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Article ; Online: Mechanistic drivers of chromatin organization into compartments.

Harris, Hannah L / Rowley, M Jordan

Current opinion in genetics & development

2024 Volume 86, Page(s) 102193

Abstract: The human genome is not just a simple string of DNA, it is a complex and dynamic entity intricately folded within the cell's nucleus. This three-dimensional organization of chromatin, the combination of DNA and proteins in the nucleus, is crucial for ... ...

Abstract	The human genome is not just a simple string of DNA, it is a complex and dynamic entity intricately folded within the cell's nucleus. This three-dimensional organization of chromatin, the combination of DNA and proteins in the nucleus, is crucial for many biological processes and has been prominently studied for its intricate relationship to gene expression. Indeed, the transcriptional machinery does not operate in isolation but interacts intimately with the folded chromatin structure. Techniques for chromatin conformation capture, including genome-wide sequencing approaches, have revealed key organizational features of chromatin, such as the formation of loops by CCCTC-binding factor (CTCF) and the division of loci into chromatin compartments. While much of the recent research and reviews have focused on CTCF loops, we discuss several new revelations that have emerged concerning chromatin compartments, with a particular focus on what is known about mechanistic drivers of compartmentalization. These insights challenge the traditional views of chromatin organization and reveal the complexity behind the formation and maintenance of chromatin compartments.
Language	English
Publishing date	2024-04-15
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	1077312-5
ISSN	1879-0380 ; 0959-437X
ISSN (online)	1879-0380
ISSN	0959-437X
DOI	10.1016/j.gde.2024.102193
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Article ; Online: Implications of Dosage Deficiencies in CTCF and Cohesin on Genome Organization, Gene Expression, and Human Neurodevelopment.

Cummings, Christopher T / Rowley, M Jordan

Genes

2022 Volume 13, Issue 4

Abstract: Properly organizing DNA within the nucleus is critical to ensure normal downstream nuclear functions. CTCF and cohesin act as major architectural proteins, working in concert to generate thousands of high-intensity chromatin loops. Due to their central ... ...

Abstract	Properly organizing DNA within the nucleus is critical to ensure normal downstream nuclear functions. CTCF and cohesin act as major architectural proteins, working in concert to generate thousands of high-intensity chromatin loops. Due to their central role in loop formation, a massive research effort has been dedicated to investigating the mechanism by which CTCF and cohesin create these loops. Recent results lead to questioning the direct impact of CTCF loops on gene expression. Additionally, results of controlled depletion experiments in cell lines has indicated that genome architecture may be somewhat resistant to incomplete deficiencies in CTCF or cohesin. However, heterozygous human genetic deficiencies in CTCF and cohesin have illustrated the importance of their dosage in genome architecture, cellular processes, animal behavior, and disease phenotypes. Thus, the importance of considering CTCF or cohesin levels is especially made clear by these heterozygous germline variants that characterize genetic syndromes, which are increasingly recognized in clinical practice. Defined primarily by developmental delay and intellectual disability, the phenotypes of CTCF and cohesin deficiency illustrate the importance of architectural proteins particularly in neurodevelopment. We discuss the distinct roles of CTCF and cohesin in forming chromatin loops, highlight the major role that dosage of each protein plays in the amplitude of observed effects on gene expression, and contrast these results to heterozygous mutation phenotypes in murine models and clinical patients. Insights highlighted by this comparison have implications for future research into these newly emerging genetic syndromes.
MeSH term(s)	Animals ; CCCTC-Binding Factor/genetics ; CCCTC-Binding Factor/metabolism ; Cell Cycle Proteins ; Chromatin/genetics ; Chromosomal Proteins, Non-Histone ; Gene Expression ; Humans ; Mice ; Syndrome ; Cohesins
Chemical Substances	CCCTC-Binding Factor ; CTCF protein, human ; Cell Cycle Proteins ; Chromatin ; Chromosomal Proteins, Non-Histone
Language	English
Publishing date	2022-03-25
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2527218-4
ISSN	2073-4425 ; 2073-4425
ISSN (online)	2073-4425
ISSN	2073-4425
DOI	10.3390/genes13040583
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Article ; Online: An environmentally relevant mixture of Perfluoroalkyl Substances (PFAS) impacts proliferation, steroid hormone synthesis, and gene transcription in primary human granulosa cells.

Clark, Kendra L / Shukla, Mamta / George, Jitu W / Gustin, Stephanie / Rowley, M Jordan / Davis, John S

Toxicological sciences : an official journal of the Society of Toxicology

2024

Abstract: Perfluoroalkyl substances (PFAS) are a group of synthetic chemicals that are resistant to biodegradation and are environmentally persistent. PFAS are found in many consumer products and are a major source of water and soil contamination. This study ... ...

