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Article ; Online: Gene regulation in time and space during X-chromosome inactivation.

Loda, Agnese / Collombet, Samuel / Heard, Edith

2022 Volume 23, Issue 4, Page(s) 231–249

Abstract: X-chromosome inactivation (XCI) is the epigenetic mechanism that ensures X-linked dosage compensation between cells of females (XX karyotype) and males (XY). XCI is essential for female embryos to survive through development and requires the accurate ... ...

Abstract	X-chromosome inactivation (XCI) is the epigenetic mechanism that ensures X-linked dosage compensation between cells of females (XX karyotype) and males (XY). XCI is essential for female embryos to survive through development and requires the accurate spatiotemporal regulation of many different factors to achieve remarkable chromosome-wide gene silencing. As a result of XCI, the active and inactive X chromosomes are functionally and structurally different, with the inactive X chromosome undergoing a major conformational reorganization within the nucleus. In this Review, we discuss the multiple layers of genetic and epigenetic regulation that underlie initiation of XCI during development and then maintain it throughout life, in light of the most recent findings in this rapidly advancing field. We discuss exciting new insights into the regulation of X inactive-specific transcript (XIST), the trigger and master regulator of XCI, and into the mechanisms and dynamics that underlie the silencing of nearly all X-linked genes. Finally, given the increasing interest in understanding the impact of chromosome organization on gene regulation, we provide an overview of the factors that are thought to reshape the 3D structure of the inactive X chromosome and of the relevance of such structural changes for XCI establishment and maintenance.
MeSH term(s)	Epigenesis, Genetic/genetics ; Female ; Gene Silencing ; Humans ; Male ; RNA, Long Noncoding/genetics ; X Chromosome/genetics ; X Chromosome Inactivation/genetics
Chemical Substances	RNA, Long Noncoding
Language	English
Publishing date	2022-01-10
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2031313-5
ISSN	1471-0080 ; 1471-0072
ISSN (online)	1471-0080
ISSN	1471-0072
DOI	10.1038/s41580-021-00438-7
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Xist RNA in action: Past, present, and future.

Loda, Agnese / Heard, Edith

PLoS genetics

2019 Volume 15, Issue 9, Page(s) e1008333

Abstract: In mammals, dosage compensation of sex chromosomal genes between females (XX) and males (XY) is achieved through X-chromosome inactivation (XCI). The X-linked X-inactive-specific transcript (Xist) long noncoding RNA is indispensable for XCI and initiates ...

Abstract	In mammals, dosage compensation of sex chromosomal genes between females (XX) and males (XY) is achieved through X-chromosome inactivation (XCI). The X-linked X-inactive-specific transcript (Xist) long noncoding RNA is indispensable for XCI and initiates the process early during development by spreading in cis across the X chromosome from which it is transcribed. During XCI, Xist RNA triggers gene silencing, recruits a plethora of chromatin modifying factors, and drives a major structural reorganization of the X chromosome. Here, we review our knowledge of the multitude of epigenetic events orchestrated by Xist RNA to allow female mammals to survive through embryonic development by establishing and maintaining proper dosage compensation. In particular, we focus on recent studies characterizing the interaction partners of Xist RNA, and we discuss how they have affected the field by addressing long-standing controversies or by giving rise to new research perspectives that are currently being explored. This review is dedicated to the memory of Denise Barlow, pioneer of genomic imprinting and functional long noncoding RNAs (lncRNAs), whose work has revolutionized the epigenetics field and continues to inspire generations of scientists.
MeSH term(s)	Animals ; Dosage Compensation, Genetic/genetics ; Dosage Compensation, Genetic/physiology ; Epigenesis, Genetic/genetics ; Female ; Gene Silencing/physiology ; Humans ; Male ; Mammals/genetics ; RNA, Long Noncoding/genetics ; RNA, Long Noncoding/metabolism ; RNA, Long Noncoding/physiology ; X Chromosome/genetics ; X Chromosome Inactivation/genetics
Chemical Substances	RNA, Long Noncoding ; XIST non-coding RNA
Language	English
Publishing date	2019-09-19
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2186725-2
ISSN	1553-7404 ; 1553-7390
ISSN (online)	1553-7404
ISSN	1553-7390
DOI	10.1371/journal.pgen.1008333
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Deciphering High-Resolution 3D Chromatin Organization via Capture Hi-C.

