Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles.
Interactions of cell-autonomous circadian oscillators with diurnal cycles govern the temporal compartmentalization of cell physiology in mammals. To understand the transcriptional and epigenetic basis of diurnal rhythms in mouse liver genome-wide, we generated temporal DNA occupancy profiles by RNA...
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oai:doaj.org-article:39ea2125b291414090a9397d877a00532021-11-18T05:37:20ZGenome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles.1544-91731545-788510.1371/journal.pbio.1001442https://doaj.org/article/39ea2125b291414090a9397d877a00532012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23209382/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Interactions of cell-autonomous circadian oscillators with diurnal cycles govern the temporal compartmentalization of cell physiology in mammals. To understand the transcriptional and epigenetic basis of diurnal rhythms in mouse liver genome-wide, we generated temporal DNA occupancy profiles by RNA polymerase II (Pol II) as well as profiles of the histone modifications H3K4me3 and H3K36me3. We used these data to quantify the relationships of phases and amplitudes between different marks. We found that rhythmic Pol II recruitment at promoters rather than rhythmic transition from paused to productive elongation underlies diurnal gene transcription, a conclusion further supported by modeling. Moreover, Pol II occupancy preceded mRNA accumulation by 3 hours, consistent with mRNA half-lives. Both methylation marks showed that the epigenetic landscape is highly dynamic and globally remodeled during the 24-hour cycle. While promoters of transcribed genes had tri-methylated H3K4 even at their trough activity times, tri-methylation levels reached their peak, on average, 1 hour after Pol II. Meanwhile, rhythms in tri-methylation of H3K36 lagged transcription by 3 hours. Finally, modeling profiles of Pol II occupancy and mRNA accumulation identified three classes of genes: one showing rhythmicity both in transcriptional and mRNA accumulation, a second class with rhythmic transcription but flat mRNA levels, and a third with constant transcription but rhythmic mRNAs. The latter class emphasizes widespread temporally gated posttranscriptional regulation in the mouse liver.Gwendal Le MartelotDonatella CanellaLaura SymulEugenia MigliavaccaFederica GilardiRobin LiechtiOlivier MartinKeith HarshmanMauro DelorenziBéatrice DesvergneWinship HerrBart DeplanckeUeli SchiblerJacques RougemontNicolas GuexNouria HernandezFelix NaefCycliX ConsortiumPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 10, Iss 11, p e1001442 (2012) |
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DOAJ |
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Biology (General) QH301-705.5 |
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Biology (General) QH301-705.5 Gwendal Le Martelot Donatella Canella Laura Symul Eugenia Migliavacca Federica Gilardi Robin Liechti Olivier Martin Keith Harshman Mauro Delorenzi Béatrice Desvergne Winship Herr Bart Deplancke Ueli Schibler Jacques Rougemont Nicolas Guex Nouria Hernandez Felix Naef CycliX Consortium Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. |
| description |
Interactions of cell-autonomous circadian oscillators with diurnal cycles govern the temporal compartmentalization of cell physiology in mammals. To understand the transcriptional and epigenetic basis of diurnal rhythms in mouse liver genome-wide, we generated temporal DNA occupancy profiles by RNA polymerase II (Pol II) as well as profiles of the histone modifications H3K4me3 and H3K36me3. We used these data to quantify the relationships of phases and amplitudes between different marks. We found that rhythmic Pol II recruitment at promoters rather than rhythmic transition from paused to productive elongation underlies diurnal gene transcription, a conclusion further supported by modeling. Moreover, Pol II occupancy preceded mRNA accumulation by 3 hours, consistent with mRNA half-lives. Both methylation marks showed that the epigenetic landscape is highly dynamic and globally remodeled during the 24-hour cycle. While promoters of transcribed genes had tri-methylated H3K4 even at their trough activity times, tri-methylation levels reached their peak, on average, 1 hour after Pol II. Meanwhile, rhythms in tri-methylation of H3K36 lagged transcription by 3 hours. Finally, modeling profiles of Pol II occupancy and mRNA accumulation identified three classes of genes: one showing rhythmicity both in transcriptional and mRNA accumulation, a second class with rhythmic transcription but flat mRNA levels, and a third with constant transcription but rhythmic mRNAs. The latter class emphasizes widespread temporally gated posttranscriptional regulation in the mouse liver. |
| format |
article |
| author |
Gwendal Le Martelot Donatella Canella Laura Symul Eugenia Migliavacca Federica Gilardi Robin Liechti Olivier Martin Keith Harshman Mauro Delorenzi Béatrice Desvergne Winship Herr Bart Deplancke Ueli Schibler Jacques Rougemont Nicolas Guex Nouria Hernandez Felix Naef CycliX Consortium |
| author_facet |
Gwendal Le Martelot Donatella Canella Laura Symul Eugenia Migliavacca Federica Gilardi Robin Liechti Olivier Martin Keith Harshman Mauro Delorenzi Béatrice Desvergne Winship Herr Bart Deplancke Ueli Schibler Jacques Rougemont Nicolas Guex Nouria Hernandez Felix Naef CycliX Consortium |
| author_sort |
Gwendal Le Martelot |
| title |
Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. |
| title_short |
Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. |
| title_full |
Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. |
| title_fullStr |
Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. |
| title_full_unstemmed |
Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. |
| title_sort |
genome-wide rna polymerase ii profiles and rna accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2012 |
| url |
https://doaj.org/article/39ea2125b291414090a9397d877a0053 |
| work_keys_str_mv |
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