On emerging nuclear order

Although the nonrandom nature of interphase chromosome arrangement is widely accepted, how nuclear organization relates to genomic function remains unclear. Nuclear subcompartments may play a role by offering rich microenvironments that regulate chromatin state and ensure optimal transcriptional efficiency. Technological advances now provide genome-wide and four-dimensional analyses, permitting global characterizations of nuclear order. These approaches will help uncover how seemingly separate nuclear processes may be coupled and aid in the effort to understand the role of nuclear organization in development and disease.

[1]  S. Hell Far-Field Optical Nanoscopy , 2007, Science.

[2]  P. Anderson More is different. , 1972, Science.

[3]  G. Blobel,et al.  Gene gating: a hypothesis. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[4]  E. Bertolino,et al.  Transcriptional repression mediated by repositioning of genes to the nuclear lamina , 2008, Nature.

[5]  T. Misteli The concept of self-organization in cellular architecture , 2001, The Journal of cell biology.

[6]  Peter R Cook,et al.  Specialized transcription factories. , 2006, Biochemical Society symposium.

[7]  T. Cremer,et al.  Evolutionarily conserved, cell type and species-specific higher order chromatin arrangements in interphase nuclei of primates , 2007, Chromosoma.

[8]  Roy Riblet,et al.  Subnuclear Compartmentalization of Immunoglobulin Loci During Lymphocyte Development , 2002, Science.

[9]  J. Shapiro,et al.  Why repetitive DNA is essential to genome function , 2005, Biological reviews of the Cambridge Philosophical Society.

[10]  Jennifer A. Mitchell,et al.  Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells , 2010, Nature Genetics.

[11]  C. Nusbaum,et al.  Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements. , 2006, Genome research.

[12]  V. Isaeva Self-organization in biological systems , 2012, Biology Bulletin.

[13]  D. Gray,et al.  Nonequivalent nuclear location of immunoglobulin alleles in B lymphocytes , 2001, Nature Immunology.

[14]  M. Gabut,et al.  Inheritance of Polycomb-dependent chromosomal interactions in Drosophila. , 2003, Genes & development.

[15]  J. Ragoussis,et al.  Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. , 2000, Journal of cell science.

[16]  N. Amariglio,et al.  The nuclear-envelope protein and transcriptional repressor LAP2β interacts with HDAC3 at the nuclear periphery, and induces histone H4 deacetylation , 2005, Journal of Cell Science.

[17]  W. D. Laat,et al.  An evaluation of 3C-based methods to capture DNA interactions , 2007, Nature Methods.

[18]  D. Engelke,et al.  Nucleolar Clustering of Dispersed tRNA Genes , 2003, Science.

[19]  E. Heard,et al.  The ins and outs of gene regulation and chromosome territory organisation. , 2007, Current opinion in cell biology.

[20]  Tom Misteli,et al.  Spatial Positioning A New Dimension in Genome Function , 2004, Cell.

[21]  Peter R. Cook,et al.  Predicting three-dimensional genome structure from transcriptional activity , 2002, Nature Genetics.

[22]  K. Helin,et al.  Polycomb group protein-mediated repression of transcription. , 2010, Trends in biochemical sciences.

[23]  A. Conesa,et al.  Initial Genomics of the Human Nucleolus , 2010, PLoS genetics.

[24]  Karl Rohr,et al.  Chromatin domains and the interchromatin compartment form structurally defined and functionally interacting nuclear networks , 2006, Chromosome Research.

[25]  R. Eils,et al.  Three-Dimensional Maps of All Chromosomes in Human Male Fibroblast Nuclei and Prometaphase Rosettes , 2005, PLoS biology.

[26]  Thomas Cremer,et al.  Revealing the high-resolution three-dimensional network of chromatin and interchromatin space: A novel electron-microscopic approach to reconstructing nuclear architecture , 2009, Chromosome Research.

[27]  B. van Steensel,et al.  Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus , 1993, The Journal of cell biology.

[28]  Sara Ahmed,et al.  DNA zip codes control an ancient mechanism for gene targeting to the nuclear periphery , 2010, Nature Cell Biology.

