Advances in higher-order chromatin architecture: the move towards 4D genome
1
조회
0
다운로드
2
인용
0
참고문헌
키워드
초록
In eukaryotes, the genome is hierarchically packed inside the nucleus, which facilitates physical contact between cis-regulatory elements (CREs), such as enhancers and promoters. Accumulating evidence highlights the critical role of higherorder chromatin structure in precise regulation of spatiotemporal gene expression under diverse biological contexts including lineage commitment and cell activation by external stimulus. Genomics and imaging-based technologies, such as Hi-C and DNA fluorescence in situ hybridization (FISH), have revealed the key principles of genome folding, while newly developed tools focus on improvement in resolution, throughput and modality at single-cell and population levels, and challenge the knowledge obtained through conventional approaches. In this review, we discuss recent advances in our understanding of principles of higher-order chromosome conformation and technologies to investigate 4D chromatin interactions.
Abstract
In eukaryotes, the genome is hierarchically packed inside the nucleus, which facilitates physical contact between cis-regulatory elements (CREs), such as enhancers and promoters. Accumulating evidence highlights the critical role of higherorder chromatin structure in precise regulation of spatiotemporal gene expression under diverse biological contexts including lineage commitment and cell activation by external stimulus. Genomics and imaging-based technologies, such as Hi-C and DNA fluorescence in situ hybridization (FISH), have revealed the key principles of genome folding, while newly developed tools focus on improvement in resolution, throughput and modality at single-cell and population levels, and challenge the knowledge obtained through conventional approaches. In this review, we discuss recent advances in our understanding of principles of higher-order chromosome conformation and technologies to investigate 4D chromatin interactions.
참고문헌 (107)
- Van Bortle K, "Nuclear organization and genome function", Annu Rev Cell Dev Biol, 28, pp.163~187 (2012)
- Rowley MJ, "Organizational principles of 3D genome architecture", Nat Rev Genet, 19, pp.789~800 (2018)
- Bonev B, "Organization and function of the 3D genome", Nat Rev Genet, 17, pp.661~678 (2016)
- Zheng H, "The role of 3D genome organization in development and cell differentiation", Nat Rev Mol Cell Biol, 20, pp.535~550 (2019)
- Dekker J, "The 4D nucleome project", Nature, 549, pp.219~226 (2017)
- Sparks TM, "Evolving methodologies and concepts in 4D nucleome research", Curr Opin Cell Biol, 64, pp.105~111 (2020)
- Kempfer R, "Methods for mapping 3D chromosome architecture", Nat Rev Genet, 21, pp.207~226 (2020)
- Beagrie RA, "Complex multi-enhancer contacts captured by genome architecture mapping", Nature, 543, pp.519~524 (2017)
- Beliveau BJ, "Versatile design and synthesis platform for visualizing genomes with Oligopaint FISH probes", Proc Natl Acad Sci U S A, 109, pp.21301~21306 (2012)
- Bintu B, "Super-resolution chromatin tracing reveals domains and cooperative interactions in single cells", Science, 362, pp.eaau1783~ (2018)
- Hu M, "Chromatin tracing : imaging 3D genome and nucleome", Trends Cell Biol, 31, pp.5~8 (2021)
- Wang S, "Spatial organization of chromatin domains and compartments in single chromosomes", Science, 353, pp.598~602 (2016)
- Li G, "Joint profiling of DNA methylation and chromatin architecture in single cells", Nat Methods, 16, pp.991~993 (2019)
- Lee DS, "Simultaneous profiling of 3D genome structure and DNA methylation in single human cells", Nat Methods, 16, pp.999~1006 (2019)
- Su JH, "Genome-scale imaging of the 3D organization and transcriptional activity of chromatin", Cell, 182, pp.1641e26~1659e26 (2020)
- Nagano T, "Single-cell Hi-C reveals cell-to-cell variability in chromosome structure", Nature, 502, pp.59~64 (2013)
