BUR Kinase Selectively Regulates H3 K4 Trimethylation and H2B Ubiquitylation through Recruitment of the PAF Elongation Complex

Laribee, R. Nicholas; Krogan, Nevan J.; Xiao, Tiaojiang; Shibata, Yoichiro; Hughes, Timothy R.; Greenblatt, Jack; Strahl, Brian D.

doi:10.1016/j.cub.2005.07.028

Cited by 152 publications

(182 citation statements)

References 37 publications

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“…2B). Thus, H2B-Lys-123 ubiquitination is dispensable for up-regulation of H3-Lys-4 dimethylation, but not trimethylation, at the coding sequences of the PHO84, ADH1, and PYK1 genes, consistent with a recent study demonstrating the role of H2B-Lys-123 ubiquitination in the regulation of H3-Lys-4 tri-but not dimethylation (48). Similarly, Henry et al (30) have also demonstrated that H3-Lys-4 trimethylation, but not dimethylation, at GAL1 is regulated by H2B-Lys-123 ubiquitination.…”

Section: H2b-lys-123 Ubiquitination Upregulates H3-lys-4 Tri-but Not supporting

confidence: 90%

“…Similarly, Henry et al (30) have also demonstrated that H2B-Lys-123 ubiquitination regulates only tri-but not dimethylation of H3-Lys-4 at GAL1. Furthermore, a recent biochemical study (48) has demonstrated the role of H2B-Lys-123 ubiquitination in the regulation of only H3-Lys-4 trimethylation. Taken together, H2B-Lys-123 ubiquitination is differentially required for regulation of H3-Lys-4 di-and trimethylation at the active genes, revealing a complex regulation of H3-Lys-4 methylation in vivo.…”

Section: Discussionmentioning

confidence: 99%

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Functional Analysis of H2B-Lys-123 Ubiquitination in Regulation of H3-Lys-4 Methylation and Recruitment of RNA Polymerase II at the Coding Sequences of Several Active Genes in Vivo

Shukla

Stanojevic

Duan

et al. 2006

Journal of Biological Chemistry

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Previous biochemical studies have demonstrated that Lys-123 ubiquitination of histone H2B is globally required for up-regulation of mono-, di, and trimethylation of Lys-4 of histone H3. However, recent studies have implicated H2B-Lys-123 ubiquitination in the regulation of di-and trimethylation, but not monomethylation, of H3-Lys-4 in vivo. Using a formaldehydebased cross-linking and chromatin immunoprecipitation assay, we show that H3-Lys-4 trimethylation, but not dimethylation, is up-regulated by H2B-Lys-123 ubiquitination in vivo at the coding sequences of a set of transcriptionally active genes such as ADH1, PHO84, and PYK1. Both the ubiquitination of H2B-Lys-123 and the methylation of H3-Lys-4 are dispensable for recruitment of RNA polymerase II to the coding sequences of these genes, and hence, their transcription is not altered in the absence of these covalent modifications. However, recruitment of RNA polymerase II to the coding sequence of a galactoseinducible gene, GAL1, is significantly reduced in the absence of H2B-Lys-123 ubiquitination but not H3-Lys-4 methylation. Consistently, transcription of GAL1 is altered in the H2B-K123R point mutant strain. Finally, we show that H3-Lys-4 methylation does not regulate H3-Lys-9/14 acetylation. Collectively, our data reveal a "trans-tail" regulation of H3-Lys-4 tribut not dimethylation by H2B-Lys-123 ubiquitination, and these modifications are dispensable for transcription of a certain set of genes in vivo.The eukaryotic genome is packaged into chromatin that is an array of nucleosomes; in each nucleosomes, 146 bp of DNA is wrapped around an octamer of core histone proteins, H2A, H2B, H3, and H4 (1). Chromatin is a dynamic structure that modulates the access of regulatory factors to the genetic material. Thus, transcription and other cellular processes that require access to DNA are regulated by chromatin structure, and therefore, a precise coordination and organization of events in opening and closing the chromatin is crucial for these cellular processes to happen normally.Post-translational modifications (e.g. acetylation, phosphorylation, ubiquitination, and methylation) of the histones affect chromatin structure directly by altering DNA-histone interactions within and between nucleosomes, thus changing higher order chromatin structure (2). Histone modifications are, therefore, the key determinants in defining the active and repressed states of the chromatin (3-8). For example, methylation of H3-Lys-4 is correlated with gene activation, whereas H3-Lys-9 methylation results in repression and heterochromatin formation. Furthermore, histone acetylation is generally correlated with gene activation, although there are exceptions to this rule.Histone methylation on specific Lys or Arg residues is carried out by CARM1, PRMT1, and SET domain-containing enzymes (9, 10). The CARM1 and PRMT1 mediate Arg methylation, whereas Lys is methylated by the SET domain-containing enzymes (9, 10). In Saccharomyces cerevisiae, Arg methylation of histones has not been demonstrated...