Abstract	Perfluoroalkyl substances (PFAS) are a group of synthetic chemicals that are resistant to biodegradation and are environmentally persistent. PFAS are found in many consumer products and are a major source of water and soil contamination. This study investigated the effects of an environmentally relevant PFAS mixture [perfluorooctanoic acid (PFOA), perfluorooctanesulfonic acid (PFOS), perfluorohexanesulfonic acid (PFHxS)] on the transcriptome and function of human granulosa cells (hGCs). Primary hGCs were harvested from follicular aspirates of healthy, reproductive-age women who were undergoing oocyte retrieval for in vitro fertilization. LC/MS-MS was performed to identify PFAS compounds in pure follicular fluid. Cells were cultured with vehicle control or a PFAS mixture (2 nM PFHxS, 7 nM PFOA, 10 nM PFOS) for 96h. Analyses of cell proliferation/apoptosis, steroidogenesis, and gene expression were measured via MTT assays/immunofluorescence, ELISA/western blotting, and RNA sequencing/bioinformatics, respectively. PFOA, PFOS, and PFHxS were detected in 100% of follicle fluid samples. Increased cell proliferation was observed in hGCs treated with the PFAS mixture with no impacts on cellular apoptosis. The PFAS mixture also altered steroid hormone synthesis, increasing both FSH-stimulated and basal progesterone secretion and concomitant upregulation of STAR protein. RNA sequencing revealed inherent differences in transcriptomic profiles in hGCs after PFAS exposure. This study demonstrates functional and transcriptomic changes in hGCs after exposure to a PFAS mixture, improving our knowledge about the impacts of PFAS exposures and female reproductive health. These findings suggest that PFAS compounds can disrupt normal granulosa cell function with possible long-term consequences on overall reproductive health.
Language	English
Publishing date	2024-04-11
Publishing country	United States
Document type	Journal Article
ZDB-ID	1420885-4
ISSN	1096-0929 ; 1096-6080
ISSN (online)	1096-0929
ISSN	1096-6080
DOI	10.1093/toxsci/kfae049
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Article: Considerations and caveats for analyzing chromatin compartments.

Kalluchi, Achyuth / Harris, Hannah L / Reznicek, Timothy E / Rowley, M Jordan

Frontiers in molecular biosciences

2023 Volume 10, Page(s) 1168562

Abstract: Genomes are organized into nuclear compartments, separating active from inactive chromatin. Chromatin compartments are readily visible in a large number of species by experiments that map chromatin conformation genome-wide. When analyzing these maps, a ... ...

Abstract	Genomes are organized into nuclear compartments, separating active from inactive chromatin. Chromatin compartments are readily visible in a large number of species by experiments that map chromatin conformation genome-wide. When analyzing these maps, a common step is the identification of genomic intervals that interact within A (active) and B (inactive) compartments. It has also become increasingly common to identify and analyze subcompartments. We review different strategies to identify A/B and subcompartment intervals, including a discussion of various machine-learning approaches to predict these features. We then discuss the strengths and limitations of current strategies and examine how these aspects of analysis may have impacted our understanding of chromatin compartments.
Language	English
Publishing date	2023-04-05
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2814330-9
ISSN	2296-889X
ISSN	2296-889X
DOI	10.3389/fmolb.2023.1168562
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Article: HiCrayon reveals distinct layers of multi-state 3D chromatin organization.

Nolan, Ben / Harris, Hannah L / Kalluchi, Achyuth / Reznicek, Timothy E / Cummings, Christopher T / Rowley, M Jordan

bioRxiv : the preprint server for biology

2024

Abstract: The co-visualization of chromatin conformation with 1D 'omics data is key to the multi-omics driven data analysis of 3D genome organization. Chromatin contact maps are often shown as 2D heatmaps and visually compared to 1D genomic data by simple ... ...

