Lola-I is a promoter pioneer factor that establishes de novo Pol II pausing during development

While the accessibility of enhancers is dynamically regulated during development, promoters tend to be constitutively accessible and poised for activation by paused Pol II. By studying Lola-I, a Drosophila zinc finger transcription factor, we show here that the promoter state can also be subject to...

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Published inNature communications Vol. 14; no. 1; pp. 5862 - 14
Main Authors Ramalingam, Vivekanandan, Yu, Xinyang, Slaughter, Brian D., Unruh, Jay R., Brennan, Kaelan J., Onyshchenko, Anastasiia, Lange, Jeffrey J., Natarajan, Malini, Buck, Michael, Zeitlinger, Julia
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 21.09.2023
Nature Publishing Group
Nature Portfolio
Subjects
14/32
45/23
49/15
49/88
49/90
49/91
631/208/200
631/208/212
64/24
82/29
82/51
Accessibility
Animals
DNA-directed RNA polymerase
Drosophila - genetics
Embryo, Mammalian
Embryogenesis
Embryonic Development
Embryonic growth stage
Enhancers
Gene expression
Humanities and Social Sciences
multidisciplinary
Nucleosomes
Nucleosomes - genetics
Promoter Regions, Genetic - genetics
Promoters
RNA polymerase
RNA polymerase II
RNA Polymerase II - genetics
Science
Science (multidisciplinary)
Zinc finger proteins
Online AccessGet full text
ISSN2041-1723
2041-1723
DOI10.1038/s41467-023-41408-1

