Live imaging of nascent RNA dynamics reveals distinct types of transcriptional pulse regulation
Transcription of genes can be discontinuous, occurring in pulses or bursts. It is not clear how properties of transcriptional pulses vary between different genes. We compared the pulsing of five housekeeping and five developmentally induced genes by direct imaging of single gene transcriptional even...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2012-05, Vol.109 (19), p.7350-7355 |
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| container_title | Proceedings of the National Academy of Sciences - PNAS |
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| creator | Muramoto, Tetsuya Cannon, Danielle Gierliński, Marek Corrigan, Adam Barton, Geoffrey J Chubb, Jonathan R |
| description | Transcription of genes can be discontinuous, occurring in pulses or bursts. It is not clear how properties of transcriptional pulses vary between different genes. We compared the pulsing of five housekeeping and five developmentally induced genes by direct imaging of single gene transcriptional events in individual living Dictyostelium cells. Each gene displayed its own transcriptional signature, differing in probability of firing and pulse duration, frequency, and intensity. In contrast to the prevailing view from both prokaryotes and eukaryotes that transcription displays binary behavior, strongly expressed housekeeping genes altered the magnitude of their transcriptional pulses during development. These nonbinary "tunable" responses may be better suited than stochastic switch behavior for housekeeping functions. Analysis of RNA synthesis kinetics using fluorescence recovery after photobleaching implied modulation of housekeeping-gene pulse strength occurs at the level of transcription initiation rather than elongation. In addition, disparities between single cell and population measures of transcript production suggested differences in RNA stability between gene classes. Analysis of stability using RNAseq revealed no major global differences in stability between developmental and housekeeping transcripts, although strongly induced RNAs showed unusually rapid decay, indicating tight regulation of expression. |
| doi_str_mv | 10.1073/pnas.1117603109 |
| format | Article |
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It is not clear how properties of transcriptional pulses vary between different genes. We compared the pulsing of five housekeeping and five developmentally induced genes by direct imaging of single gene transcriptional events in individual living Dictyostelium cells. Each gene displayed its own transcriptional signature, differing in probability of firing and pulse duration, frequency, and intensity. In contrast to the prevailing view from both prokaryotes and eukaryotes that transcription displays binary behavior, strongly expressed housekeeping genes altered the magnitude of their transcriptional pulses during development. These nonbinary "tunable" responses may be better suited than stochastic switch behavior for housekeeping functions. Analysis of RNA synthesis kinetics using fluorescence recovery after photobleaching implied modulation of housekeeping-gene pulse strength occurs at the level of transcription initiation rather than elongation. In addition, disparities between single cell and population measures of transcript production suggested differences in RNA stability between gene classes. Analysis of stability using RNAseq revealed no major global differences in stability between developmental and housekeeping transcripts, although strongly induced RNAs showed unusually rapid decay, indicating tight regulation of expression.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1117603109</identifier><identifier>PMID: 22529358</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Algorithms ; Biological Sciences ; Biosynthesis ; Blotting, Northern ; Cell lines ; Cells ; Cellular differentiation ; Developmental biology ; Dictyostelium ; Dictyostelium - cytology ; Dictyostelium - genetics ; Dictyostelium - growth & development ; essential genes ; eukaryotic cells ; Fluorescence ; Fluorescence Recovery After Photobleaching ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation, Developmental ; Genes ; Genes, Protozoan - genetics ; Housekeeping ; image analysis ; Kinetics ; Models, Genetic ; photobleaching ; probability ; prokaryotic cells ; Pulse duration ; Reverse Transcriptase Polymerase Chain Reaction ; Ribonucleic acid ; RNA ; RNA Stability ; RNA, Protozoan - genetics ; RNA, Protozoan - metabolism ; Single-Cell Analysis - methods ; Stem cells ; transcription (genetics) ; Transcription, Genetic - genetics</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2012-05, Vol.109 (19), p.7350-7355</ispartof><rights>copyright © 1993-2008 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences May 8, 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c590t-4ba3e1d8971a3014a0d6c82942a7afc9f5790a838de94f302a6a215e7c5be80c3</citedby><cites>FETCH-LOGICAL-c590t-4ba3e1d8971a3014a0d6c82942a7afc9f5790a838de94f302a6a215e7c5be80c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/109/19.