Genomic positional conservation identifies topological anchor point RNAs linked to developmental loci

The mammalian genome is transcribed into large numbers of long noncoding RNAs (lncRNAs), but the definition of functional lncRNA groups has proven difficult, partly due to their low sequence conservation and lack of identified shared properties. Here we consider promoter conservation and positional...

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Published inGenome Biology Vol. 19; no. 1; p. 32
Main Authors Amaral, Paulo P, Leonardi, Tommaso, Han, Namshik, Viré, Emmanuelle, Gascoigne, Dennis K, Arias-Carrasco, Raúl, Büscher, Magdalena, Pandolfini, Luca, Zhang, Anda, Pluchino, Stefano, Maracaja-Coutinho, Vinicius, Nakaya, Helder I, Hemberg, Martin, Shiekhattar, Ramin, Enright, Anton J, Kouzarides, Tony
Format Journal Article
LanguageEnglish
Published England BioMed Central 15.03.2018
BMC
Subjects
Animals
Base Sequence
Cancer
Cell cycle
Chromatin
Chromatin - chemistry
Chromatin architecture
Conserved Sequence
Development
Gene expression
Gene Expression Regulation, Developmental
Genetic Loci
Genome
Genomes
Humans
lncRNAs
Metastases
Mice
Neoplasms - genetics
Nucleotide Motifs
Nucleotide sequence
Phenotypes
Promoter Regions, Genetic
Ribonucleic acid
RNA
RNA polymerase
RNA, Long Noncoding - chemistry
RNA, Long Noncoding - genetics
RNA-binding protein
Stem cells
Topology
Transcription factors
Transcription Factors - genetics
Zinc finger
Zinc finger proteins
Chromatin architecture
lncRNAs
Development
Topology
Zinc finger
Cancer
Online AccessGet full text