- Nagano T, "Cell-cycle dynamics of chromosomal organization at single-cell resolution", Nature, 547, pp.61~67 (2017)
- Gorkin DU, "The 3D genome in transcriptional regulation and pluripotency", Cell Stem Cell, 14, pp.762~775 (2014)
- Cremer T, "Chromosome territories", Cold Spring Harb Perspect Biol, 2, pp.a003889~ (2010)
- Lieberman-Aiden E, "Comprehensive mapping of long-range interactions reveals folding principles of the human genome", Science, 326, pp.289~293 (2009)
- Solovei I, "LBR and lamin A", C sequentially tether peripheral heterochromatin and inversely regulate differentiation, 2013, pp.152, 584~598
- Hildebrand EM, "Mechanisms and functions of chromosome compartmentalization", Trends Biochem Sci, 45, pp.385~396 (2020)
- Hu S, "Disruption of nuclear speckles reduces chromatin interactions in active compartments", Epigenetics Chromatin, 12, pp.43~ (2019)
- Alberti S, "Considerations and challenges in studying liquid-liquid phase separation and biomolecular condensates", Cell, 176, pp.419~434 (2019)
- Strom AR, "Phase separation drives heterochromatin domain formation", Nature, 547, pp.241~245 (2017)
- Larson AG, "Liquid droplet formation by HP1alpha suggests a role for phase separation in heterochromatin", Nature, 547, pp.236~240 (2017)
- Sanulli S, "HP1reshapes nucleosome core to promote phase separation of heterochromatin", Nature, 575, pp.390~394 (2019)
- Wang L, "Histone modifications regulate chromatin compartmentalization by contributing to a phase separation mechanism", Mol Cell, 76, pp.646e6~659e6 (2019)
- Plys AJ, "Phase separation of Polycomb-repressive complex 1 is governed by a charged disordered region of CBX2", Genes Dev, 33, pp.799~813 (2019)
- Gibson BA, "Organization of chromatin by intrinsic and regulated phase separation", Cell, 179, pp.470e21~484e21 (2019)
- Laflamme G, "Biomolecular condensates as arbiters of biochemical reactions inside the nucleus", Commun Biol, 3, pp.773~ (2020)
- Dixon JR, "Topological domains in mammalian genomes identified by analysis of chromatin interactions", Nature, 485, pp.376~380 (2012)
- Nora EP, "Spatial partitioning of the regulatory landscape of the X-inactivation centre", Nature, 485, pp.381~385 (2012)
- Sexton T, "Threedimensional folding and functional organization principles of the Drosophila genome", Cell, 148, pp.458~472 (2012)
- Zuin J, "Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells", Proc Natl Acad Sci U S A, 111, pp.996~1001 (2014)
- Rao SS, "A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping", Cell, 159, pp.1665~1680 (2014)
- Eres IE, "A TAD Skeptic : Is 3D genome topology conserved?", Trends Genet, 37, pp.216~223 (2020)
- Eres IE, "Reorganization of 3D genome structure may contribute to gene regulatory evolution in primates", PLoS Genet, 15, pp.e1008278~ (2019)
- Dong P, "3D chromatin architecture of large plant genomes determined by local a", b compartments, 2017, pp.10, 1497~1509
- Xie T, "Biased gene retention during diploidization in Brassica linked to three-dimensional genome organization", Nat Plants, 5, pp.822~832 (2019)
- Finn EH, "Extensive heterogeneity and intrinsic variation in spatial genome organization", Cell, 176, pp.1502~1515 (2019)
- Flyamer IM, "Singlenucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition", Nature, 544, pp.110~114 (2017)
- Tan L, "Three-dimensional genome structures of single diploid human cells", Science, 361, pp.924~928 (2018)
- Pombo A, "Three-dimensional genome architecture : players and mechanisms", Nat Rev Mol Cell Biol, 16, pp.245~257 (2015)
- Javierre BM, "Lineagespecific genome architecture links enhancers and noncoding disease variants to target gene promoters", Cell, 167, pp.1369~1384 (2016)
- Schoenfelder S, "Long-range enhancerpromoter contacts in gene expression control", Nat Rev Genet, 20, pp.437~455 (2019)
- Yokoshi M, "Visualizing the role of boundary elements in enhancer-promoter communication", Mol Cell, 78, pp.224~235 (2020)
