Cotranscriptional Set2 Methylation of Histone H3 Lysine 36 Recruits a Repressive Rpd3 Complex

Keogh, Michael Christopher; Kurdistani, Siavash K.; Morris, Stephanie A.; Ahn, Shihyun; Podolny, Vladimir; Collins, Sean R.; Schuldiner, Maya; Chin, K.-D. Henry; Punna, Thanuja; Thompson, Natalie; Boone, Charles; Emili, Andrew; Weissman, Jonathan S.; Hughes, Timothy R.; Strahl, Brian D.; Grunstein, Michael; Greenblatt, Jack; Buratowski, Stephen; Krogan, Nevan J.

doi:10.1016/j.cell.2005.10.025

Cited by 741 publications

(864 citation statements)

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“…3). Based on the recent evidence that Set2p-mediated methylation of H3K36 is involved in the recruitment of a repressive Rpd3 complex (35)(36)(37), the simplest explanation of these observations is that this complex negatively regulates both meiotic recombination and transcription. This negative regulation is likely to be a consequence of a closed chromatin structure caused by Rpd3p-mediated deacetylation.…”

Section: Discussionmentioning

confidence: 99%

“…HIS4 hotspot in wild-type, set2, rpd3, and set2 rpd3 strains Loss of the Rpd3p deacetylase results in increased acetylation of many sites in H3 and H4 histones (56,57), whereas loss of the Set2p methylase directly affects only methylation of H3K36 (34). The Set2p-mediated methylation, however, helps recruit a repressive Rpd3p-containing complex to chromatin, and elevated histone acetylation was observed for several loci in set2 mutant strains (35,37). Consequently, we examined the histone acetylation levels at H3K27 by chromatin immunoprecipitation (ChIP analysis) in the diploids FX1 (wild-type), JDM1093 (set2), JDM1095 (rpd3), and JDM1096 (set2 rpd3).…”

Section: Measurement Of Meiosis-specific Dsbs At Thementioning

confidence: 99%

“…We examined mutants of SET2 (encoding an H3K36 histone methylase, 34), since it has been recently reported (35)(36)(37) that Set2p-dependent methylation recruits an Rpd3p-containing repressive complex (Rpd3C[S]). We also examined the effects of eliminating Dot1p, an H3K79 histone methyltransferase (38,39).…”

Section: Introductionmentioning

confidence: 99%

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The histone methylase Set2p and the histone deacetylase Rpd3p repress meiotic recombination at the HIS4 meiotic recombination hotspot in Saccharomyces cerevisiae

et al. 2008

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The rate of meiotic recombination in the yeast Saccharomyces cerevisiae varies widely in different regions of the genome with some genes having very high levels of recombination (hotspots). A variety of experiments done in yeast suggest that hotspots are a feature of chromatin structure rather than a feature of primary DNA sequence. We examined the effects of mutating a variety of enzymes that affect chromatin structure on the recombination activity of the well-characterized HIS4 hotspot including the Set2p and Dot1p histone methylases, the Hda1p and Rpd3p histone deacetylases, the Sin4p global transcription regulator, and a deletion of one of the two copies of the genes encoding histone H3-H4. Loss of Set2p or Rpd3p substantially elevated HIS4 hotspot activity, and loss of Hda1p had a smaller stimulatory effect; none of the other alterations had a significant effect. The increase of HIS4 hotspot activity in set2 and rpd3 strains is likely to be related to the recent finding that histone H3 methylation by Set2p directs deacetylation of histones by Rpd3p. IntroductionThe rate of meiotic recombination varies considerably at different positions in the yeast genome (1,2). This variation reflects differences in the frequency of local meiosis-specific doublestrand DNA breaks (DSBs), the recombination-initiating lesion (3,4) catalyzed by Spo11p and associated proteins (5). There are several lines of evidence that the frequency of DSBs is regulated by elements of chromatin structure rather than primary DNA sequence (2). First, recombination hotspots exhibit hypersensitivity to nucleases (6-10). Some loci (8,9) undergo meiosis-specific alterations in nuclease sensitivity prior to DSB formation, although no such changes are observed at other loci (6). Since all nuclease-hypersensitive regions are not meiotic Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.Conflicts of interest None. NIH Public AccessAuthor Manuscript DNA Repair (Amst) (6,10), "open" chromatin appears necessary, but not sufficient, for meiotic recombination hotspot activity. Second, insertion of a nucleosome-excluding sequence into the yeast genome creates a recombination hotspot (11). Third, the activity of some hotspots requires the binding of transcription factors, but not high levels of transcription (2). This result has been interpreted as indicating that chromatin modifications associated with transcription factor binding stimulate both transcription and recombination. Finally, some mutants that affect chromatin modifications reduce the frequency of meiosis-specific DSBs. In the yeast S. pombe, mutatio...

