Diverse Roles and Interactions of the SWI/SNF Chromatin Remodeling Complex Revealed Using Global Approaches

Euskirchen, Ghia; Auerbach, Raymond K.; Davidov, Eugene; Gianoulis, Tara A.; Zhong, Guoneng; Rozowsky, Joel; Bhardwaj, Nitin; Gerstein, Mark; Snyder, M

doi:10.1371/journal.pgen.1002008

Cited by 201 publications

(222 citation statements)

References 89 publications

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“…At the same time, these comparative studies have shed light on several other pathways, such as the regulation of pathogenic defense responses, which are also influenced by the loss of SWP73B function and thus deserve attention in future examinations. We also noted that the ChIP-Seq data show that localization of SWP73B is not confined to promoters but shows a wider distribution in gene bodies and 39-UTRs, as reported previously for human SWI/SNF complexes (Euskirchen et al, 2011). It thus remains a challenge to determine how the swp73b mutation influences overall localization of SWI/SNF complexes in different regions of gene targets at the genome-wide level.…”

Section: Discussionsupporting

confidence: 76%

SWP73 Subunits of Arabidopsis SWI/SNF Chromatin Remodeling Complexes Play Distinct Roles in Leaf and Flower Development

et al. 2015

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(T.J.S.)Arabidopsis thaliana SWP73A and SWP73B are homologs of mammalian BRAHMA-associated factors (BAF60s) that tether SWITCH/SUCROSE NONFERMENTING chromatin remodeling complexes to transcription factors of genes regulating various cell differentiation pathways. Here, we show that Arabidopsis thaliana SWP73s modulate several important developmental pathways. While undergoing normal vegetative development, swp73a mutants display reduced expression of FLOWERING LOCUS C and early flowering in short days. By contrast, swp73b mutants are characterized by retarded growth, severe defects in leaf and flower development, delayed flowering, and male sterility. MNase-Seq, transcript profiling, and ChIP-Seq studies demonstrate that SWP73B binds the promoters of ASYMMETRIC LEAVES1 and 2, KANADI1 and 3, and YABBY2, 3, and 5 genes, which regulate leaf development and show coordinately altered transcription in swp73b plants. Lack of SWP73B alters the expression patterns of APETALA1, APETALA3, and the MADS box gene AGL24, whereas other floral organ identity genes show reduced expression correlating with defects in flower development. Consistently, SWP73B binds to the promoter regions of APETALA1 and 3, SEPALLATA3, LEAFY, UNUSUAL FLORAL ORGANS, TERMINAL FLOWER1, AGAMOUS-LIKE24, and SUPPRESSOR OF CONSTANS OVEREXPRESSION1 genes, and the swp73b mutation alters nucleosome occupancy on most of these loci. In conclusion, SWP73B acts as important modulator of major developmental pathways, while SWP73A functions in flowering time control.

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Section: Discussionsupporting

confidence: 76%

SWP73 Subunits of Arabidopsis SWI/SNF Chromatin Remodeling Complexes Play Distinct Roles in Leaf and Flower Development

et al. 2015

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“…Given the roles of DNA and chromatin modification networks in transcriptional regulation, future studies that identify the DNA target sites of these proteins in mESCs and mEpiSCs should be highly informative. Genome binding sites of core SWI/SNF components and their protein-protein interactions, have revealed a complex picture of diverse activities and both repression and activation of gene-expression by SWI/SNF complexes (50). The potentially different and significant patterns of DNA-binding of SWI/SNF components in mESCs and mEpiSCs and their significance remain to be discovered.…”

Section: Discussionmentioning

confidence: 99%

DNA and Chromatin Modification Networks Distinguish Stem Cell Pluripotent Ground States

Song¹,

Saha²,

Gokulrangan³

et al. 2012

Molecular & Cellular Proteomics

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Pluripotent stem cells are capable of differentiating into all cell types of the body and therefore hold tremendous promise for regenerative medicine. Despite their widespread use in laboratories across the world, a detailed understanding of the molecular mechanisms that regulate the pluripotent state is currently lacking. Mouse embryonic (mESC) and epiblast (mEpiSC) stem cells are two closely related classes of pluripotent stem cells, derived from distinct embryonic tissues. Although both mESC and mEpiSC are pluripotent, these cell types show important differences in their properties suggesting distinct pluripotent ground states. To understand the molecular basis of pluripotency, we analyzed the nuclear proteomes of mESCs and mEpiSCs to identify protein networks that regulate their respective pluripotent states. Our study used label-free LC-MS/MS to identify and quantify 1597 proteins in embryonic and epiblast stem cell nuclei. Immunoblotting of a selected protein subset was used to confirm that key components of chromatin regulatory networks are differentially expressed in mESCs and mEpiSCs. Specifically, we identify differential expression of DNA methylation, ATP-dependent chromatin remodeling and nucleosome remodeling networks in mESC and mEpiSC nuclei. This study is the first comparative study of protein networks in cells representing the two distinct, pluripotent states, and points to the importance of DNA and chromatin modification processes in regulating pluripotency. In addition, by integrating our data with existing pluripotency networks, we provide detailed maps of protein networks that regulate pluripotency that will further both the fundamental understanding of pluripotency as well as efforts to reliably control the differentiation of these cells into functional cell fates. Molecular & Cellular Proteomics