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41593018$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41593018$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22529358$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Muramoto, Tetsuya</creatorcontrib><creatorcontrib>Cannon, Danielle</creatorcontrib><creatorcontrib>Gierliński, Marek</creatorcontrib><creatorcontrib>Corrigan, Adam</creatorcontrib><creatorcontrib>Barton, Geoffrey J</creatorcontrib><creatorcontrib>Chubb, Jonathan R</creatorcontrib><title>Live imaging of nascent RNA dynamics reveals distinct types of transcriptional pulse regulation</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Transcription of genes can be discontinuous, occurring in pulses or bursts. It is not clear how properties of transcriptional pulses vary between different genes. We compared the pulsing of five housekeeping and five developmentally induced genes by direct imaging of single gene transcriptional events in individual living Dictyostelium cells. Each gene displayed its own transcriptional signature, differing in probability of firing and pulse duration, frequency, and intensity. In contrast to the prevailing view from both prokaryotes and eukaryotes that transcription displays binary behavior, strongly expressed housekeeping genes altered the magnitude of their transcriptional pulses during development. These nonbinary "tunable" responses may be better suited than stochastic switch behavior for housekeeping functions. Analysis of RNA synthesis kinetics using fluorescence recovery after photobleaching implied modulation of housekeeping-gene pulse strength occurs at the level of transcription initiation rather than elongation. In addition, disparities between single cell and population measures of transcript production suggested differences in RNA stability between gene classes. Analysis of stability using RNAseq revealed no major global differences in stability between developmental and housekeeping transcripts, although strongly induced RNAs showed unusually rapid decay, indicating tight regulation of expression.</description><subject>Algorithms</subject><subject>Biological Sciences</subject><subject>Biosynthesis</subject><subject>Blotting, Northern</subject><subject>Cell lines</subject><subject>Cells</subject><subject>Cellular differentiation</subject><subject>Developmental biology</subject><subject>Dictyostelium</subject><subject>Dictyostelium - cytology</subject><subject>Dictyostelium - genetics</subject><subject>Dictyostelium - growth & development</subject><subject>essential genes</subject><subject>eukaryotic cells</subject><subject>Fluorescence</subject><subject>Fluorescence Recovery After Photobleaching</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genes</subject><subject>Genes, Protozoan - genetics</subject><subject>Housekeeping</subject><subject>image analysis</subject><subject>Kinetics</subject><subject>Models, Genetic</subject><subject>photobleaching</subject><subject>probability</subject><subject>prokaryotic cells</subject><subject>Pulse duration</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA Stability</subject><subject>RNA, Protozoan - genetics</subject><subject>RNA, Protozoan - metabolism</subject><subject>Single-Cell Analysis - methods</subject><subject>Stem cells</subject><subject>transcription (genetics)</subject><subject>Transcription, Genetic - genetics</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc1v1DAQxS0EokvhzAmIxKWXtOOvxL5UqiooSCuQgJ6tWcdZvMrGwU5W2v8eR7tsCycutuT5zZPfe4S8pnBJoeZXQ4_pklJaV8Ap6CdkkU9aVkLDU7IAYHWpBBNn5EVKGwDQUsFzcsaYZJpLtSBm6Xeu8Ftc-35dhLbIgtb1Y_Hty03R7HvcepuK6HYOu1Q0Po2-t2Mx7geXZnyM2Ccb_TD60GNXDFOXXObXU4fz00vyrM2b7tXxPif3Hz_8uP1ULr_efb69WZZWahhLsULuaKN0TZEDFQhNZRXTgmGNrdWtrDWg4qpxWrQcGFbIqHS1lSunwPJzcn3QHabV1jWzhYidGWK2FvcmoDd_T3r_06zDzvAcg-JVFrg4CsTwa3JpNFufk-g67F2YkqHAQEmhtPgPlLIMQ8Uy-v4fdBOmmIM6UBRAMJqpqwNlY0gpuvb0bwpm7tnMPZuHnvPG28d2T_yfYjPw7gjMmw9y2lBtai4hE28OxCaNIZ4QQaXODTxSaDEYXEefzP13lruBPK3m0H4DAqHBkA</recordid><startdate>20120508</startdate><enddate>20120508</enddate><creator>Muramoto, Tetsuya</creator><creator>Cannon, Danielle</creator><creator>Gierliński, Marek</creator><creator>Corrigan, Adam</creator><creator>Barton, Geoffrey J</creator><creator>Chubb, Jonathan R</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20120508</creationdate><title>Live imaging of nascent RNA dynamics reveals distinct types of transcriptional pulse regulation</title><author>Muramoto, Tetsuya ; 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It is not clear how properties of transcriptional pulses vary between different genes. We compared the pulsing of five housekeeping and five developmentally induced genes by direct imaging of single gene transcriptional events in individual living Dictyostelium cells. Each gene displayed its own transcriptional signature, differing in probability of firing and pulse duration, frequency, and intensity. In contrast to the prevailing view from both prokaryotes and eukaryotes that transcription displays binary behavior, strongly expressed housekeeping genes altered the magnitude of their transcriptional pulses during development. These nonbinary "tunable" responses may be better suited than stochastic switch behavior for housekeeping functions. Analysis of RNA synthesis kinetics using fluorescence recovery after photobleaching implied modulation of housekeeping-gene pulse strength occurs at the level of transcription initiation rather than elongation. In addition, disparities between single cell and population measures of transcript production suggested differences in RNA stability between gene classes. Analysis of stability using RNAseq revealed no major global differences in stability between developmental and housekeeping transcripts, although strongly induced RNAs showed unusually rapid decay, indicating tight regulation of expression.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>22529358</pmid><doi>10.1073/pnas.1117603109</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Algorithms Biological Sciences Biosynthesis Blotting, Northern Cell lines Cells Cellular differentiation Developmental biology Dictyostelium Dictyostelium - cytology Dictyostelium - genetics Dictyostelium - growth & development essential genes eukaryotic cells Fluorescence Fluorescence Recovery After Photobleaching Gene expression Gene Expression Profiling Gene Expression Regulation, Developmental Genes Genes, Protozoan - genetics Housekeeping image analysis Kinetics Models, Genetic photobleaching probability prokaryotic cells Pulse duration Reverse Transcriptase Polymerase Chain Reaction Ribonucleic acid RNA RNA Stability RNA, Protozoan - genetics RNA, Protozoan - metabolism Single-Cell Analysis - methods Stem cells transcription (genetics) Transcription, Genetic - genetics |
| title | Live imaging of nascent RNA dynamics reveals distinct types of transcriptional pulse regulation |
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