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Section: H2b-lys-123 Ubiquitination Upregulates H3-lys-4 Tri-but Not supporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Functional Analysis of H2B-Lys-123 Ubiquitination in Regulation of H3-Lys-4 Methylation and Recruitment of RNA Polymerase II at the Coding Sequences of Several Active Genes in Vivo

Shukla

Stanojevic

Duan

et al. 2006

Journal of Biological Chemistry

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“…We now know that monoubiquitination of H2B is required for H3K4 di-and trimethylation in yeast and that this crosstalk pathway is highly conserved from yeast to human [6,40,41]. Although the past several years brought about a watershed of information regarding the factors/proteins required for proper H2B monoubiquitination [6,[40][41][42][43][44][45][46][47][48], the molecular mechanism for this histone crosstalk was poorly understood. Recent studies in yeast S. cerevisiae demonstrated that monoubiquitination of histone H2B regulates COMPASS' compositional assembly, and therefore, proper H3K4 methylation [49].…”

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confidence: 99%

Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation

Shilatifard

2008

Current Opinion in Cell Biology

437

408

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Chromosomal surfaces are ornamented with a variety of posttranslational modifications of histones, which are required for the regulation of many of the DNA-templated processes. Such histone modifications include acetylation, sumoylation, phosphorylation, ubiquitination and methylation. Histone modifications can either function by disrupting chromosomal contacts or by regulating nonhistone protein interactions with chromatin. In this review, recent findings will be discussed regarding the regulation of the implementation and physiological significance for one such histone modification, histone H3 Lysine 4 (H3K4) methylation by the yeast COMPASS and mammalian COMPASS-like complexes.All DNA-templated processes are regulated by chromatin and its posttranslational modifications. The nucleosome, which is the fundamental unit of chromatin, is composed of 146 base pairs of DNA wrapped twice around an octamer of the four core histones (H3, H4, H2A, and H2B) [1][2][3]. Structural studies demonstrated that the unstructured histone N-terminal tails protrude outward from the nucleosomes and are available for interactions with other neighboring histones or non-histone proteins. Many residues within the histone N-terminal tails and a few within the histone core can be altered by posttranslational modifications [1]. To date, there are at least five types of posttranslational modifications found on histones, these include: acetylation, phosphorylation, ubiquitination, sumoylation, and methylation [4,5]. Almost all of these modifications have been shown to be reversible, and their implementation and removal are fundamental to the regulation of a diverse set of biological processes such as replication, repair, recombination, transcription and RNA processing [4,5]. This review will focus mainly on the most recent studies of one type of histone modification, histone H3 lysine 4 (H3K4) methylation. Histone lysine methylationHistones are methylated either on their arginine and/or lysine residues [6,7]. The lysine residues are methylated on the ε-nitrogen by either the SET domain or the non-SET domain-containing lysine methyltransferases (KMTs). A large number of enzymes have been characterized which are capable of methylating specific lysine residues on histones ( Table 1). The ε-nitrogen can also be modified by lysine acetyl transferases (KATs) and methylation and acetylation of lysine are mutually exclusive. Indeed, many sites of histone methylation are also sites of acetylation.Correspondence and proofs should be sent to the following address: Ali Shilatifard, Stowers Institute for Medical Research, 1000 East 50th Street, Kansas City, MO 64110, Office (816) 926-4465, Email: ASH@Stowers-Institute.org. 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 for...

