Cargando…
Cross-regulome profiling of RNA polymerases highlights the regulatory role of polymerase III on mRNA transcription by maintaining local chromatin architecture
BACKGROUND: Mammalian cells have three types of RNA polymerases (Pols), Pol I, II, and III. However, the extent to which these polymerases are cross-regulated and the underlying mechanisms remain unclear. RESULTS: We employ genome-wide profiling after acute depletion of Pol I, Pol II, or Pol III to...
Autores principales: | , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9703767/ https://www.ncbi.nlm.nih.gov/pubmed/36443871 http://dx.doi.org/10.1186/s13059-022-02812-w |
_version_ | 1784839923896942592 |
---|---|
author | Jiang, Yongpeng Huang, Jie Tian, Kai Yi, Xiao Zheng, Haonan Zhu, Yi Guo, Tiannan Ji, Xiong |
author_facet | Jiang, Yongpeng Huang, Jie Tian, Kai Yi, Xiao Zheng, Haonan Zhu, Yi Guo, Tiannan Ji, Xiong |
author_sort | Jiang, Yongpeng |
collection | PubMed |
description | BACKGROUND: Mammalian cells have three types of RNA polymerases (Pols), Pol I, II, and III. However, the extent to which these polymerases are cross-regulated and the underlying mechanisms remain unclear. RESULTS: We employ genome-wide profiling after acute depletion of Pol I, Pol II, or Pol III to assess cross-regulatory effects between these Pols. We find that these enzymes mainly affect the transcription of their own target genes, while certain genes are transcribed by the other polymerases. Importantly, the most active type of crosstalk is exemplified by the fact that Pol III depletion affects Pol II transcription. Pol II genes with transcription changes upon Pol III depletion are enriched in diverse cellular functions, and Pol III binding sites are found near their promoters. However, these Pol III binding sites do not correspond to transfer RNAs. Moreover, we demonstrate that Pol III regulates Pol II transcription and chromatin binding of the facilitates chromatin transcription (FACT) complex to alter local chromatin structures, which in turn affects the Pol II transcription rate. CONCLUSIONS: Our results support a model suggesting that RNA polymerases show cross-regulatory effects: Pol III affects local chromatin structures and the FACT-Pol II axis to regulate the Pol II transcription rate at certain gene loci. This study provides a new perspective for understanding the dysregulation of Pol III in various tissues affected by developmental diseases. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02812-w. |
format | Online Article Text |
id | pubmed-9703767 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-97037672022-11-29 Cross-regulome profiling of RNA polymerases highlights the regulatory role of polymerase III on mRNA transcription by maintaining local chromatin architecture Jiang, Yongpeng Huang, Jie Tian, Kai Yi, Xiao Zheng, Haonan Zhu, Yi Guo, Tiannan Ji, Xiong Genome Biol Research BACKGROUND: Mammalian cells have three types of RNA polymerases (Pols), Pol I, II, and III. However, the extent to which these polymerases are cross-regulated and the underlying mechanisms remain unclear. RESULTS: We employ genome-wide profiling after acute depletion of Pol I, Pol II, or Pol III to assess cross-regulatory effects between these Pols. We find that these enzymes mainly affect the transcription of their own target genes, while certain genes are transcribed by the other polymerases. Importantly, the most active type of crosstalk is exemplified by the fact that Pol III depletion affects Pol II transcription. Pol II genes with transcription changes upon Pol III depletion are enriched in diverse cellular functions, and Pol III binding sites are found near their promoters. However, these Pol III binding sites do not correspond to transfer RNAs. Moreover, we demonstrate that Pol III regulates Pol II transcription and chromatin binding of the facilitates chromatin transcription (FACT) complex to alter local chromatin structures, which in turn affects the Pol II transcription rate. CONCLUSIONS: Our results support a model suggesting that RNA polymerases show cross-regulatory effects: Pol III affects local chromatin structures and the FACT-Pol II axis to regulate the Pol II transcription rate at certain gene loci. This study provides a new perspective for understanding the dysregulation of Pol III in various tissues affected by developmental diseases. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02812-w. BioMed Central 2022-11-28 /pmc/articles/PMC9703767/ /pubmed/36443871 http://dx.doi.org/10.1186/s13059-022-02812-w Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Jiang, Yongpeng Huang, Jie Tian, Kai Yi, Xiao Zheng, Haonan Zhu, Yi Guo, Tiannan Ji, Xiong Cross-regulome profiling of RNA polymerases highlights the regulatory role of polymerase III on mRNA transcription by maintaining local chromatin architecture |
title | Cross-regulome profiling of RNA polymerases highlights the regulatory role of polymerase III on mRNA transcription by maintaining local chromatin architecture |
title_full | Cross-regulome profiling of RNA polymerases highlights the regulatory role of polymerase III on mRNA transcription by maintaining local chromatin architecture |
title_fullStr | Cross-regulome profiling of RNA polymerases highlights the regulatory role of polymerase III on mRNA transcription by maintaining local chromatin architecture |
title_full_unstemmed | Cross-regulome profiling of RNA polymerases highlights the regulatory role of polymerase III on mRNA transcription by maintaining local chromatin architecture |
title_short | Cross-regulome profiling of RNA polymerases highlights the regulatory role of polymerase III on mRNA transcription by maintaining local chromatin architecture |
title_sort | cross-regulome profiling of rna polymerases highlights the regulatory role of polymerase iii on mrna transcription by maintaining local chromatin architecture |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9703767/ https://www.ncbi.nlm.nih.gov/pubmed/36443871 http://dx.doi.org/10.1186/s13059-022-02812-w |
work_keys_str_mv | AT jiangyongpeng crossregulomeprofilingofrnapolymeraseshighlightstheregulatoryroleofpolymeraseiiionmrnatranscriptionbymaintaininglocalchromatinarchitecture AT huangjie crossregulomeprofilingofrnapolymeraseshighlightstheregulatoryroleofpolymeraseiiionmrnatranscriptionbymaintaininglocalchromatinarchitecture AT tiankai crossregulomeprofilingofrnapolymeraseshighlightstheregulatoryroleofpolymeraseiiionmrnatranscriptionbymaintaininglocalchromatinarchitecture AT yixiao crossregulomeprofilingofrnapolymeraseshighlightstheregulatoryroleofpolymeraseiiionmrnatranscriptionbymaintaininglocalchromatinarchitecture AT zhenghaonan crossregulomeprofilingofrnapolymeraseshighlightstheregulatoryroleofpolymeraseiiionmrnatranscriptionbymaintaininglocalchromatinarchitecture AT zhuyi crossregulomeprofilingofrnapolymeraseshighlightstheregulatoryroleofpolymeraseiiionmrnatranscriptionbymaintaininglocalchromatinarchitecture AT guotiannan crossregulomeprofilingofrnapolymeraseshighlightstheregulatoryroleofpolymeraseiiionmrnatranscriptionbymaintaininglocalchromatinarchitecture AT jixiong crossregulomeprofilingofrnapolymeraseshighlightstheregulatoryroleofpolymeraseiiionmrnatranscriptionbymaintaininglocalchromatinarchitecture |