C‐ing the Genome: A Compendium of Chromosome Conformation Capture Methods to Study Higher‐Order Chromatin Organization

Three‐dimensional organization of the chromatin has important roles in transcription, replication, DNA repair, and pathologic events such as translocations. There are two fundamental ways to study higher‐order chromatin organization: microscopic and molecular approaches. In this review, we briefly introduce the molecular approaches, focusing on chromosome conformation capture or “3C” technology and its derivatives, which can be used to probe chromatin folding at resolutions beyond that provided by microscopy techniques. We further discuss the different types of data generated by the 3C‐based methods and how they can be used to answer distinct biological questions. J. Cell. Physiol. 230: 31–35, 2016. © 2015 Wiley Periodicals, Inc.

[1]  Reza Kalhor,et al.  Genome architectures revealed by tethered chromosome conformation capture and population-based modeling , 2011, Nature Biotechnology.

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

[3]  Raymond K. Auerbach,et al.  Extensive Promoter-Centered Chromatin Interactions Provide a Topological Basis for Transcription Regulation , 2012, Cell.

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

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

[6]  Job Dekker,et al.  Molecular Cell Review The Hierarchy of the 3 D Genome , 2013 .

[7]  Jennifer E. Phillips-Cremins,et al.  Architectural Protein Subclasses Shape 3D Organization of Genomes during Lineage Commitment , 2013, Cell.

[8]  William Stafford Noble,et al.  Genomic Interaction Profiles in Breast Cancer Reveal Altered Chromatin Architecture , 2013, PloS one.

[9]  J. Dekker,et al.  The hierarchy of the 3D genome. , 2013, Molecular cell.

[10]  Kelly M. McGarvey,et al.  A novel 6C assay uncovers Polycomb-mediated higher order chromatin conformations. , 2008, Genome research.

[11]  Chee Seng Chan,et al.  CTCF-Mediated Functional Chromatin Interactome in Pluripotent Cells , 2011, Nature Genetics.

[12]  A. Ashworth,et al.  Unbiased analysis of potential targets of breast cancer susceptibility loci by Capture Hi-C , 2014, Genome research.

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

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

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

[16]  Elzo de Wit,et al.  4C technology: protocols and data analysis. , 2012, Methods in enzymology.

[17]  Pierre Chartrand,et al.  Genome-wide scanning of HoxB1-associated loci in mouse ES cells using an open-ended Chromosome Conformation Capture methodology , 2006, Chromosome Research.

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

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

[20]  Job Dekker,et al.  Analysis of long-range chromatin interactions using Chromosome Conformation Capture. , 2012, Methods.

[21]  Cameron S. Osborne,et al.  The pluripotent regulatory circuitry connecting promoters to their long-range interacting elements , 2015, Genome research.

[22]  L. Mirny,et al.  Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data , 2013, Nature Reviews Genetics.

[23]  Peter Fraser,et al.  Sensitive detection of chromatin coassociations using enhanced chromosome conformation capture on chip , 2012, Nature Protocols.

[24]  H. Tanabe,et al.  Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription. , 2009, Developmental cell.

[25]  Mathieu Blanchette,et al.  Classifying leukemia types with chromatin conformation data , 2014, Genome Biology.

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

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

[28]  Edith Heard,et al.  Segmental folding of chromosomes: A basis for structural and regulatory chromosomal neighborhoods? , 2013, BioEssays : news and reviews in molecular, cellular and developmental biology.

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

[30]  Elzo de Wit,et al.  Determining long-range chromatin interactions for selected genomic sites using 4C-seq technology: from fixation to computation. , 2012, Methods.

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

[32]  Josée Dostie,et al.  From cells to chromatin: capturing snapshots of genome organization with 5C technology. , 2012, Methods.

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

[34]  M. Kladde,et al.  Interaction between transcription regulatory regions of prolactin chromatin. , 1993, Science.

[35]  J. Rougemont,et al.  The Dynamic Architecture of Hox Gene Clusters , 2011, Science.

[36]  Wange Lu,et al.  Klf4 organizes long-range chromosomal interactions with the oct4 locus in reprogramming and pluripotency. , 2013, Cell stem cell.

[37]  Eric S. Lander,et al.  A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping , 2015, Cell.

[38]  P. Fraser,et al.  3D genome architecture from populations to single cells. , 2015, Current opinion in genetics & development.

[39]  Noam Kaplan,et al.  The Hitchhiker's guide to Hi-C analysis: practical guidelines. , 2015, Methods.

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

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

[42]  Wouter de Laat,et al.  A Regulatory Archipelago Controls Hox Genes Transcription in Digits , 2011, Cell.

[43]  J. Dekker,et al.  The long-range interaction landscape of gene promoters , 2012, Nature.

[44]  C. Glass,et al.  Control of VEGF-A transcriptional programs by pausing and genomic compartmentalization , 2014, Nucleic acids research.

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

[46]  Rachel Patton McCord,et al.  Correlated alterations in genome organization, histone methylation, and DNA–lamin A/C interactions in Hutchinson-Gilford progeria syndrome , 2013, Genome research.

[47]  Thomas Cremer,et al.  Chromosome territories--a functional nuclear landscape. , 2006, Current opinion in cell biology.

[48]  C. Glass,et al.  Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. , 2010, Molecular cell.

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

[50]  J. Lawrence,et al.  Spatial re-organization of myogenic regulatory sequences temporally controls gene expression , 2015, Nucleic acids research.

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

[52]  J. Dekker,et al.  Hi-C: a comprehensive technique to capture the conformation of genomes. , 2012, Methods.

[53]  R. Flavell,et al.  Interchromosomal associations between alternatively expressed loci , 2005, Nature.

[54]  Robert S Illingworth,et al.  Spatial genome organization: contrasting views from chromosome conformation capture and fluorescence in situ hybridization , 2014, Genes & development.

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

[56]  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.

[57]  Job Dekker,et al.  The three 'C' s of chromosome conformation capture: controls, controls, controls , 2005, Nature Methods.

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

[59]  Boris Lenhard,et al.  Cohesin-based chromatin interactions enable regulated gene expression within preexisting architectural compartments , 2013, Genome research.

[60]  Michael S. Becker,et al.  Spatial Organization of the Mouse Genome and Its Role in Recurrent Chromosomal Translocations , 2012, Cell.