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“…The first breakthrough came with the identification of the budding yeast protein Bre1 [38,39], which, together with the ubiquitin-conjugating enzyme Rad6, serves as the E3 ligase in the monoubiquitylation of the yeast histone H2B on lysine 123 (K123) within transcribed chromatin [38][39][40][41]. Notably, H2B monoubiquitylation was subsequently found to be required for di-and trimethylation of lysine 4 and lysine 79 of histone H3 at transcribed chromatin [42][43][44][45][46][47][48]. This pathway is conserved from yeast to mammals, and is dependent on a host of additional proteins that converge at the elongating RNA Pol II [41,[49][50][51][52][53][54].…”

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confidence: 99%

RNF20–RNF40: A ubiquitin‐driven link between gene expression and the DNA damage response

et al. 2011

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a b s t r a c tThe DNA damage response (DDR) is emerging as a vast signaling network that temporarily modulates numerous aspects of cellular metabolism in the face of DNA lesions, especially critical ones such as the double strand break (DSB). The DDR involves extensive dynamics of protein post-translational modifications, most notably phosphorylation and ubiquitylation. The DSB response is mobilized primarily by the ATM protein kinase, which phosphorylates a plethora of key players in its various branches. It is based on a core of proteins dedicated to the damage response, and a cadre of proteins borrowed temporarily from other cellular processes to help meet the challenge. A recently identified novel component of the DDR pathway -histone H2B monoubiquitylationexemplifies this principle. In mammalian cells, H2B monoubiquitylation is driven primarily by an E3 ubiquitin ligase composed of the two RING finger proteins RNF20 and RNF40. Generation of monoubiquitylated histone H2B (H2Bub) has been known to be coupled to gene transcription, presumably modulating chromatin decondensation at transcribed regions. New evidence indicates that the regulatory function of H2Bub on gene expression can selectively enhance or suppress the expression of distinct subsets of genes through a mechanism involving the hPAF1 complex and the TFIIS protein. This delicate regulatory process specifically affects genes that control cell growth and genome stability, and places RNF20 and RNF40 in the realm of tumor suppressor proteins. In parallel, it was found that following DSB induction, the H2B monoubiquitylation module is recruited to damage sites where it induces local H2Bub, which in turn is required for timely recruitment of DSB repair protein and, subsequently, timely DSB repair. This pathway represents a crossroads of the DDR and chromatin organization, and is a typical example of how the DDR calls to action functional modules that in unprovoked cells regulate other processes. Ó 2011 Federation of European Biochemical Societies. Published by Elsevier B.V. The DNA damage response: borrowing functional modules in an emergencyCellular metabolism is controlled by numerous, interlocked signaling networks. These networks are constantly responding to internal and external stimuli related to the cell's normal life cycle and functions, and to threats to its well being. A major threat to cellular homeostasis is subversion of its genomic stability, which may lead to undue cell death or to neoplasia [1,2]. DNA damage caused by internal or external damaging agents is a major danger to the integrity of the cellular genome. The cellular defense system against this threat is the DNA damage response (DDR) -an elaborate signaling network activated by DNA damage, which swiftly modulates many physiological processes [3,4]. A strong trigger of the DDR is the DNA double-strand break (DSB) [5,6]. DSBs are induced by ionizing radiation, radiomimetic chemicals, reactive oxygen species formed in the course of normal metabolism, and can also result from replic...

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BUR Kinase Selectively Regulates H3 K4 Trimethylation and H2B Ubiquitylation through Recruitment of the PAF Elongation Complex

Cited by 152 publications

References 37 publications

Functional Analysis of H2B-Lys-123 Ubiquitination in Regulation of H3-Lys-4 Methylation and Recruitment of RNA Polymerase II at the Coding Sequences of Several Active Genes in Vivo

Functional Analysis of H2B-Lys-123 Ubiquitination in Regulation of H3-Lys-4 Methylation and Recruitment of RNA Polymerase II at the Coding Sequences of Several Active Genes in Vivo

Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation

RNF20–RNF40: A ubiquitin‐driven link between gene expression and the DNA damage response

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