The long non‐coding RNA Paupar promotes KAP1‐dependent chromatin changes and regulates olfactory bulb neurogenesis
Many long non‐coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their in vivo roles and mechanisms of action remain poorly understood. Paupar , a CNS‐expressed lncRNA, controls neuroblastoma cell growth by binding and modulating the activity of transcriptional...
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| Vydáno v: | The EMBO journal Ročník 37; číslo 10 |
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| Hlavní autoři: | , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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London
Nature Publishing Group UK
15.05.2018
Springer Nature B.V John Wiley and Sons Inc |
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| ISSN: | 0261-4189, 1460-2075, 1460-2075 |
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| Abstract | Many long non‐coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their
in vivo
roles and mechanisms of action remain poorly understood.
Paupar
, a CNS‐expressed lncRNA, controls neuroblastoma cell growth by binding and modulating the activity of transcriptional regulatory elements in a genome‐wide manner. We show here that the
Paupar
lncRNA directly binds KAP1, an essential epigenetic regulatory protein, and thereby regulates the expression of shared target genes important for proliferation and neuronal differentiation.
Paupar
promotes KAP1 chromatin occupancy and H3K9me3 deposition at a subset of distal targets, through the formation of a ribonucleoprotein complex containing
Paupar
, KAP1 and the PAX6 transcription factor.
Paupar
‐KAP1 genome‐wide co‐occupancy reveals a fourfold enrichment of overlap between
Paupar
and KAP1 bound sequences, the majority of which also appear to associate with PAX6. Furthermore, both
Paupar
and
Kap1
loss‐of‐function
in vivo
disrupt olfactory bulb neurogenesis. These observations provide important conceptual insights into the
trans
‐acting modes of lncRNA‐mediated epigenetic regulation and the mechanisms of KAP1 genomic recruitment, and identify
Paupar
and
Kap1
as regulators of neurogenesis
in vivo
.
Synopsis
The formation of an RNP complex containing a long non‐coding RNA (lncRNA), a chromatin regulator and transcription factor illustrates how a single nuclear lncRNA can regulate transcription of multiple target genes in
trans
.
The CNS‐expressed lncRNA
Paupar
interacts with the TRIM28/TIF1/KAP1 chromatin regulatory protein.
Paupar
acts in
trans
to promote KAP1 chromatin occupancy and H3K9me3 deposition at a subset of bound target sites.
Paupar
regulation in
trans
requires the formation of a ribonucleoprotein complex containing
Paupar
, KAP1 and non‐KRAB‐ZNF transcription factors such as PAX6.
Paupar
and KAP1 function as regulators of olfactory bulb neurogenesis
in vivo
.
Graphical Abstract
Complex formation between a long non‐coding RNA (lncRNA), a chromatin regulator and transcription factor illustrates how nuclear lncRNAs can regulate transcription in
trans
. |
|---|---|
| AbstractList | Many long non‐coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their
in vivo
roles and mechanisms of action remain poorly understood.
Paupar
, a CNS‐expressed lncRNA, controls neuroblastoma cell growth by binding and modulating the activity of transcriptional regulatory elements in a genome‐wide manner. We show here that the
Paupar
lncRNA directly binds KAP1, an essential epigenetic regulatory protein, and thereby regulates the expression of shared target genes important for proliferation and neuronal differentiation.
Paupar
promotes KAP1 chromatin occupancy and H3K9me3 deposition at a subset of distal targets, through the formation of a ribonucleoprotein complex containing
Paupar
, KAP1 and the PAX6 transcription factor.
Paupar
‐KAP1 genome‐wide co‐occupancy reveals a fourfold enrichment of overlap between
Paupar
and KAP1 bound sequences, the majority of which also appear to associate with PAX6. Furthermore, both
Paupar
and
Kap1
loss‐of‐function
in vivo
disrupt olfactory bulb neurogenesis. These observations provide important conceptual insights into the
trans
‐acting modes of lncRNA‐mediated epigenetic regulation and the mechanisms of KAP1 genomic recruitment, and identify
Paupar
and
Kap1
as regulators of neurogenesis
in vivo
.
Synopsis
The formation of an RNP complex containing a long non‐coding RNA (lncRNA), a chromatin regulator and transcription factor illustrates how a single nuclear lncRNA can regulate transcription of multiple target genes in
trans
.