Abstract	The co-visualization of chromatin conformation with 1D 'omics data is key to the multi-omics driven data analysis of 3D genome organization. Chromatin contact maps are often shown as 2D heatmaps and visually compared to 1D genomic data by simple juxtaposition. While common, this strategy is imprecise, placing the onus on the reader to align features with each other. To remedy this, we developed HiCrayon, an interactive tool that facilitates the integration of 3D chromatin organization maps and 1D datasets. This visualization method integrates data from genomic assays directly into the chromatin contact map by coloring interactions according to 1D signal. HiCrayon is implemented using R shiny and python to create a graphical user interface (GUI) application, available in both web or containerized format to promote accessibility. HiCrayon is implemented in R, and includes a graphical user interface (GUI), as well as a slimmed-down web-based version that lets users quickly produce publication-ready images. We demonstrate the utility of HiCrayon in visualizing the effectiveness of compartment calling and the relationship between ChIP-seq and various features of chromatin organization. We also demonstrate the improved visualization of other 3D genomic phenomena, such as differences between loops associated with CTCF/cohesin vs. those associated with H3K27ac. We then demonstrate HiCrayon's visualization of organizational changes that occur during differentiation and use HiCrayon to detect compartment patterns that cannot be assigned to either A or B compartments, revealing a distinct 3rd chromatin compartment. Overall, we demonstrate the utility of co-visualizing 2D chromatin conformation with 1D genomic signals within the same matrix to reveal fundamental aspects of genome organization. Local version: https://github.com/JRowleyLab/HiCrayon Web version: https://jrowleylab.com/HiCrayon.
Language	English
Publishing date	2024-02-12
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.02.11.579821
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Article ; Online: Regulation of CTCF loop formation during pancreatic cell differentiation.

Lyu, Xiaowen / Rowley, M Jordan / Kulik, Michael J / Dalton, Stephen / Corces, Victor G

Nature communications

2023 Volume 14, Issue 1, Page(s) 6314

Abstract: Transcription reprogramming during cell differentiation involves targeting enhancers to genes responsible for establishment of cell fates. To understand the contribution of CTCF-mediated chromatin organization to cell lineage commitment, we analyzed 3D ... ...

Abstract	Transcription reprogramming during cell differentiation involves targeting enhancers to genes responsible for establishment of cell fates. To understand the contribution of CTCF-mediated chromatin organization to cell lineage commitment, we analyzed 3D chromatin architecture during the differentiation of human embryonic stem cells into pancreatic islet organoids. We find that CTCF loops are formed and disassembled at different stages of the differentiation process by either recruitment of CTCF to new anchor sites or use of pre-existing sites not previously involved in loop formation. Recruitment of CTCF to new sites in the genome involves demethylation of H3K9me3 to H3K9me2, demethylation of DNA, recruitment of pioneer factors, and positioning of nucleosomes flanking the new CTCF sites. Existing CTCF sites not involved in loop formation become functional loop anchors via the establishment of new cohesin loading sites containing NIPBL and YY1 at sites between the new anchors. In both cases, formation of new CTCF loops leads to strengthening of enhancer promoter interactions and increased transcription of genes adjacent to loop anchors. These results suggest an important role for CTCF and cohesin in controlling gene expression during cell differentiation.
MeSH term(s)	Humans ; CCCTC-Binding Factor/genetics ; CCCTC-Binding Factor/metabolism ; Cell Cycle Proteins/genetics ; Cell Cycle Proteins/metabolism ; Cell Differentiation/genetics ; Chromatin ; DNA/metabolism ; Protein Binding
Chemical Substances	CCCTC-Binding Factor ; Cell Cycle Proteins ; Chromatin ; DNA (9007-49-2) ; NIPBL protein, human ; CTCF protein, human
Language	English
Publishing date	2023-10-09
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-41964-6
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Article ; Online: Considerations and caveats for analyzing chromatin compartments

Achyuth Kalluchi / Hannah L. Harris / Timothy E. Reznicek / M. Jordan Rowley

Frontiers in Molecular Biosciences, Vol

2023 Volume 10

Abstract	Genomes are organized into nuclear compartments, separating active from inactive chromatin. Chromatin compartments are readily visible in a large number of species by experiments that map chromatin conformation genome-wide. When analyzing these maps, a common step is the identification of genomic intervals that interact within A (active) and B (inactive) compartments. It has also become increasingly common to identify and analyze subcompartments. We review different strategies to identify A/B and subcompartment intervals, including a discussion of various machine-learning approaches to predict these features. We then discuss the strengths and limitations of current strategies and examine how these aspects of analysis may have impacted our understanding of chromatin compartments.
Keywords	compartments ; Hi-C ; Micro-C ; chromatin organization ; eigenvector ; subcompartment ; Biology (General) ; QH301-705.5
Language	English
Publishing date	2023-04-01T00:00:00Z
Publisher	Frontiers Media S.A.
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Regulation of CTCF loop formation during pancreatic cell differentiation

Xiaowen Lyu / M. Jordan Rowley / Michael J. Kulik / Stephen Dalton / Victor G. Corces

Nature Communications, Vol 14, Iss 1, Pp 1-

2023 Volume 18

Abstract: Abstract Transcription reprogramming during cell differentiation involves targeting enhancers to genes responsible for establishment of cell fates. To understand the contribution of CTCF-mediated chromatin organization to cell lineage commitment, we ... ...

