Yin Yang 1 intronic binding sequences and splicing elicit intron-mediated enhancement of ubiquitin C gene expression
In a number of organisms, introns affect expression of the gene in which they are contained. Our previous studies revealed that the 5'-UTR intron of human ubiquitin C (UbC) gene is responsible for the boost of reporter gene expression and is able to bind, in vitro, Yin Yang 1 (YY1) trans-acting...
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| description | In a number of organisms, introns affect expression of the gene in which they are contained. Our previous studies revealed that the 5'-UTR intron of human ubiquitin C (UbC) gene is responsible for the boost of reporter gene expression and is able to bind, in vitro, Yin Yang 1 (YY1) trans-acting factor. In this work, we demonstrate that intact YY1 binding sequences are required for maximal promoter activity and YY1 silencing causes downregulation of luciferase mRNA levels. However, YY1 motifs fail to enhance gene expression when the intron is moved upstream of the proximal promoter, excluding the typical enhancer hypothesis and supporting a context-dependent action, like intron-mediated enhancement (IME). Yet, almost no expression is seen in the construct containing an unspliceable version of UbC intron, indicating that splicing is essential for promoter activity. Moreover, mutagenesis of YY1 binding sites and YY1 knockdown negatively affect UbC intron removal from both endogenous and reporter transcripts. Modulation of splicing efficiency by YY1 cis-elements and protein factor may thus be part of the mechanism(s) by which YY1 controls UbC promoter activity. Our data highlight the first evidence of the involvement of a sequence-specific DNA binding factor in IME. |
| doi_str_mv | 10.1371/journal.pone.0065932 |
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Our previous studies revealed that the 5'-UTR intron of human ubiquitin C (UbC) gene is responsible for the boost of reporter gene expression and is able to bind, in vitro, Yin Yang 1 (YY1) trans-acting factor. In this work, we demonstrate that intact YY1 binding sequences are required for maximal promoter activity and YY1 silencing causes downregulation of luciferase mRNA levels. However, YY1 motifs fail to enhance gene expression when the intron is moved upstream of the proximal promoter, excluding the typical enhancer hypothesis and supporting a context-dependent action, like intron-mediated enhancement (IME). Yet, almost no expression is seen in the construct containing an unspliceable version of UbC intron, indicating that splicing is essential for promoter activity. Moreover, mutagenesis of YY1 binding sites and YY1 knockdown negatively affect UbC intron removal from both endogenous and reporter transcripts. Modulation of splicing efficiency by YY1 cis-elements and protein factor may thus be part of the mechanism(s) by which YY1 controls UbC promoter activity. Our data highlight the first evidence of the involvement of a sequence-specific DNA binding factor in IME.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0065932</identifier><identifier>PMID: 23776572</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis of Variance ; Binding sites ; Binding Sites - genetics ; Biochemistry ; Biology ; Blotting, Western ; C gene ; Chromatin Immunoprecipitation ; Deoxyribonucleic acid ; DNA ; DNA Primers - genetics ; Electrophoretic Mobility Shift Assay ; Enhancer Elements, Genetic - genetics ; Gene expression ; Gene Expression Regulation - genetics ; Gene Knockdown Techniques ; Gene sequencing ; Genes ; Genetic engineering ; Genetic research ; Humans ; Immunoprecipitation ; Introns ; Introns - genetics ; Luciferase ; Luciferases ; Mammals ; Molecular biology ; Mutagenesis ; Nucleotide sequence ; Oryza ; Promoter Regions, Genetic - genetics ; Promoters (Genetics) ; Proteins ; Real-Time Polymerase Chain Reaction ; Reporter gene ; Reverse Transcriptase Polymerase Chain Reaction ; RNA ; RNA Splicing - genetics ; Signal transduction ; Splicing ; Stem cells ; Studies ; Ubiquitin ; Ubiquitin C - genetics ; Ubiquitin C - metabolism ; YY1 protein ; YY1 Transcription Factor - genetics ; YY1 Transcription Factor - metabolism</subject><ispartof>PloS one, 2013-06, Vol.8 (6), p.e65932</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Bianchi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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>2013 Bianchi et al 2013 Bianchi et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-ea6762d98ce6fe1913a510194ee6f791c8bb8e8cd95e02d971b8fcf85dec1aea3</citedby><cites>FETCH-LOGICAL-c692t-ea6762d98ce6fe1913a510194ee6f791c8bb8e8cd95e02d971b8fcf85dec1aea3</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/PMC3680475/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3680475/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23776572$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Buratti, Emanuele</contributor><creatorcontrib>Bianchi, Marzia</creatorcontrib><creatorcontrib>Crinelli, Rita</creatorcontrib><creatorcontrib>Giacomini, Elisa</creatorcontrib><creatorcontrib>Carloni, Elisa</creatorcontrib><creatorcontrib>Radici, Lucia</creatorcontrib><creatorcontrib>Magnani, Mauro</creatorcontrib><title>Yin