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The Evolution of Epigenetic Regulators CTCF and BORIS/CTCFL in Amniotes

CTCF is an essential, ubiquitously expressed DNA-binding protein responsible for insulator function, nuclear architecture, and transcriptional control within vertebrates. The gene CTCF was proposed to have duplicated in early mammals, giving rise to a paralogue called “brother of regulator of imprin...

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Autores principales: Hore, Timothy A., Deakin, Janine E., Marshall Graves, Jennifer A.
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2008
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2515639/
https://www.ncbi.nlm.nih.gov/pubmed/18769711
http://dx.doi.org/10.1371/journal.pgen.1000169
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author Hore, Timothy A.
Deakin, Janine E.
Marshall Graves, Jennifer A.
author_facet Hore, Timothy A.
Deakin, Janine E.
Marshall Graves, Jennifer A.
author_sort Hore, Timothy A.
collection PubMed
description CTCF is an essential, ubiquitously expressed DNA-binding protein responsible for insulator function, nuclear architecture, and transcriptional control within vertebrates. The gene CTCF was proposed to have duplicated in early mammals, giving rise to a paralogue called “brother of regulator of imprinted sites” (BORIS or CTCFL) with DNA binding capabilities similar to CTCF, but testis-specific expression in humans and mice. CTCF and BORIS have opposite regulatory effects on human cancer-testis genes, the anti-apoptotic BAG1 gene, the insulin-like growth factor 2/H19 imprint control region (IGF2/H19 ICR), and show mutually exclusive expression in humans and mice, suggesting that they are antagonistic epigenetic regulators. We discovered orthologues of BORIS in at least two reptilian species and found traces of its sequence in the chicken genome, implying that the duplication giving rise to BORIS occurred much earlier than previously thought. We analysed the expression of CTCF and BORIS in a range of amniotes by conventional and quantitative PCR. BORIS, as well as CTCF, was found widely expressed in monotremes (platypus) and reptiles (bearded dragon), suggesting redundancy or cooperation between these genes in a common amniote ancestor. However, we discovered that BORIS expression was gonad-specific in marsupials (tammar wallaby) and eutherians (cattle), implying that a functional change occurred in BORIS during the early evolution of therian mammals. Since therians show imprinting of IGF2 but other vertebrate taxa do not, we speculate that CTCF and BORIS evolved specialised functions along with the evolution of imprinting at this and other loci, coinciding with the restriction of BORIS expression to the germline and potential antagonism with CTCF.
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spelling pubmed-25156392008-08-29 The Evolution of Epigenetic Regulators CTCF and BORIS/CTCFL in Amniotes Hore, Timothy A. Deakin, Janine E. Marshall Graves, Jennifer A. PLoS Genet Research Article CTCF is an essential, ubiquitously expressed DNA-binding protein responsible for insulator function, nuclear architecture, and transcriptional control within vertebrates. The gene CTCF was proposed to have duplicated in early mammals, giving rise to a paralogue called “brother of regulator of imprinted sites” (BORIS or CTCFL) with DNA binding capabilities similar to CTCF, but testis-specific expression in humans and mice. CTCF and BORIS have opposite regulatory effects on human cancer-testis genes, the anti-apoptotic BAG1 gene, the insulin-like growth factor 2/H19 imprint control region (IGF2/H19 ICR), and show mutually exclusive expression in humans and mice, suggesting that they are antagonistic epigenetic regulators. We discovered orthologues of BORIS in at least two reptilian species and found traces of its sequence in the chicken genome, implying that the duplication giving rise to BORIS occurred much earlier than previously thought. We analysed the expression of CTCF and BORIS in a range of amniotes by conventional and quantitative PCR. BORIS, as well as CTCF, was found widely expressed in monotremes (platypus) and reptiles (bearded dragon), suggesting redundancy or cooperation between these genes in a common amniote ancestor. However, we discovered that BORIS expression was gonad-specific in marsupials (tammar wallaby) and eutherians (cattle), implying that a functional change occurred in BORIS during the early evolution of therian mammals. Since therians show imprinting of IGF2 but other vertebrate taxa do not, we speculate that CTCF and BORIS evolved specialised functions along with the evolution of imprinting at this and other loci, coinciding with the restriction of BORIS expression to the germline and potential antagonism with CTCF. Public Library of Science 2008-08-29 /pmc/articles/PMC2515639/ /pubmed/18769711 http://dx.doi.org/10.1371/journal.pgen.1000169 Text en Hore et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Hore, Timothy A.
Deakin, Janine E.
Marshall Graves, Jennifer A.
The Evolution of Epigenetic Regulators CTCF and BORIS/CTCFL in Amniotes
title The Evolution of Epigenetic Regulators CTCF and BORIS/CTCFL in Amniotes
title_full The Evolution of Epigenetic Regulators CTCF and BORIS/CTCFL in Amniotes
title_fullStr The Evolution of Epigenetic Regulators CTCF and BORIS/CTCFL in Amniotes
title_full_unstemmed The Evolution of Epigenetic Regulators CTCF and BORIS/CTCFL in Amniotes
title_short The Evolution of Epigenetic Regulators CTCF and BORIS/CTCFL in Amniotes
title_sort evolution of epigenetic regulators ctcf and boris/ctcfl in amniotes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2515639/
https://www.ncbi.nlm.nih.gov/pubmed/18769711
http://dx.doi.org/10.1371/journal.pgen.1000169
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