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Abstract While the accessibility of enhancers is dynamically regulated during development, promoters tend to be constitutively accessible and poised for activation by paused Pol II. By studying Lola-I, a Drosophila zinc finger transcription factor, we show here that the promoter state can also be subject to developmental regulation independently of gene activation. Lola-I is ubiquitously expressed at the end of embryogenesis and causes its target promoters to become accessible and acquire paused Pol II throughout the embryo. This promoter transition is required but not sufficient for tissue-specific target gene activation. Lola-I mediates this function by depleting promoter nucleosomes, similar to the action of pioneer factors at enhancers. These results uncover a level of regulation for promoters that is normally found at enhancers and reveal a mechanism for the de novo establishment of paused Pol II at promoters. Gene promoters are very often poised for expression by paused RNA polymerase II. Here, Ramalingam et al., identify a mechanism for the de novo establishment of paused Pol II at promoters and study its effects on expression.
AbstractList While the accessibility of enhancers is dynamically regulated during development, promoters tend to be constitutively accessible and poised for activation by paused Pol II. By studying Lola-I, a Drosophila zinc finger transcription factor, we show here that the promoter state can also be subject to developmental regulation independently of gene activation. Lola-I is ubiquitously expressed at the end of embryogenesis and causes its target promoters to become accessible and acquire paused Pol II throughout the embryo. This promoter transition is required but not sufficient for tissue-specific target gene activation. Lola-I mediates this function by depleting promoter nucleosomes, similar to the action of pioneer factors at enhancers. These results uncover a level of regulation for promoters that is normally found at enhancers and reveal a mechanism for the de novo establishment of paused Pol II at promoters.
While the accessibility of enhancers is dynamically regulated during development, promoters tend to be constitutively accessible and poised for activation by paused Pol II. By studying Lola-I, a Drosophila zinc finger transcription factor, we show here that the promoter state can also be subject to developmental regulation independently of gene activation. Lola-I is ubiquitously expressed at the end of embryogenesis and causes its target promoters to become accessible and acquire paused Pol II throughout the embryo. This promoter transition is required but not sufficient for tissue-specific target gene activation. Lola-I mediates this function by depleting promoter nucleosomes, similar to the action of pioneer factors at enhancers. These results uncover a level of regulation for promoters that is normally found at enhancers and reveal a mechanism for the de novo establishment of paused Pol II at promoters. Gene promoters are very often poised for expression by paused RNA polymerase II. Here, Ramalingam et al., identify a mechanism for the de novo establishment of paused Pol II at promoters and study its effects on expression.
While the accessibility of enhancers is dynamically regulated during development, promoters tend to be constitutively accessible and poised for activation by paused Pol II. By studying Lola-I, a Drosophila zinc finger transcription factor, we show here that the promoter state can also be subject to developmental regulation independently of gene activation. Lola-I is ubiquitously expressed at the end of embryogenesis and causes its target promoters to become accessible and acquire paused Pol II throughout the embryo. This promoter transition is required but not sufficient for tissue-specific target gene activation. Lola-I mediates this function by depleting promoter nucleosomes, similar to the action of pioneer factors at enhancers. These results uncover a level of regulation for promoters that is normally found at enhancers and reveal a mechanism for the de novo establishment of paused Pol II at promoters.
Abstract While the accessibility of enhancers is dynamically regulated during development, promoters tend to be constitutively accessible and poised for activation by paused Pol II. By studying Lola-I, a Drosophila zinc finger transcription factor, we show here that the promoter state can also be subject to developmental regulation independently of gene activation. Lola-I is ubiquitously expressed at the end of embryogenesis and causes its target promoters to become accessible and acquire paused Pol II throughout the embryo. This promoter transition is required but not sufficient for tissue-specific target gene activation. Lola-I mediates this function by depleting promoter nucleosomes, similar to the action of pioneer factors at enhancers. These results uncover a level of regulation for promoters that is normally found at enhancers and reveal a mechanism for the de novo establishment of paused Pol II at promoters.
While the accessibility of enhancers is dynamically regulated during development, promoters tend to be constitutively accessible and poised for activation by paused Pol II. By studying Lola-I, a Drosophila zinc finger transcription factor, we show here that the promoter state can also be subject to developmental regulation independently of gene activation. Lola-I is ubiquitously expressed at the end of embryogenesis and causes its target promoters to become accessible and acquire paused Pol II throughout the embryo. This promoter transition is required but not sufficient for tissue-specific target gene activation. Lola-I mediates this function by depleting promoter nucleosomes, similar to the action of pioneer factors at enhancers. These results uncover a level of regulation for promoters that is normally found at enhancers and reveal a mechanism for the de novo establishment of paused Pol II at promoters.Gene promoters are very often poised for expression by paused RNA polymerase II. Here, Ramalingam et al., identify a mechanism for the de novo establishment of paused Pol II at promoters and study its effects on expression.
While the accessibility of enhancers is dynamically regulated during development, promoters tend to be constitutively accessible and poised for activation by paused Pol II. By studying Lola-I, a Drosophila zinc finger transcription factor, we show here that the promoter state can also be subject to developmental regulation independently of gene activation. Lola-I is ubiquitously expressed at the end of embryogenesis and causes its target promoters to become accessible and acquire paused Pol II throughout the embryo. This promoter transition is required but not sufficient for tissue-specific target gene activation. Lola-I mediates this function by depleting promoter nucleosomes, similar to the action of pioneer factors at enhancers. These results uncover a level of regulation for promoters that is normally found at enhancers and reveal a mechanism for the de novo establishment of paused Pol II at promoters.While the accessibility of enhancers is dynamically regulated during development, promoters tend to be constitutively accessible and poised for activation by paused Pol II. By studying Lola-I, a Drosophila zinc finger transcription factor, we show here that the promoter state can also be subject to developmental regulation independently of gene activation. Lola-I is ubiquitously expressed at the end of embryogenesis and causes its target promoters to become accessible and acquire paused Pol II throughout the embryo. This promoter transition is required but not sufficient for tissue-specific target gene activation. Lola-I mediates this function by depleting promoter nucleosomes, similar to the action of pioneer factors at enhancers. These results uncover a level of regulation for promoters that is normally found at enhancers and reveal a mechanism for the de novo establishment of paused Pol II at promoters.
ArticleNumber 5862
Author Lange, Jeffrey J.
Unruh, Jay R.
Natarajan, Malini
Brennan, Kaelan J.
Onyshchenko, Anastasiia
Ramalingam, Vivekanandan
Zeitlinger, Julia
Buck, Michael
Yu, Xinyang
Slaughter, Brian D.
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PublicationDateYYYYMMDD 2023-09-21
PublicationDate_xml – month: 09
  year: 2023
  text: 2023-09-21
  day: 21
PublicationDecade 2020
PublicationPlace London
PublicationPlace_xml – name: London
– name: England
PublicationTitle Nature communications
PublicationTitleAbbrev Nat Commun
PublicationTitleAlternate Nat Commun
PublicationYear 2023
Publisher Nature Publishing Group UK
Nature Publishing Group
Nature Portfolio
Publisher_xml – name: Nature Publishing Group UK
– name: Nature Publishing Group
– name: Nature Portfolio
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  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg2522
– volume: 54
  start-page: 367
  year: 2020
  ident: 41408_CR9
  publication-title: Annu. Rev. Genet.
  doi: 10.1146/annurev-genet-030220-015007
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Snippet While the accessibility of enhancers is dynamically regulated during development, promoters tend to be constitutively accessible and poised for activation by...
Abstract While the accessibility of enhancers is dynamically regulated during development, promoters tend to be constitutively accessible and poised for...
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SubjectTerms 14/32
45/23
49/15
49/88
49/90
49/91
631/208/200
631/208/212
64/24
82/29
82/51
Accessibility
Animals
DNA-directed RNA polymerase
Drosophila - genetics
Embryo, Mammalian
Embryogenesis
Embryonic Development
Embryonic growth stage
Enhancers
Gene expression
Humanities and Social Sciences
multidisciplinary
Nucleosomes
Nucleosomes - genetics
Promoter Regions, Genetic - genetics
Promoters
RNA polymerase
RNA polymerase II
RNA Polymerase II - genetics
Science
Science (multidisciplinary)
Zinc finger proteins
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Title Lola-I is a promoter pioneer factor that establishes de novo Pol II pausing during development
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