Functional elements of the cis-regulatory lincRNA-p21
The p53-induced long noncoding RNA (lncRNA) lincRNA-p21 is proposed to act in cis to promote p53-dependent expression of the neighboring cell cycle gene, Cdkn1a/p21. The molecular mechanism through which the transcribed lincRNA-p21 regulatory locus activates p21 expression remains poorly understood....
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| Published in | Cell reports (Cambridge) Vol. 39; no. 3; p. 110687 |
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| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
19.04.2022
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| Subjects | |
| Online Access | Get full text |
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| Abstract | The p53-induced long noncoding RNA (lncRNA) lincRNA-p21 is proposed to act in cis to promote p53-dependent expression of the neighboring cell cycle gene, Cdkn1a/p21. The molecular mechanism through which the transcribed lincRNA-p21 regulatory locus activates p21 expression remains poorly understood. To elucidate the functional elements of cis-regulation, we generate a series of genetic models that disrupt DNA regulatory elements, the transcription of lincRNA-p21, or the accumulation of mature lincRNA-p21. Unexpectedly, we determine that full-length transcription, splicing, and accumulation of lincRNA-p21 are dispensable for the chromatin organization of the locus and for cis-regulation. Instead, we find that production of lincRNA-p21 through conserved regions in exon 1 of lincRNA-p21 promotes cis-activation. These findings demonstrate that the activation of nascent transcription from this lncRNA locus, but not the generation or accumulation of a mature lncRNA transcript, is necessary to enact local gene expression control.
[Display omitted]
•p53 regulates the neighboring p21 and lincRNA-p21 cooperatively•Production of nascent lincRNA-p21 promotes p21 expression in cis•Conserved elements in nascent lincRNA-p21 contribute to cis-activation•Transcription, processing, and accumulation of full-length lincRNA-p21 are dispensable
Winkler et al. analyze a series of genetic models to show that full-length production, splicing, and transcript accumulation of the long noncoding RNA lincRNA-p21 are dispensable for its role as a transcriptional activator of the neighboring gene p21. Instead, nascent transcription through conserved regions of lincRNA-p21 is sufficient for cis-activation. |
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| AbstractList | The p53-induced long noncoding RNA (lncRNA)
lincRNA-p21
is proposed to act in
cis
to promote p53-dependent expression of the neighboring cell cycle gene,
Cdkn1a/p21
. The molecular mechanism through which the transcribed
lincRNA-p21
regulatory locus activates
p21
expression remains poorly understood. To elucidate the functional elements of
cis
-regulation, we generate a series of genetic models that disrupt DNA regulatory elements, the transcription of
lincRNA-p21
, or the accumulation of mature
lincRNA-p21
. Unexpectedly, we determine that full-length transcription, splicing, and accumulation of
lincRNA-p21
are dispensable for the chromatin organization of the locus and for
cis
-regulation. Instead, we find that production of
lincRNA-p21
through conserved regions in exon 1 of
lincRNA-p21
promotes
cis
-activation. These findings demonstrate that the activation of nascent transcription from this lncRNA locus, but not the generation or accumulation of a mature lncRNA transcript, is necessary to enact local gene expression control.
Winkler et al. analyze a series of genetic models to show that full-length production, splicing, and transcript accumulation of the long noncoding RNA
lincRNA-p21
are dispensable for its role as a transcriptional activator of the neighboring gene
p21
. Instead, nascent transcription through conserved regions of
lincRNA-p21
is sufficient for
cis
-activation. The p53-induced long noncoding RNA (lncRNA) lincRNA-p21 is proposed to act in cis to promote p53-dependent expression of the neighboring cell cycle gene, Cdkn1a/p21. The molecular mechanism through which the transcribed lincRNA-p21 regulatory locus activates p21 expression remains poorly understood. To elucidate the functional elements of cis-regulation, we generate a series of genetic models that disrupt DNA regulatory elements, the transcription of lincRNA-p21, or the accumulation of mature lincRNA-p21. Unexpectedly, we determine that full-length transcription, splicing, and accumulation of lincRNA-p21 are dispensable for the chromatin organization of the locus and for cis-regulation. Instead, we find that production of lincRNA-p21 through conserved regions in exon 1 of lincRNA-p21 promotes cis-activation. These findings demonstrate that the activation of nascent transcription from this lncRNA locus, but not the generation or accumulation of a mature lncRNA transcript, is necessary to enact local gene expression control.The p53-induced long noncoding RNA (lncRNA) lincRNA-p21 is proposed to act in cis to promote p53-dependent expression of the neighboring cell cycle gene, Cdkn1a/p21. The molecular mechanism through which the transcribed lincRNA-p21 regulatory locus activates p21 expression remains poorly understood. To elucidate the functional elements of cis-regulation, we generate a series of genetic models that disrupt DNA regulatory elements, the transcription of lincRNA-p21, or the accumulation of mature lincRNA-p21. Unexpectedly, we determine that full-length transcription, splicing, and accumulation of lincRNA-p21 are dispensable for the chromatin organization of the locus and for cis-regulation. Instead, we find that production of lincRNA-p21 through conserved regions in exon 1 of lincRNA-p21 promotes cis-activation. These findings demonstrate that the activation of nascent transcription from this lncRNA locus, but not