The PPARγ locus makes long-range chromatin interactions with selected tissue-specific gene loci during adipocyte differentiation in a protein kinase A dependent manner
Differentiation signaling results in reprogramming of cellular gene expression that leads to morphological changes and functional specialization of a precursor cell. This global change in gene expression involves temporal regulation of differentiation-specific genes that are located throughout the g...
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| Veröffentlicht in: | PloS one 2014, Vol.9 (1), p.e86140-e86140 |
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| creator | LeBlanc, Scott E Wu, Qiong Barutcu, A Rasim Xiao, Hengyi Ohkawa, Yasuyuki Imbalzano, Anthony N |
| description | Differentiation signaling results in reprogramming of cellular gene expression that leads to morphological changes and functional specialization of a precursor cell. This global change in gene expression involves temporal regulation of differentiation-specific genes that are located throughout the genome, raising the idea that genome structure may also be re-organized during cell differentiation to facilitate regulated gene expression. Using in vitro adipocyte differentiation as a model, we explored whether gene organization within the nucleus is altered upon exposure of precursor cells to signaling molecules that induce adipogenesis. The peroxisome proliferator-activated receptor gamma (PPARγ) nuclear hormone receptor is a master determinant of adipogenesis and is required for adipose differentiation. We utilized the chromosome conformation capture (3C) assay to determine whether the position of the PPARγ locus relative to other adipogenic genes is changed during differentiation. We report that the PPARγ2 promoter is transiently positioned in proximity to the promoters of genes encoding adipokines and lipid droplet associated proteins at 6 hours post-differentiation, a time that precedes expression of any of these genes. In contrast, the PPARγ2 promoter was not in proximity to the EF1α promoter, which drives expression of a constitutively active, housekeeping gene that encodes a translation elongation factor, nor was the PPARγ2 promoter in proximity to the promoter driving the expression of the C/EBPα regulatory protein. The formation of the long-range, intergenic interactions involving the PPARγ2 promoter required the regulatory factor C/EBPβ, elevated cyclic AMP (cAMP) levels, and protein kinase A (PKA) signaling. We conclude that genome organization is dynamically remodeled in response to adipogenic signaling, and we speculate that these transient inter-genic interactions may be formed for the purposes of selecting some of the transcriptionally silent tissue-specific loci for subsequent transcriptional activation. |
| doi_str_mv | 10.1371/journal.pone.0086140 |
| format | Article |
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This global change in gene expression involves temporal regulation of differentiation-specific genes that are located throughout the genome, raising the idea that genome structure may also be re-organized during cell differentiation to facilitate regulated gene expression. Using in vitro adipocyte differentiation as a model, we explored whether gene organization within the nucleus is altered upon exposure of precursor cells to signaling molecules that induce adipogenesis. The peroxisome proliferator-activated receptor gamma (PPARγ) nuclear hormone receptor is a master determinant of adipogenesis and is required for adipose differentiation. We utilized the chromosome conformation capture (3C) assay to determine whether the position of the PPARγ locus relative to other adipogenic genes is changed during differentiation. We report that the PPARγ2 promoter is transiently positioned in proximity to the promoters of genes encoding adipokines and lipid droplet associated proteins at 6 hours post-differentiation, a time that precedes expression of any of these genes. In contrast, the PPARγ2 promoter was not in proximity to the EF1α promoter, which drives expression of a constitutively active, housekeeping gene that encodes a translation elongation factor, nor was the PPARγ2 promoter in proximity to the promoter driving the expression of the C/EBPα regulatory protein. The formation of the long-range, intergenic interactions involving the PPARγ2 promoter required the regulatory factor C/EBPβ, elevated cyclic AMP (cAMP) levels, and protein kinase A (PKA) signaling. We conclude that genome organization is dynamically remodeled in response to adipogenic signaling, and we speculate that these transient inter-genic interactions may be formed for the purposes of selecting some of the transcriptionally silent tissue-specific loci for subsequent transcriptional activation.