[29]  J. Bewersdorf,et al.  The nuclear periphery of embryonic stem cells is a transcriptionally permissive and repressive compartment , 2009, Journal of Cell Science.

[30]  Daniel G. Miller,et al.  A Unifying Genetic Model for Facioscapulohumeral Muscular Dystrophy , 2010, Science.

[31]  Charles Kooperberg,et al.  The emergence of lineage-specific chromosomal topologies from coordinate gene regulation , 2009, Proceedings of the National Academy of Sciences.

[32]  C. Cremer,et al.  Rabl's model of the interphase chromosome arrangement tested in Chinise hamster cells by premature chromosome condensation and laser-UV-microbeam experiments , 2004, Human Genetics.

[33]  M. Kozubek,et al.  Arrangement of chromosome 11 and 22 territories, EWSR1 and FLI1 genes, and other genetic elements of these chromosomes in human lymphocytes and Ewing sarcoma cells , 2003, Human Genetics.

[34]  Steven H. Strogatz,et al.  Nonlinear Dynamics and Chaos , 2024 .

[35]  D. Engelke,et al.  Nucleolar localization of early tRNA processing. , 1998, Genes & development.

[36]  F. Hediger,et al.  Nuclear pore association confers optimal expression levels for an inducible yeast gene , 2006, Nature.

[37]  Chris Arney Sync: The Emerging Science of Spontaneous Order , 2007 .

[38]  J. Sedat,et al.  The Mcp element mediates stable long-range chromosome-chromosome interactions in Drosophila. , 2006, Molecular biology of the cell.

[39]  M. Niepel,et al.  The nuclear pore complex: bridging nuclear transport and gene regulation , 2010, Nature Reviews Molecular Cell Biology.

[40]  T. Misteli Beyond the Sequence: Cellular Organization of Genome Function , 2011 .

[41]  A. Reymond,et al.  The effect of translocation-induced nuclear reorganization on gene expression. , 2010, Genome research.

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

[43]  J. Aten,et al.  High resolution analysis of interphase chromosome domains. , 2000, Journal of cell science.

[44]  E. Liu,et al.  An Oestrogen Receptor α-bound Human Chromatin Interactome , 2009, Nature.

[45]  A. Corbett,et al.  Actively Transcribed GAL Genes Can Be Physically Linked to the Nuclear Pore by the SAGA Chromatin Modifying Complex* , 2007, Journal of Biological Chemistry.

[46]  G. Hannon,et al.  Ezh2 Orchestrates Gene Expression for the Stepwise Differentiation of Tissue-Specific Stem Cells , 2009, Cell.

[47]  W. L. Ruzzo,et al.  Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. , 2010, Developmental cell.

[48]  J. Thyberg,et al.  Protein Tpr is required for establishing nuclear pore-associated zones of heterochromatin exclusion , 2010, The EMBO journal.

[49]  Anne E Carpenter,et al.  Long-Range Directional Movement of an Interphase Chromosome Site , 2006, Current Biology.

[50]  Thomas Cremer,et al.  Functional nuclear architecture studied by microscopy: present and future. , 2010, International review of cell and molecular biology.

[51]  Thomas Cremer,et al.  Rise, fall and resurrection of chromosome territories: a historical perspective. Part I. The rise of chromosome territories. , 2006, European journal of histochemistry : EJH.

[52]  M. Gerstein,et al.  Annotating non-coding regions of the genome , 2010, Nature Reviews Genetics.

[53]  R Eils,et al.  Three-dimensional reconstruction of painted human interphase chromosomes: active and inactive X chromosome territories have similar volumes but differ in shape and surface structure , 1996, The Journal of cell biology.

[54]  Thomas Cremer,et al.  Nuclear Architecture of Rod Photoreceptor Cells Adapts to Vision in Mammalian Evolution , 2009, Cell.

[55]  Peter Fraser,et al.  The role of transcription factories in large-scale structure and dynamics of interphase chromatin. , 2007, Seminars in cell & developmental biology.

[56]  Tom Misteli,et al.  Tissue-specific spatial organization of genomes , 2004, Genome Biology.

[57]  A. Gregory Matera,et al.  Actin-dependent intranuclear repositioning of an active gene locus in vivo , 2007, The Journal of cell biology.

