Heterochromatin drives compartmentalization of inverted and conventional nuclei.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
06 2019
Historique:
received: 11 01 2018
accepted: 26 04 2019
pubmed: 7 6 2019
medline: 6 2 2020
entrez: 7 6 2019
Statut: ppublish

Résumé

The nucleus of mammalian cells displays a distinct spatial segregation of active euchromatic and inactive heterochromatic regions of the genome

Identifiants

pubmed: 31168090
doi: 10.1038/s41586-019-1275-3
pii: 10.1038/s41586-019-1275-3
pmc: PMC7206897
mid: NIHMS1058556
doi:

Substances chimiques

Euchromatin 0
Heterochromatin 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

395-399

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM114190
Pays : United States
Organisme : NHGRI NIH HHS
ID : R01 HG003143
Pays : United States
Organisme : NHGRI NIH HHS
ID : RM1 HG007743
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Organisme : NIDDK NIH HHS
ID : U54 DK107980
Pays : United States

Commentaires et corrections

Type : ErratumIn

Références

Solovei, I., Thanisch, K. & Feodorova, Y. How to rule the nucleus: divide et impera. Curr. Opin. Cell Biol. 40, 47–59 (2016).
doi: 10.1016/j.ceb.2016.02.014
van Steensel, B. & Belmont, A. S. Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression. Cell 169, 780–791 (2017).
doi: 10.1016/j.cell.2017.04.022
Bonev, B. & Cavalli, G. Organization and function of the 3D genome. Nat. Rev. Genet. 17, 661–678 (2016).
doi: 10.1038/nrg.2016.112
Jerabek, H. & Heermann, D. W. How chromatin looping and nuclear envelope attachment affect genome organization in eukaryotic cell nuclei. Int. Rev. Cell Mol. Biol. 307, 351–381 (2014).
doi: 10.1016/B978-0-12-800046-5.00010-2
Jost, D., Carrivain, P., Cavalli, G. & Vaillant, C. Modeling epigenome folding: formation and dynamics of topologically associated chromatin domains. Nucleic Acids Res. 42, 9553–9561 (2014).
doi: 10.1093/nar/gku698
Lee, S. S., Tashiro, S., Awazu, A. & Kobayashi, R. A new application of the phase-field method for understanding the mechanisms of nuclear architecture reorganization. J. Math. Biol. 74, 333–354 (2017).
doi: 10.1007/s00285-016-1031-3
Di Pierro, M., Zhang, B., Aiden, E. L., Wolynes, P. G. & Onuchic, J. N. Transferable model for chromosome architecture. Proc. Natl Acad. Sci. USA 113, 12168–12173 (2016).
doi: 10.1073/pnas.1613607113
Nuebler, J., Fudenberg, G., Imakaev, M., Abdennur, N. & Mirny, L. A. Chromatin organization by an interplay of loop extrusion and compartmental segregation. Proc. Natl Acad. Sci. USA 115, E6697–E6706 (2018).
van de Werken, H. J. G. et al. Small chromosomal regions position themselves autonomously according to their chromatin class. Genome Res. 27, 922–933 (2017).
doi: 10.1101/gr.213751.116
Larson, A. G. et al. Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin. Nature 547, 236–240 (2017).
doi: 10.1038/nature22822
Strom, A. R. et al. Phase separation drives heterochromatin domain formation. Nature 547, 241–245 (2017).
doi: 10.1038/nature22989
Machida, S. et al. Structural basis of heterochromatin formation by human HP1. Mol. Cell 69, 385–397 (2018).
doi: 10.1016/j.molcel.2017.12.011
Ganai, N., Sengupta, S. & Menon, G. I. Chromosome positioning from activity-based segregation. Nucleic Acids Res. 42, 4145–4159 (2014).
doi: 10.1093/nar/gkt1417
Grosberg, A. Y. & Joanny, J.-F. Nonequilibrium statistical mechanics of mixtures of particles in contact with different thermostats. Phys. Rev. E 92, 032118 (2015).
doi: 10.1103/PhysRevE.92.032118
Smrek, J. & Kremer, K. Small activity differences drive phase separation in active–passive polymer mixtures. Phys. Rev. Lett. 118, 098002 (2017).
doi: 10.1103/PhysRevLett.118.098002
Stevens, T. J. et al. 3D structures of individual mammalian genomes studied by single-cell Hi-C. Nature 544, 59–64 (2017).
doi: 10.1038/nature21429
Hilbert, L. et al. Transcription organizes euchromatin similar to an active microemulsion. Preprint at https://www.biorxiv.org/content/10.1101/234112v2 (2018).
Zheng, X. et al. Lamins organize the global three-dimensional genome from the nuclear periphery. Mol. Cell 71, 802–815 (2018).
doi: 10.1016/j.molcel.2018.05.017
Solovei, I. et al. Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137, 356–368 (2009).
doi: 10.1016/j.cell.2009.01.052
Solovei, I. et al. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152, 584–598 (2013).
doi: 10.1016/j.cell.2013.01.009
Eberhart, A. et al. Epigenetics of eu- and heterochromatin in inverted and conventional nuclei from mouse retina. Chromosome Res. 21, 535–554 (2013).
doi: 10.1007/s10577-013-9375-7
Tan, L., Xing, D., Chang, C.-H., Li, H. & Xie, X. S. Three-dimensional genome structures of single sensory neurons in mouse visual and olfactory systems. Nat. Struct. Mol. Biol. 26, 297–307 (2019).
Imakaev, M. et al. Iterative correction of Hi-C data reveals hallmarks of chromosome organization. Nat. Methods 9, 999–1003 (2012).
doi: 10.1038/nmeth.2148