The CNS‐expressed lncRNA
Paupar
interacts with the TRIM28/TIF1/KAP1 chromatin regulatory protein.
Paupar
acts in
trans
to promote KAP1 chromatin occupancy and H3K9me3 deposition at a subset of bound target sites.
Paupar
regulation in
trans
requires the formation of a ribonucleoprotein complex containing
Paupar
, KAP1 and non‐KRAB‐ZNF transcription factors such as PAX6.
Paupar
and KAP1 function as regulators of olfactory bulb neurogenesis
in vivo
.
Graphical Abstract
Complex formation between a long non‐coding RNA (lncRNA), a chromatin regulator and transcription factor illustrates how nuclear lncRNAs can regulate transcription in
trans
. Many long non‐coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their in vivo roles and mechanisms of action remain poorly understood. Paupar, a CNS‐expressed lncRNA, controls neuroblastoma cell growth by binding and modulating the activity of transcriptional regulatory elements in a genome‐wide manner. We show here that the Paupar lncRNA directly binds KAP1, an essential epigenetic regulatory protein, and thereby regulates the expression of shared target genes important for proliferation and neuronal differentiation. Paupar promotes KAP1 chromatin occupancy and H3K9me3 deposition at a subset of distal targets, through the formation of a ribonucleoprotein complex containing Paupar, KAP1 and the PAX6 transcription factor. Paupar‐KAP1 genome‐wide co‐occupancy reveals a fourfold enrichment of overlap between Paupar and KAP1 bound sequences, the majority of which also appear to associate with PAX6. Furthermore, both Paupar and Kap1 loss‐of‐function in vivo disrupt olfactory bulb neurogenesis. These observations provide important conceptual insights into the trans‐acting modes of lncRNA‐mediated epigenetic regulation and the mechanisms of KAP1 genomic recruitment, and identify Paupar and Kap1 as regulators of neurogenesis in vivo. Many long non‐coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their in vivo roles and mechanisms of action remain poorly understood. Paupar, a CNS‐expressed lncRNA, controls neuroblastoma cell growth by binding and modulating the activity of transcriptional regulatory elements in a genome‐wide manner. We show here that the Paupar lncRNA directly binds KAP1, an essential epigenetic regulatory protein, and thereby regulates the expression of shared target genes important for proliferation and neuronal differentiation. Paupar promotes KAP1 chromatin occupancy and H3K9me3 deposition at a subset of distal targets, through the formation of a ribonucleoprotein complex containing Paupar, KAP1 and the PAX6 transcription factor. Paupar‐KAP1 genome‐wide co‐occupancy reveals a fourfold enrichment of overlap between Paupar and KAP1 bound sequences, the majority of which also appear to associate with PAX6. Furthermore, both Paupar and Kap1 loss‐of‐function in vivo disrupt olfactory bulb neurogenesis. These observations provide important conceptual insights into the trans‐acting modes of lncRNA‐mediated epigenetic regulation and the mechanisms of KAP1 genomic recruitment, and identify Paupar and Kap1 as regulators of neurogenesis in vivo. Synopsis The formation of an RNP complex containing a long non‐coding RNA (lncRNA), a chromatin regulator and transcription factor illustrates how a single nuclear lncRNA can regulate transcription of multiple target genes in trans. The CNS‐expressed lncRNA Paupar interacts with the TRIM28/TIF1/KAP1 chromatin regulatory protein. Paupar acts in trans to promote KAP1 chromatin occupancy and H3K9me3 deposition at a subset of bound target sites. Paupar regulation in trans requires the formation of a ribonucleoprotein complex containing Paupar, KAP1 and non‐KRAB‐ZNF transcription factors such as PAX6. Paupar and KAP1 function as regulators of olfactory bulb neurogenesis in vivo. Complex formation between a long non‐coding RNA (lncRNA), a chromatin regulator and transcription factor illustrates how nuclear lncRNAs can regulate transcription in trans. Many long non‐coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their in vivo roles and mechanisms of action remain poorly understood. Paupar, a CNS‐expressed lncRNA, controls neuroblastoma cell growth by binding and modulating the activity of transcriptional regulatory elements in a genome‐wide manner. We show here that the Paupar lncRNA directly binds KAP1, an essential