation in Methylation-Silenced Genes. Mol. Cell. Biol.
27: 7462-7474
[Abstract]
[Full Text]
-
Schwabish, M. A., Struhl, K.
(2007). The Swi/Snf Complex Is Important for Histone Eviction during Transcriptional Activation and RNA Polymerase II Elongation In Vivo. Mol. Cell. Biol.
27: 6987-6995
[Abstract]
[Full Text]
-
Adkins, M. W., Williams, S. K., Linger, J., Tyler, J. K.
(2007). Chromatin Disassembly from the PHO5 Promoter Is Essential for the Recruitment of the General Transcription Machinery and Coactivators. Mol. Cell. Biol.
27: 6372-6382
[Abstract]
[Full Text]
-
Duina, A. A., Rufiange, A., Bracey, J., Hall, J., Nourani, A., Winston, F.
(2007). Evidence that the Localization of the Elongation Factor Spt16 Across Transcribed Genes Is Dependent Upon Histone H3 Integrity in Saccharomyces cerevisiae. Genetics
177: 101-112
[Abstract]
[Full Text]
-
Ewing, A. K., Attner, M., Chakravarti, D.
(2007). Novel Regulatory Role for Human Acf1 in Transcriptional Repression of Vitamin D3 Receptor-Regulated Genes. Mol. Endocrinol.
21: 1791-1806
[Abstract]
[Full Text]
-
Peckham, H. E., Thurman, R. E., Fu, Y., Stamatoyannopoulos, J. A., Noble, W. S., Struhl, K., Weng, Z.
(2007). Nucleosome positioning signals in genomic DNA. Genome Res
17: 1170-1177
[Abstract]
[Full Text]
-
Gligoris, T., Thireos, G., Tzamarias, D.
(2007). The Tup1 Corepressor Directs Htz1 Deposition at a Specific Promoter Nucleosome Marking the GAL1 Gene for Rapid Activation. Mol. Cell. Biol.
27: 4198-4205
[Abstract]
[Full Text]
-
Tanny, J. C., Erdjument-Bromage, H., Tempst, P., Allis, C. D.
(2007). Ubiquitylation of histone H2B controls RNA polymerase II transcription elongation independently of histone H3 methylation. Genes Dev.
21: 835-847
[Abstract]
[Full Text]
-
Sertil, O., Vemula, A., Salmon, S. L., Morse, R. H., Lowry, C. V.
(2007). Direct Role for the Rpd3 Complex in Transcriptional Induction of the Anaerobic DAN/TIR Genes in Yeast. Mol. Cell. Biol.
27: 2037-2047
[Abstract]
[Full Text]
-
Dion, M. F., Kaplan, T., Kim, M., Buratowski, S., Friedman, N., Rando, O. J.
(2007). Dynamics of Replication-Independent Histone Turnover in Budding Yeast. Science
315: 1405-1408
[Abstract]
[Full Text]
-
Shukla, A., Bajwa, P., Bhaumik, S. R.
(2006). SAGA-associated Sgf73p facilitates formation of the preinitiation complex assembly at the promoters either in a HAT-dependent or independent manner in vivo. Nucleic Acids Res
34: 6225-6232
[Abstract]
[Full Text]
-
Jimeno-Gonzalez, S., Gomez-Herreros, F., Alepuz, P. M., Chavez, S.
(2006). A Gene-Specific Requirement for FACT during Transcription Is Related to the Chromatin Organization of the Transcribed Region. Mol. Cell. Biol.
26: 8710-8721
[Abstract]
[Full Text]
-
Linger, J., Tyler, J. K.
(2006). Global Replication-Independent Histone H4 Exchange in Budding Yeast. Eukaryot Cell
5: 1780-1787
[Abstract]
[Full Text]
-
Grainger, D. C., Hurd, D., Goldberg, M. D., Busby, S. J. W.
(2006). Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res
34: 4642-4652
[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]
-
Zanton, S. J., Pugh, B. F.
(2006). Full and partial genome-wide assembly and disassembly of the yeast transcription machinery in response to heat shock.. Genes Dev.