[58]  Peter Teague,et al.  Differences in the Localization and Morphology of Chromosomes in the Human Nucleus , 1999, The Journal of cell biology.

[59]  Kristian Helin,et al.  The Polycomb Group Protein Suz12 Is Required for Embryonic Stem Cell Differentiation , 2007, Molecular and Cellular Biology.

[60]  P. Flicek,et al.  Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. , 2010, Molecular cell.

[61]  F. Boisvert,et al.  The multifunctional nucleolus , 2007, Nature Reviews Molecular Cell Biology.

[62]  Y. Woo,et al.  Nuclear positioning, higher-order folding, and gene expression of Mmu15 sequences are refractory to chromosomal translocation , 2011, Chromosoma.

[63]  D. Jackson,et al.  Visualization of focal sites of transcription within human nuclei. , 1993, The EMBO journal.

[64]  T. Misteli,et al.  Spatial genome organization during T-cell differentiation , 2004, Cytogenetic and Genome Research.

[65]  F. Pérez-Willard,et al.  Focused ion beam (FIB) combined with high resolution scanning electron microscopy: a promising tool for 3D analysis of chromosome architecture. , 2009, Journal of structural biology.

[66]  S. Kosak,et al.  A genetic analysis of chromosome territory looping: diverse roles for distal regulatory elements , 2004, Chromosome Research.

[67]  S. Dalton,et al.  Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. , 2010, Genome research.

[68]  Tom Misteli,et al.  Spatial proximity of translocation-prone gene loci in human lymphomas , 2003, Nature Genetics.

[69]  Prabhakar R. Gudla,et al.  Disease-specific gene repositioning in breast cancer , 2009, The Journal of cell biology.

[70]  Mark Groudine,et al.  Form follows function: The genomic organization of cellular differentiation. , 2004, Genes & development.

[71]  B. Steensel,et al.  Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture–on-chip (4C) , 2006, Nature Genetics.

[72]  Eric S. Lander,et al.  Hi-C: A Method to Study the Three-dimensional Architecture of Genomes. , 2010, Journal of visualized experiments : JoVE.

[73]  L. Schermelleh,et al.  Functional nuclear organization of transcription and DNA replication: a topographical marriage between chromatin domains and the interchromatin compartment. , 2010, Cold Spring Harbor symposia on quantitative biology.

[74]  W. Dewey,et al.  Visualization of interphase chromosomes. , 1977, Journal of cell science.

[75]  William Stafford Noble,et al.  A Three-Dimensional Model of the Yeast Genome , 2010, Nature.

[76]  S. Strogatz Exploring complex networks , 2001, Nature.

[77]  W. Ashby,et al.  Principles of the self-organizing dynamic system. , 1947, The Journal of general psychology.

[78]  Dirk Schübeler,et al.  Global Reorganization of Replication Domains During Embryonic Stem Cell Differentiation , 2008, PLoS biology.

[79]  Thomas Cremer,et al.  4D Chromatin dynamics in cycling cells , 2010 .

[80]  P. Silver,et al.  Global histone acetylation induces functional genomic reorganization at mammalian nuclear pore complexes. , 2008, Genes & development.

[81]  Steven H. Strogatz,et al.  Nonlinear Dynamics and Chaos: With Applications to Physics, Biology, Chemistry, and Engineering , 1994 .

[82]  A. Pombo,et al.  Intermingling of Chromosome Territories in Interphase Suggests Role in Translocations and Transcription-Dependent Associations , 2006, PLoS biology.

[83]  D. Scalzo,et al.  Coordinate Gene Regulation during Hematopoiesis Is Related to Genomic Organization , 2007, PLoS biology.

[84]  T. Misteli,et al.  Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus , 2006, Journal of Cell Science.

[85]  Fraser McBlane,et al.  Molecular Signatures of Self-Renewal, Differentiation, and Lineage Choice in Multipotential Hemopoietic Progenitor Cells In Vitro , 2004, Molecular and Cellular Biology.

[86]  J. Dekker,et al.  Genomics tools for the unraveling of chromosome architecture , 2010, Nature Biotechnology.

