Mammalian Period represses and de-represses transcription by displacing CLOCK–BMAL1 from promoters in a Cryptochrome-dependent manner
The mammalian circadian clock is based on a transcription-translation feedback loop (TTFL) consolidated by secondary loops. In the primary TTFL, the circadian locomotor output cycles kaput (CLOCK)–brain and muscle Arnt-like protein-1 (BMAL1) heterodimer acts as the transcriptional activator, and Cry...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 113; no. 41; pp. E6072 - E6079 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
11.10.2016
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| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The mammalian circadian clock is based on a transcription-translation feedback loop (TTFL) consolidated by secondary loops. In the primary TTFL, the circadian locomotor output cycles kaput (CLOCK)–brain and muscle Arnt-like protein-1 (BMAL1) heterodimer acts as the transcriptional activator, and Cryptochrome (CRY) and Period (PER) proteins function as repressors. PER represses by displacing CLOCK–BMAL1 from promoters in a CRY-dependent manner. Interestingly, genes with complex promoters may either be repressed or de-repressed by PER, depending on the particular promoter regulatory elements. Here, using mouse cell lines with defined knockout mutations in clock genes, RNA-seq, ChIP-seq, and reporter gene assays coupled with measurements of DNA–protein interactions in nuclear extracts, we elucidate the dual functions of PER as repressor and de-repressor in a context-dependent manner. |
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| AbstractList | Significance
The mammalian circadian clock is controlled by a transcription-translation feedback loop consisting of transcriptional activators circadian locomotor output cycles kaput (CLOCK)–brain and muscle Arnt-like protein-1 (BMAL1), which function as a complex at E/E'-box elements, and repressors Cryptochrome 1 (CRY1)/CRY2 and PER1/PER2. CRYs repress upon binding as CRY–CLOCK–BMAL1–E-box complexes. Period proteins (PERs) repress by removing the heterotrimeric complexes from the E-box. We report here that in the
Cry1
promoter, the CRY1–CLOCK–BMAL1–E-box complex represses a transcriptional activator acting in cis, and removal of the heterotrimeric complex by PER2 de-represses the transcriptional activator. ChIP-seq and RNA-seq experiments identified other genes also de-repressed by PER2. These data clarify the role of PER2 and reveal the level of complexity in regulation of
Cry1
and other circadian-controlled genes.
The mammalian circadian clock is based on a transcription-translation feedback loop (TTFL) consolidated by secondary loops. In the primary TTFL, the circadian locomotor output cycles kaput (CLOCK)–brain and muscle Arnt-like protein-1 (BMAL1) heterodimer acts as the transcriptional activator, and Cryptochrome (CRY) and Period (PER) proteins function as repressors. PER represses by displacing CLOCK–BMAL1 from promoters in a CRY-dependent manner. Interestingly, genes with complex promoters may either be repressed or de-repressed by PER, depending on the particular promoter regulatory elements. Here, using mouse cell lines with defined knockout mutations in clock genes, RNA-seq, ChIP-seq, and reporter gene assays coupled with measurements of DNA–protein interactions in nuclear extracts, we elucidate the dual functions of PER as repressor and de-repressor in a context-dependent manner. The mammalian circadian clock is based on a transcription-translation feedback loop (TTFL) consolidated by secondary loops. In the primary TTFL, the circadian locomotor output cycles kaput (CLOCK)-brain and muscle Arnt-like protein-1 (BMAL1) heterodimer acts as the transcriptional activator, and Cryptochrome (CRY) and Period (PER) proteins function as repressors. PER represses by displacing CLOCK-BMAL1 from promoters in a CRY-dependent manner. Interestingly, genes with complex promoters may either be repressed or de-repressed by PER, depending on the particular promoter regulatory elements. Here, using mouse cell lines with defined knockout mutations in clock genes, RNA-seq, ChIP-seq, and reporter gene assays coupled with measurements of DNA-protein interactions in nuclear extracts, we elucidate the dual functions of PER as repressor and de-repressor in a context-dependent manner. The mammalian circadian clock is controlled by a transcription-translation feedback loop consisting of