Coupling 1D modifications and 3D nuclear organization: data, models and function.

Over the past decade, advances in molecular methods have strikingly improved the resolution at which nuclear genome folding can be analyzed. This revealed a wealth of conserved features organizing the one dimensional DNA molecule into tridimensional nuclear domains. In this review, we briefly summarize the main findings and highlight how models based on polymer physics shed light on the principles underlying the formation of these domains. Finally, we discuss the mechanistic similarities allowing self-organization of these structures and the functional importance of these in the maintenance of transcriptional programs.

[1]  Neva C. Durand,et al.  A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping , 2014, Cell.

[2]  Wolfgang Huber,et al.  Enhancer loops appear stable during development and are associated with paused polymerase , 2014, Nature.

[3]  W. D. Laat,et al.  A Decade of 3c Technologies: Insights into Nuclear Organization References , 2022 .

[4]  Jill M Dowen,et al.  Control of Cell Identity Genes Occurs in Insulated Neighborhoods in Mammalian Chromosomes , 2014, Cell.

[5]  J. Haber,et al.  Effect of Chromosome Tethering on Nuclear Organization in Yeast , 2014, PloS one.

[6]  D. Duboule,et al.  Convergent evolution of complex regulatory landscapes and pleiotropy at Hox loci , 2014, Science.

[7]  G. I. Menon,et al.  Chromosome positioning from activity-based segregation , 2014, Nucleic acids research.

[8]  D. Heermann,et al.  Expression-Dependent Folding of Interphase Chromatin , 2012, PloS one.

[9]  Romain Koszul,et al.  Metagenomic chromosome conformation capture (meta3C) unveils the diversity of chromosome organization in microorganisms , 2014, eLife.

[10]  William Stafford Noble,et al.  Comparative analysis of metazoan chromatin , 2014 .

[11]  Neva C. Durand,et al.  Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes , 2015, Proceedings of the National Academy of Sciences.

[12]  Leonid A. Mirny,et al.  Super-resolution imaging reveals distinct chromatin folding for different epigenetic states , 2015, Nature.

[13]  Roel van Driel,et al.  Depletion of the Chromatin Looping Proteins CTCF and Cohesin Causes Chromatin Compaction: Insight into Chromatin Folding by Polymer Modelling , 2014, PLoS Comput. Biol..

[14]  Jing Liang,et al.  Chromatin architecture reorganization during stem cell differentiation , 2015, Nature.

[15]  J. Vilar,et al.  Systems biophysics of gene expression. , 2013, Biophysical journal.

[16]  Patrick Schorderet,et al.  Chromatin topology is coupled to Polycomb group protein subnuclear organization , 2016, Nature Communications.

[17]  Daniel Jost,et al.  Bifurcation in epigenetics: implications in development, proliferation, and diseases. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[18]  P. Meister,et al.  From single genes to entire genomes: the search for a function of nuclear organization , 2016, Development.

[19]  B. Müller-Hill,et al.  Quality and position of the three lac operators of E. coli define efficiency of repression. , 1994, The EMBO journal.

[20]  Bertrand R. Caré,et al.  Chromatin epigenomic domain folding: size matters , 2015 .

[21]  Shlomo Havlin,et al.  Crumpled globule model of the three-dimensional structure of DNA , 1993 .

[22]  Guillaume J. Filion,et al.  Distinct structural transitions of chromatin topological domains correlate with coordinated hormone-induced gene regulation , 2014, Genes & development.

[23]  S. Nechaev,et al.  A statistical model of intra-chromosome contact maps. , 2013, Soft matter.

[24]  C. Dean,et al.  A Polycomb-based switch underlying quantitative epigenetic memory , 2011, Nature.

[25]  D. Schwarzer,et al.  Dynamic and flexible H3K9me3 bridging via HP1β dimerization establishes a plastic state of condensed chromatin , 2016, Nature Communications.

[26]  J. Sedat,et al.  Spatial partitioning of the regulatory landscape of the X-inactivation centre , 2012, Nature.

