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A Mammalian Conserved Element Derived from SINE Displays Enhancer Properties Recapitulating Satb2 Expression in Early-Born Callosal Projection Neurons

Short interspersed repetitive elements (SINEs) are highly repeated sequences that account for a significant proportion of many eukaryotic genomes and are usually considered “junk DNA”. However, we previously discovered that many AmnSINE1 loci are evolutionarily conserved across mammalian genomes, su...

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Autores principales: Tashiro, Kensuke, Teissier, Anne, Kobayashi, Naoki, Nakanishi, Akiko, Sasaki, Takeshi, Yan, Kuo, Tarabykin, Victor, Vigier, Lisa, Sumiyama, Kenta, Hirakawa, Mika, Nishihara, Hidenori, Pierani, Alessandra, Okada, Norihiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3234267/
https://www.ncbi.nlm.nih.gov/pubmed/22174821
http://dx.doi.org/10.1371/journal.pone.0028497
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author Tashiro, Kensuke
Teissier, Anne
Kobayashi, Naoki
Nakanishi, Akiko
Sasaki, Takeshi
Yan, Kuo
Tarabykin, Victor
Vigier, Lisa
Sumiyama, Kenta
Hirakawa, Mika
Nishihara, Hidenori
Pierani, Alessandra
Okada, Norihiro
author_facet Tashiro, Kensuke
Teissier, Anne
Kobayashi, Naoki
Nakanishi, Akiko
Sasaki, Takeshi
Yan, Kuo
Tarabykin, Victor
Vigier, Lisa
Sumiyama, Kenta
Hirakawa, Mika
Nishihara, Hidenori
Pierani, Alessandra
Okada, Norihiro
author_sort Tashiro, Kensuke
collection PubMed
description Short interspersed repetitive elements (SINEs) are highly repeated sequences that account for a significant proportion of many eukaryotic genomes and are usually considered “junk DNA”. However, we previously discovered that many AmnSINE1 loci are evolutionarily conserved across mammalian genomes, suggesting that they may have acquired significant functions involved in controlling mammalian-specific traits. Notably, we identified the AS021 SINE locus, located 390 kbp upstream of Satb2. Using transgenic mice, we showed that this SINE displays specific enhancer activity in the developing cerebral cortex. The transcription factor Satb2 is expressed by cortical neurons extending axons through the corpus callosum and is a determinant of callosal versus subcortical projection. Mouse mutants reveal a crucial function for Sabt2 in corpus callosum formation. In this study, we compared the enhancer activity of the AS021 locus with Satb2 expression during telencephalic development in the mouse. First, we showed that the AS021 enhancer is specifically activated in early-born Satb2(+) neurons. Second, we demonstrated that the activity of the AS021 enhancer recapitulates the expression of Satb2 at later embryonic and postnatal stages in deep-layer but not superficial-layer neurons, suggesting the possibility that the expression of Satb2 in these two subpopulations of cortical neurons is under genetically distinct transcriptional control. Third, we showed that the AS021 enhancer is activated in neurons projecting through the corpus callosum, as described for Satb2(+) neurons. Notably, AS021 drives specific expression in axons crossing through the ventral (TAG1(−)/NPY(+)) portion of the corpus callosum, confirming that it is active in a subpopulation of callosal neurons. These data suggest that exaptation of the AS021 SINE locus might be involved in enhancement of Satb2 expression, leading to the establishment of interhemispheric communication via the corpus callosum, a eutherian-specific brain structure.
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spelling pubmed-32342672011-12-15 A Mammalian Conserved Element Derived from SINE Displays Enhancer Properties Recapitulating Satb2 Expression in Early-Born Callosal Projection Neurons Tashiro, Kensuke Teissier, Anne Kobayashi, Naoki Nakanishi, Akiko Sasaki, Takeshi Yan, Kuo Tarabykin, Victor Vigier, Lisa Sumiyama, Kenta Hirakawa, Mika Nishihara, Hidenori Pierani, Alessandra Okada, Norihiro PLoS One Research Article Short interspersed repetitive elements (SINEs) are highly repeated sequences that account for a significant proportion of many eukaryotic genomes and are usually considered “junk DNA”. However, we previously discovered that many AmnSINE1 loci are evolutionarily conserved across mammalian genomes, suggesting that they may have acquired significant functions involved in controlling mammalian-specific traits. Notably, we identified the AS021 SINE locus, located 390 kbp upstream of Satb2. Using transgenic mice, we showed that this SINE displays specific enhancer activity in the developing cerebral cortex. The transcription factor Satb2 is expressed by cortical neurons extending axons through the corpus callosum and is a determinant of callosal versus subcortical projection. Mouse mutants reveal a crucial function for Sabt2 in corpus callosum formation. In this study, we compared the enhancer activity of the AS021 locus with Satb2 expression during telencephalic development in the mouse. First, we showed that the AS021 enhancer is specifically activated in early-born Satb2(+) neurons. Second, we demonstrated that the activity of the AS021 enhancer recapitulates the expression of Satb2 at later embryonic and postnatal stages in deep-layer but not superficial-layer neurons, suggesting the possibility that the expression of Satb2 in these two subpopulations of cortical neurons is under genetically distinct transcriptional control. Third, we showed that the AS021 enhancer is activated in neurons projecting through the corpus callosum, as described for Satb2(+) neurons. Notably, AS021 drives specific expression in axons crossing through the ventral (TAG1(−)/NPY(+)) portion of the corpus callosum, confirming that it is active in a subpopulation of callosal neurons. These data suggest that exaptation of the AS021 SINE locus might be involved in enhancement of Satb2 expression, leading to the establishment of interhemispheric communication via the corpus callosum, a eutherian-specific brain structure. Public Library of Science 2011-12-08 /pmc/articles/PMC3234267/ /pubmed/22174821 http://dx.doi.org/10.1371/journal.pone.0028497 Text en Tashiro 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
Tashiro, Kensuke
Teissier, Anne
Kobayashi, Naoki
Nakanishi, Akiko
Sasaki, Takeshi
Yan, Kuo
Tarabykin, Victor
Vigier, Lisa
Sumiyama, Kenta
Hirakawa, Mika
Nishihara, Hidenori
Pierani, Alessandra
Okada, Norihiro
A Mammalian Conserved Element Derived from SINE Displays Enhancer Properties Recapitulating Satb2 Expression in Early-Born Callosal Projection Neurons
title A Mammalian Conserved Element Derived from SINE Displays Enhancer Properties Recapitulating Satb2 Expression in Early-Born Callosal Projection Neurons
title_full A Mammalian Conserved Element Derived from SINE Displays Enhancer Properties Recapitulating Satb2 Expression in Early-Born Callosal Projection Neurons
title_fullStr A Mammalian Conserved Element Derived from SINE Displays Enhancer Properties Recapitulating Satb2 Expression in Early-Born Callosal Projection Neurons
title_full_unstemmed A Mammalian Conserved Element Derived from SINE Displays Enhancer Properties Recapitulating Satb2 Expression in Early-Born Callosal Projection Neurons
title_short A Mammalian Conserved Element Derived from SINE Displays Enhancer Properties Recapitulating Satb2 Expression in Early-Born Callosal Projection Neurons
title_sort mammalian conserved element derived from sine displays enhancer properties recapitulating satb2 expression in early-born callosal projection neurons
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3234267/
https://www.ncbi.nlm.nih.gov/pubmed/22174821
http://dx.doi.org/10.1371/journal.pone.0028497
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