the generation or accumulation of a mature lncRNA transcript, is necessary to enact local gene expression control. The p53-induced long noncoding RNA (lncRNA) lincRNA-p21 is proposed to act in cis to promote p53-dependent expression of the neighboring cell cycle gene, Cdkn1a/p21. The molecular mechanism through which the transcribed lincRNA-p21 regulatory locus activates p21 expression remains poorly understood. To elucidate the functional elements of cis-regulation, we generate a series of genetic models that disrupt DNA regulatory elements, the transcription of lincRNA-p21, or the accumulation of mature lincRNA-p21. Unexpectedly, we determine that full-length transcription, splicing, and accumulation of lincRNA-p21 are dispensable for the chromatin organization of the locus and for cis-regulation. Instead, we find that production of lincRNA-p21 through conserved regions in exon 1 of lincRNA-p21 promotes cis-activation. These findings demonstrate that the activation of nascent transcription from this lncRNA locus, but not the generation or accumulation of a mature lncRNA transcript, is necessary to enact local gene expression control. The p53-induced long noncoding RNA (lncRNA) lincRNA-p21 is proposed to act in cis to promote p53-dependent expression of the neighboring cell cycle gene, Cdkn1a/p21. The molecular mechanism through which the transcribed lincRNA-p21 regulatory locus activates p21 expression remains poorly understood. To elucidate the functional elements of cis-regulation, we generate a series of genetic models that disrupt DNA regulatory elements, the transcription of lincRNA-p21, or the accumulation of mature lincRNA-p21. Unexpectedly, we determine that full-length transcription, splicing, and accumulation of lincRNA-p21 are dispensable for the chromatin organization of the locus and for cis-regulation. Instead, we find that production of lincRNA-p21 through conserved regions in exon 1 of lincRNA-p21 promotes cis-activation. These findings demonstrate that the activation of nascent transcription from this lncRNA locus, but not the generation or accumulation of a mature lncRNA transcript, is necessary to enact local gene expression control. [Display omitted] •p53 regulates the neighboring p21 and lincRNA-p21 cooperatively•Production of nascent lincRNA-p21 promotes p21 expression in cis•Conserved elements in nascent lincRNA-p21 contribute to cis-activation•Transcription, processing, and accumulation of full-length lincRNA-p21 are dispensable Winkler et al. analyze a series of genetic models to show that full-length production, splicing, and transcript accumulation of the long noncoding RNA lincRNA-p21 are dispensable for its role as a transcriptional activator of the neighboring gene p21. Instead, nascent transcription through conserved regions of lincRNA-p21 is sufficient for cis-activation. |
| ArticleNumber | 110687 |
| Author | Williams, Adam Dimitrova, Nadya Zimmer, Joshua T. Simon, Matthew D. Jimenez, Maria Winkler, Lauren |
| AuthorAffiliation | 5 Lead contact 4 The Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA 1 Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT 06511, USA 3 Institute for Biomolecular Design and Discovery, Yale University, West Haven, CT 06516, USA 2 Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06511, USA |
| AuthorAffiliation_xml | – name: 1 Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT 06511, USA – name: 3 Institute for Biomolecular Design and Discovery, Yale University, West Haven, CT 06516, USA – name: 4 The Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA – name: 2 Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06511, USA – name: 5 Lead contact |
| Author_xml | – sequence: 1 givenname: Lauren surname: Winkler fullname: Winkler, Lauren organization: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT 06511, USA – sequence: 2 givenname: Maria surname: Jimenez fullname: Jimenez, Maria organization: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT 06511, USA – sequence: 3 givenname: Joshua T. surname: Zimmer fullname: Zimmer, Joshua T. organization: Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06511, USA – sequence: 4 givenname: Adam surname: Williams fullname: Williams, Adam organization: The Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA – sequence: 5 givenname: Matthew D. surname: Simon fullname: Simon, Matthew D. organization: Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06511, USA – sequence: 6 givenname: Nadya surname: Dimitrova fullname: Dimitrova, Nadya email: nadya.dimitrova@yale.edu organization: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT 06511, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35443176$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2022 The Author(s) Copyright © 2022 The Author(s). Published by Elsevier Inc. All rights reserved. |
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| Keywords | long noncoding RNA cis-regulation CP: Molecular biology transcription lincRNA-p21 genetic models |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS L.W. and N.D. designed the study, performed experiments, analyzed data, generated figures, and prepared the manuscript. M.J. performed experiments and analyzed data. A.W. enabled the generation of the mouse models with input from L.W. and N.D. J.Z. and M.S. performed analysis of metabolically labeled RNA. All authors approved the final manuscript. |
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| SubjectTerms | cis-regulation genetic models lincRNA-p21 long noncoding RNA RNA, Long Noncoding - genetics RNA, Long Noncoding - metabolism transcription Tumor Suppressor Protein p53 - genetics Tumor Suppressor Protein p53 - metabolism |
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| Title | Functional elements of the cis-regulatory lincRNA-p21 |
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