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Article ; Online: Enhancer-promoter contact formation requires RNAPII and antagonizes loop extrusion.

Zhang, Shu / Übelmesser, Nadine / Barbieri, Mariano / Papantonis, Argyris

2023 Volume 55, Issue 5, Page(s) 832–840

Abstract: Homotypic chromatin interactions and loop extrusion are thought to be the two main drivers of mammalian chromosome folding. Here we tested the role of RNA polymerase II (RNAPII) across different scales of interphase chromatin organization in a cellular ... ...

Abstract	Homotypic chromatin interactions and loop extrusion are thought to be the two main drivers of mammalian chromosome folding. Here we tested the role of RNA polymerase II (RNAPII) across different scales of interphase chromatin organization in a cellular system allowing for its rapid, auxin-mediated degradation. We combined Micro-C and computational modeling to characterize subsets of loops differentially gained or lost upon RNAPII depletion. Gained loops, extrusion of which was antagonized by RNAPII, almost invariably formed by engaging new or rewired CTCF anchors. Lost loops selectively affected contacts between enhancers and promoters anchored by RNAPII, explaining the repression of most genes. Surprisingly, promoter-promoter interactions remained essentially unaffected by polymerase depletion, and cohesin occupancy was sustained. Together, our findings reconcile the role of RNAPII in transcription with its direct involvement in setting-up regulatory three-dimensional chromatin contacts genome wide, while also revealing an impact on cohesin loop extrusion.
MeSH term(s)	Animals ; RNA Polymerase II/genetics ; RNA Polymerase II/metabolism ; CCCTC-Binding Factor/genetics ; CCCTC-Binding Factor/metabolism ; Chromatin/genetics ; Chromosomes/metabolism ; Cell Cycle Proteins/genetics ; Cell Cycle Proteins/metabolism ; Promoter Regions, Genetic/genetics ; Mammals/genetics
Chemical Substances	RNA Polymerase II (EC 2.7.7.-) ; CCCTC-Binding Factor ; Chromatin ; Cell Cycle Proteins
Language	English
Publishing date	2023-04-03
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1108734-1
ISSN	1546-1718 ; 1061-4036
ISSN (online)	1546-1718
ISSN	1061-4036
DOI	10.1038/s41588-023-01364-4
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Zs.MG 46: Show issues

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Article ; Online: Pervasive structural heterogeneity rewires glioblastoma chromosomes to sustain patient-specific transcriptional programs.

Xie, Ting / Danieli-Mackay, Adi / Buccarelli, Mariachiara / Barbieri, Mariano / Papadionysiou, Ioanna / D'Alessandris, Q Giorgio / Robens, Claudia / Übelmesser, Nadine / Vinchure, Omkar Suhas / Lauretti, Liverana / Fotia, Giorgio / Schwarz, Roland F / Wang, Xiaotao / Ricci-Vitiani, Lucia / Gopalakrishnan, Jay / Pallini, Roberto / Papantonis, Argyris

Nature communications

2024 Volume 15, Issue 1, Page(s) 3905

Abstract: Glioblastoma multiforme (GBM) encompasses brain malignancies marked by phenotypic and transcriptional heterogeneity thought to render these tumors aggressive, resistant to therapy, and inevitably recurrent. However, little is known about how the spatial ... ...