Abstract	Abstract Transcription reprogramming during cell differentiation involves targeting enhancers to genes responsible for establishment of cell fates. To understand the contribution of CTCF-mediated chromatin organization to cell lineage commitment, we analyzed 3D chromatin architecture during the differentiation of human embryonic stem cells into pancreatic islet organoids. We find that CTCF loops are formed and disassembled at different stages of the differentiation process by either recruitment of CTCF to new anchor sites or use of pre-existing sites not previously involved in loop formation. Recruitment of CTCF to new sites in the genome involves demethylation of H3K9me3 to H3K9me2, demethylation of DNA, recruitment of pioneer factors, and positioning of nucleosomes flanking the new CTCF sites. Existing CTCF sites not involved in loop formation become functional loop anchors via the establishment of new cohesin loading sites containing NIPBL and YY1 at sites between the new anchors. In both cases, formation of new CTCF loops leads to strengthening of enhancer promoter interactions and increased transcription of genes adjacent to loop anchors. These results suggest an important role for CTCF and cohesin in controlling gene expression during cell differentiation.
Keywords	Science ; Q
Subject code	571
Language	English
Publishing date	2023-10-01T00:00:00Z
Publisher	Nature Portfolio
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Predicting A/B compartments from histone modifications using deep learning.

Zheng, Suchen / Thakkar, Nitya / Harris, Hannah L / Liu, Susanna / Zhang, Megan / Gerstein, Mark / Aiden, Erez Lieberman / Rowley, M Jordan / Noble, William Stafford / Gürsoy, Gamze / Singh, Ritambhara

iScience

2024 Volume 27, Issue 5, Page(s) 109570

Abstract: The three-dimensional organization of genomes plays a crucial role in essential biological processes. The segregation of chromatin into A and B compartments highlights regions of activity and inactivity, providing a window into the genomic activities ... ...

Abstract	The three-dimensional organization of genomes plays a crucial role in essential biological processes. The segregation of chromatin into A and B compartments highlights regions of activity and inactivity, providing a window into the genomic activities specific to each cell type. Yet, the steep costs associated with acquiring Hi-C data, necessary for studying this compartmentalization across various cell types, pose a significant barrier in studying cell type specific genome organization. To address this, we present a prediction tool called compartment prediction using recurrent neural networks (CoRNN), which predicts compartmentalization of 3D genome using histone modification enrichment. CoRNN demonstrates robust cross-cell-type prediction of A/B compartments with an average AuROC of 90.9%. Cell-type-specific predictions align well with known functional elements, with H3K27ac and H3K36me3 identified as highly predictive histone marks. We further investigate our mispredictions and found that they are located in regions with ambiguous compartmental status. Furthermore, our model's generalizability is validated by predicting compartments in independent tissue samples, which underscores its broad applicability.
Language	English
Publishing date	2024-03-27
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2024.109570
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Article ; Online: Organizational principles of 3D genome architecture.

Rowley, M Jordan / Corces, Victor G

Nature reviews. Genetics

2018 Volume 19, Issue 12, Page(s) 789–800

Abstract: Studies of 3D chromatin organization have suggested that chromosomes are hierarchically organized into large compartments composed of smaller domains called topologically associating domains (TADs). Recent evidence suggests that compartments are smaller ... ...

Abstract	Studies of 3D chromatin organization have suggested that chromosomes are hierarchically organized into large compartments composed of smaller domains called topologically associating domains (TADs). Recent evidence suggests that compartments are smaller than previously thought and that the transcriptional or chromatin state is responsible for interactions leading to the formation of small compartmental domains in all organisms. In vertebrates, CTCF forms loop domains, probably via an extrusion process involving cohesin. CTCF loops cooperate with compartmental domains to establish the 3D organization of the genome. The continuous extrusion of the chromatin fibre by cohesin may also be responsible for the establishment of enhancer-promoter interactions and stochastic aspects of the transcription process. These observations suggest that the 3D organization of the genome is an emergent property of chromatin and its components, and thus may not be only a determinant but also a consequence of its function.
MeSH term(s)	Animals ; Chromatin/genetics ; Chromatin/metabolism ; Chromatin Assembly and Disassembly/physiology ; Enhancer Elements, Genetic/physiology ; Genome, Human/physiology ; Humans ; Promoter Regions, Genetic/physiology
Chemical Substances	Chromatin
Language	English
Publishing date	2018-10-26
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2035157-4
ISSN	1471-0064 ; 1471-0056
ISSN (online)	1471-0064
ISSN	1471-0056
DOI	10.1038/s41576-018-0060-8
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