[27]  Davide Marenduzzo,et al.  Predicting the three-dimensional folding of cis-regulatory regions in mammalian genomes using bioinformatic data and polymer models , 2016, Genome Biology.

[28]  Robert E. Kingston,et al.  Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. , 2013, Molecular cell.

[29]  D. Jost,et al.  The folding landscape of the epigenome , 2016, Physical biology.

[30]  J. Dekker,et al.  Predictive Polymer Modeling Reveals Coupled Fluctuations in Chromosome Conformation and Transcription , 2014, Cell.

[31]  Benjamin Leblanc,et al.  Polycomb-Dependent Regulatory Contacts between Distant Hox Loci in Drosophila , 2011, Cell.

[32]  D. Odom,et al.  Comparative Hi-C Reveals that CTCF Underlies Evolution of Chromosomal Domain Architecture , 2015, Cell reports.

[33]  Davide Marenduzzo,et al.  Simulated binding of transcription factors to active and inactive regions folds human chromosomes into loops, rosettes and topological domains , 2016, Nucleic acids research.

[34]  J. Dekker,et al.  Capturing Chromosome Conformation , 2002, Science.

[35]  Dieter W. Heermann,et al.  Diffusion-Driven Looping Provides a Consistent Framework for Chromatin Organization , 2010, PloS one.

[36]  B. Bernstein,et al.  SAM domain polymerization links subnuclear clustering of PRC1 to gene silencing. , 2013, Developmental cell.

[37]  Renato Paro,et al.  Silencing chromatin: comparing modes and mechanisms , 2011, Nature Reviews Genetics.

[38]  V. Orlando,et al.  The function of the epigenome in cell reprogramming , 2007, Cellular and Molecular Life Sciences.

[39]  Moritz Herrmann,et al.  Comparative analysis of metazoan chromatin organization , 2014, Nature.

[40]  I. Amit,et al.  Comprehensive mapping of long range interactions reveals folding principles of the human genome , 2011 .

[41]  Ilya M. Flyamer,et al.  Active chromatin and transcription play a key role in chromosome partitioning into topologically associating domains , 2016, Genome research.

[42]  Diana B. Marina,et al.  A conformational switch in HP1 releases auto-inhibition to drive heterochromatin assembly , 2013, Nature.

[43]  Jesse R. Dixon,et al.  Topological Domains in Mammalian Genomes Identified by Analysis of Chromatin Interactions , 2012, Nature.

[44]  J. Dekker,et al.  Structural and functional diversity of Topologically Associating Domains , 2015, FEBS letters.

[45]  L. Mirny,et al.  Chromosome Compaction by Active Loop Extrusion , 2016, Biophysical journal.

[46]  K. Sneppen,et al.  Nucleation and spreading of a heterochromatic domain in fission yeast , 2016, Nature Communications.

[47]  Scott B. Dewell,et al.  Greater Than the Sum of Parts: Complexity of the Dynamic Epigenome. , 2016, Molecular cell.

[48]  A. Tanay,et al.  Single cell Hi-C reveals cell-to-cell variability in chromosome structure , 2013, Nature.

[49]  Guido Tiana,et al.  Structural Fluctuations of the Chromatin Fiber within Topologically Associating Domains. , 2016, Biophysical journal.

[50]  S. Leibler,et al.  DNA looping and physical constraints on transcription regulation. , 2003, Journal of molecular biology.

[51]  Suliana Manley,et al.  Nanoscale spatial organization of the HoxD gene cluster in distinct transcriptional states , 2015, Proceedings of the National Academy of Sciences.

[52]  A. Visel,et al.  Disruptions of Topological Chromatin Domains Cause Pathogenic Rewiring of Gene-Enhancer Interactions , 2015, Cell.

[53]  Yan Li,et al.  A high-resolution map of three-dimensional chromatin interactome in human cells , 2013, Nature.

[54]  Mario Nicodemi,et al.  Complexity of chromatin folding is captured by the strings and binders switch model , 2012, Proceedings of the National Academy of Sciences.