Hauth, Antonia / Galupa, Rafael / Servant, Nicolas / Villacorta, Laura / Hauschulz, Kai / van Bemmel, Joke Gerarda / Loda, Agnese / Heard, Edith

Journal of visualized experiments : JoVE

2022 , Issue 188

Abstract: The spatial organization of the genome contributes to its function and regulation in many contexts, including transcription, replication, recombination, and repair. Understanding the exact causality between genome topology and function is therefore ... ...

Abstract	The spatial organization of the genome contributes to its function and regulation in many contexts, including transcription, replication, recombination, and repair. Understanding the exact causality between genome topology and function is therefore crucial and increasingly the subject of intensive research. Chromosome conformation capture technologies (3C) allow inferring the 3D structure of chromatin by measuring the frequency of interactions between any region of the genome. Here we describe a fast and simple protocol to perform Capture Hi-C, a 3C-based target enrichment method that characterizes the allele-specific 3D organization of megabased-sized genomic targets at high-resolution. In Capture Hi-C, target regions are captured by an array of biotinylated probes before downstream high-throughput sequencing. Thus, higher resolution and allele-specificity are achieved while improving the time-effectiveness and affordability of the technology. To demonstrate its strengths, the Capture Hi-C protocol was applied to the mouse X-inactivation center (Xic), the master regulatory locus of X-chromosome inactivation (XCI).
MeSH term(s)	Mice ; Animals ; Chromosome Mapping/methods ; Chromatin/genetics ; Chromosomes ; High-Throughput Nucleotide Sequencing/methods ; Genomics/methods
Chemical Substances	Chromatin
Language	English
Publishing date	2022-10-14
Publishing country	United States
Document type	Journal Article ; Video-Audio Media ; Research Support, Non-U.S. Gov't
ZDB-ID	2259946-0
ISSN	1940-087X ; 1940-087X
ISSN (online)	1940-087X
ISSN	1940-087X
DOI	10.3791/64166
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Article: Escape from X inactivation is directly modulated by levels of Xist non-coding RNA.

Hauth, Antonia / Panten, Jasper / Kneuss, Emma / Picard, Christel / Servant, Nicolas / Rall, Isabell / Pérez-Rico, Yuvia A / Clerquin, Lena / Servaas, Nila / Villacorta, Laura / Jung, Ferris / Luong, Christy / Chang, Howard Y / Zaugg, Judith B / Stegle, Oliver / Odom, Duncan T / Loda, Agnese / Heard, Edith

bioRxiv : the preprint server for biology

2024

Abstract: In placental females, one copy of the two X chromosomes is largely silenced during a narrow developmental time window, in a process mediated by the non-coding RNA ... ...

Abstract	In placental females, one copy of the two X chromosomes is largely silenced during a narrow developmental time window, in a process mediated by the non-coding RNA Xist
Language	English
Publishing date	2024-03-12
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.02.22.581559
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Article ; Online: Species-specific regulation of XIST by the JPX/FTX orthologs.

Rosspopoff, Olga / Cazottes, Emmanuel / Huret, Christophe / Loda, Agnese / Collier, Amanda J / Casanova, Miguel / Rugg-Gunn, Peter J / Heard, Edith / Ouimette, Jean-François / Rougeulle, Claire

Nucleic acids research

2023 Volume 51, Issue 5, Page(s) 2177–2194

Abstract: X chromosome inactivation (XCI) is an essential process, yet it initiates with remarkable diversity in various mammalian species. XIST, the main trigger of XCI, is controlled in the mouse by an interplay of lncRNA genes (LRGs), some of which evolved ... ...