Ou, H. D. et al. ChromEMT: visualizing 3D chromatin structure and compaction in interphase and mitotic cells. Science 357, eaag0025 (2017).
doi: 10.1126/science.aag0025
Choo, K. H. A. The Centromere (Oxford Univ. Press, 1997).
Rubinstein, M. & Colby, R. H. Polymer Physics (Oxford Univ. Press, 2003).
Biggs, R., Liu, P. Z., Stephens, A. D. & Marko, J. F. Effects of altering histone posttranslational modifications on mitotic chromosome structure and mechanics. Mol. Biol. Cell 30, 820–827 (2019).
doi: 10.1091/mbc.E18-09-0592
Helmlinger, D. et al. Glutamine-expanded ataxin-7 alters TFTC/STAGA recruitment and chromatin structure leading to photoreceptor dysfunction. PLoS Biol. 4, e67 (2006).
doi: 10.1371/journal.pbio.0040067
Tang, S.-J. Chromatin organization by repetitive elements (CORE): a genomic principle for the higher-order structure of chromosomes. Genes 2, 502–515 (2011).
doi: 10.3390/genes2030502
Rosa, A. & Everaers, R. Structure and dynamics of interphase chromosomes. PLOS Comput. Biol. 4, e1000153 (2008).
doi: 10.1371/journal.pcbi.1000153
Solovei, I. Fluorescence in situ hybridization (FISH) on tissue cryosections. in Methods Mol. Biol. 659, 71–82 (2010).
doi: 10.1007/978-1-60761-789-1_5
Eberhart, A., Kimura, H., Leonhardt, H., Joffe, B. & Solovei, I. Reliable detection of epigenetic histone marks and nuclear proteins in tissue cryosections. Chromosome Res. 20, 849–858 (2012).
doi: 10.1007/s10577-012-9318-8
Cremer, M. et al. Multicolor 3D fluorescence in situ hybridization for imaging interphase chromosomes. Methods Mol. Biol. 463, 205–239 (2018).
doi: 10.1007/978-1-59745-406-3_15
Walter, J. et al. Towards many colors in FISH on 3D-preserved interphase nuclei. Cytogenet. Genome Res. 114, 367–378 (2006).
doi: 10.1159/000094227
Feodorova, Y., Koch, M., Bultman, S., Michalakis, S. & Solovei, I. Quick and reliable method for retina dissociation and separation of rod photoreceptor perikarya from adult mice. MethodsX 2, 39–46 (2015).
doi: 10.1016/j.mex.2015.01.002
Cohen, T. V. et al. The lamin B receptor under transcriptional control of C/EBPε is required for morphological but not functional maturation of neutrophils. Hum. Mol. Genet. 17, 2921–2933 (2008).
doi: 10.1093/hmg/ddn191
Naumova, N. et al. Organization of the mitotic chromosome. Science 342, 948–953 (2013).
doi: 10.1126/science.1236083
Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010).
doi: 10.1016/j.molcel.2010.05.004
Nora, E. P. et al. Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. Cell 169, 930–944 (2017).
doi: 10.1016/j.cell.2017.05.004
Flyamer, I. M. et al. Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. Nature 544, 110–114 (2017).
doi: 10.1038/nature21711
Crane, E. et al. Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature 523, 240–244 (2015).
doi: 10.1038/nature14450
Eastman, P. et al. OpenMM 4: a reusable, extensible, hardware independent library for high performance molecular simulation. J. Chem. Theory Comput. 9, 461–469 (2013).
doi: 10.1021/ct300857j
Eastman, P. et al. OpenMM 7: rapid development of high performance algorithms for molecular dynamics. PLOS Comput. Biol. 13, e1005659 (2017).
doi: 10.1371/journal.pcbi.1005659
Abdennur, N. & Mirny, L. Cooler: scalable storage for Hi-C data and other genomically-labeled arrays. Preprint at https://www.biorxiv.org/content/10.1101/557660v1 (2019).
Shultz, L. D. et al. Mutations at the mouse ichthyosis locus are within the lamin B receptor gene: a single gene model for human Pelger–Huët anomaly. Hum. Mol. Genet. 12, 61–69 (2003).
doi: 10.1093/hmg/ddg003
Dixon, J. R. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376–380 (2012).
doi: 10.1038/nature11082
Rao, S. S. P. et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665–1680 (2014).
doi: 10.1016/j.cell.2014.11.021
Schwarzer, W. et al. Two independent modes of chromatin organization revealed by cohesin removal. Nature 551, 51–56 (2017).
doi: 10.1038/nature24281
Grant, C. E., Bailey, T. L. & Noble, W. S. FIMO: scanning for occurrences of a given motif. Bioinformatics 27, 1017–1018 (2011).
doi: 10.1093/bioinformatics/btr064
Schmidt, D. et al. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148, 335–348 (2012).
doi: 10.1016/j.cell.2011.11.058
Kerpedjiev, P. et al. HiGlass: web-based visual exploration and analysis of genome interaction maps. Genome Biol. 19, 125 (2018).
doi: 10.1186/s13059-018-1486-1
Zhang, Y. et al. Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell 148, 908–921 (2012).
doi: 10.1016/j.cell.2012.02.002
Lin, Y. C. et al. Global changes in the nuclear positioning of genes and intra- and interdomain genomic interactions that orchestrate B cell fate. Nat. Immunol. 13, 1196–1204 (2012).
doi: 10.1038/ni.2432
Kizilyaprak, C., Spehner, D., Devys, D. & Schultz, P. In vivo chromatin organization of mouse rod photoreceptors correlates with histone modifications. PLoS ONE 5, e11039 (2010).
doi: 10.1371/journal.pone.0011039

