Key points are not available for this paper at this time.
The composition of chromatin-remodeling complexes dictates how these enzymes control transcriptional programs and cellular identity. In the present study we investigated the composition of SWI/SNF complexes in embryonic stem cells (ESCs). In contrast to differentiated cells, ESCs have a biased incorporation of certain paralogous SWI/SNF subunits with low levels of BRM, BAF170, and ARID1B. Upon differentiation, the expression of these subunits increases, resulting in a higher diversity of compositionally distinct SWI/SNF enzymes. We also identified BRD7 as a novel component of the Polybromo-associated BRG1-associated factor (PBAF) complex in both ESCs and differentiated cells. Using short hairpin RNA-mediated depletion of BRG1, we showed that SWI/SNF can function as both a repressor and an activator in pluripotent cells, regulating expression of developmental modifiers and signaling components such as Nodal, ADAMTS1, BMI-1, CRABP1, and thyroid releasing hormone. Knockdown studies of PBAF-specific BRD7 and of a signature subunit within the BAF complex, ARID1A, showed that these two subcomplexes affect SWI/SNF target genes differentially, in some cases even antagonistically. This may be due to their different biochemical properties. Finally we examined the role of SWI/SNF in regulating its target genes during differentiation. We found that SWI/SNF affects recruitment of components of the preinitiation complex in a promoter-specific manner to modulate transcription positively or negatively. Taken together, our results provide insight into the function of compositionally diverse SWI/SNF enzymes that underlie their inherent gene-specific mode of action. The composition of chromatin-remodeling complexes dictates how these enzymes control transcriptional programs and cellular identity. In the present study we investigated the composition of SWI/SNF complexes in embryonic stem cells (ESCs). In contrast to differentiated cells, ESCs have a biased incorporation of certain paralogous SWI/SNF subunits with low levels of BRM, BAF170, and ARID1B. Upon differentiation, the expression of these subunits increases, resulting in a higher diversity of compositionally distinct SWI/SNF enzymes. We also identified BRD7 as a novel component of the Polybromo-associated BRG1-associated factor (PBAF) complex in both ESCs and differentiated cells. Using short hairpin RNA-mediated depletion of BRG1, we showed that SWI/SNF can function as both a repressor and an activator in pluripotent cells, regulating expression of developmental modifiers and signaling components such as Nodal, ADAMTS1, BMI-1, CRABP1, and thyroid releasing hormone. Knockdown studies of PBAF-specific BRD7 and of a signature subunit within the BAF complex, ARID1A, showed that these two subcomplexes affect SWI/SNF target genes differentially, in some cases even antagonistically. This may be due to their different biochemical properties. Finally we examined the role of SWI/SNF in regulating its target genes during differentiation. We found that SWI/SNF affects recruitment of components of the preinitiation complex in a promoter-specific manner to modulate transcription positively or negatively. Taken together, our results provide insight into the function of compositionally diverse SWI/SNF enzymes that underlie their inherent gene-specific mode of action. Chromatin plays a key role in the regulation of tissue-specific gene expression during development and differentiation (1Muller C. Leutz A. Curr. Opin. Genet. Dev. 2001; 11: 167-174Crossref PubMed Scopus (108) Google Scholar). Embryonic stem cells (ESCs) 2The abbreviations used are: ESC, embryonic stem cell; RA, retinoic acid; BAF, BRG1-associated factor; PBAF, Polybromo-associated BAF; MudPIT, multidimensional protein identification technique; shRNA, short hairpin RNA; RNAi, RNA interference; ES, embryonic stem; HA, hemagglutinin; ChIP, chromatin immunoprecipitation; TF, transcription factor; POLII, RNA polymerase II; IP, immunoprecipitation; MS, mass spectrometry; BCL7, B-cell leukemia protein 7; BRD7, bromodomain-containing protein 7; TRH, thyroid releasing hormone; PIC, preinitiation complex. possess a distinctive global chromatin structure that is characterized