5.9
CiteScore
5.9
Impact Factor
Volume 43 Issue 5
May  2016
Turn off MathJax
Article Contents

CRISPR Double Cutting through the Labyrinthine Architecture of 3D Genomes

doi: 10.1016/j.jgg.2016.03.006
More Information
  • Corresponding author: E-mail address: qwu123@gmail.com (Qiang Wu)
  • Received Date: 2016-02-05
  • Accepted Date: 2016-03-16
  • Rev Recd Date: 2016-03-03
  • Available Online: 2016-03-29
  • Publish Date: 2016-05-20
  • The genomes are organized into ordered and hierarchical topological structures in interphase nuclei. Within discrete territories of each chromosome, topologically associated domains (TADs) play important roles in various nuclear processes such as gene regulation. Inside TADs separated by relatively constitutive boundaries, distal elements regulate their gene targets through specific chromatin-looping contacts such as long-distance enhancer-promoter interactions. High-throughput sequencing studies have revealed millions of potential regulatory DNA elements, which are much more abundant than the mere ∼20,000 genes they control. The recently emerged CRISPR-Cas9 genome editing technologies have enabled efficient and precise genetic and epigenetic manipulations of genomes. The multiplexed and high-throughput CRISPR capabilities facilitate the discovery and dissection of gene regulatory elements. Here, we describe the applications of CRISPR for genome, epigenome, and 3D genome editing, focusing on CRISPR DNA-fragment editing with Cas9 and a pair of sgRNAs to investigate topological folding of chromatin TADs and developmental gene regulation.
  • loading
  • [1]
    Albertin, C.B., Simakov, O., Mitros, T. et al. The octopus genome and the evolution of cephalopod neural and morphological novelties Nature, 524 (2015),pp. 220-224
    [2]
    Ali, T., Renkawitz, R., Bartkuhn, M. Insulators and domains of gene expression Curr. Opin. Genet. Dev., 37 (2016),pp. 17-26
    [3]
    Alt, F.W., Zhang, Y., Meng, F.L. et al. Mechanisms of programmed DNA lesions and genomic instability in the immune system Cell, 152 (2013),pp. 417-429
    [4]
    Andrey, G., Montavon, T., Mascrez, B. et al. Science, 340 (2013),p. 1234167
    [5]
    Bétermier, M., Bertrand, P., Lopez, B.S. Is non-homologous end-joining really an inherently error-prone process? PLoS Genet., 10 (2014),p. e1004086
    [6]
    Badrinarayanan, A., Le, T.B., Laub, M.T. Bacterial chromosome organization and segregation Annu. Rev. Cell Dev. Biol., 31 (2015),pp. 171-199
    [7]
    Banerji, J., Rusconi, S., Schaffner, W. Cell, 27 (1981),pp. 299-308
    [8]
    Baniahmad, A., Steiner, C., Kohne, A.C. et al. Modular structure of a chicken lysozyme silencer: involvement of an unusual thyroid hormone receptor binding site Cell, 61 (1990),pp. 505-514
    [9]
    Bell, A.C., Felsenfeld, G. Nature, 405 (2000),pp. 482-485
    [10]
    Bell, A.C., West, A.G., Felsenfeld, G. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators Cell, 98 (1999),pp. 387-396
    [11]
    Bell, A.C., West, A.G., Felsenfeld, G. Insulators and boundaries: versatile regulatory elements in the eukaryotic genome Science, 291 (2001),pp. 447-450
    [12]
    Bulger, M., Groudine, M. Functional and mechanistic diversity of distal transcription enhancers Cell, 144 (2011),pp. 327-339
    [13]
    Byrne, S.M., Ortiz, L., Mali, P. et al. Multi-kilobase homozygous targeted gene replacement in human induced pluripotent stem cells Nucleic Acids Res., 43 (2015),p. e21
    [14]
    Canver, M.C., Bauer, D.E., Dass, A. et al. Characterization of genomic deletion efficiency mediated by clustered regularly interspaced palindromic repeats (CRISPR)/Cas9 nuclease system in mammalian cells J. Biol. Chem., 289 (2014),pp. 21312-21324