Yang 1 intronic binding sequences and splicing elicit intron-mediated enhancement of ubiquitin C gene expression</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>In a number of organisms, introns affect expression of the gene in which they are contained. Our previous studies revealed that the 5'-UTR intron of human ubiquitin C (UbC) gene is responsible for the boost of reporter gene expression and is able to bind, in vitro, Yin Yang 1 (YY1) trans-acting factor. In this work, we demonstrate that intact YY1 binding sequences are required for maximal promoter activity and YY1 silencing causes downregulation of luciferase mRNA levels. However, YY1 motifs fail to enhance gene expression when the intron is moved upstream of the proximal promoter, excluding the typical enhancer hypothesis and supporting a context-dependent action, like intron-mediated enhancement (IME). Yet, almost no expression is seen in the construct containing an unspliceable version of UbC intron, indicating that splicing is essential for promoter activity. Moreover, mutagenesis of YY1 binding sites and YY1 knockdown negatively affect UbC intron removal from both endogenous and reporter transcripts. Modulation of splicing efficiency by YY1 cis-elements and protein factor may thus be part of the mechanism(s) by which YY1 controls UbC promoter activity. Our data highlight the first evidence of the involvement of a sequence-specific DNA binding factor in IME.</description><subject>Analysis of Variance</subject><subject>Binding sites</subject><subject>Binding Sites - genetics</subject><subject>Biochemistry</subject><subject>Biology</subject><subject>Blotting, Western</subject><subject>C gene</subject><subject>Chromatin Immunoprecipitation</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA Primers - genetics</subject><subject>Electrophoretic Mobility Shift Assay</subject><subject>Enhancer Elements, Genetic - genetics</subject><subject>Gene expression</subject><subject>Gene Expression Regulation - genetics</subject><subject>Gene Knockdown Techniques</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genetic engineering</subject><subject>Genetic research</subject><subject>Humans</subject><subject>Immunoprecipitation</subject><subject>Introns</subject><subject>Introns - genetics</subject><subject>Luciferase</subject><subject>Luciferases</subject><subject>Mammals</subject><subject>Molecular biology</subject><subject>Mutagenesis</subject><subject>Nucleotide sequence</subject><subject>Oryza</subject><subject>Promoter Regions, Genetic - 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Our previous studies revealed that the 5'-UTR intron of human ubiquitin C (UbC) gene is responsible for the boost of reporter gene expression and is able to bind, in vitro, Yin Yang 1 (YY1) trans-acting factor. In this work, we demonstrate that intact YY1 binding sequences are required for maximal promoter activity and YY1 silencing causes downregulation of luciferase mRNA levels. However, YY1 motifs fail to enhance gene expression when the intron is moved upstream of the proximal promoter, excluding the typical enhancer hypothesis and supporting a context-dependent action, like intron-mediated enhancement (IME). Yet, almost no expression is seen in the construct containing an unspliceable version of UbC intron, indicating that splicing is essential for promoter activity. Moreover, mutagenesis of YY1 binding sites and YY1 knockdown negatively affect UbC intron removal from both endogenous and reporter transcripts. Modulation of splicing efficiency by YY1 cis-elements and protein factor may thus be part of the mechanism(s) by which YY1 controls UbC promoter activity. Our data highlight the first evidence of the involvement of a sequence-specific DNA binding factor in IME.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23776572</pmid><doi>10.1371/journal.pone.0065932</doi><tpages>e65932</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Analysis of Variance Binding sites Binding Sites - genetics Biochemistry Biology Blotting, Western C gene Chromatin Immunoprecipitation Deoxyribonucleic acid DNA DNA Primers - genetics Electrophoretic Mobility Shift Assay Enhancer Elements, Genetic - genetics Gene expression Gene Expression Regulation - genetics Gene Knockdown Techniques Gene sequencing Genes Genetic engineering Genetic research Humans Immunoprecipitation Introns Introns - genetics Luciferase Luciferases Mammals Molecular biology Mutagenesis Nucleotide sequence Oryza Promoter Regions, Genetic - genetics Promoters (Genetics) Proteins Real-Time Polymerase Chain Reaction Reporter gene Reverse Transcriptase Polymerase Chain Reaction RNA RNA Splicing - genetics Signal transduction Splicing Stem cells Studies Ubiquitin Ubiquitin C - genetics Ubiquitin C - metabolism YY1 protein YY1 Transcription Factor - genetics YY1 Transcription Factor - metabolism |
| title | Yin Yang 1 intronic binding sequences and splicing elicit intron-mediated enhancement of ubiquitin C gene expression |
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