by hyperdynamic architectural proteins (2Meshorer E. Yellajoshula D. George E. Scambler P.J. Brown D.T. Misteli T. Dev. Cell. 2006; 10: 105-116Abstract Full Text Full Text PDF PubMed Scopus (820) Google Scholar) and bivalent domains (3Bernstein B.E. Mikkelsen T.S. Xie X. Kamal M. Huebert D.J. Cuff J. Fry B. Meissner A. Wernig M. Plath K. Jaenisch R. Wagschal A. Feil R. Schreiber S.L. Lander E.S. Cell. 2006; 125: 315-326Abstract Full Text Full Text PDF PubMed Scopus (4106) Google Scholar), ultimately resulting in elevated global transcription compared with differentiated cells (4Efroni S. Duttagupta R. Cheng J. Dehghani H. Hoeppner D.J. Dash C. Bazett-Jones D.P. Le Grice S. McKay R.D. Buetow K.H. Gingeras T.R. Misteli T. Meshorer E. Cell Stem Cell. 2008; 2: 437-447Abstract Full Text Full Text PDF PubMed Scopus (508) Google Scholar). This chromatin structure is dictated by stem cell-specific transcription factors, chromatin architecture, and epigenetic regulation (5Niwa H. Development. 2007; 134: 635-646Crossref PubMed Scopus (663) Google Scholar) and is a prerequisite for self-renewal and the capacity to differentiate into the three germ layers (6Meshorer E. Misteli T. Nat. Rev. Mol. Cell Biol. 2006; 7: 540-546Crossref PubMed Scopus (558) Google Scholar). Important determinants of this unique genomic plasticity are ATP-dependent chromatin-remodeling complexes. These multisubunit enzymes catalyze non-covalent eviction, restructuring or repositioning of nucleosomes to modulate the accessibility of transcription factors and other regulatory proteins to chromosomal DNA (7Becker P.B. Horz W. Annu. Rev. Biochem. 2002; 71: 247-273Crossref PubMed Scopus (625) Google Scholar). Multiple distinct families of chromatin-remodeling complexes exist, some of which have been implicated in developmental processes (8de la Serna I.L. Ohkawa Y. Imbalzano A.N. Nat. Rev. Genet. 2006; 7: 461-473Crossref PubMed Scopus (313) Google Scholar, 9Kaeser M.D. Emerson B.M. Curr. Opin. Genet. Dev. 2006; 16: 508-512Crossref PubMed Scopus (13) Google Scholar). For example, genomic disruption of specific chromatin-remodeling components results in early embryonic lethality (10Stopka T. Skoultchi A.I. Proc. Natl. Acad. Sci. U. S. A. 2003; 100: 14097-14102Crossref PubMed Scopus (164) Google Scholar, 11Bultman S. Gebuhr T. Yee D. La Mantia C. Nicholson J. Gilliam A. Randazzo F. Metzger D. Chambon P. Crabtree G. Magnuson T. Mol. Cell. 2000; 6: 1287-1295Abstract Full Text Full Text PDF PubMed Scopus (683) Google Scholar, 12Klochendler-Yeivin A. Fiette L. Barra J. Muchardt C. Babinet C. Yaniv M. EMBO Rep. 2000; 1: 500-506Crossref PubMed Scopus (339) Google Scholar, 13Kim J.K. Huh S.O. Choi H. Lee K.S. Shin D. Lee C. Nam J.S. Kim H. Chung H. Lee H.W. Park S.D. Seong R.H. Mol. Cell. Biol. 2001; 21: 7787-7795Crossref PubMed Scopus (170) Google Scholar, 14Gao X. Tate P. Hu P. Tjian R. Skarnes W.C. Wang Z. Proc. Natl. Acad. Sci. U. S. A. 2008; 105: 6656-6661Crossref PubMed Scopus (270) Google Scholar). Other remodeling modules are required to maintain the balance between ESC self-renewal and differentiation (15Fazzio T.G. Huff J.T. Panning B. 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Proc. Natl. Acad. Sci. U. S. A. 2002; PubMed Scopus Google Scholar) with by with the cells in of and complexes in of and to cells with of or or of of protein two in two in and two in complexes for DNA of and of RNA and RNA transcription with of and polymerase a The are in of SWI/SNF in we investigated which of the SWI/SNF multisubunit complex in We used a in which subunits are into the ESC is in a resulting in multisubunit protein of and S. Dev. PubMed Scopus Google Scholar). We several characterized subunits to our to of the compositionally distinct of SWI/SNF that may be present in BAF170, and are subunits that with both BAF and complexes SWI/SNF of we the and the ESC by with and to pluripotent cells and differentiate factor or We also compared gene expression in and cells in to and found to be with a in cells. the of into with to that G. J. J. G. B. J. J. Mol. Cell. 