transcriptional activators circadian locomotor output cycles kaput (CLOCK)–brain and muscle Arnt-like protein-1 (BMAL1), which function as a complex at E/E'-box elements, and repressors Cryptochrome 1 (CRY1)/CRY2 and PER1/PER2. CRYs repress upon binding as CRY–CLOCK–BMAL1–E-box complexes. Period proteins (PERs) repress by removing the heterotrimeric complexes from the E-box. We report here that in the Cry1 promoter, the CRY1–CLOCK–BMAL1–E-box complex represses a transcriptional activator acting in cis, and removal of the heterotrimeric complex by PER2 de-represses the transcriptional activator. ChIP-seq and RNA-seq experiments identified other genes also de-repressed by PER2. These data clarify the role of PER2 and reveal the level of complexity in regulation of Cry1 and other circadian-controlled genes. The mammalian circadian clock is based on a transcription-translation feedback loop (TTFL) consolidated by secondary loops. In the primary TTFL, the circadian locomotor output cycles kaput (CLOCK)–brain and muscle Arnt-like protein-1 (BMAL1) heterodimer acts as the transcriptional activator, and Cryptochrome (CRY) and Period (PER) proteins function as repressors. PER represses by displacing CLOCK–BMAL1 from promoters in a CRY-dependent manner. Interestingly, genes with complex promoters may either be repressed or de-repressed by PER, depending on the particular promoter regulatory elements. Here, using mouse cell lines with defined knockout mutations in clock genes, RNA-seq, ChIP-seq, and reporter gene assays coupled with measurements of DNA–protein interactions in nuclear extracts, we elucidate the dual functions of PER as repressor and de-repressor in a context-dependent manner. |
| Author | Chiou, Yi-Ying Ye, Rui Yang, Yanyan Rashid, Naim Selby, Christopher P. Sancar, Aziz |
| Author_xml | – sequence: 1 givenname: Yi-Ying surname: Chiou fullname: Chiou, Yi-Ying organization: Department of Biochemistry and Biophysics, University of North Carolina School of Medicine, Chapel Hill, NC 27599 – sequence: 2 givenname: Yanyan surname: Yang fullname: Yang, Yanyan organization: Department of Biochemistry and Biophysics, University of North Carolina School of Medicine, Chapel Hill, NC 27599 – sequence: 3 givenname: Naim surname: Rashid fullname: Rashid, Naim organization: Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, NC 27599 – sequence: 4 givenname: Rui surname: Ye fullname: Ye, Rui organization: Department of Biochemistry and Biophysics, University of North Carolina School of Medicine, Chapel Hill, NC 27599 – sequence: 5 givenname: Christopher P. surname: Selby fullname: Selby, Christopher P. organization: Department of Biochemistry and Biophysics, University of North Carolina School of Medicine, Chapel Hill, NC 27599 – sequence: 6 givenname: Aziz surname: Sancar fullname: Sancar, Aziz organization: Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, NC 27599 |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27688755$$D View this record in MEDLINE/PubMed |
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| Copyright | Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles Copyright National Academy of Sciences Oct 11, 2016 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Contributed by Aziz Sancar, August 17, 2016 (sent for review July 15, 2016; reviewed by Carl Hirschie Johnson and Andrew C. Liu) 1Y.-Y.C., Y.Y., and N.R. contributed equally to this work. Reviewers: C.H.J., Vanderbilt University; and A.C.L., University of Memphis. Author contributions: Y.-Y.C., R.Y., and A.S. designed research; Y.-Y.C., Y.Y., and R.Y. performed research; Y.-Y.C., Y.Y., and N.R. analyzed data; and C.P.S. and A.S. wrote the paper. |
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| Snippet | The mammalian circadian clock is based on a transcription-translation feedback loop (TTFL) consolidated by secondary loops. In the primary TTFL, the circadian... Significance The mammalian circadian clock is controlled by a transcription-translation feedback loop consisting of transcriptional activators circadian... The mammalian circadian clock is controlled by a transcription-translation feedback loop consisting of transcriptional activators circadian locomotor output... |
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| Title | Mammalian Period represses and de-represses transcription by displacing CLOCK–BMAL1 from promoters in a Cryptochrome-dependent manner |
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