Abstract	X chromosome inactivation (XCI) is an essential process, yet it initiates with remarkable diversity in various mammalian species. XIST, the main trigger of XCI, is controlled in the mouse by an interplay of lncRNA genes (LRGs), some of which evolved concomitantly to XIST and have orthologues across all placental mammals. Here, we addressed the functional conservation of human orthologues of two such LRGs, FTX and JPX. By combining analysis of single-cell RNA-seq data from early human embryogenesis with various functional assays in matched human and mouse pluripotent stem- or differentiated post-XCI cells, we demonstrate major functional differences for these orthologues between species, independently of primary sequence conservation. While the function of FTX is not conserved in humans, JPX stands as a major regulator of XIST expression in both species. However, we show that different entities of JPX control the production of XIST at various steps depending on the species. Altogether, our study highlights the functional versatility of LRGs across evolution, and reveals that functional conservation of orthologous LRGs may involve diversified mechanisms of action. These findings represent a striking example of how the evolvability of LRGs can provide adaptative flexibility to constrained gene regulatory networks.
MeSH term(s)	Pregnancy ; Humans ; Female ; Mice ; Animals ; Placenta/metabolism ; X Chromosome Inactivation/genetics ; RNA, Long Noncoding/genetics ; RNA, Long Noncoding/metabolism ; Mammals/genetics ; Embryo, Mammalian/metabolism
Chemical Substances	RNA, Long Noncoding
Language	English
Publishing date	2023-02-02
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	186809-3
ISSN	1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
ISSN (online)	1362-4962 ; 1362-4954
ISSN	0301-5610 ; 0305-1048
DOI	10.1093/nar/gkad029
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Article ; Online: Simultaneous RNA-DNA FISH in Mouse Preimplantation Embryos.

Magaraki, Aristea / Loda, Agnese / Gribnau, Joost / Baarends, Willy M

Methods in molecular biology (Clifton, N.J.)

2018 Volume 1861, Page(s) 131–147

Abstract: Fluorescent in situ hybridization (FISH) is a powerful cytogenetic technique that allows the visualization and quantification of RNA and DNA molecules in different cellular contexts. In general, FISH applications help to advance research, cytogenetics, ... ...

Abstract	Fluorescent in situ hybridization (FISH) is a powerful cytogenetic technique that allows the visualization and quantification of RNA and DNA molecules in different cellular contexts. In general, FISH applications help to advance research, cytogenetics, and diagnostics. DNA FISH can be applied, for example, for gene mapping and for detecting genetic aberrations. RNA FISH provides information about gene expression. However, in cases where RNA and DNA molecules need to be detected in the same sample, the result is often compromised by the fact that the tissue sample is damaged due to the multitude of processing steps that are required for each application. In addition, the sequential application of RNA and DNA FISH protocols on the same sample is very time consuming. Here we describe a brief protocol that enables the combined and simultaneous detection of Xist RNA and centromeric DNA of chromosome 6 in mouse preimplantation embryos. In addition, we describe how to generate indirect-labeled probes starting from BACs. This protocol may be applied to any combination of RNA and DNA detection.
MeSH term(s)	Animals ; Blastocyst/chemistry ; Blastocyst/metabolism ; Cells, Cultured ; Centromere/metabolism ; DNA/analysis ; Epigenomics/methods ; Female ; Gene Expression Regulation, Developmental ; In Situ Hybridization, Fluorescence/methods ; Male ; Mice ; RNA, Long Noncoding/analysis ; X Chromosome Inactivation
Chemical Substances	RNA, Long Noncoding ; XIST non-coding RNA ; DNA (9007-49-2)
Language	English
Publishing date	2018-09-14
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-8766-5_11
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: A novel approach to differentiate rat embryonic stem cells in vitro reveals a role for RNF12 in activation of X chromosome inactivation.

Magaraki, Aristea / Loda, Agnese / Gontan, Cristina / Merzouk, Sarra / Sleddens-Linkels, Esther / Meek, Stephen / Baarends, Willy M / Burdon, Tom / Gribnau, Joost

Scientific reports

2019 Volume 9, Issue 1, Page(s) 6068

Abstract: X chromosome inactivation (XCI) is a mammalian specific, developmentally regulated process relying on several mechanisms including antisense transcription, non-coding RNA-mediated silencing, and recruitment of chromatin remodeling complexes. In vitro ... ...

