Hierarchical folding and reorganization of chromosomes are linked to transcriptional changes in cellular differentiation
Mammalian chromosomes fold into arrays of megabase‐sized topologically associating domains (TADs), which are arranged into compartments spanning multiple megabases of genomic DNA. TADs have internal substructures that are often cell type specific, but their higher‐order organization remains elusive....
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| Published in | Molecular systems biology Vol. 11; no. 12; pp. 852 - n/a |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.12.2015
EMBO Press John Wiley and Sons Inc Springer Nature |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Mammalian chromosomes fold into arrays of megabase‐sized topologically associating domains (TADs), which are arranged into compartments spanning multiple megabases of genomic DNA. TADs have internal substructures that are often cell type specific, but their higher‐order organization remains elusive. Here, we investigate TAD higher‐order interactions with Hi‐C through neuronal differentiation and show that they form a hierarchy of domains‐within‐domains (metaTADs) extending across genomic scales up to the range of entire chromosomes. We find that TAD interactions are well captured by tree‐like, hierarchical structures irrespective of cell type. metaTAD tree structures correlate with genetic, epigenomic and expression features, and structural tree rearrangements during differentiation are linked to transcriptional state changes. Using polymer modelling, we demonstrate that hierarchical folding promotes efficient chromatin packaging without the loss of contact specificity, highlighting a role far beyond the simple need for packing efficiency.
Synopsis
Genome‐wide mapping of chromatin architecture reveals a hierarchical folding of chromatin that involves higher‐order domains interactions across the whole chromosomes, reflects epigenomic features and reorganizes upon differentiation‐induced gene expression changes.
Chromatin architecture is mapped genome‐wide using Hi‐C and a neuronal differentiation model from mESC to post‐mitotic neurons.
Mammalian chromosomes fold hierarchically in a manner that reflects epigenomic features and involves higher‐order domains (metaTADs) up to the chromosome scale.
metaTAD topologies are relatively conserved through differentiation, and their reorganization is related to gene expression changes.
Polymer modelling shows that hierarchical chromatin folding promotes efficient packaging without the loss of contact specificity.
Graphical Abstract
Genome‐wide mapping of chromatin architecture reveals a hierarchical folding of chromatin that involves higher‐order domains interactions across the whole chromosomes, reflects epigenomic features and reorganizes upon differentiation‐induced gene expression changes. |
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| AbstractList | Abstract Mammalian chromosomes fold into arrays of megabase‐sized topologically associating domains (TADs), which are arranged into compartments spanning multiple megabases of genomic DNA. TADs have internal substructures that are often cell type specific, but their higher‐order organization remains elusive. Here, we investigate TAD higher‐order interactions with Hi‐C through neuronal differentiation and show that they form a hierarchy of domains‐within‐domains (metaTADs) extending across genomic scales up to the range of entire chromosomes. We find that TAD interactions are well captured by tree‐like, hierarchical structures irrespective of cell type. metaTAD tree structures correlate with genetic, epigenomic and expression features, and structural tree rearrangements during differentiation are linked to transcriptional state changes. Using polymer modelling, we demonstrate that hierarchical folding promotes efficient chromatin packaging without the loss of contact specificity, highlighting a role far beyond the simple need for packing efficiency. Mammalian chromosomes fold into arrays of megabase‐sized topologically associating domains ( TAD s), which are arranged into compartments spanning multiple megabases of genomic DNA . TAD s have internal substructures that are often cell type specific, but their higher‐order organization remains elusive. Here, we investigate TAD higher‐order interactions with Hi‐C through neuronal differentiation and show that they form a hierarchy of domains‐within‐domains (meta TAD s) extending across genomic scales up to the range of entire chromosomes. We find that TAD interactions are well captured by tree‐like, hierarchical structures irrespective of cell type. meta TAD tree structures correlate with genetic, epigenomic and expression features, and structural tree rearrangements during differentiation are linked to transcriptional state changes. Using polymer modelling, we demonstrate that hierarchical folding promotes efficient chromatin packaging without