Abstract	Glioblastoma multiforme (GBM) encompasses brain malignancies marked by phenotypic and transcriptional heterogeneity thought to render these tumors aggressive, resistant to therapy, and inevitably recurrent. However, little is known about how the spatial organization of GBM genomes underlies this heterogeneity and its effects. Here, we compile a cohort of 28 patient-derived glioblastoma stem cell-like lines (GSCs) known to reflect the properties of their tumor-of-origin; six of these were primary-relapse tumor pairs from the same patient. We generate and analyze 5 kbp-resolution chromosome conformation capture (Hi-C) data from all GSCs to systematically map thousands of standalone and complex structural variants (SVs) and the multitude of neoloops arising as a result. By combining Hi-C, histone modification, and gene expression data with chromatin folding simulations, we explain how the pervasive, uneven, and idiosyncratic occurrence of neoloops sustains tumor-specific transcriptional programs via the formation of new enhancer-promoter contacts. We also show how even moderately recurrent neoloops can relate to patient-specific vulnerabilities. Together, our data provide a resource for dissecting GBM biology and heterogeneity, as well as for informing therapeutic approaches.
MeSH term(s)	Glioblastoma/genetics ; Glioblastoma/pathology ; Humans ; Brain Neoplasms/genetics ; Brain Neoplasms/pathology ; Gene Expression Regulation, Neoplastic ; Chromatin/metabolism ; Chromatin/genetics ; Neoplastic Stem Cells/metabolism ; Neoplastic Stem Cells/pathology ; Cell Line, Tumor ; Genetic Heterogeneity ; Promoter Regions, Genetic/genetics ; Transcription, Genetic ; Enhancer Elements, Genetic/genetics ; Chromosomes, Human/genetics
Chemical Substances	Chromatin
Language	English
Publishing date	2024-05-09
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; 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/s41467-024-48053-2
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Article: Competition between transcription and loop extrusion modulates promoter and enhancer dynamics.

Platania, Angeliki / Erb, Cathie / Barbieri, Mariano / Molcrette, Bastien / Grandgirard, Erwan / de Kort, Marit Ac / Meaburn, Karen / Taylor, Tiegh / Shchuka, Virlana M / Kocanova, Silvia / Oliveira, Guilherme Monteiro / Mitchell, Jennifer A / Soutoglou, Evi / Lenstra, Tineke L / Molina, Nacho / Papantonis, Argyris / Bystricky, Kerstin / Sexton, Tom

bioRxiv : the preprint server for biology

2023

Abstract: The spatiotemporal configuration of genes with distal regulatory elements, and the impact of chromatin mobility on transcription, remain unclear. Loop extrusion is an attractive model for bringing genetic elements together, but how this functionally ... ...

Abstract	The spatiotemporal configuration of genes with distal regulatory elements, and the impact of chromatin mobility on transcription, remain unclear. Loop extrusion is an attractive model for bringing genetic elements together, but how this functionally interacts with transcription is also largely unknown. We combine live tracking of genomic loci and nascent transcripts with molecular dynamics simulations to assess the 4D arrangement of the
Language	English
Publishing date	2023-04-26
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.04.25.538222
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Article: Competition between transcription and loop extrusion modulates promoter and enhancer dynamics.

Sexton, Tom / Platania, Angeliki / Erb, Cathie / Barbieri, Mariano / Molcrette, Bastien / Grandgirard, Erwan / de Kort, Marit / Meabum, Karen / Taylor, Tiegh / Shchuka, Virlana / Kocanova, Silvia / Oliveira, Guilherme / Mitchell, Jennifer / Soutoglou, Evi / Lenstra, Tineke / Molina, Nacho / Papantonis, Argyris / Bystricky, Keratin

Research square

2023

Abstract	The spatiotemporal configuration of genes with distal regulatory elements, and the impact of chromatin mobility on transcription, remain unclear. Loop extrusion is an attractive model for bringing genetic elements together, but how this functionally interacts with transcription is also largely unknown. We combine live tracking of genomic loci and nascent transcripts with molecular dynamics simulations to assess the spatiotemporal arrangement of the
Language	English
Publishing date	2023-08-16
Publishing country	United States
Document type	Preprint
DOI	10.21203/rs.3.rs-3164817/v1
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Article: Inference of chromosome 3D structures from GAM data by a physics computational approach

Fiorillo, Luca / Bianco, Simona / Chiariello, Andrea M / Barbieri, Mariano / Esposito, Andrea / Annunziatella, Carlo / Conte, Mattia / Corrado, Alfonso / Prisco, Antonella / Pombo, Ana / Nicodemi, Mario

Methods. 2019 Sept. 27,

2019

Abstract: The combination of modelling and experimental advances can provide deep insights for understanding chromatin 3D organization and ultimately its underlying mechanisms. In particular, models of polymer physics can help comprehend the complexity of genomic ... ...

