Female naïve human pluripotent stem cells carry X chromosomes with Xa-like and Xi-like folding conformations

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Abstract

Three-dimensional (3D) genomics shows immense promise for studying X chromosome inactivation (XCI) by interrogating changes to the X chromosomes’ 3D states. Here, we sought to characterize the 3D state of the X chromosome in naïve and primed human pluripotent stem cells (hPSCs). Using chromatin tracing, we analyzed X chromosome folding conformations in these cells with megabase genomic resolution. X chromosomes in female naïve hPSCs exhibit folding conformations similar to the active X chromosome (Xa) and the inactive X chromosome (Xi) in somatic cells. However, naïve X chromosomes do not exhibit the chromatin compaction typically associated with these somatic X chromosome states. In H7 naïve human embryonic stem cells, XIST accumulation observed on damaged X chromosomes demonstrates the potential for naïve hPSCs to activate XCI-related mechanisms. Overall, our findings provide insight into the X chromosome status of naïve hPSCs with a single-chromosome resolution and are critical in understanding the unique epigenetic regulation in early embryonic cells.

Abstract

Chromatin tracing was used at single-chromosome resolution to define the 3D state of X chromosomes in human stem cells.

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Most cited references 83

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Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities.

Sven Heinz, Christopher Benner, Nathanael Spann … (2010)

Genome-scale studies have revealed extensive, cell type-specific colocalization of transcription factors, but the mechanisms underlying this phenomenon remain poorly understood. Here, we demonstrate in macrophages and B cells that collaborative interactions of the common factor PU.1 with small sets of macrophage- or B cell lineage-determining transcription factors establish cell-specific binding sites that are associated with the majority of promoter-distal H3K4me1-marked genomic regions. PU.1 binding initiates nucleosome remodeling, followed by H3K4 monomethylation at large numbers of genomic regions associated with both broadly and specifically expressed genes. These locations serve as beacons for additional factors, exemplified by liver X receptors, which drive both cell-specific gene expression and signal-dependent responses. Together with analyses of transcription factor binding and H3K4me1 patterns in other cell types, these studies suggest that simple combinations of lineage-determining transcription factors can specify the genomic sites ultimately responsible for both cell identity and cell type-specific responses to diverse signaling inputs. Copyright 2010 Elsevier Inc. All rights reserved.

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Suhas Rao, Miriam H Huntley, Neva Durand … (2014)

We use in situ Hi-C to probe the 3D architecture of genomes, constructing haploid and diploid maps of nine cell types. The densest, in human lymphoblastoid cells, contains 4.9 billion contacts, achieving 1 kb resolution. We find that genomes are partitioned into contact domains (median length, 185 kb), which are associated with distinct patterns of histone marks and segregate into six subcompartments. We identify ∼10,000 loops. These loops frequently link promoters and enhancers, correlate with gene activation, and show conservation across cell types and species. Loop anchors typically occur at domain boundaries and bind CTCF. CTCF sites at loop anchors occur predominantly (>90%) in a convergent orientation, with the asymmetric motifs "facing" one another. The inactive X chromosome splits into two massive domains and contains large loops anchored at CTCF-binding repeats. Copyright © 2014 Elsevier Inc. All rights reserved.

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Author and article information

Contributors

Benjamin Patterson:

ORCID: https://orcid.org/0009-0008-4132-9407

Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing - original draft

Bing Yang:

ORCID: https://orcid.org/0000-0002-9355-2538

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Yoshiaki Tanaka:

ORCID: https://orcid.org/0000-0002-2078-9374

Role: Formal analysisRole: Software

Kun-Yong Kim:

ORCID: https://orcid.org/0000-0001-8968-0177

Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: Validation

Bilal Cakir:

ORCID: https://orcid.org/0000-0003-4610-0317

Role: ConceptualizationRole: MethodologyRole: VisualizationRole: Writing - review & editing

Yangfei Xiang:

ORCID: https://orcid.org/0000-0002-6256-6312

Role: ResourcesRole: Writing - review & editing

Jonghun Kim: Role: InvestigationRole: Validation

Siyuan Wang:

ORCID: https://orcid.org/0000-0001-6550-4064

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

In-Hyun Park:

ORCID: https://orcid.org/0000-0001-7748-1293

Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing - original draft

Journal

Journal ID (nlm-ta): Sci Adv

Journal ID (iso-abbrev): Sci Adv

Journal ID (publisher-id): sciadv

Journal ID (hwp): advances

Title: Science Advances

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2375-2548

Publication date Collection: August 2023

Publication date (Electronic, pub): 04 August 2023

Volume: 9

Issue: 31

Electronic Location Identifier: eadf2245

Affiliations

[ ¹ ]Department of Genetics, Yale Stem Cell Center, Yale School of Medicine, New Haven, CT 06520, USA.

[ ² ]Department of Genetics, and Department of Cell Biology, Yale School of Medicine, New Haven, CT 06520, USA.

Author notes

[* ]Corresponding author. Email: siyuan.wang@ 123456yale.edu (S.W.); inhyun.park@ 123456yale.edu (I.-H.P.)

[†]

These authors contributed equally to this work.

[‡]

Present address: Maisonneuve-Rosemont Hospital Research Center, Department of Medicine, University of Montreal, QC H1T 2M4, Canada.

[§]

Present address: School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, China.

Author information

Benjamin Patterson https://orcid.org/0009-0008-4132-9407

Bing Yang https://orcid.org/0000-0002-9355-2538

Yoshiaki Tanaka https://orcid.org/0000-0002-2078-9374

Kun-Yong Kim https://orcid.org/0000-0001-8968-0177

Bilal Cakir https://orcid.org/0000-0003-4610-0317

Yangfei Xiang https://orcid.org/0000-0002-6256-6312

Siyuan Wang https://orcid.org/0000-0001-6550-4064

In-Hyun Park https://orcid.org/0000-0001-7748-1293

Article

Publisher ID: adf2245

DOI: 10.1126/sciadv.adf2245

PMC ID: 10403202

PubMed ID: 37540754

SO-VID: 8067675c-8a26-4f4c-aba3-aab98417fe9c

Copyright © Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.