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Female-biased expression of long non-coding RNAs in domains that escape X-inactivation in mouse

BACKGROUND: Sexual dimorphism in brain gene expression has been recognized in several animal species. However, the relevant regulatory mechanisms remain poorly understood. To investigate whether sex-biased gene expression in mammalian brain is globally regulated or locally regulated in diverse brain...

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Autores principales: Reinius, Björn, Shi, Chengxi, Hengshuo, Liu, Sandhu, Kuljeet Singh, Radomska, Katarzyna J, Rosen, Glenn D, Lu, Lu, Kullander, Klas, Williams, Robert W, Jazin, Elena
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3091755/
https://www.ncbi.nlm.nih.gov/pubmed/21047393
http://dx.doi.org/10.1186/1471-2164-11-614
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author Reinius, Björn
Shi, Chengxi
Hengshuo, Liu
Sandhu, Kuljeet Singh
Radomska, Katarzyna J
Rosen, Glenn D
Lu, Lu
Kullander, Klas
Williams, Robert W
Jazin, Elena
author_facet Reinius, Björn
Shi, Chengxi
Hengshuo, Liu
Sandhu, Kuljeet Singh
Radomska, Katarzyna J
Rosen, Glenn D
Lu, Lu
Kullander, Klas
Williams, Robert W
Jazin, Elena
author_sort Reinius, Björn
collection PubMed
description BACKGROUND: Sexual dimorphism in brain gene expression has been recognized in several animal species. However, the relevant regulatory mechanisms remain poorly understood. To investigate whether sex-biased gene expression in mammalian brain is globally regulated or locally regulated in diverse brain structures, and to study the genomic organisation of brain-expressed sex-biased genes, we performed a large scale gene expression analysis of distinct brain regions in adult male and female mice. RESULTS: This study revealed spatial specificity in sex-biased transcription in the mouse brain, and identified 173 sex-biased genes in the striatum; 19 in the neocortex; 12 in the hippocampus and 31 in the eye. Genes located on sex chromosomes were consistently over-represented in all brain regions. Analysis on a subset of genes with sex-bias in more than one tissue revealed Y-encoded male-biased transcripts and X-encoded female-biased transcripts known to escape X-inactivation. In addition, we identified novel coding and non-coding X-linked genes with female-biased expression in multiple tissues. Interestingly, the chromosomal positions of all of the female-biased non-coding genes are in close proximity to protein-coding genes that escape X-inactivation. This defines X-chromosome domains each of which contains a coding and a non-coding female-biased gene. Lack of repressive chromatin marks in non-coding transcribed loci supports the possibility that they escape X-inactivation. Moreover, RNA-DNA combined FISH experiments confirmed the biallelic expression of one such novel domain. CONCLUSION: This study demonstrated that the amount of genes with sex-biased expression varies between individual brain regions in mouse. The sex-biased genes identified are localized on many chromosomes. At the same time, sexually dimorphic gene expression that is common to several parts of the brain is mostly restricted to the sex chromosomes. Moreover, the study uncovered multiple female-biased non-coding genes that are non-randomly co-localized on the X-chromosome with protein-coding genes that escape X-inactivation. This raises the possibility that expression of long non-coding RNAs may play a role in modulating gene expression in domains that escape X-inactivation in mouse.
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spelling pubmed-30917552011-05-11 Female-biased expression of long non-coding RNAs in domains that escape X-inactivation in mouse Reinius, Björn Shi, Chengxi Hengshuo, Liu Sandhu, Kuljeet Singh Radomska, Katarzyna J Rosen, Glenn D Lu, Lu Kullander, Klas Williams, Robert W Jazin, Elena BMC Genomics Research Article BACKGROUND: Sexual dimorphism in brain gene expression has been recognized in several animal species. However, the relevant regulatory mechanisms remain poorly understood. To investigate whether sex-biased gene expression in mammalian brain is globally regulated or locally regulated in diverse brain structures, and to study the genomic organisation of brain-expressed sex-biased genes, we performed a large scale gene expression analysis of distinct brain regions in adult male and female mice. RESULTS: This study revealed spatial specificity in sex-biased transcription in the mouse brain, and identified 173 sex-biased genes in the striatum; 19 in the neocortex; 12 in the hippocampus and 31 in the eye. Genes located on sex chromosomes were consistently over-represented in all brain regions. Analysis on a subset of genes with sex-bias in more than one tissue revealed Y-encoded male-biased transcripts and X-encoded female-biased transcripts known to escape X-inactivation. In addition, we identified novel coding and non-coding X-linked genes with female-biased expression in multiple tissues. Interestingly, the chromosomal positions of all of the female-biased non-coding genes are in close proximity to protein-coding genes that escape X-inactivation. This defines X-chromosome domains each of which contains a coding and a non-coding female-biased gene. Lack of repressive chromatin marks in non-coding transcribed loci supports the possibility that they escape X-inactivation. Moreover, RNA-DNA combined FISH experiments confirmed the biallelic expression of one such novel domain. CONCLUSION: This study demonstrated that the amount of genes with sex-biased expression varies between individual brain regions in mouse. The sex-biased genes identified are localized on many chromosomes. At the same time, sexually dimorphic gene expression that is common to several parts of the brain is mostly restricted to the sex chromosomes. Moreover, the study uncovered multiple female-biased non-coding genes that are non-randomly co-localized on the X-chromosome with protein-coding genes that escape X-inactivation. This raises the possibility that expression of long non-coding RNAs may play a role in modulating gene expression in domains that escape X-inactivation in mouse. BioMed Central 2010-11-03 /pmc/articles/PMC3091755/ /pubmed/21047393 http://dx.doi.org/10.1186/1471-2164-11-614 Text en Copyright ©2010 Reinius et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Reinius, Björn
Shi, Chengxi
Hengshuo, Liu
Sandhu, Kuljeet Singh
Radomska, Katarzyna J
Rosen, Glenn D
Lu, Lu
Kullander, Klas
Williams, Robert W
Jazin, Elena
Female-biased expression of long non-coding RNAs in domains that escape X-inactivation in mouse
title Female-biased expression of long non-coding RNAs in domains that escape X-inactivation in mouse
title_full Female-biased expression of long non-coding RNAs in domains that escape X-inactivation in mouse
title_fullStr Female-biased expression of long non-coding RNAs in domains that escape X-inactivation in mouse
title_full_unstemmed Female-biased expression of long non-coding RNAs in domains that escape X-inactivation in mouse
title_short Female-biased expression of long non-coding RNAs in domains that escape X-inactivation in mouse
title_sort female-biased expression of long non-coding rnas in domains that escape x-inactivation in mouse
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3091755/
https://www.ncbi.nlm.nih.gov/pubmed/21047393
http://dx.doi.org/10.1186/1471-2164-11-614
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