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0086140</identifier><identifier>PMID: 24465921</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>3T3-L1 Cells ; Adipocytes ; Adipogenesis ; Adipokines - genetics ; Animals ; Biology ; Carrier Proteins - genetics ; CCAAT-Enhancer-Binding Protein-beta - metabolism ; Cell differentiation ; Chromatin ; Chromatin - metabolism ; Chromosomes ; Cyclic AMP ; Cyclic AMP-Dependent Protein Kinases - metabolism ; Developmental biology ; Differentiation (biology) ; Elongation ; Gene expression ; Gene Expression Regulation, Developmental ; Gene loci ; Gene regulation ; Genes ; Genetic Loci ; Genomes ; Genomics ; Kinases ; Laboratories ; Medical schools ; Mice ; Nuclei ; Nuclei (cytology) ; Perilipin-1 ; Phosphoproteins - genetics ; PPAR gamma - genetics ; Promoter Regions, Genetic ; Protein kinase A ; Proteins ; Proximity ; Signal Transduction ; Signaling ; Specialization ; Transcription activation ; Translation elongation</subject><ispartof>PloS one, 2014, Vol.9 (1), p.e86140-e86140</ispartof><rights>2014 LeBlanc et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2014 LeBlanc et al 2014 LeBlanc et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-183c677e4485611c692b7906aa1b5536355ee22dddc17ec61f1797615a135be83</citedby><cites>FETCH-LOGICAL-c526t-183c677e4485611c692b7906aa1b5536355ee22dddc17ec61f1797615a135be83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3896465/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3896465/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2929,4025,23871,27928,27929,27930,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24465921$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Nurminsky, Dmitry I.</contributor><creatorcontrib>LeBlanc, Scott E</creatorcontrib><creatorcontrib>Wu, Qiong</creatorcontrib><creatorcontrib>Barutcu, A Rasim</creatorcontrib><creatorcontrib>Xiao, Hengyi</creatorcontrib><creatorcontrib>Ohkawa, Yasuyuki</creatorcontrib><creatorcontrib>Imbalzano, Anthony N</creatorcontrib><title>The PPARγ locus makes long-range chromatin interactions with selected tissue-specific gene loci during adipocyte differentiation in a protein kinase A dependent manner</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Differentiation signaling results in reprogramming of cellular gene expression that leads to morphological changes and functional specialization of a precursor cell. 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We conclude that genome organization is dynamically remodeled in response to adipogenic signaling, and we speculate that these transient inter-genic interactions may be formed for the purposes of selecting some of the transcriptionally silent tissue-specific loci for subsequent transcriptional activation.</description><subject>3T3-L1 Cells</subject><subject>Adipocytes</subject><subject>Adipogenesis</subject><subject>Adipokines - genetics</subject><subject>Animals</subject><subject>Biology</subject><subject>Carrier Proteins - genetics</subject><subject>CCAAT-Enhancer-Binding Protein-beta - metabolism</subject><subject>Cell differentiation</subject><subject>Chromatin</subject><subject>Chromatin - metabolism</subject><subject>Chromosomes</subject><subject>Cyclic AMP</subject><subject>Cyclic AMP-Dependent Protein Kinases - metabolism</subject><subject>Developmental biology</subject><subject>Differentiation (biology)</subject><subject>Elongation</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene loci</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Genetic Loci</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Kinases</subject><subject>Laboratories</subject><subject>Medical schools</subject><subject>Mice</subject><subject>Nuclei</subject><subject>Nuclei (cytology)</subject><subject>Perilipin-1</subject><subject>Phosphoproteins - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>LeBlanc, Scott E</au><au>Wu, Qiong</au><au>Barutcu, A Rasim</au><au>Xiao, Hengyi</au><au>Ohkawa, Yasuyuki</au><au>Imbalzano, Anthony N</au><au>Nurminsky, Dmitry I.