Abstract	The combination of modelling and experimental advances can provide deep insights for understanding chromatin 3D organization and ultimately its underlying mechanisms. In particular, models of polymer physics can help comprehend the complexity of genomic contact maps, as those emerging from technologies such as Hi-C, GAM or SPRITE. Here we discuss a method to reconstruct 3D structures from Genome Architecture Mapping (GAM) data, based on PRISMR, a computational approach introduced to find the minimal polymer model best describing Hi-C input data from only polymer physics. After recapitulating the PRISMR procedure, we describe how we extended it for treating GAM data. We successfully test the method on a 6 Mb region around the Sox9 gene and, at a lower resolution, on the whole chromosome 7 in mouse embryonic stem cells. The PRISMR derived 3D structures from GAM co-segregation data are finally validated against independent Hi-C contact maps. The method results to be versatile and robust, hinting that it can be similarly applied to different experimental data, such as SPRITE or microscopy distance data.
Keywords	chromatin ; embryonic stem cells ; genes ; genomics ; mice ; microscopy ; models ; physics ; polymers
Language	English
Dates of publication	2019-0927
Publishing place	Elsevier Inc.
Document type	Article
Note	Pre-press version
ZDB-ID	1066584-5
ISSN	1095-9130 ; 1046-2023
ISSN (online)	1095-9130
ISSN	1046-2023
DOI	10.1016/j.ymeth.2019.09.018
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Inference of chromosome 3D structures from GAM data by a physics computational approach.

Methods (San Diego, Calif.)

2019 Volume 181-182, Page(s) 70–79

Abstract	The combination of modelling and experimental advances can provide deep insights for understanding chromatin 3D organization and ultimately its underlying mechanisms. In particular, models of polymer physics can help comprehend the complexity of genomic contact maps, as those emerging from technologies such as Hi-C, GAM or SPRITE. Here we discuss a method to reconstruct 3D structures from Genome Architecture Mapping (GAM) data, based on PRISMR, a computational approach introduced to find the minimal polymer model best describing Hi-C input data from only polymer physics. After recapitulating the PRISMR procedure, we describe how we extended it for treating GAM data. We successfully test the method on a 6 Mb region around the Sox9 gene and, at a lower resolution, on the whole chromosome 7 in mouse embryonic stem cells. The PRISMR derived 3D structures from GAM co-segregation data are finally validated against independent Hi-C contact maps. The method results to be versatile and robust, hinting that it can be similarly applied to different experimental data, such as SPRITE or microscopy distance data.
MeSH term(s)	Animals ; Chromosome Mapping/methods ; Chromosomes/chemistry ; Chromosomes/genetics ; Genetic Loci ; Genome ; Mice ; Models, Chemical ; Molecular Conformation ; Mouse Embryonic Stem Cells ; Physics/methods ; Polymers/chemistry ; SOX9 Transcription Factor/genetics
Chemical Substances	Polymers ; SOX9 Transcription Factor ; Sox9 protein, mouse
Language	English
Publishing date	2019-10-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1066584-5
ISSN	1095-9130 ; 1046-2023
ISSN (online)	1095-9130
ISSN	1046-2023
DOI	10.1016/j.ymeth.2019.09.018
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Article ; Online: Conformation regulation of the X chromosome inactivation center: a model.