- Galupa R, "Enhancer-promoter communication : thinking outside the TAD", Trends Genet, 36, pp.459~461 (2020)
- Beagan JA, "On the existence and functionality of topologically associating domains", Nat Genet, 52, pp.8~16 (2020)
- Terakawa T, "The condensin complex is a mechanochemical motor that translocates along DNA", Science, 358, pp.672~676 (2017)
- Ganji M, "Real-time imaging of DNA loop extrusion by condensin", Science, 360, pp.102~105 (2018)
- Stigler J, "Single-molecule imaging reveals a collapsed conformational state for DNA-bound cohesin", Cell Rep, 15, pp.988~998 (2016)
- Davidson IF, "Rapid movement and transcriptional re-localization of human cohesin on DNA", EMBO J, 35, pp.2671~2685 (2016)
- Kanke M, "Cohesin acetylation and Wapl-Pds5 oppositely regulate translocation of cohesin along DNA", EMBO J, 35, pp.2686~2698 (2016)
- Dixon JR, "Chromatin domains : the unit of chromosome organization", Mol Cell, 62, pp.668~680 (2016)
- Deng W, "Reactivation of developmentally silenced globin genes by forced chromatin looping", Cell, 158, pp.849~860 (2014)
- Palstra RJ, "The beta-globin nuclear compartment in development and erythroid differentiation", Nat Genet, 35, pp.190~194 (2003)
- Robson MI, "Regulatory landscaping : how enhancer-promoter communication is sculpted in 3D", Mol Cell, 74, pp.1110~1122 (2019)
- Mifsud B, "Mapping long-range promoter contacts in human cells with high-resolution capture Hi-C", Nat Genet, 47, pp.598~606 (2015)
- Pattison JM, "Retinoic acid and BMP4 cooperate with p63 to alter chromatin dynamics during surface epithelial commitment", Nat Genet, 50, pp.1658~1665 (2018)
- Mumbach MR, "Enhancer connectome in primary human cells identifies target genes of disease-associated DNA elements", Nat Genet, 49, pp.1602~1612 (2017)
- Mumbach MR, "HiChIP : efficient and sensitive analysis of protein-directed genome architecture", Nat Methods, 13, pp.919~922 (2016)
- Rubin AJ, "Lineage-specific dynamic and pre-established enhancerpromoter contacts cooperate in terminal differentiation", Nat Genet, 49, pp.1522~1528 (2017)
- Kagey MH, "Mediator and cohesin connect gene expression and chromatin architecture", Nature, 467, pp.430~435 (2010)
- Kim S, "Mechanisms of interplay between transcription factors and the 3D genome", Mol Cell, 76, pp.306~319 (2019)
- Weintraub AS, "YY1 Is a structural regulator of enhancer-promoter loops", Cell, 171, pp.1573~1588 (2017)
- Thakur J, "Architectural RNA in chromatin organization", Biochem Soc Trans, 48, pp.1967~1978 (2020)
- Isoda T, "Non-coding transcription instructs chromatin folding and compartmentalization to dictate enhancer-promoter communication and T cell fate", Cell, 171, pp.103~119 (2017)
- Dekker J, "Capturing chromosome conformation", Science, 295, pp.1306~1311 (2002)
- van de Werken HJ, "Robust 4C-seq data analysis to screen for regulatory DNA interactions", Nat Methods, 9, pp.969~972 (2012)
- Dostie J, "Chromosome conformation capture carbon copy(5C). : a massively parallel solution for mapping interactions between genomic elements", Genome Res, 16, pp.1299~1309 (2006)
- Hsieh TH, "Mapping nucleosome resolution chromosome folding in yeast by Micro-C", Cell, 162, pp.108~119 (2015)
- Hsieh TS, "Resolving the 3D landscape of transcription-linked mammalian chromatin folding", Mol Cell, 78, pp.539~553 (2020)
- Ma W, "Fine-scale chromatin interaction maps reveal the cis-regulatory landscape of human lincRNA genes", Nat Methods, 12, pp.71~78 (2015)
- Ramani V, "Mapping 3D genome architecture through in situ DNase Hi-C", Nat Protoc, 11, pp.2104~2121 (2016)
- Fullwood MJ, "An oestrogen-receptor-alpha-bound human chromatin interactome", Nature, 462, pp.58~64 (2009)
- Li X, "Long-read ChIA-PET for base-pair-resolution mapping of haplotype-specific chromatin interactions", Nat Protoc, 12, pp.899~915 (2017)