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Using mass the and in expression of the subunits we the SWI/SNF subunits ARID1A, BRG1, BAF170, and with the The of SWI/SNF the and and examined by subunits into complexes by unique with other BAF We that the for the in with the of the the showed a between the other examined This is with the that the of complexes and and in that is in ESCs and that the expression its its expression and incorporation in SWI/SNF complexes in the of or both of its levels are in complexes of the of BAF170, we this by Specific of the by unique of SWI/SNF components in the ESC and The control a of two different subunits certain of paralogous subunits and in we in our that be to specific and are subunits W. J. Y. S. Muchardt C. Yaniv M. Crabtree EMBO J. PubMed Scopus Google Scholar), the unique in our the identification of or We of the paralogous subunits within their as in our of SWI/SNF cells. we found that in ESCs specific paralogous subunits In the of our results that the protein in in ESCs in with its low expression during early development S. E. Dev. 2001; PubMed Scopus Google Scholar). This is also the for the of which we Wang W. Y. A. Crabtree Dev. 2002; 16: PubMed Scopus Google Scholar). in contrast to cells, and in ESCs their and ARID1A, that these subunits are BAF enzymes to with transcriptional as to complexes with that with transcriptional Wang X. A. M. E. EMBO J. 2007; 26: PubMed Scopus Google Scholar), that in ESCs SWI/SNF be compositionally for a in in a of SWI/SNF we a biased of paralogous SWI/SNF subunits in pluripotent cells, we examined the in SWI/SNF composition during ESC differentiation. We used for and to differentiate pluripotent stem cells into SWI/SNF complexes cells a of as S. Dev. 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We in subunit transcription the in SWI/SNF composition by their RNA expression levels We in expression of and in and This our of protein levels and the of these We also a in the in by of differentiation. an by the in both and unique in mass we this by we that these The we by different by for are in of in a B-cell SWI/SNF of complexes ESCs and cells identified unique a protein family and protein that as SWI/SNF subunits These are found in SWI/SNF of the subunit used for The family by the proteins is of function for its in chromosomal in D. J. E. K. D. PubMed Google Scholar). We also found BRD7, which to with A. J. Cell. 2000; PubMed Scopus Google Scholar) and C. J. M. Wang W. J. Cell. Biochem. 2006; PubMed Scopus Google Scholar). by the proteins been characterized by Crabtree and J. M. H. R. 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We complexes the biochemical as the of SWI/SNF complexes both BAF and this we both and complexes in an of the subunit BRG1, the present in ESCs the of SWI/SNF a that by the of DNA and complexes a higher that to the of This by the of This that compositionally distinct subcomplexes have different which may specialized to BAF and and their to target SWI/SNF as an or a the transcriptional of SWI/SNF in pluripotent ESCs and its target we a depletion to a ESCs in with targeting or a and RNA of in a of genes of which by the and expression of genes This that SWI/SNF can both as an activator and a repressor in pluripotent cells the gene of target we found that in the as between BAF and we regulation of these genes BAF, PBAF, or both this we cells with targeting the BAF signature subunit ARID1A, the PBAF-specific subunit BRD7, or the present in the protein of their target with a in target RNA to and we a of identified target genes with the The expression of of these genes by targeting BRG1, that SWI/SNF their conserved gene with retinoic protein releasing and protein genes by with BRG1, that SWI/SNF their These genes protein and with SWI/SNF target genes that BAF complexes are required for targeting BRD7 a different and in the of the PBAF-specific subunit BRD7, the expression of Nodal, and of transcription of two and by the of BRD7 in an manner compared with that of we of the complex with the genomic of target genes in ESCs the transcriptional of target Nodal, and as by the in DNA by the compared with a control ESCs with a control or with or BRD7, we an of target the of both Taken together, these results that BAF and subcomplexes can the expression of specific target genes of their different biochemical properties. SWI/SNF differentiation affects regulation of target we the chromatin of two target genes differentiation We and of the and of in their levels differentiation and is a that in the resulting in the of thyroid expression is to be by several signaling protein and and of transcription M. C. A. C. J.K. J.S. A.N. J. 2001; PubMed Scopus Google Scholar), factor Y. T. M. K. S. T. M. PubMed Scopus Google Scholar), and thyroid hormone. is an in development to be by K. H. Lee C. W. Dev. 