epigenetic regulatory protein, and thereby regulates the expression of shared target genes important for proliferation and neuronal differentiation. Paupar promotes KAP1 chromatin occupancy and H3K9me3 deposition at a subset of distal targets, through the formation of a ribonucleoprotein complex containing Paupar, KAP1 and the PAX6 transcription factor. Paupar‐KAP1 genome‐wide co‐occupancy reveals a fourfold enrichment of overlap between Paupar and KAP1 bound sequences, the majority of which also appear to associate with PAX6. Furthermore, both Paupar and Kap1 loss‐of‐function in vivo disrupt olfactory bulb neurogenesis. These observations provide important conceptual insights into the trans‐acting modes of lncRNA‐mediated epigenetic regulation and the mechanisms of KAP1 genomic recruitment, and identify Paupar and Kap1 as regulators of neurogenesis in vivo. Many long non-coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their roles and mechanisms of action remain poorly understood. , a CNS-expressed lncRNA, controls neuroblastoma cell growth by binding and modulating the activity of transcriptional regulatory elements in a genome-wide manner. We show here that the lncRNA directly binds KAP1, an essential epigenetic regulatory protein, and thereby regulates the expression of shared target genes important for proliferation and neuronal differentiation. promotes KAP1 chromatin occupancy and H3K9me3 deposition at a subset of distal targets, through the formation of a ribonucleoprotein complex containing , KAP1 and the PAX6 transcription factor. -KAP1 genome-wide co-occupancy reveals a fourfold enrichment of overlap between and KAP1 bound sequences, the majority of which also appear to associate with PAX6. Furthermore, both and loss-of-function disrupt olfactory bulb neurogenesis. These observations provide important conceptual insights into the -acting modes of lncRNA-mediated epigenetic regulation and the mechanisms of KAP1 genomic recruitment, and identify and as regulators of neurogenesis . Many long non-coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their in vivo roles and mechanisms of action remain poorly understood. Paupar, a CNS-expressed lncRNA, controls neuroblastoma cell growth by binding and modulating the activity of transcriptional regulatory elements in a genome-wide manner. We show here that the Paupar lncRNA directly binds KAP1, an essential epigenetic regulatory protein, and thereby regulates the expression of shared target genes important for proliferation and neuronal differentiation. Paupar promotes KAP1 chromatin occupancy and H3K9me3 deposition at a subset of distal targets, through the formation of a ribonucleoprotein complex containing Paupar, KAP1 and the PAX6 transcription factor. Paupar-KAP1 genome-wide co-occupancy reveals a fourfold enrichment of overlap between Paupar and KAP1 bound sequences, the majority of which also appear to associate with PAX6. Furthermore, both Paupar and Kap1 loss-of-function in vivo disrupt olfactory bulb neurogenesis. These observations provide important conceptual insights into the trans-acting modes of lncRNA-mediated epigenetic regulation and the mechanisms of KAP1 genomic recruitment, and identify Paupar and Kap1 as regulators of neurogenesis in vivo.Many long non-coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their in vivo roles and mechanisms of action remain poorly understood. Paupar, a CNS-expressed lncRNA, controls neuroblastoma cell growth by binding and modulating the activity of transcriptional regulatory elements in a genome-wide manner. We show here that the Paupar lncRNA directly binds KAP1, an essential epigenetic regulatory protein, and thereby regulates the expression of shared target genes important for proliferation and neuronal differentiation. Paupar promotes KAP1 chromatin occupancy and H3K9me3 deposition at a subset of distal targets, through the formation of a ribonucleoprotein complex containing Paupar, KAP1 and the PAX6 transcription factor. Paupar-KAP1 genome-wide co-occupancy reveals a fourfold enrichment of overlap between Paupar and KAP1 bound sequences, the majority of which also appear to associate with PAX6. Furthermore, both Paupar and Kap1 loss-of-function in vivo disrupt olfactory bulb neurogenesis. These observations provide important conceptual insights into the trans-acting modes of lncRNA-mediated epigenetic regulation and the mechanisms of KAP1 genomic recruitment, and identify Paupar and Kap1 as regulators of neurogenesis in vivo. |