the loss of contact specificity, highlighting a role far beyond the simple need for packing efficiency. Mammalian chromosomes fold into arrays of megabase-sized topologically associating domains (TADs), which are arranged into compartments spanning multiple megabases of genomic DNA. TADs have internal substructures that are often cell type specific, but their higher-order organization remains elusive. Here, we investigate TAD higher-order interactions with Hi-C through neuronal differentiation and show that they form a hierarchy of domains-within-domains (metaTADs) extending across genomic scales up to the range of entire chromosomes. We find that TAD interactions are well captured by tree-like, hierarchical structures irrespective of cell type. metaTAD tree structures correlate with genetic, epigenomic and expression features, and structural tree rearrangements during differentiation are linked to transcriptional state changes. Using polymer modelling, we demonstrate that hierarchical folding promotes efficient chromatin packaging without the loss of contact specificity, highlighting a role far beyond the simple need for packing efficiency. Mammalian chromosomes fold into arrays of megabase‐sized topologically associating domains (TADs), which are arranged into compartments spanning multiple megabases of genomic DNA. TADs have internal substructures that are often cell type specific, but their higher‐order organization remains elusive. Here, we investigate TAD higher‐order interactions with Hi‐C through neuronal differentiation and show that they form a hierarchy of domains‐within‐domains (metaTADs) extending across genomic scales up to the range of entire chromosomes. We find that TAD interactions are well captured by tree‐like, hierarchical structures irrespective of cell type. metaTAD tree structures correlate with genetic, epigenomic and expression features, and structural tree rearrangements during differentiation are linked to transcriptional state changes. Using polymer modelling, we demonstrate that hierarchical folding promotes efficient chromatin packaging without the loss of contact specificity, highlighting a role far beyond the simple need for packing efficiency. Synopsis Genome‐wide mapping of chromatin architecture reveals a hierarchical folding of chromatin that involves higher‐order domains interactions across the whole chromosomes, reflects epigenomic features and reorganizes upon differentiation‐induced gene expression changes. Chromatin architecture is mapped genome‐wide using Hi‐C and a neuronal differentiation model from mESC to post‐mitotic neurons. Mammalian chromosomes fold hierarchically in a manner that reflects epigenomic features and involves higher‐order domains (metaTADs) up to the chromosome scale. metaTAD topologies are relatively conserved through differentiation, and their reorganization is related to gene expression changes. Polymer modelling shows that hierarchical chromatin folding promotes efficient packaging without the loss of contact specificity. Genome‐wide mapping of chromatin architecture reveals a hierarchical folding of chromatin that involves higher‐order domains interactions across the whole chromosomes, reflects epigenomic features and reorganizes upon differentiation‐induced gene expression changes. Mammalian chromosomes fold into arrays of megabase‐sized topologically associating domains (TADs), which are arranged into compartments spanning multiple megabases of genomic DNA. TADs have internal substructures that are often cell type specific, but their higher‐order organization remains elusive. Here, we investigate TAD higher‐order interactions with Hi‐C through neuronal differentiation and show that they form a hierarchy of domains‐within‐domains (metaTADs) extending across genomic scales up to the range of entire chromosomes. We find that TAD interactions are well captured by tree‐like, hierarchical structures irrespective of cell type. metaTAD tree structures correlate with genetic, epigenomic and expression features, and structural tree rearrangements during differentiation are linked to transcriptional state changes. Using polymer modelling, we demonstrate that hierarchical folding promotes efficient chromatin packaging without the loss of contact specificity, highlighting a role far beyond the simple need for packing efficiency. Synopsis Genome‐wide mapping of chromatin architecture reveals a hierarchical folding of chromatin that involves higher‐order domains interactions across the whole chromosomes, reflects epigenomic features and reorganizes upon differentiation‐induced gene expression changes. Chromatin architecture is mapped genome‐wide using Hi‐C and a neuronal differentiation model from mESC to post‐mitotic neurons. Mammalian chromosomes fold hierarchically in a manner that reflects epigenomic features and involves higher‐order domains (metaTADs) up to the chromosome scale. metaTAD topologies are relatively conserved through differentiation, and their reorganization is related to gene expression changes. Polymer modelling shows that hierarchical chromatin folding promotes efficient packaging without the loss of contact specificity. Graphical Abstract Genome‐wide mapping of chromatin architecture reveals a hierarchical folding of chromatin that involves higher‐order domains interactions across the whole chromosomes, reflects epigenomic features and reorganizes upon differentiation‐induced gene expression changes. |