Abstract	X chromosome inactivation (XCI) is a mammalian specific, developmentally regulated process relying on several mechanisms including antisense transcription, non-coding RNA-mediated silencing, and recruitment of chromatin remodeling complexes. In vitro modeling of XCI, through differentiation of embryonic stem cells (ESCs), provides a powerful tool to study the dynamics of XCI, overcoming the need for embryos, and facilitating genetic modification of key regulatory players. However, to date, robust initiation of XCI in vitro has been mostly limited to mouse pluripotent stem cells. Here, we adapted existing protocols to establish a novel monolayer differentiation protocol for rat ESCs to study XCI. We show that differentiating rat ESCs properly downregulate pluripotency factor genes, and present female specific Xist RNA accumulation and silencing of X-linked genes. We also demonstrate that RNF12 seems to be an important player in regulation of initiation of XCI in rat, acting as an Xist activator. Our work provides the basis to investigate the mechanisms directing the XCI process in a model organism different from the mouse.
MeSH term(s)	Animals ; Cell Differentiation ; Cells, Cultured ; Embryo, Mammalian ; Embryonic Stem Cells/physiology ; Female ; Male ; Models, Animal ; Primary Cell Culture ; RNA, Long Noncoding/metabolism ; Rats ; Ubiquitin-Protein Ligases/physiology ; X Chromosome Inactivation/physiology
Chemical Substances	RNA, Long Noncoding ; XIST non-coding RNA ; Rlim protein, rat (EC 2.3.2.27) ; Ubiquitin-Protein Ligases (EC 2.3.2.27)
Language	English
Publishing date	2019-04-15
Publishing country	England
Document type	Journal Article
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-019-42246-2
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Article ; Online: Chromatin-Mediated Reversible Silencing of Sense-Antisense Gene Pairs in Embryonic Stem Cells Is Consolidated upon Differentiation

Loos, Friedemann / Loda, Agnese / van Wijk, Louise / Grootegoed, J. Anton / Gribnau, Joost

Molecular and Cellular Biology. 2015 July 1, v. 35, no. 14 p.2436-2447

2015

Abstract: Genome-wide gene expression studies have indicated that the eukaryotic genome contains many gene pairs showing overlapping sense and antisense transcription. Regulation of these coding and/or noncoding gene pairs involves intricate regulatory mechanisms. ...

Abstract	Genome-wide gene expression studies have indicated that the eukaryotic genome contains many gene pairs showing overlapping sense and antisense transcription. Regulation of these coding and/or noncoding gene pairs involves intricate regulatory mechanisms. In the present study, we utilized an enhanced green fluorescent protein (EGFP)-tagged reporter plasmid cis linked to a doxycycline-inducible antisense promoter, generating antisense transcription that fully overlaps EGFP, to study the mechanism and dynamics of gene silencing after induction of noncoding antisense transcription in undifferentiated and differentiating mouse embryonic stem cells (ESCs). We found that EGFP silencing is reversible in ESCs but is locked into a stable state upon ESC differentiation. Reversible silencing in ESCs is chromatin dependent and is associated with accumulation of trimethylated lysine 36 on histone H3 (H3K36me3) at the EGFP promoter region. In differentiating ESCs, antisense transcription-induced accumulation of H3K36me3 was associated with an increase in CpG methylation at the EGFP promoter. Repression of the sense promoter was affected by small-molecule inhibitors which interfere with DNA methylation and histone demethylation pathways. Our results indicate a general mechanism for silencing of fully overlapping sense-antisense gene pairs involving antisense transcription-induced accumulation of H3K36me3 at the sense promoter, resulting in reversible silencing of the sense partner, which is stabilized during ESC differentiation by CpG methylation.
Keywords	DNA methylation ; chromatin ; demethylation ; gene expression ; genes ; green fluorescent protein ; histones ; lysine ; mice ; plasmids ; promoter regions
Language	English
Dates of publication	2015-0701
Size	p. 2436-2447.
Publishing place	Taylor & Francis
Document type	Article ; Online
ZDB-ID	779397-2
ISSN	1098-5549 ; 0270-7306
ISSN (online)	1098-5549
ISSN	0270-7306
DOI	10.1128/MCB.00029-15
Database	NAL-Catalogue (AGRICOLA)

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Zs.A 1666: Show issues

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Article ; Online: Chromatin-Mediated Reversible Silencing of Sense-Antisense Gene Pairs in Embryonic Stem Cells Is Consolidated upon Differentiation.

Loos, Friedemann / Loda, Agnese / van Wijk, Louise / Grootegoed, J Anton / Gribnau, Joost