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Section: Discussionmentioning

confidence: 99%

Section: Measurement Of Meiosis-specific Dsbs At Thementioning

confidence: 99%

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The histone methylase Set2p and the histone deacetylase Rpd3p repress meiotic recombination at the HIS4 meiotic recombination hotspot in Saccharomyces cerevisiae

et al. 2008

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“…Studies in yeast have shown that methylation of H3-K36 by SET2 recruits histone deacetylase to transcribed regions and links to phosphorylation of the C-terminal domain of RNA polymerase II and the process of transcriptional elongation (Carrozza et al, 2005;Joshi and Struhl, 2005;Keogh et al, 2005). Of interest, Carrozza et al reported that the histone deacetylation occurs at coding regions and suppresses intragenic transcription.…”

Section: Functions Of Jumonji Family Proteins In Transcription and Chmentioning

confidence: 99%

Roles of jumonji and jumonji family genes in chromatin regulation and development

Takeuchi

Watanabe

Takano-Shimizu

et al. 2006

Developmental Dynamics

177

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The jumonji (jmj) gene was identified by a mouse gene trap approach and has essential roles in the development of multiple tissues. The Jmj protein has a DNA binding domain, ARID, and two conserved jmj domains (jmjN and jmjC). In many diverse species including bacteria, fungi, plants, and animals, there are many jumonji family proteins that have only the jmjC domain or both jmj domains. Recently, Jmj protein was found to be a transcriptional repressor. Several proteins in the jumonji family are involved in transcriptional repression and/or chromatin regulation. Most recently, one of the human members has been shown to be a histone demethylase, and the jmjC domain is essential for the demethylase activity. Meanwhile, more and more evidence indicating that the jumonji family proteins play important roles during development is accumulating. Many proteins in the jumonji family may regulate chromatin and gene expression, and control development through various signaling pathways. Here, we highlight the roles of jmj and jumonji family proteins in chromatin regulation and development. Developmental Dynamics 235: 2449 -2459, 2006.

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“…Several important predictions arising from this E-MAP for novel gene functions have recently been studied and confirmed (10)(11)(12)(13)(14)(15)(16)(17). One such prediction was a connection between SET2, a histone methyltransferase, and Rpd3C(S), a histone deacetylation complex that contains the chromodomain protein Eaf3p as well as Rco1p.…”

Section: Introductionmentioning

confidence: 79%

Quantitative genetic analysis in Saccharomyces cerevisiae using epistatic miniarray profiles (E-MAPs) and its application to chromatin functions

Schuldiner

Collins

Weissman

et al. 2006

Methods

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The use of the budding yeast Saccharomyces cerevisiae as a simple eukaryotic model system for the study of chromatin assembly and regulation has allowed rapid discovery of genes that influence this complex process. The functions of many of the proteins encoded by these geneshave not yet been fully characterized. Here, we describe a high-throughput methodology that can be used to illuminate gene function and discuss its application to a set of genes involved in the creation, maintenance and remodeling of chromatin structure. Our technique, termed EMAPs, involves the generation of quantitative genetic interaction maps that reveal the function and organization of cellular proteins and networks.

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Cotranscriptional Set2 Methylation of Histone H3 Lysine 36 Recruits a Repressive Rpd3 Complex

Cited by 741 publications

References 84 publications

The histone methylase Set2p and the histone deacetylase Rpd3p repress meiotic recombination at the HIS4 meiotic recombination hotspot in Saccharomyces cerevisiae

The histone methylase Set2p and the histone deacetylase Rpd3p repress meiotic recombination at the HIS4 meiotic recombination hotspot in Saccharomyces cerevisiae

Roles of jumonji and jumonji family genes in chromatin regulation and development

Quantitative genetic analysis in Saccharomyces cerevisiae using epistatic miniarray profiles (E-MAPs) and its application to chromatin functions

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