Scialdone, Antonio / Cataudella, Ilaria / Barbieri, Mariano / Prisco, Antonella / Nicodemi, Mario

PLoS computational biology

2011 Volume 7, Issue 10, Page(s) e1002229

Abstract: X-Chromosome Inactivation (XCI) is the process whereby one, randomly chosen X becomes transcriptionally silenced in female cells. XCI is governed by the Xic, a locus on the X encompassing an array of genes which interact with each other and with key ... ...

Abstract	X-Chromosome Inactivation (XCI) is the process whereby one, randomly chosen X becomes transcriptionally silenced in female cells. XCI is governed by the Xic, a locus on the X encompassing an array of genes which interact with each other and with key molecular factors. The mechanism, though, establishing the fate of the X's, and the corresponding alternative modifications of the Xic architecture, is still mysterious. In this study, by use of computer simulations, we explore the scenario where chromatin conformations emerge from its interaction with diffusing molecular factors. Our aim is to understand the physical mechanisms whereby stable, non-random conformations are established on the Xic's, how complex architectural changes are reliably regulated, and how they lead to opposite structures on the two alleles. In particular, comparison against current experimental data indicates that a few key cis-regulatory regions orchestrate the organization of the Xic, and that two major molecular regulators are involved.
MeSH term(s)	Animals ; Cell Nucleus/chemistry ; Cell Nucleus/genetics ; Chromatin/chemistry ; Chromatin/genetics ; Chromatin Assembly and Disassembly ; Computational Biology ; Computer Simulation ; Female ; Male ; Mice ; Models, Genetic ; Thermodynamics ; X Chromosome Inactivation
Chemical Substances	Chromatin
Language	English
Publishing date	2011-10-27
Publishing country	United States
Document type	Journal Article
ZDB-ID	2193340-6
ISSN	1553-7358 ; 1553-734X
ISSN (online)	1553-7358
ISSN	1553-734X
DOI	10.1371/journal.pcbi.1002229
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Article: A polymer model explains the complexity of large-scale chromatin folding

Barbieri, Mariano / Fraser, James / Lavitas, Liron-Mark / Chotalia, Mita / Dostie, Josée / Pombo, Ana / Nicodemi, Mario

Nucleus. 2013 July 1, v. 4, no. 4

2013

Abstract: The underlying global organization of chromatin within the cell nucleus has been the focus of intense recent research. Hi-C methods have allowed for the detection of genome-wide chromatin interactions, revealing a complex large-scale organization where ... ...

Abstract	The underlying global organization of chromatin within the cell nucleus has been the focus of intense recent research. Hi-C methods have allowed for the detection of genome-wide chromatin interactions, revealing a complex large-scale organization where chromosomes tend to partition into megabase-sized “topological domains” of local chromatin interactions and intra-chromosomal contacts extends over much longer scales, in a cell-type and chromosome specific manner. Until recently, the distinct chromatin folding properties observed experimentally have been difficult to explain in a single conceptual framework. We reported that a simple polymer-physics model of chromatin, the strings and binders switch (SBS) model, succeeds in describing the full range of chromatin configurations observed in vivo. The SBS model simulates the interactions between randomly diffusing binding molecules and binding sites on a polymer chain. It explains how polymer architectural patterns can be established, how different stable conformations can be produced and how conformational changes can be reliably regulated by simple strategies, such as protein upregulation or epigenetic modifications, via fundamental thermodynamics mechanisms.
Keywords	chromatin ; epigenetics ; models ; polymers ; thermodynamics
Language	English
Dates of publication	2013-0701
Size	p. 267-273.
Publishing place	Taylor & Francis
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	2619626-8
ISSN	1949-1042 ; 1949-1034
ISSN (online)	1949-1042
ISSN	1949-1034
DOI	10.4161/nucl.25432
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Article ; Online: Active and poised promoter states drive folding of the extended HoxB locus in mouse embryonic stem cells.