- Fang R, "Mapping of long-range chromatin interactions by proximity ligation-assisted ChIP-seq", Cell Res, 26, pp.1345~1348 (2016)
- Hughes JR, "Analysis of hundreds of cis-regulatory landscapes at high resolution in a single, high-throughput experiment", Nat Genet, 46, pp.205~212 (2014)
- Mumbach MR, "HiChIRP reveals RNA-associated chromosome conformation", Nat Methods, 16, pp.489~492 (2019)
- Ramani V, "Massively multiplex single-cell Hi-C", Nat Methods, 14, pp.263~266 (2017)
- Cusanovich DA, "Multiplex single cell profiling of chromatin accessibility by combinatorial cellular indexing", Science, 348, pp.910~914 (2015)
- Klein AM, "Droplet barcoding for single-cell transcriptomics applied to embryonic stem cells", Cell, 161, pp.1187~1201 (2015)
- Macosko EZ, "Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets", Cell, 161, pp.1202~1214 (2015)
- Rotem A, "Single-cell ChIP-seq reveals cell subpopulations defined by chromatin state", Nat Biotechnol, 33, pp.1165~1172 (2015)
- Ramani V, "Sci-Hi-C : A single-cell Hi-C method for mapping 3D genome organization in large number of single cells", Methods, 170, pp.61~68 (2020)
- Quinodoz SA, "Higherorder inter-chromosomal hubs shape 3D genome organization in the nucleus", Cell, 174, pp.744~757 (2018)
- Zheng M, "Multiplex chromatin interactions with single-molecule precision", Nature, 566, pp.558~562 (2019)
- Wang G, "Tyramide signal amplification method in multiple-label immunofluorescence confocal microscopy", Methods, 18, pp.459~464 (1999)
- Chen Y, "Mapping 3D genome organization relative to nuclear compartments using TSA-Seq as a cytological ruler", J Cell Biol, 217, pp.4025~4048 (2018)
- Zhang L, "TSA-seq reveals a largely conserved genome organization relative to nuclear speckles with small position changes tightly correlated with gene expression changes", Genome Res, 31, pp.251~264 (2020)
- Speicher MR, "Karyotyping human chromosomes by combinatorial multi-fluor FISH", Nat Genet, 12, pp.368~375 (1996)
- Agbleke AA, "Advances in chromatin and chromosome research : perspectives from multiple fields", Mol Cell, 79, pp.881~901 (2020)
- Gnirke A, "Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing", Nat Biotechnol, 27, pp.182~189 (2009)
- Beliveau BJ, "Single-molecule super-resolution imaging of chromosomes and in situ haplotype visualization using Oligopaint FISH probes", Nat Commun, 6, pp.7147~ (2015)
- Mateo LJ, "Visualizing DNA folding and RNA in embryos at single-cell resolution", Nature, 568, pp.49~54 (2019)
- Sawh AN, "Lamina-dependent stretching and unconventional chromosome compartments in early C. elegans embryos", Mol Cell, 78, pp.96~111 (2020)
- Liu M, "Multiplexed imaging of nucleome architectures in single cells of mammalian tissue", Nat Commun, 11, pp.2907~ (2020)
- Lakadamyali M, "Visualizing the genome in high resolution challenges our textbook understanding", Nat Methods, 17, pp.371~379 (2020)
- Chen B, "Dynamic imaging of genomic loci in living human cells by an optimized CRISPR", Cas system, 2013, pp.155, 1479~1491
- Ma H, "Multicolor CRISPR labeling of chromosomal loci in human cells", Proc Natl Acad Sci U S A, 112, pp.3002~3007 (2015)
- Shao S, "Long-term dual-color tracking of genomic loci by modified sgRNAs of the CRISPR", Cas9 system, 2016, pp.44, e86~
- Wang S, "An RNA-aptamer-based two-color CRISPR labeling system", Sci Rep, 6, pp.26857~ (2016)
- Fu Y, "CRISPR-dCas9 and sgRNA scaffolds enable dual-colour live imaging of satellite sequences and repeat-enriched individual loci", Nat Commun, 7, pp.11707~ (2016)
- Ma H, "Multiplexed labeling of genomic loci with dCas9 and engineered sgRNAs using CRISPRainbow", Nat Biotechnol, 34, pp.528~530 (2016)
- Chen B, "Efficient labeling and imaging of protein-coding genes in living cells using CRISPR-Tag", Nat Commun, 9, pp.5065~ (2018)
- Gu B, "Transcription-coupled changes in nuclear mobility of mammalian cis-regulatory elements", Science, 359, pp.1050~1055 (2018)