Molecular and cellular biology

2015 Volume 35, Issue 14, Page(s) 2436–2447

Abstract	Genome-wide gene expression studies have indicated that the eukaryotic genome contains many gene pairs showing overlapping sense and antisense transcription. Regulation of these coding and/or noncoding gene pairs involves intricate regulatory mechanisms. In the present study, we utilized an enhanced green fluorescent protein (EGFP)-tagged reporter plasmid cis linked to a doxycycline-inducible antisense promoter, generating antisense transcription that fully overlaps EGFP, to study the mechanism and dynamics of gene silencing after induction of noncoding antisense transcription in undifferentiated and differentiating mouse embryonic stem cells (ESCs). We found that EGFP silencing is reversible in ESCs but is locked into a stable state upon ESC differentiation. Reversible silencing in ESCs is chromatin dependent and is associated with accumulation of trimethylated lysine 36 on histone H3 (H3K36me3) at the EGFP promoter region. In differentiating ESCs, antisense transcription-induced accumulation of H3K36me3 was associated with an increase in CpG methylation at the EGFP promoter. Repression of the sense promoter was affected by small-molecule inhibitors which interfere with DNA methylation and histone demethylation pathways. Our results indicate a general mechanism for silencing of fully overlapping sense-antisense gene pairs involving antisense transcription-induced accumulation of H3K36me3 at the sense promoter, resulting in reversible silencing of the sense partner, which is stabilized during ESC differentiation by CpG methylation.
MeSH term(s)	Animals ; Cell Differentiation/genetics ; Cells, Cultured ; Chromatin/genetics ; Chromatin/metabolism ; CpG Islands/genetics ; DNA Methylation ; DNA, Antisense/genetics ; Doxycycline/pharmacology ; Embryonic Stem Cells/cytology ; Embryonic Stem Cells/metabolism ; Flow Cytometry ; Gene Expression/drug effects ; Gene Silencing ; Green Fluorescent Proteins/genetics ; Green Fluorescent Proteins/metabolism ; Histones/metabolism ; Lysine/metabolism ; Methylation ; Mice, 129 Strain ; Mice, Transgenic ; Models, Genetic ; Promoter Regions, Genetic/genetics
Chemical Substances	Chromatin ; DNA, Antisense ; Histones ; Green Fluorescent Proteins (147336-22-9) ; Lysine (K3Z4F929H6) ; Doxycycline (N12000U13O)
Language	English
Publishing date	2015-07
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	779397-2
ISSN	1098-5549 ; 0270-7306
ISSN (online)	1098-5549
ISSN	0270-7306
DOI	10.1128/MCB.00029-15
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Article ; Online: Xist and Tsix Transcription Dynamics Is Regulated by the X-to-Autosome Ratio and Semistable Transcriptional States.

Loos, Friedemann / Maduro, Cheryl / Loda, Agnese / Lehmann, Johannes / Kremers, Gert-Jan / Ten Berge, Derk / Grootegoed, J Anton / Gribnau, Joost

Molecular and cellular biology

2016 Volume 36, Issue 21, Page(s) 2656–2667

Abstract: In female mammals, X chromosome inactivation (XCI) is a key process in the control of gene dosage compensation between X-linked genes and autosomes. Xist and Tsix, two overlapping antisense-transcribed noncoding genes, are central elements of the X ... ...

Abstract	In female mammals, X chromosome inactivation (XCI) is a key process in the control of gene dosage compensation between X-linked genes and autosomes. Xist and Tsix, two overlapping antisense-transcribed noncoding genes, are central elements of the X inactivation center (Xic) regulating XCI. Xist upregulation results in the coating of the entire X chromosome by Xist RNA in cis, whereas Tsix transcription acts as a negative regulator of Xist Here, we generated Xist and Tsix reporter mouse embryonic stem (ES) cell lines to study the genetic and dynamic regulation of these genes upon differentiation. Our results revealed mutually antagonistic roles for Tsix on Xist and vice versa and indicate the presence of semistable transcriptional states of the Xic locus predicting the outcome of XCI. These transcriptional states are instructed by the X-to-autosome ratio, directed by regulators of XCI, and can be modulated by tissue culture conditions.
MeSH term(s)	Alleles ; Animals ; Cell Line ; Chromosomes, Mammalian/genetics ; Female ; Gene Expression Regulation ; Gene Regulatory Networks ; Genes, Reporter ; Genetic Loci ; Mice ; Models, Genetic ; RNA, Long Noncoding/genetics ; RNA, Long Noncoding/metabolism ; Transcription, Genetic ; X Chromosome/genetics ; X Chromosome Inactivation/genetics
Chemical Substances	RNA, Long Noncoding ; Tsix transcript, mouse ; XIST non-coding RNA
Language	English
Publishing date	2016-10-13
Publishing country	United States
Document type	Journal Article
ZDB-ID	779397-2
ISSN	1098-5549 ; 0270-7306
ISSN (online)	1098-5549
ISSN	0270-7306
DOI	10.1128/MCB.00183-16
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