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“…As shown in Fig. 3A, 26 of these proteins form a highly interconnected network representing diverse chromatin-related protein functions, including the chromatin remodeling factors BPTF and RSF1, and several core components of the SWI/SNF complex (ARID1A, SMARCA4, SMARCC1, and SMARCC2)-a chromatin remodeling complex that preferentially associates with regulatory elements connected to transcription and chromosome organization (27). In addition, chromatin modification enzymes involved in deacetylation (HDAC2) and methylation (DNMT1, KDM1A, and PRMT5) were also integrated into this network.…”

Section: Functional Network Analysis Predicts a Prominent Role For Chmentioning

confidence: 99%

Functional Proteomics Establishes the Interaction of SIRT7 with Chromatin Remodeling Complexes and Expands Its Role in Regulation of RNA Polymerase I Transcription

Tsai¹,

Greco²,

Boonmee

et al. 2012

Molecular & Cellular Proteomics

121

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Among mammalian sirtuins, SIRT7 is the only enzyme residing in nucleoli where ribosomal DNA is transcribed. Recent reports established that SIRT7 associates with RNA Pol I machinery and is required for rDNA transcription. Although defined by its homology to the yeast histone deacetylase Sir2, current knowledge suggests that SIRT7 itself has little to no deacetylase activity. Because only two SIRT7 interactions have been thus far described: RNA Pol I and upstream binding factor, identification of proteins and complexes associating with SIRT7 is critical to understanding its functions. Here, we present the first characterization of SIRT7 interaction networks. We have systematically investigated protein interactions of three EGFP-tagged SIRT7 constructs: wild type, a point mutation affecting rDNA transcription, and a deletion mutant lacking the predicted coiled-coil domain. A combinatorial proteomics and bioinformatics approach was used to integrate gene ontology classifications, functional protein networks, and normalized abundances of proteins coisolated with SIRT7. The resulting refined proteomic data set confirmed SIRT7 interactions with RNA Pol I and upstream binding factor and highlighted association with factors involved in RNA Pol I-and II-dependent transcriptional processes and several nucleolus-localized chromatin remodeling complexes. Particularly enriched were members of the B-WICH complex, such as Mybbp1a, WSTF, and SNF2h. Prominent interactions were validated by a selected reaction monitoring-like approach using metabolic labeling with stable isotopes, confocal microscopy, reciprocal immunoaffinity precipitation, and co-isolation with endogenous SIRT7. To extend the current knowledge of mechanisms involved in SIRT7-dependent regulation of rDNA transcription, we showed that small interfering RNA-mediated SIRT7 knockdown leads to reduced levels of RNA Pol I protein, but not messenger RNA, which was confirmed in diverse cell types. The correlation between histone acetylation status and transcriptional regulation is well established in that hyperacetylation is commonly associated with transcriptional activation, whereas hypoacetylation is associated with transcriptional repression (1-3). In eukaryotes, Sir2-like proteins form a family of enzymes known as sirtuins (4). Distinct from class I and II histone deacetylases (HDACs), which facilitate hydrolysis of acetyl-lysine as a bimolecular reaction (5), sirtuins consume an equimolar amount of nicotinamide adenine dinucleotide (NAD ϩ ) for each hydrolysis reaction and generate nicotinamide, O-acetyl ADP-ribose, and deacetylated substrate as end products (4). Based on homology of the sirtuin core domain, there are seven sirtuins (SIRT1-7) in human cells with functions not limited to histone deacetylation, because many additional cellular proteins have been identified as substrates (4, 6). In addition, the localizations of human sirtuins are distributed across multiple organelles including nucleolus, nucleus, cytoplasm, and mitochondria (7).Systematic monitorin...

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Diverse Roles and Interactions of the SWI/SNF Chromatin Remodeling Complex Revealed Using Global Approaches

Cited by 201 publications

References 89 publications

SWP73 Subunits of Arabidopsis SWI/SNF Chromatin Remodeling Complexes Play Distinct Roles in Leaf and Flower Development

SWP73 Subunits of Arabidopsis SWI/SNF Chromatin Remodeling Complexes Play Distinct Roles in Leaf and Flower Development

DNA and Chromatin Modification Networks Distinguish Stem Cell Pluripotent Ground States

Functional Proteomics Establishes the Interaction of SIRT7 with Chromatin Remodeling Complexes and Expands Its Role in Regulation of RNA Polymerase I Transcription

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