Principles for RNA metabolism and alternative transcription initiation within closely spaced promoters
Yun Chen, Albin Sandelin, Torben Heick Jensen and colleagues describe general rules governing the expression of reverse-oriented promoter upstream transcripts (PROMPTs) based on the orientation and proximity of promoter pairs. They characterize how the distance between promoters affects the expressi...
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| Veröffentlicht in: | Nature genetics 2016-09, Vol.48 (9), p.984-994 |
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| creator | Chen, Yun Pai, Athma A Herudek, Jan Lubas, Michal Meola, Nicola Järvelin, Aino I Andersson, Robin Pelechano, Vicent Steinmetz, Lars M Jensen, Torben Heick Sandelin, Albin |
| description | Yun Chen, Albin Sandelin, Torben Heick Jensen and colleagues describe general rules governing the expression of reverse-oriented promoter upstream transcripts (PROMPTs) based on the orientation and proximity of promoter pairs. They characterize how the distance between promoters affects the expression of PROMPTs and the usage of alternate mRNA transcription start sites.
Mammalian transcriptomes are complex and formed by extensive promoter activity. In addition, gene promoters are largely divergent and initiate transcription of reverse-oriented promoter upstream transcripts (PROMPTs). Although PROMPTs are commonly terminated early, influenced by polyadenylation sites, promoters often cluster so that the divergent activity of one might impact another. Here we found that the distance between promoters strongly correlates with the expression, stability and length of their associated PROMPTs. Adjacent promoters driving divergent mRNA transcription support PROMPT formation, but owing to polyadenylation site constraints, these transcripts tend to spread into the neighboring mRNA on the same strand. This mechanism to derive new alternative mRNA transcription start sites (TSSs) is also evident at closely spaced promoters supporting convergent mRNA transcription. We suggest that basic building blocks of divergently transcribed core promoter pairs, in combination with the wealth of TSSs in mammalian genomes, provide a framework with which evolution shapes transcriptomes. |
| doi_str_mv | 10.1038/ng.3616 |
| format | Article |
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Mammalian transcriptomes are complex and formed by extensive promoter activity. In addition, gene promoters are largely divergent and initiate transcription of reverse-oriented promoter upstream transcripts (PROMPTs). Although PROMPTs are commonly terminated early, influenced by polyadenylation sites, promoters often cluster so that the divergent activity of one might impact another. Here we found that the distance between promoters strongly correlates with the expression, stability and length of their associated PROMPTs. Adjacent promoters driving divergent mRNA transcription support PROMPT formation, but owing to polyadenylation site constraints, these transcripts tend to spread into the neighboring mRNA on the same strand. This mechanism to derive new alternative mRNA transcription start sites (TSSs) is also evident at closely spaced promoters supporting convergent mRNA transcription. We suggest that basic building blocks of divergently transcribed core promoter pairs, in combination with the wealth of TSSs in mammalian genomes, provide a framework with which evolution shapes transcriptomes.</description><identifier>ISSN: 1061-4036</identifier><identifier>ISSN: 1546-1718</identifier><identifier>EISSN: 1546-1718</identifier><identifier>DOI: 10.1038/ng.3616</identifier><identifier>PMID: 27455346</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>13/89 ; 38/39 ; 38/91 ; 45/15 ; 45/77 ; 631/114/2164 ; 631/208/200 ; 631/337/2019 ; Agriculture ; Alternative Splicing - genetics ; analysis ; Animal Genetics and Genomics ; Annotations ; Biomedicine ; Cancer Research ; Gene expression ; Gene Function ; Genetic research ; Genetic transcription ; Genomes ; Grants ; High-Throughput Nucleotide Sequencing ; Human Genetics ; Humans ; Laboratories ; Mammals ; Medicin och hälsovetenskap ; Models, Genetic ; Polyadenylation ; Principles ; Promoter Regions, Genetic - genetics ; Promoters (Genetics) ; Properties ; RNA - genetics ; RNA - metabolism ; Transcription Initiation Site ; Transcription, Genetic - genetics</subject><ispartof>Nature genetics, 2016-09, Vol.48 (9), p.984-994</ispartof><rights>Springer Nature America, Inc. 2016</rights><rights>COPYRIGHT 2016 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Sep 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c653t-864a0954f8fe4cad0d5c99c36726202bfc327b668f718a7853ee8a40fed5cd53</citedby><cites>FETCH-LOGICAL-c653t-864a0954f8fe4cad0d5c99c36726202bfc327b668f718a7853ee8a40fed5cd53</cites><orcidid>0000-0002-7109-7378 ; 0000-0003-1516-879X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,552,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27455346$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:134145020$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Yun</creatorcontrib><creatorcontrib>Pai, Athma A</creatorcontrib><creatorcontrib>Herudek, Jan</creatorcontrib><creatorcontrib>Lubas, Michal</creatorcontrib><creatorcontrib>Meola, Nicola</creatorcontrib><creatorcontrib>Järvelin, Aino I</creatorcontrib><creatorcontrib>Andersson, Robin</creatorcontrib><creatorcontrib>Pelechano, Vicent</creatorcontrib><creatorcontrib>Steinmetz, Lars M</creatorcontrib><creatorcontrib>Jensen, Torben Heick</creatorcontrib><creatorcontrib>Sandelin, Albin</creatorcontrib><title>Principles for RNA metabolism and alternative transcription initiation within closely spaced promoters</title><title>Nature genetics</title><addtitle>Nat Genet</addtitle><addtitle>Nat Genet</addtitle><description>Yun Chen, Albin Sandelin, Torben Heick Jensen and colleagues describe general rules governing the expression of reverse-oriented promoter upstream transcripts (PROMPTs) based on the orientation and proximity of promoter pairs. They characterize how the distance between promoters affects the expression of PROMPTs and the usage of alternate mRNA transcription start sites.