20: 2250-2265
[Abstract]
[Full Text]
-
Workman, J. L.
(2006). Nucleosome displacement in transcription. Genes Dev.
20: 2009-2017
[Abstract]
[Full Text]
-
Tamburini, B. A., Carson, J. J., Linger, J. G., Tyler, J. K.
(2006). Dominant Mutants of the Saccharomyces cerevisiae ASF1 Histone Chaperone Bypass the Need for CAF-1 in Transcriptional Silencing by Altering Histone and Sir Protein Recruitment. Genetics
173: 599-610
[Abstract]
[Full Text]
-
Lemasson, I., Polakowski, N. J., Laybourn, P. J., Nyborg, J. K.
(2006). Tax-dependent Displacement of Nucleosomes during Transcriptional Activation of Human T-Cell Leukemia Virus Type 1. J. Biol. Chem.
281: 13075-13082
[Abstract]
[Full Text]
-
Millar, C. B., Xu, F., Zhang, K., Grunstein, M.
(2006). Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast.. Genes Dev.
20: 711-722
[Abstract]
[Full Text]
-
Korber, P., Barbaric, S., Luckenbach, T., Schmid, A., Schermer, U. J., Blaschke, D., Horz, W.
(2006). The Histone Chaperone Asf1 Increases the Rate of Histone Eviction at the Yeast PHO5 and PHO8 Promoters. J. Biol. Chem.
281: 5539-5545
[Abstract]
[Full Text]
-
Nourani, A., Robert, F., Winston, F.
(2006). Evidence that Spt2/Sin1, an HMG-Like Factor, Plays Roles in Transcription Elongation, Chromatin Structure, and Genome Stability in Saccharomyces cerevisiae. Mol. Cell. Biol.
26: 1496-1509
[Abstract]
[Full Text]
-
Choi, E. S., Shin, J. A, Kim, H. S., Jang, Y. K.
(2005). Dynamic regulation of replication independent deposition of histone H3 in fission yeast. Nucleic Acids Res
33: 7102-7110
[Abstract]
[Full Text]
-
Rao, B., Shibata, Y., Strahl, B. D., Lieb, J. D.
(2005). Dimethylation of Histone H3 at Lysine 36 Demarcates Regulatory and Nonregulatory Chromatin Genome-Wide. Mol. Cell. Biol.
25: 9447-9459
[Abstract]
[Full Text]
-
Milgrom, E., West, R. W. Jr., Gao, C., Shen, W.-C. W.
(2005). TFIID and Spt-Ada-Gcn5-Acetyltransferase Functions Probed by Genome-wide Synthetic Genetic Array Analysis Using a Saccharomyces cerevisiae taf9-ts Allele. Genetics
171: 959-973
[Abstract]
[Full Text]
-
Zhao, J., Herrera-Diaz, J., Gross, D. S.
(2005). Domain-Wide Displacement of Histones by Activated Heat Shock Factor Occurs Independently of Swi/Snf and Is Not Correlated with RNA Polymerase II Density. Mol. Cell. Biol.
25: 8985-8999
[Abstract]
[Full Text]
-
Yuan, G.-C., Liu, Y.-J., Dion, M. F., Slack, M. D., Wu, L. F., Altschuler, S. J., Rando, O. J.
(2005). Genome-Scale Identification of Nucleosome Positions in S. cerevisiae. Science
309: 626-630
[Abstract]
[Full Text]
-
Schwartz, B. E., Ahmad, K.
(2005). Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev.
19: 804-814
[Abstract]
[Full Text]
-
Thiriet, C., Hayes, J. J.
(2005). Replication-independent core histone dynamics at transcriptionally active loci in vivo. Genes Dev.
19: 677-682
[Abstract]
[Full Text]
-
EMRE, N.C.T., BERGER, S.L.
(2004). Histone H2B Ubiquitylation and Deubiquitylation in Genomic Regulation. Cold Spring Harb Symp Quant Biol
69: 289-300
[Abstract]