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Wang Z. Sharova L. Sharov A.A. Ling C. Piao Y. Aiba K. Matoba R. Wang W. Ko M.S. Stem Cells (Dayton). 2008; 26: 1155-1165Crossref PubMed Scopus (139) Google Scholar). expression is with the of S. E. Dev. 2001; PubMed Scopus Google Scholar). The and for incorporation into the remodeling complex, and both can SWI/SNF to their specific target genes selective with transcription factors S. Emerson B.M. Mol. Cell. 2003; 11: Full Text Full Text PDF PubMed Scopus Google Scholar). a of in the of expression is to target genes by the of SWI/SNF complexes. This may provide a for the of and expression in ESCs is to a of target genes several that are by SWI/SNF in ESCs incorporation of two signature subunits of the BAF complex, and to confer of SWI/SNF regulatory genes Wang X. A. M. E. EMBO J. 2007; 26: PubMed Scopus Google Scholar). that in ESCs SWI/SNF a which with higher incorporation of the Upon differentiation, the in and in that compositionally SWI/SNF is into a Other studies have an in Z. Wang Z. Sharova L. Sharov A.A. Ling C. Piao Y. Aiba K. Matoba R. Wang W. Ko M.S. Stem Cells (Dayton). 2008; 26: 1155-1165Crossref PubMed Scopus (139) Google Scholar) differentiation. Wang and Z. Wang Z. Sharova L. Sharov A.A. Ling C. Piao Y. Aiba K. Matoba R. Wang W. Ko M.S. Stem Cells (Dayton). 2008; 26: 1155-1165Crossref PubMed Scopus (139) Google Scholar) protein our of into SWI/SNF complexes by mass and transcriptional of we found that the diversity of and subunits differentiation, the to transcriptional our is the identification of BRD7 as a PBAF-specific We found BRD7 present in pluripotent differentiated and cells, for its incorporation in a of mass we found of the protein that the signature of BRD7, and We to the of in complexes of the of that the BRD7 a that with C. J. M. Wang W. J. Cell. 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Taken together, these studies that chromatin remodeling can function to transcriptional This diversity is to be dictated by the chromatin of target genes and the specific can as a recruitment for chromatin-remodeling we that is a factor in selective SWI/SNF recruitment and function the a the of SWI/SNF and also to transcription this be to the of selective BAF and complex recruitment and how to the in a several components of SWI/SNF have been to be for of the mass S. Gebuhr T. Yee D. La Mantia C. Nicholson J. Gilliam A. Randazzo F. Metzger D. Chambon P. Crabtree G. Magnuson T. Mol. Cell. 2000; 6: 1287-1295Abstract Full Text Full Text PDF PubMed Scopus (683) Google Scholar, 12Klochendler-Yeivin A. Fiette L. Barra J. Muchardt C. Babinet C. Yaniv M. EMBO Rep. 2000; 1: 500-506Crossref PubMed Scopus (339) Google Scholar, 13Kim J.K. Huh S.O. Choi H. Lee K.S. Shin D. Lee C. Nam J.S. Kim H. Chung H. Lee H.W. Park S.D. Seong R.H. Mol. Cell. Biol. 2001; 21: 7787-7795Crossref PubMed Scopus (170) Google Scholar, 14Gao X. Tate P. Hu P. Tjian R. Skarnes W.C. Wang Z. Proc. Natl. Acad. Sci. U. S. A. 2008; 105: 6656-6661Crossref PubMed Scopus (270) Google Scholar). are depletion that is required for ESC (4Efroni S. Duttagupta R. Cheng J. Dehghani H. Hoeppner D.J. Dash C. Bazett-Jones D.P. Le Grice S. McKay R.D. Buetow K.H. Gingeras T.R. Misteli T. Meshorer E. Cell Stem Cell. 2008; 2: 437-447Abstract Full Text Full Text PDF PubMed Scopus (508) Google Scholar) in to transcriptional In this SWI/SNF been to and the DNA (8de la Serna I.L. Ohkawa Y. Imbalzano A.N. Nat. Rev. Genet. 2006; 7: 461-473Crossref PubMed Scopus (313) Google Scholar, C. J. Cell. 2006; PubMed Scopus Google Scholar, A. E. Yaniv M. Mol. Cell. Biol. 2006; 26: PubMed Scopus Google Scholar). into the for SWI/SNF in these and other processes a of its to We Wang and for the of Imbalzano for and for expression for and for and of the Emerson for and with
Kaeser et al. (Tue,) studied this question.