| Author | Pavlaki, Ioanna Woodcock, Dan J Alammari, Farah Szele, Francis G Sirey, Tamara Ponting, Chris P Vance, Keith W Sun, Bin Lee, Sheena Clark, Neil |
| AuthorAffiliation | 4 Warwick Systems Biology Centre University of Warwick Coventry UK 2 Department of Physiology, Anatomy and Genetics University of Oxford Oxford UK 3 MRC Human Genetics Unit The Institute of Genetics and Molecular Medicine Western General Hospital University of Edinburgh Edinburgh UK 1 Department of Biology and Biochemistry University of Bath Bath UK |
| AuthorAffiliation_xml | – name: 4 Warwick Systems Biology Centre University of Warwick Coventry UK – name: 3 MRC Human Genetics Unit The Institute of Genetics and Molecular Medicine Western General Hospital University of Edinburgh Edinburgh UK – name: 2 Department of Physiology, Anatomy and Genetics University of Oxford Oxford UK – name: 1 Department of Biology and Biochemistry University of Bath Bath UK |
| Author_xml | – sequence: 1 givenname: Ioanna orcidid: 0000-0003-2514-0977 surname: Pavlaki fullname: Pavlaki, Ioanna organization: Department of Biology and Biochemistry, University of Bath – sequence: 2 givenname: Farah surname: Alammari fullname: Alammari, Farah organization: Department of Physiology, Anatomy and Genetics, University of Oxford – sequence: 3 givenname: Bin surname: Sun fullname: Sun, Bin organization: Department of Physiology, Anatomy and Genetics, University of Oxford – sequence: 4 givenname: Neil surname: Clark fullname: Clark, Neil organization: MRC Human Genetics Unit, The Institute of Genetics and Molecular Medicine, Western General Hospital, University of Edinburgh – sequence: 5 givenname: Tamara surname: Sirey fullname: Sirey, Tamara organization: MRC Human Genetics Unit, The Institute of Genetics and Molecular Medicine, Western General Hospital, University of Edinburgh – sequence: 6 givenname: Sheena surname: Lee fullname: Lee, Sheena organization: Department of Physiology, Anatomy and Genetics, University of Oxford – sequence: 7 givenname: Dan J surname: Woodcock fullname: Woodcock, Dan J organization: Warwick Systems Biology Centre, University of Warwick – sequence: 8 givenname: Chris P surname: Ponting fullname: Ponting, Chris P organization: MRC Human Genetics Unit, The Institute of Genetics and Molecular Medicine, Western General Hospital, University of Edinburgh – sequence: 9 givenname: Francis G surname: Szele fullname: Szele, Francis G organization: Department of Physiology, Anatomy and Genetics, University of Oxford – sequence: 10 givenname: Keith W orcidid: 0000-0002-3411-8213 surname: Vance fullname: Vance, Keith W email: k.w.vance@bath.ac.uk organization: Department of Biology and Biochemistry, University of Bath |
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| Keywords | neurogenesis lncRNA KAP1 chromatin gene regulation |
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| Publisher | Nature Publishing Group UK Springer Nature B.V John Wiley and Sons Inc |
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589 year: 2010 end-page: 595 article-title: Fast and accurate long‐read alignment with Burrows‐Wheeler transform publication-title: Bioinformatics – volume: 20 start-page: 1258 year: 2013 end-page: 1264 article-title: PRC2 binds active promoters and contacts nascent RNAs in embryonic stem cells publication-title: Nat Struct Mol Biol – volume: 286 start-page: 26267 year: 2011 end-page: 26276 article-title: KAP1 protein: an enigmatic master regulator of the genome publication-title: J Biol Chem – volume: 10 start-page: 332 year: 2016 article-title: Traumatic brain injury activation of the adult subventricular zone neurogenic niche publication-title: Front Neurosci – volume: 30 start-page: 2114 year: 2014 end-page: 2120 article-title: Trimmomatic: a flexible trimmer for Illumina sequence data publication-title: Bioinformatics – volume: 5 start-page: e1000617 year: 2009 article-title: Genomic and transcriptional co‐localization of protein‐coding and long non‐coding RNA pairs in the developing brain publication-title: PLoS Genet – volume: 28 start-page: 248 year: 2005 end-page: 254 article-title: Integrating new neurons into the adult olfactory bulb: joining the