Mammalian transcriptomes are complex and formed by extensive promoter activity. In addition, gene promoters are largely divergent and initiate transcription of reverse-oriented promoter upstream transcripts (PROMPTs). Although PROMPTs are commonly terminated early, influenced by polyadenylation sites, promoters often cluster so that the divergent activity of one might impact another. Here we found that the distance between promoters strongly correlates with the expression, stability and length of their associated PROMPTs. Adjacent promoters driving divergent mRNA transcription support PROMPT formation, but owing to polyadenylation site constraints, these transcripts tend to spread into the neighboring mRNA on the same strand. This mechanism to derive new alternative mRNA transcription start sites (TSSs) is also evident at closely spaced promoters supporting convergent mRNA transcription. We suggest that basic building blocks of divergently transcribed core promoter pairs, in combination with the wealth of TSSs in mammalian genomes, provide a framework with which evolution shapes transcriptomes.</description><subject>13/89</subject><subject>38/39</subject><subject>38/91</subject><subject>45/15</subject><subject>45/77</subject><subject>631/114/2164</subject><subject>631/208/200</subject><subject>631/337/2019</subject><subject>Agriculture</subject><subject>Alternative Splicing - genetics</subject><subject>analysis</subject><subject>Animal Genetics and Genomics</subject><subject>Annotations</subject><subject>Biomedicine</subject><subject>Cancer Research</subject><subject>Gene expression</subject><subject>Gene Function</subject><subject>Genetic research</subject><subject>Genetic transcription</subject><subject>Genomes</subject><subject>Grants</subject><subject>High-Throughput Nucleotide Sequencing</subject><subject>Human Genetics</subject><subject>Humans</subject><subject>Laboratories</subject><subject>Mammals</subject><subject>Medicin och hälsovetenskap</subject><subject>Models, Genetic</subject><subject>Polyadenylation</subject><subject>Principles</subject><subject>Promoter Regions, Genetic - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SwePub Articles full text</collection><jtitle>Nature genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Yun</au><au>Pai, Athma A</au><au>Herudek, Jan</au><au>Lubas, Michal</au><au>Meola, Nicola</au><au>Järvelin, Aino I</au><au>Andersson, Robin</au><au>Pelechano, Vicent</au><au>Steinmetz, Lars M</au><au>Jensen, Torben Heick</au><au>Sandelin, Albin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Principles for RNA metabolism and alternative transcription initiation within closely spaced promoters</atitle><jtitle>Nature genetics</jtitle><stitle>Nat Genet</stitle><addtitle>Nat Genet</addtitle><date>2016-09-01</date><risdate>2016</risdate><volume>48</volume><issue>9</issue><spage>984</spage><epage>994</epage><pages>984-994</pages><issn>1061-4036</issn><issn>1546-1718</issn><eissn>1546-1718</eissn><abstract>Yun Chen, Albin Sandelin, Torben Heick Jensen and colleagues describe general rules governing the expression of reverse-oriented promoter upstream transcripts (PROMPTs) based on the orientation and proximity of promoter pairs. They characterize how the distance between promoters affects the expression of PROMPTs and the usage of alternate mRNA transcription start sites.
Mammalian transcriptomes are complex and formed by extensive promoter activity. In addition, gene promoters are largely divergent and initiate transcription of reverse-oriented promoter upstream transcripts (PROMPTs). Although PROMPTs are commonly terminated early, influenced by polyadenylation sites, promoters often cluster so that the divergent activity of one might impact another. Here we found that the distance between promoters strongly correlates with the expression, stability and length of their associated PROMPTs. Adjacent promoters driving divergent mRNA transcription support PROMPT formation, but owing to polyadenylation site constraints, these transcripts tend to spread into the neighboring mRNA on the same strand. This mechanism to derive new alternative mRNA transcription start sites (TSSs) is also evident at closely spaced promoters supporting convergent mRNA transcription. We suggest that basic building blocks of divergently transcribed core promoter pairs, in combination with the wealth of TSSs in mammalian genomes, provide a framework with which evolution shapes transcriptomes.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>27455346</pmid><doi>10.1038/ng.3616</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-7109-7378</orcidid><orcidid>https://orcid.org/0000-0003-1516-879X</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 13/89 38/39 38/91 45/15 45/77 631/114/2164 631/208/200 631/337/2019 Agriculture Alternative Splicing - genetics analysis Animal Genetics and Genomics Annotations Biomedicine Cancer Research Gene expression Gene Function Genetic research Genetic transcription Genomes Grants High-Throughput Nucleotide Sequencing Human Genetics Humans Laboratories Mammals Medicin och hälsovetenskap Models, Genetic Polyadenylation Principles Promoter Regions, Genetic - genetics Promoters (Genetics) Properties RNA - genetics RNA - metabolism Transcription Initiation Site Transcription, Genetic - genetics |
| title | Principles for RNA metabolism and alternative transcription initiation within closely spaced promoters |
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