[87]  Elizabeth Kerr,et al.  Recruitment to the Nuclear Periphery Can Alter Expression of Genes in Human Cells , 2008, PLoS genetics.

[88]  T. Misteli,et al.  Activation of the Cellular DNA Damage Response in the Absence of DNA Lesions , 2008, Science.

[89]  Ulrich Wagner,et al.  Chromatin-Bound Nuclear Pore Components Regulate Gene Expression in Higher Eukaryotes , 2010, Cell.

[90]  Matthias Merkenschlager,et al.  Association of Transcriptionally Silent Genes with Ikaros Complexes at Centromeric Heterochromatin , 1997, Cell.

[91]  S. Gasser,et al.  The nuclear envelope and transcriptional control , 2007, Nature Reviews Genetics.

[92]  M. Fornerod,et al.  Characterization of the Drosophila melanogaster genome at the nuclear lamina , 2006, Nature Genetics.

[93]  D. Jackson,et al.  Regional specialization in human nuclei: visualization of discrete sites of transcription by RNA polymerase III , 1999, The EMBO journal.

[94]  M. Fornerod,et al.  Nucleoporins Directly Stimulate Expression of Developmental and Cell-Cycle Genes Inside the Nucleoplasm , 2010, Cell.

[95]  B. Jones,et al.  Repeated elements coordinate the spatial organization of the yeast genome , 2006, Yeast.

[96]  Mark E. J. Newman,et al.  Structure and Dynamics of Networks , 2009 .

[97]  M. Surani,et al.  The Polycomb-Group GeneEzh2 Is Required for Early Mouse Development , 2001, Molecular and Cellular Biology.

[98]  S. Tapscott,et al.  Networking the nucleus , 2010, Molecular systems biology.

[99]  Thomas Cremer,et al.  4D chromatin dynamics in cycling cells: Theodor Boveri's hypotheses revisited. , 2010, Nucleus.

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

[101]  A. Ponti,et al.  The spatial dynamics of tissue-specific promoters during C. elegans development. , 2010, Genes & development.

[102]  P. Freemont,et al.  The Human Polycomb Group Complex Associates with Pericentromeric Heterochromatin to Form a Novel Nuclear Domain , 1998, The Journal of cell biology.

[103]  M. Groudine,et al.  The locus control region is required for association of the murine beta-globin locus with engaged transcription factories during erythroid maturation. , 2006, Genes & development.

[104]  Job Dekker,et al.  Integrating one-dimensional and three-dimensional maps of genomes , 2010, Journal of Cell Science.

[105]  K. Sandhu,et al.  Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions , 2006, Nature Genetics.

[106]  U. K. Laemmli,et al.  Chromatin Boundaries in Budding Yeast The Nuclear Pore Connection , 2002, Cell.

[107]  T. Cremer,et al.  Chromosome territories. , 2010, Cold Spring Harbor perspectives in biology.

[108]  Yoshihiro Ohta,et al.  Active RNA Polymerases: Mobile or Immobile Molecular Machines? , 2010, PLoS biology.

[109]  U. K. Laemmli,et al.  Nup-PI: the nucleopore-promoter interaction of genes in yeast. , 2006, Molecular cell.

[110]  Pamela A. Silver,et al.  Genome-Wide Localization of the Nuclear Transport Machinery Couples Transcriptional Status and Nuclear Organization , 2004, Cell.

[111]  Prabhakar R. Gudla,et al.  Allele-specific nuclear positioning of the monoallelically expressed astrocyte marker GFAP. , 2008, Genes & development.

[112]  Thomas Cremer,et al.  Non-random radial higher-order chromatin arrangements in nuclei of diploid human cells , 2004, Chromosome Research.

[113]  Job Dekker,et al.  Gene Regulation in the Third Dimension , 2008, Science.

[114]  Juliet A. Ellis,et al.  The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. , 2001, Human molecular genetics.

[115]  L. Wessels,et al.  Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions , 2008, Nature.

[116]  B. Daneholt,et al.  Close coupling between transcription and exit of mRNP from the cell nucleus. , 2008, Experimental cell research.

[117]  A. Tero,et al.  Rules for Biologically Inspired Adaptive Network Design , 2010, Science.