    [15]
    Canver, M.C., Smith, E.C., Sher, F. et al. Nature, 527 (2015),pp. 192-197
    [16]
    Carlson, D.F., Tan, W., Lillico, S.G. et al. Efficient TALEN-mediated gene knockout in livestock Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 17382-17387
    [17]
    Carroll, D. Genome engineering with targetable nucleases Annu. Rev. Biochem., 83 (2014),pp. 409-439
    [18]
    Ceccaldi, R., Rondinelli, B., D'Andrea, A.D. Repair pathway choices and consequences at the double-strand break Trends Cell Biol., 26 (2016),pp. 52-64
    [19]
    Chen, B., Gilbert, L.A., Cimini, B.A. et al. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system Cell, 155 (2013),pp. 1479-1491
    [20]
    Chen, W.V., Alvarez, F.J., Lefebvre, J.L. et al. Functional significance of isoform diversification in the protocadherin gamma gene cluster Neuron, 75 (2012),pp. 402-409
    [21]
    Chiruvella, K.K., Liang, Z., Wilson, T.E. Repair of double-strand breaks by end joining Cold Spring Harb. Perspect. Biol., 5 (2013),p. a012757
    [22]
    Cho, S.W., Kim, S., Kim, J.M. et al. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease Nat. Biotechnol., 31 (2013),pp. 230-232
    [23]
    Choi, P.S., Meyerson, M. Targeted genomic rearrangements using CRISPR/Cas technology Nat. Commun., 5 (2014),p. 3728
    [24]
    Chong, J.A., Tapia-Ramirez, J., Kim, S. et al. REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons Cell, 80 (1995),pp. 949-957
    [25]
    Chu, V.T., Weber, T., Wefers, B. et al. Increasing the efficiency of homology-directed repair for CRISPR-Cas9-induced precise gene editing in mammalian cells Nat. Biotechnol., 33 (2015),pp. 543-548
    [26]
    Chung, J.H., Whiteley, M., Felsenfeld, G. Cell, 74 (1993),pp. 505-514
    [27]
    Cong, L., Ran, F.A., Cox, D. et al. Multiplex genome engineering using CRISPR/Cas systems Science, 339 (2013),pp. 819-823
    [28]
    Cremer, T., Cremer, C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells Nat. Rev. Genet., 2 (2001),pp. 292-301
    [29]
    de Laat, W., Duboule, D. Topology of mammalian developmental enhancers and their regulatory landscapes Nature, 502 (2013),pp. 499-506
    [30]
    de Wit, E., Vos, E.S., Holwerda, S.J. et al. CTCF binding polarity determines chromatin looping Mol. Cell, 60 (2015),pp. 676-684
    [31]
    Dekker, J., Rippe, K., Dekker, M. et al. Capturing chromosome conformation Science, 295 (2002),pp. 1306-1311
    [32]
    Deng, W., Shi, X., Tjian, R. et al. Proc. Natl. Acad. Sci. USA, 112 (2015),pp. 11870-11875
    [33]
    Dixon, J.R., Jung, I., Selvaraj, S. et al. Chromatin architecture reorganization during stem cell differentiation Nature, 518 (2015),pp. 331-336
    [34]
    Dixon, J.R., Selvaraj, S., Yue, F. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions Nature, 485 (2012),pp. 376-380
    [35]
    Doudna, J.A., Charpentier, E. Genome editing. The new frontier of genome engineering with CRISPR-Cas9 Science, 346 (2014),p. 1258096
    [36]
    Dowen, J.M., Fan, Z.P., Hnisz, D. et al. Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes Cell, 159 (2014),pp. 374-387
    [37]
    Dzantiev, L., Constantin, N., Genschel, J. et al. A defined human system that supports bidirectional mismatch-provoked excision Mol. Cell, 15 (2004),pp. 31-41
    [38]
    ENCODE Project Consortium An integrated encyclopedia of DNA elements in the human genome Nature, 489 (2012),pp. 57-74
    [39]
    Ernst, J., Kheradpour, P., Mikkelsen, T.S. et al. Mapping and analysis of chromatin state dynamics in nine human cell types Nature, 473 (2011),pp. 43-49
    [40]