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Abstract The mammalian genome is transcribed into large numbers of long noncoding RNAs (lncRNAs), but the definition of functional lncRNA groups has proven difficult, partly due to their low sequence conservation and lack of identified shared properties. Here we consider promoter conservation and positional conservation as indicators of functional commonality. We identify 665 conserved lncRNA promoters in mouse and human that are preserved in genomic position relative to orthologous coding genes. These positionally conserved lncRNA genes are primarily associated with developmental transcription factor loci with which they are coexpressed in a tissue-specific manner. Over half of positionally conserved RNAs in this set are linked to chromatin organization structures, overlapping binding sites for the CTCF chromatin organiser and located at chromatin loop anchor points and borders of topologically associating domains (TADs). We define these RNAs as topological anchor point RNAs (tapRNAs). Characterization of these noncoding RNAs and their associated coding genes shows that they are functionally connected: they regulate each other's expression and influence the metastatic phenotype of cancer cells in vitro in a similar fashion. Furthermore, we find that tapRNAs contain conserved sequence domains that are enriched in motifs for zinc finger domain-containing RNA-binding proteins and transcription factors, whose binding sites are found mutated in cancers. This work leverages positional conservation to identify lncRNAs with potential importance in genome organization, development and disease. The evidence that many developmental transcription factors are physically and functionally connected to lncRNAs represents an exciting stepping-stone to further our understanding of genome regulation.
AbstractList Abstract Background The mammalian genome is transcribed into large numbers of long noncoding RNAs (lncRNAs), but the definition of functional lncRNA groups has proven difficult, partly due to their low sequence conservation and lack of identified shared properties. Here we consider promoter conservation and positional conservation as indicators of functional commonality. Results We identify 665 conserved lncRNA promoters in mouse and human that are preserved in genomic position relative to orthologous coding genes. These positionally conserved lncRNA genes are primarily associated with developmental transcription factor loci with which they are coexpressed in a tissue-specific manner. Over half of positionally conserved RNAs in this set are linked to chromatin organization structures, overlapping binding sites for the CTCF chromatin organiser and located at chromatin loop anchor points and borders of topologically associating domains (TADs). We define these RNAs as topological anchor point RNAs (tapRNAs). Characterization of these noncoding RNAs and their associated coding genes shows that they are functionally connected: they regulate each other’s expression and influence the metastatic phenotype of cancer cells in vitro in a similar fashion. Furthermore, we find that tapRNAs contain conserved sequence domains that are enriched in motifs for zinc finger domain-containing RNA-binding proteins and transcription factors, whose binding sites are found mutated in cancers. Conclusions This work leverages positional conservation to identify lncRNAs with potential importance in genome organization, development and disease. The evidence that many developmental transcription factors are physically and functionally connected to lncRNAs represents an exciting stepping-stone to further our understanding of genome regulation.
BACKGROUNDThe mammalian genome is transcribed into large numbers of long noncoding RNAs (lncRNAs), but the definition of functional lncRNA groups has proven difficult, partly due to their low sequence conservation and lack of identified shared properties. Here we consider promoter conservation and positional conservation as indicators of functional commonality.RESULTSWe identify 665 conserved lncRNA promoters in mouse and human that are preserved in genomic position relative to orthologous coding genes. These positionally conserved lncRNA genes are primarily associated with developmental transcription factor loci with which they are coexpressed in a tissue-specific manner. Over half of positionally conserved RNAs in this set are linked to chromatin organization structures, overlapping binding sites for the CTCF chromatin organiser and located at chromatin loop anchor points and borders of topologically associating domains (TADs). We define these RNAs as topological anchor point RNAs (tapRNAs). Characterization of these noncoding RNAs and their associated coding genes shows that they are functionally connected: they regulate each other's expression and influence the metastatic phenotype of cancer cells in vitro in a similar fashion. Furthermore, we find that tapRNAs contain conserved sequence domains that are enriched in motifs for zinc finger domain-containing RNA-binding proteins and transcription factors, whose binding sites are found mutated in cancers.CONCLUSIONSThis work leverages positional conservation to identify lncRNAs with potential importance in genome organization, development and disease. The evidence that many developmental transcription factors are physically and functionally connected to lncRNAs represents an exciting stepping-stone to further our understanding of genome regulation.
Background The mammalian genome is transcribed into large numbers of long noncoding RNAs (lncRNAs), but the definition of functional lncRNA groups has proven difficult, partly due to their low sequence conservation and lack of identified shared properties. Here we consider promoter conservation and positional conservation as indicators of functional commonality. Results We identify 665 conserved lncRNA promoters in mouse and human that are preserved in genomic position relative to orthologous coding genes. These positionally conserved lncRNA genes are primarily associated with developmental transcription factor loci with which they are coexpressed in a tissue-specific manner. Over half of positionally conserved RNAs in this set are linked to chromatin organization structures, overlapping binding sites for the CTCF chromatin organiser and located at chromatin loop anchor points and borders of topologically associating domains (TADs). We define these RNAs as topological anchor point RNAs (tapRNAs). Characterization of these noncoding RNAs and their associated coding genes shows that they are functionally connected: they regulate each other’s expression and influence the metastatic phenotype of cancer cells in vitro in a similar fashion. Furthermore, we find that tapRNAs contain conserved sequence domains that are enriched in motifs for zinc finger domain-containing RNA-binding proteins and transcription factors, whose binding sites are found mutated in cancers. Conclusions This work leverages positional conservation to identify lncRNAs with potential importance in genome organization, development and disease. The evidence that many developmental transcription factors are physically and functionally connected to lncRNAs represents an exciting stepping-stone to further our understanding of genome regulation.
The mammalian genome is transcribed into large numbers of long noncoding RNAs (lncRNAs), but the definition of functional lncRNA groups has proven difficult, partly due to their low sequence conservation and lack of identified shared properties. Here we consider promoter conservation and positional conservation as indicators of functional commonality. We identify 665 conserved lncRNA promoters in mouse and human that are preserved in genomic position relative to orthologous coding genes. These positionally conserved lncRNA genes are primarily associated with developmental transcription factor loci with which they are coexpressed in a tissue-specific manner. Over half of positionally conserved RNAs in this set are linked to chromatin organization structures, overlapping binding sites for the CTCF chromatin organiser and located at chromatin loop anchor points and borders of topologically associating domains (TADs). We define these RNAs as topological anchor point RNAs (tapRNAs). Characterization of these noncoding RNAs and their associated coding genes shows that they are functionally connected: they regulate each other's expression and influence the metastatic phenotype of cancer cells in vitro in a similar fashion. Furthermore, we find that tapRNAs contain conserved sequence domains that are enriched in motifs for zinc finger domain-containing RNA-binding proteins and transcription factors, whose binding sites are found mutated in cancers. This work leverages positional conservation to identify lncRNAs with potential importance in genome organization, development and disease. The evidence that many developmental transcription factors are physically and functionally connected to lncRNAs represents an exciting stepping-stone to further our understanding of genome regulation.
ArticleNumber 32
Author Shiekhattar, Ramin
Viré, Emmanuelle
Enright, Anton J
Maracaja-Coutinho, Vinicius
Arias-Carrasco, Raúl
Pandolfini, Luca
Gascoigne, Dennis K
Zhang, Anda
Nakaya, Helder I
Kouzarides, Tony
Leonardi, Tommaso
Hemberg, Martin
Büscher, Magdalena
Amaral, Paulo P
Han, Namshik
Pluchino, Stefano
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Issue 1
Keywords Chromatin architecture
lncRNAs
Development
Topology
Zinc finger
Cancer
Language English
License Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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Snippet The mammalian genome is transcribed into large numbers of long noncoding RNAs (lncRNAs), but the definition of functional lncRNA groups has proven difficult,...
Background The mammalian genome is transcribed into large numbers of long noncoding RNAs (lncRNAs), but the definition of functional lncRNA groups has proven...
BACKGROUNDThe mammalian genome is transcribed into large numbers of long noncoding RNAs (lncRNAs), but the definition of functional lncRNA groups has proven...
Abstract Background The mammalian genome is transcribed into large numbers of long noncoding RNAs (lncRNAs), but the definition of functional lncRNA groups has...
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StartPage 32
SubjectTerms Animals
Base Sequence
Cancer
Cell cycle
Chromatin
Chromatin - chemistry
Chromatin architecture
Conserved Sequence
Development
Gene expression
Gene Expression Regulation, Developmental
Genetic Loci
Genome
Genomes
Humans
lncRNAs
Metastases
Mice
Neoplasms - genetics
Nucleotide Motifs
Nucleotide sequence
Phenotypes
Promoter Regions, Genetic
Ribonucleic acid
RNA
RNA polymerase
RNA, Long Noncoding - chemistry
RNA, Long Noncoding - genetics
RNA-binding protein
Stem cells
Topology
Transcription factors
Transcription Factors - genetics
Zinc finger
Zinc finger proteins
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Title Genomic positional conservation identifies topological anchor point RNAs linked to developmental loci
URI https://www.ncbi.nlm.nih.gov/pubmed/29540241
https://www.proquest.com/docview/2207152150/abstract/
https://search.proquest.com/docview/2014144815
https://pubmed.ncbi.nlm.nih.gov/PMC5853149
https://doaj.org/article/ba55c45d1fc5416e815d876c54e498ef
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