Auteurs

Martin Falk (M)

Institute for Medical Engineering and Science, and Department of Physics, Massachusetts Institute of Technology, Cambridge, MA, USA.

Yana Feodorova (Y)

Department of Medical Biology, Medical University-Plovdiv, Plovdiv, Bulgaria.
Biozentrum, Ludwig Maximilians University Munich, Planegg-Martinsried, Germany.

Natalia Naumova (N)

Howard Hughes Medical Institute, and Program in Systems Biology, Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, MA, USA.
Epinomics Inc, Menlo Park, CA, USA.

Maxim Imakaev (M)

Institute for Medical Engineering and Science, and Department of Physics, Massachusetts Institute of Technology, Cambridge, MA, USA.

Bryan R Lajoie (BR)

Howard Hughes Medical Institute, and Program in Systems Biology, Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, MA, USA.
Illumina Inc, San Diego, CA, USA.

Heinrich Leonhardt (H)

Biozentrum, Ludwig Maximilians University Munich, Planegg-Martinsried, Germany.

Boris Joffe (B)

Biozentrum, Ludwig Maximilians University Munich, Planegg-Martinsried, Germany.

Job Dekker (J)

Howard Hughes Medical Institute, and Program in Systems Biology, Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, MA, USA.

Geoffrey Fudenberg (G)

Institute for Medical Engineering and Science, and Department of Physics, Massachusetts Institute of Technology, Cambridge, MA, USA. geoff.fudenberg@gmail.com.
Gladstone Institutes of Data Science and Biotechnology, University of California, San Francisco, San Francisco, CA, USA. geoff.fudenberg@gmail.com.

Irina Solovei (I)

Biozentrum, Ludwig Maximilians University Munich, Planegg-Martinsried, Germany. irina.solovei@lrz.uni-muenchen.de.

Leonid A Mirny (LA)

Institute for Medical Engineering and Science, and Department of Physics, Massachusetts Institute of Technology, Cambridge, MA, USA. leonid@mit.edu.

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