Barbieri, Mariano / Xie, Sheila Q / Torlai Triglia, Elena / Chiariello, Andrea M / Bianco, Simona / de Santiago, Inês / Branco, Miguel R / Rueda, David / Nicodemi, Mario / Pombo, Ana

Nature structural & molecular biology

2017 Volume 24, Issue 6, Page(s) 515–524

Abstract: Gene expression states influence the 3D conformation of the genome through poorly understood mechanisms. Here, we investigate the conformation of the murine HoxB locus, a gene-dense genomic region containing closely spaced genes with distinct activation ... ...

Abstract	Gene expression states influence the 3D conformation of the genome through poorly understood mechanisms. Here, we investigate the conformation of the murine HoxB locus, a gene-dense genomic region containing closely spaced genes with distinct activation states in mouse embryonic stem (ES) cells. To predict possible folding scenarios, we performed computer simulations of polymer models informed with different chromatin occupancy features that define promoter activation states or binding sites for the transcription factor CTCF. Single-cell imaging of the locus folding was performed to test model predictions. While CTCF occupancy alone fails to predict the in vivo folding at genomic length scale of 10 kb, we found that homotypic interactions between active and Polycomb-repressed promoters co-occurring in the same DNA fiber fully explain the HoxB folding patterns imaged in single cells. We identify state-dependent promoter interactions as major drivers of chromatin folding in gene-dense regions.
MeSH term(s)	Animals ; Chromatin/metabolism ; Computer Simulation ; DNA/chemistry ; DNA/metabolism ; Embryonic Stem Cells/physiology ; Fluorescent Antibody Technique ; Genetic Loci ; In Situ Hybridization, Fluorescence ; Mice ; Microscopy, Confocal ; Nucleic Acid Conformation ; Promoter Regions, Genetic ; Protein Binding ; Single-Cell Analysis ; Transcription Factors/metabolism
Chemical Substances	Chromatin ; Transcription Factors ; DNA (9007-49-2)
Language	English
Publishing date	2017-04-24
Publishing country	United States
Document type	Journal Article
ZDB-ID	2126708-X
ISSN	1545-9985 ; 1545-9993
ISSN (online)	1545-9985
ISSN	1545-9993
DOI	10.1038/nsmb.3402
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Article ; Online: A polymer model explains the complexity of large-scale chromatin folding.

Barbieri, Mariano / Fraser, James / Lavitas, Liron-Mark / Chotalia, Mita / Dostie, Josée / Pombo, Ana / Nicodemi, Mario

Nucleus (Austin, Tex.)

2013 Volume 4, Issue 4, Page(s) 267–273

Abstract	The underlying global organization of chromatin within the cell nucleus has been the focus of intense recent research. Hi-C methods have allowed for the detection of genome-wide chromatin interactions, revealing a complex large-scale organization where chromosomes tend to partition into megabase-sized "topological domains" of local chromatin interactions and intra-chromosomal contacts extends over much longer scales, in a cell-type and chromosome specific manner. Until recently, the distinct chromatin folding properties observed experimentally have been difficult to explain in a single conceptual framework. We reported that a simple polymer-physics model of chromatin, the strings and binders switch (SBS) model, succeeds in describing the full range of chromatin configurations observed in vivo. The SBS model simulates the interactions between randomly diffusing binding molecules and binding sites on a polymer chain. It explains how polymer architectural patterns can be established, how different stable conformations can be produced and how conformational changes can be reliably regulated by simple strategies, such as protein upregulation or epigenetic modifications, via fundamental thermodynamics mechanisms.
MeSH term(s)	Cell Nucleus ; Chromatin/chemistry ; Chromatin/metabolism ; Humans ; Models, Molecular ; Polymers/chemistry ; Polymers/metabolism
Chemical Substances	Chromatin ; Polymers
Language	English
Publishing date	2013-06-19
Publishing country	United States
Document type	Journal Article
ZDB-ID	2619626-8
ISSN	1949-1042 ; 1949-1034
ISSN (online)	1949-1042
ISSN	1949-1034
DOI	10.4161/nucl.25432
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