network, life‐death decisions, and the effects of sensory experience publication-title: Trends Neurosci – volume: 138 start-page: 5333 year: 2011 end-page: 5343 article-title: TRIM28 is required by the mouse KRAB domain protein ZFP568 to control convergent extension and morphogenesis of extra‐embryonic tissues publication-title: Development – volume: 143 start-page: 46 year: 2010 end-page: 58 article-title: Long noncoding RNAs with enhancer‐like function in human cells publication-title: Cell – volume: 3 start-page: e1883 year: 2008 article-title: Efficient electroporation of the postnatal rodent forebrain publication-title: PLoS One – volume: 350 start-page: 548 year: 2011 end-page: 558 article-title: TIF1beta association with HP1 is essential for post‐gastrulation development, but not for Sertoli cell functions during spermatogenesis publication-title: Dev Biol – volume: 31 start-page: 1833 year: 2011 end-page: 1847 article-title: Functional analysis of KAP1 genomic recruitment publication-title: Mol Cell Biol – volume: 500 start-page: 598 year: 2013 end-page: 602 article-title: lncRNA‐dependent mechanisms of androgen‐receptor‐regulated gene activation programs publication-title: Nature – volume: 51 start-page: 156 year: 2013 end-page: 173 article-title: Tandem stem‐loops in roX RNAs act together to mediate X chromosome dosage compensation in publication-title: Mol Cell – volume: 44 start-page: W160 year: 2016 end-page: W165 article-title: deepTools2: a next generation web server for deep‐sequencing data analysis publication-title: Nucleic Acids Res – volume: 44 start-page: 667 year: 2011 end-page: 678 article-title: Genomic maps of long noncoding RNA occupancy reveal principles of RNA‐chromatin interactions publication-title: Mol Cell – volume: 16 start-page: 919 year: 2002 end-page: 932 article-title: SETDB1: a novel KAP‐1‐associated histone H3, lysine 9‐specific methyltransferase that contributes to HP1‐mediated silencing of euchromatic genes by KRAB zinc‐finger proteins publication-title: Genes Dev – volume: 40 start-page: 939 year: 2010 end-page: 953 article-title: Genome‐wide identification of polycomb‐associated RNAs by RIP‐seq publication-title: Mol Cell |
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| Snippet | Many long non‐coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their
in vivo
roles and mechanisms of action remain... Many long non‐coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their in vivo roles and mechanisms of action remain... Many long non-coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their roles and mechanisms of action remain poorly... Many long non‐coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their in vivo roles and mechanisms of action remain... Many long non-coding RNAs (lncRNAs) are expressed during central nervous system (CNS) development, yet their in vivo roles and mechanisms of action remain... |
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| SubjectTerms | Animals Animals, Newborn Cell Cycle Cell Proliferation Cells, Cultured Central nervous system Chromatin Chromatin - genetics Deposition EMBO09 EMBO27 EMBO36 Epigenesis, Genetic Epigenetics Gene expression gene regulation Genes Genomes Genomics KAP1 lncRNA Mice Neural Stem Cells - cytology Neural Stem Cells - metabolism Neuroblastoma Neuroblastoma - genetics Neuroblastoma - metabolism Neuroblastoma - pathology Neurogenesis Non-coding RNA Olfaction Olfactory bulb Olfactory Bulb - cytology Olfactory Bulb - metabolism Pax6 protein PAX6 Transcription Factor - genetics PAX6 Transcription Factor - metabolism Proteins Regulators Regulatory Elements, Transcriptional Regulatory sequences Ribonucleic acid RNA RNA, Long Noncoding - genetics RNA, Long Noncoding - metabolism Transcription factors Tripartite Motif-Containing Protein 28 - genetics Tripartite Motif-Containing Protein 28 - metabolism |
| Title | The long non‐coding RNA Paupar promotes KAP1‐dependent chromatin changes and regulates olfactory bulb neurogenesis |
| URI | https://link.springer.com/article/10.15252/embj.201798219 https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fembj.201798219 https://www.ncbi.nlm.nih.gov/pubmed/29661885 https://www.proquest.com/docview/2047314162 https://www.proquest.com/docview/2026421272 https://pubmed.ncbi.nlm.nih.gov/PMC5978383 |
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