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The PPARγ locus makes long-range chromatin interactions with selected tissue-specific gene loci during adipocyte differentiation in a protein kinase A dependent manner</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014</date><risdate>2014</risdate><volume>9</volume><issue>1</issue><spage>e86140</spage><epage>e86140</epage><pages>e86140-e86140</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Differentiation signaling results in reprogramming of cellular gene expression that leads to morphological changes and functional specialization of a precursor cell. This global change in gene expression involves temporal regulation of differentiation-specific genes that are located throughout the genome, raising the idea that genome structure may also be re-organized during cell differentiation to facilitate regulated gene expression. Using in vitro adipocyte differentiation as a model, we explored whether gene organization within the nucleus is altered upon exposure of precursor cells to signaling molecules that induce adipogenesis. The peroxisome proliferator-activated receptor gamma (PPARγ) nuclear hormone receptor is a master determinant of adipogenesis and is required for adipose differentiation. We utilized the chromosome conformation capture (3C) assay to determine whether the position of the PPARγ locus relative to other adipogenic genes is changed during differentiation. We report that the PPARγ2 promoter is transiently positioned in proximity to the promoters of genes encoding adipokines and lipid droplet associated proteins at 6 hours post-differentiation, a time that precedes expression of any of these genes. In contrast, the PPARγ2 promoter was not in proximity to the EF1α promoter, which drives expression of a constitutively active, housekeeping gene that encodes a translation elongation factor, nor was the PPARγ2 promoter in proximity to the promoter driving the expression of the C/EBPα regulatory protein. The formation of the long-range, intergenic interactions involving the PPARγ2 promoter required the regulatory factor C/EBPβ, elevated cyclic AMP (cAMP) levels, and protein kinase A (PKA) signaling. We conclude that genome organization is dynamically remodeled in response to adipogenic signaling, and we speculate that these transient inter-genic interactions may be formed for the purposes of selecting some of the transcriptionally silent tissue-specific loci for subsequent transcriptional activation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24465921</pmid><doi>10.1371/journal.pone.0086140</doi><oa>free_for_read</oa></addata></record> |
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| language | eng |
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| subjects | 3T3-L1 Cells Adipocytes Adipogenesis Adipokines - genetics Animals Biology Carrier Proteins - genetics CCAAT-Enhancer-Binding Protein-beta - metabolism Cell differentiation Chromatin Chromatin - metabolism Chromosomes Cyclic AMP Cyclic AMP-Dependent Protein Kinases - metabolism Developmental biology Differentiation (biology) Elongation Gene expression Gene Expression Regulation, Developmental Gene loci Gene regulation Genes Genetic Loci Genomes Genomics Kinases Laboratories Medical schools Mice Nuclei Nuclei (cytology) Perilipin-1 Phosphoproteins - genetics PPAR gamma - genetics Promoter Regions, Genetic Protein kinase A Proteins Proximity Signal Transduction Signaling Specialization Transcription activation Translation elongation |
| title | The PPARγ locus makes long-range chromatin interactions with selected tissue-specific gene loci during adipocyte differentiation in a protein kinase A dependent manner |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-12T01%3A11%3A00IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20PPAR%CE%B3%20locus%20makes%20long-range%20chromatin%20interactions%20with%20selected%20tissue-specific%20gene%20loci%20during%20adipocyte%20differentiation%20in%20a%20protein%20kinase%20A%20dependent%20manner&rft.jtitle=PloS%20one&rft.au=LeBlanc,%20Scott%20E&rft.date=2014&rft.volume=9&rft.issue=1&rft.spage=e86140&rft.epage=e86140&rft.pages=e86140-e86140&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0086140&rft_dat=%3Cproquest_plos_%3E1492690576%3C/proquest_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1490679741&rft_id=info:pmid/24465921&rft_doaj_id=oai_doaj_org_article_ffbb415a4b4f4408801553c920027961&rfr_iscdi=true |