| Author | Schueler, Markus Pombo, Ana Kraemer, Dorothee CA Nicodemi, Mario Carninci, Piero Forrest, Alistair RR Morris, Kelly J Chiariello, Andrea M Xie, Sheila Q Hayashizaki, Yoshihide Fraser, James Rito, Tiago Aitken, Stuart Ferrai, Carmelo Laudanno, Giovanni Jaeger, Ines Semple, Colin A Kawaji, Hideya Moore, Benjamin L Dostie, Josée Itoh, Masayoshi Barbieri, Mariano |
| AuthorAffiliation | 6 RIKEN Preventive Medicine and Diagnosis Innovation Program Wako Saitama Japan 1 Department of Biochemistry Goodman Cancer Centre McGill University Montréal QC Canada 7 Division of Genomic Technologies RIKEN Center for Life Science Technologies Yokohama Kanagawa Japan 9 Single Molecule Imaging Group MRC Clinical Sciences Centre Imperial College London Hammersmith Hospital Campus London UK 10 Cardiff School of Biosciences Cardiff UK 2 Epigenetic Regulation and Chromatin Architecture Group Berlin Institute for Medical Systems Biology Max‐Delbrück Centre for Molecular Medicine Berlin‐Buch Germany 3 Genome Function Group MRC Clinical Sciences Centre Imperial College London Hammersmith Hospital Campus London UK 11 Systems Biology and Genomics Harry Perkins Institute of Medical Research Nedlands WA Australia 4 Dipartimento di Fisica Università di Napoli Federico II INFN Napoli CNR‐SPIN Complesso Universitario di Monte Sant'Angelo Naples Italy 5 MRC Human Genetics Unit MRC IGMM University of Edinburg |
| AuthorAffiliation_xml | – name: 2 Epigenetic Regulation and Chromatin Architecture Group Berlin Institute for Medical Systems Biology Max‐Delbrück Centre for Molecular Medicine Berlin‐Buch Germany – name: 6 RIKEN Preventive Medicine and Diagnosis Innovation Program Wako Saitama Japan – name: 4 Dipartimento di Fisica Università di Napoli Federico II INFN Napoli CNR‐SPIN Complesso Universitario di Monte Sant'Angelo Naples Italy – name: 11 Systems Biology and Genomics Harry Perkins Institute of Medical Research Nedlands WA Australia – name: 10 Cardiff School of Biosciences Cardiff UK – name: 8 Stem Cell Neurogenesis Group MRC Clinical Sciences Centre Imperial College London Hammersmith Hospital Campus London UK – name: 5 MRC Human Genetics Unit MRC IGMM University of Edinburgh Edinburgh UK – name: 9 Single Molecule Imaging Group MRC Clinical Sciences Centre Imperial College London Hammersmith Hospital Campus London UK – name: 1 Department of Biochemistry Goodman Cancer Centre McGill University Montréal QC Canada – name: 3 Genome Function Group MRC Clinical Sciences Centre Imperial College London Hammersmith Hospital Campus London UK – name: 7 Division of Genomic Technologies RIKEN Center for Life Science Technologies Yokohama Kanagawa Japan |
| Author_xml | – sequence: 1 givenname: James surname: Fraser fullname: Fraser, James organization: Department of Biochemistry, Goodman Cancer Centre, McGill University – sequence: 2 givenname: Carmelo surname: Ferrai fullname: Ferrai, Carmelo organization: Epigenetic Regulation and Chromatin Architecture Group, Berlin Institute for Medical Systems Biology, Max‐Delbrück Centre for Molecular Medicine, Genome Function Group, MRC Clinical Sciences Centre, Imperial College London, Hammersmith Hospital Campus – sequence: 3 givenname: Andrea M surname: Chiariello fullname: Chiariello, Andrea M organization: Dipartimento di Fisica, Università di Napoli Federico II, INFN Napoli, CNR‐SPIN, Complesso Universitario di Monte Sant'Angelo – sequence: 4 givenname: Markus surname: Schueler fullname: Schueler, Markus organization: Epigenetic Regulation and Chromatin Architecture Group, Berlin Institute for Medical Systems Biology, Max‐Delbrück Centre for Molecular Medicine – sequence: 5 givenname: Tiago surname: Rito fullname: Rito, Tiago organization: Epigenetic Regulation and Chromatin Architecture Group, Berlin Institute for Medical Systems Biology, Max‐Delbrück Centre for Molecular Medicine – sequence: 6 givenname: Giovanni surname: Laudanno fullname: Laudanno, Giovanni organization: Dipartimento di Fisica, Università di Napoli Federico II, INFN Napoli, CNR‐SPIN, Complesso Universitario di Monte Sant'Angelo – sequence: 7 givenname: Mariano surname: Barbieri fullname: Barbieri, Mariano organization: Epigenetic Regulation and Chromatin Architecture Group, Berlin Institute for Medical Systems Biology, Max‐Delbrück Centre for Molecular Medicine – sequence: 8 givenname: Benjamin L surname: Moore fullname: Moore, Benjamin L organization: MRC Human Genetics Unit, MRC IGMM, University of Edinburgh – sequence: 9 givenname: Dorothee CA surname: Kraemer fullname: Kraemer, Dorothee CA organization: Epigenetic Regulation and Chromatin Architecture Group, Berlin Institute for Medical Systems Biology, Max‐Delbrück Centre for Molecular Medicine – sequence: 10 givenname: Stuart surname: Aitken fullname: Aitken, Stuart organization: MRC Human Genetics Unit, MRC IGMM, University of Edinburgh – sequence: 11 givenname: Sheila Q surname: Xie fullname: Xie, Sheila Q organization: Genome Function Group, MRC Clinical Sciences Centre, Imperial College London, Hammersmith Hospital Campus, Single Molecule Imaging Group, MRC Clinical Sciences Centre, Imperial College London, Hammersmith Hospital Campus – sequence: 12 givenname: Kelly J surname: Morris fullname: Morris, Kelly J organization: Epigenetic Regulation and Chromatin Architecture Group, Berlin Institute for Medical Systems Biology, Max‐Delbrück Centre for Molecular Medicine, Genome Function Group, MRC Clinical Sciences Centre, Imperial College London, Hammersmith Hospital Campus – sequence: 13 givenname: Masayoshi surname: Itoh fullname: Itoh, Masayoshi organization: RIKEN Preventive Medicine and Diagnosis Innovation Program, Division of Genomic Technologies, RIKEN Center for Life Science Technologies – sequence: 14 givenname: Hideya surname: Kawaji fullname: Kawaji, Hideya organization: RIKEN Preventive Medicine and Diagnosis Innovation Program, Division of Genomic Technologies, RIKEN Center for Life Science Technologies – sequence: 15 givenname: Ines surname: Jaeger fullname: Jaeger, Ines organization: Stem Cell Neurogenesis Group, MRC Clinical Sciences Centre, Imperial College London, Hammersmith Hospital Campus, Cardiff School of Biosciences – sequence: 16 givenname: Yoshihide surname: Hayashizaki fullname: Hayashizaki, Yoshihide organization: RIKEN Preventive Medicine and Diagnosis Innovation Program – sequence: 17 givenname: Piero surname: Carninci fullname: Carninci, Piero organization: Division of Genomic Technologies, RIKEN Center for Life Science Technologies – sequence: 18 givenname: Alistair RR surname: Forrest fullname: Forrest, Alistair RR organization: Division of Genomic Technologies, RIKEN Center for Life Science Technologies, Systems Biology and Genomics, Harry Perkins Institute of Medical Research – sequence: 20 givenname: Colin A surname: Semple fullname: Semple, Colin A email: colin.semple@igmm.ed.ac.uk organization: MRC Human Genetics Unit, MRC IGMM, University of Edinburgh – sequence: 21 givenname: Josée surname: Dostie fullname: Dostie, Josée email: josee.dostie@mcgill.ca organization: Department of Biochemistry, Goodman Cancer Centre, McGill University – sequence: 22 givenname: Ana surname: Pombo fullname: Pombo, Ana email: ana.pombo@mdc-berlin.de organization: Epigenetic Regulation and Chromatin Architecture Group, Berlin Institute for Medical Systems Biology, Max‐Delbrück Centre for Molecular Medicine, Genome Function Group, MRC Clinical Sciences Centre, Imperial College London, Hammersmith Hospital Campus – sequence: 23 givenname: Mario surname: Nicodemi fullname: Nicodemi, Mario email: mario.nicodemi@na.infn.it organization: Dipartimento di Fisica, Università di Napoli Federico II, INFN Napoli, CNR‐SPIN, Complesso Universitario di Monte Sant'Angelo |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26700852$$D View this record in MEDLINE/PubMed |
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| Snippet | Mammalian chromosomes fold into arrays of megabase‐sized topologically associating domains (TADs), which are arranged into compartments spanning multiple... Mammalian chromosomes fold into arrays of megabase-sized topologically associating domains (TADs), which are arranged into compartments spanning multiple... Mammalian chromosomes fold into arrays of megabase‐sized topologically associating domains ( TAD s), which are arranged into compartments spanning multiple... Abstract Mammalian chromosomes fold into arrays of megabase‐sized topologically associating domains (TADs), which are arranged into compartments spanning... |
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| SubjectTerms | Animals Cell Differentiation Cell division Cells, Cultured Chromatin Chromatin - chemistry Chromatin Assembly and Disassembly chromatin contacts chromosome architecture Chromosomes Chromosomes - chemistry Datasets Deoxyribonucleic acid Differentiation (biology) DNA Domains EMBO09 EMBO11 EMBO17 Epigenesis, Genetic epigenetics Folding Gene expression Gene Expression Regulation Genomes Innovations Mammals Mice Mouse Embryonic Stem Cells - cytology Neurons Neurons - cytology Packaging polymer modelling Stem cells Structural hierarchy Substructures Transcription Transcription, Genetic Trees |
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| Title | Hierarchical folding and reorganization of chromosomes are linked to transcriptional changes in cellular differentiation |
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