[55]  Wei Wang,et al.  Constructing 3D interaction maps from 1D epigenomes , 2016, Nature Communications.

[56]  J. Dekker,et al.  Condensin-Driven Remodeling of X-Chromosome Topology during Dosage Compensation , 2015, Nature.

[57]  Leonor Saiz,et al.  DNA looping: the consequences and its control. , 2006, Current opinion in structural biology.

[58]  Leonid A. Mirny,et al.  Chromatin Loops as Allosteric Modulators of Enhancer-Promoter Interactions , 2014, bioRxiv.

[59]  S. Mundlos,et al.  Formation of new chromatin domains determines pathogenicity of genomic duplications , 2016, Nature.

[60]  Christophe Zimmer,et al.  A Predictive Computational Model of the Dynamic 3D Interphase Yeast Nucleus , 2012, Current Biology.

[61]  L. Mirny The fractal globule as a model of chromatin architecture in the cell , 2011, Chromosome Research.

[62]  F. Spitz Gene regulation at a distance: From remote enhancers to 3D regulatory ensembles. , 2016, Seminars in cell & developmental biology.

[63]  K. Sneppen,et al.  Theoretical Analysis of Epigenetic Cell Memory by Nucleosome Modification , 2007, Cell.

[64]  Ralf Everaers,et al.  Structure and Dynamics of Interphase Chromosomes , 2008, PLoS Comput. Biol..

[65]  John F. Marko,et al.  Self-organization of domain structures by DNA-loop-extruding enzymes , 2012, Nucleic acids research.

[66]  L. Mirny,et al.  Formation of Chromosomal Domains in Interphase by Loop Extrusion , 2015, bioRxiv.

[67]  Anton Goloborodko,et al.  Compaction and segregation of sister chromatids via active loop extrusion , 2016, bioRxiv.

[68]  Michael Q. Zhang,et al.  CRISPR Inversion of CTCF Sites Alters Genome Topology and Enhancer/Promoter Function , 2015, Cell.

[69]  Kurt Kremer,et al.  From a melt of rings to chromosome territories: the role of topological constraints in genome folding , 2013, Reports on progress in physics. Physical Society.

[70]  Daniel Jost,et al.  Modeling epigenome folding: formation and dynamics of topologically associated chromatin domains , 2014, Nucleic acids research.

[71]  Benno Müller-Hill,et al.  Induction of the lac promoter in the absence of DNA loops and the stoichiometry of induction , 2006, Nucleic acids research.

[72]  K. Nasmyth THE GENOME : Joining , Resolving , and Separating Sister Chromatids During Mitosis and Meiosis , 2006 .

[73]  A. Mirsky,et al.  REPRESSED AND ACTIVE CHROMATIN ISOLATED FROM INTERPHASE LYMPHOCYTES. , 1963, Proceedings of the National Academy of Sciences of the United States of America.

[74]  Sharon Y. R. Dent,et al.  Chromatin modifiers and remodellers: regulators of cellular differentiation , 2013, Nature Reviews Genetics.

[75]  S. Sugiyama,et al.  The genome folding mechanism in yeast. , 2013, Journal of biochemistry.

[76]  Julien Dorier,et al.  Models that include supercoiling of topological domains reproduce several known features of interphase chromosomes , 2013, Nucleic acids research.

[77]  Jie Liang,et al.  Spatial confinement is a major determinant of the folding landscape of human chromosomes , 2014, Nucleic acids research.

[78]  S. Q. Xie,et al.  Hierarchical folding and reorganization of chromosomes are linked to transcriptional changes in cellular differentiation , 2015, Molecular systems biology.

[79]  Job Dekker,et al.  Organization of the Mitotic Chromosome , 2013, Science.

[80]  A. Tanay,et al.  Three-Dimensional Folding and Functional Organization Principles of the Drosophila Genome , 2012, Cell.

[81]  N. Brockdorff,et al.  The interplay of histone modifications – writers that read , 2015, EMBO reports.