    Esumi, S., Kakazu, N., Taguchi, Y. et al. Monoallelic yet combinatorial expression of variable exons of the protocadherin-alpha gene cluster in single neurons Nat. Genet., 37 (2005),pp. 171-176
    [41]
    Festenstein, R., Tolaini, M., Corbella, P. et al. Locus control region function and heterochromatin-induced position effect variegation Science, 271 (1996),pp. 1123-1125
    [42]
    Filippova, G.N., Fagerlie, S., Klenova, E.M. et al. Mol. Cell. Biol., 16 (1996),pp. 2802-2813
    [43]
    Flavahan, W.A., Drier, Y., Liau, B.B. et al. Nature, 529 (2016),pp. 110-114
    [44]
    Fullwood, M.J., Liu, M.H., Pan, Y.F. et al. An oestrogen-receptor-alpha-bound human chromatin interactome Nature, 462 (2009),pp. 58-64
    [45]
    Garrett, A.M., Schreiner, D., Lobas, M.A. et al. γ-protocadherins control cortical dendrite arborization by regulating the activity of a FAK/PKC/MARCKS signaling pathway Neuron, 74 (2012),pp. 269-276
    [46]
    Gibcus, J.H., Dekker, J. The hierarchy of the 3D genome Mol. Cell, 49 (2013),pp. 773-782
    [47]
    Golan-Mashiach, M., Grunspan, M., Emmanuel, R. et al. Identification of CTCF as a master regulator of the clustered protocadherin genes Nucleic Acids Res., 40 (2011),pp. 3378-3391
    [48]
    Golic, K.G., Golic, M.M. Genetics, 144 (1996),pp. 1693-1711
    [49]
    Gómez-Marín, C., Tena, J.J., Acemel, R.D. et al. Evolutionary comparison reveals that diverging CTCF sites are signatures of ancestral topological associating domains borders Proc. Natl. Acad. Sci. USA, 112 (2015),pp. 7542-7547
    [50]
    Guo, Y., Monahan, K., Wu, H. et al. CTCF/cohesin-mediated DNA looping is required for protocadherin alpha promoter choice Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 21081-21086
    [51]
    Guo, Y., Xu, Q., Canzio, D. et al. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function Cell, 162 (2015),pp. 900-910
    [52]
    Gupta, A., Hall, V.L., Kok, F.O. et al. Targeted chromosomal deletions and inversions in zebrafish Genome Res., 23 (2013),pp. 1008-1017
    [53]
    Handoko, L., Xu, H., Li, G. et al. CTCF-mediated functional chromatin interactome in pluripotent cells Nat. Genet., 43 (2011),pp. 630-638
    [54]
    Hardison, R., Slightom, J.L., Gumucio, D.L. et al. Gene, 205 (1997),pp. 73-94
    [55]
    Hardison, R.C. Variable evolutionary signatures at the heart of enhancers Nat. Genet., 42 (2010),pp. 734-735
    [56]
    Hark, A.T., Schoenherr, C.J., Katz, D.J. et al. Nature, 405 (2000),pp. 486-489
    [57]
    Heintzman, N.D., Stuart, R.K., Hon, G. et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome Nat. Genet., 39 (2007),pp. 311-318
    [58]
    Herault, Y., Rassoulzadegan, M., Cuzin, F. et al. Engineering chromosomes in mice through targeted meiotic recombination (TAMERE) Nat. Genet., 20 (1998),pp. 381-384
    [59]
    Hilton, I.B., D'Ippolito, A.M., Vockley, C.M. et al. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers Nat. Biotechnol., 33 (2015),pp. 510-517
    [60]
    Holohan, E.E., Kwong, C., Adryan, B. et al. PLoS Genet., 3 (2007),p. e112
    [61]
    Hou, C., Dale, R., Dean, A. Cell type specificity of chromatin organization mediated by CTCF and cohesin Proc. Natl. Acad. Sci. USA, 107 (2010),pp. 3651-3656
    [62]
    Hsu, P.D., Lander, E.S., Zhang, F. Development and applications of CRISPR-Cas9 for genome engineering Cell, 157 (2014),pp. 1262-1278
    [63]
    Hwang, W.Y., Fu, Y., Reyon, D. et al. Efficient genome editing in zebrafish using a CRISPR-Cas system Nat. Biotechnol., 31 (2013),pp. 227-229
    [64]
    Imakaev, M.V., Fudenberg, G., Mirny, L.A. Modeling chromosomes: beyond pretty pictures FEBS Lett., 589 (2015),pp. 3031-3036
    [65]
    International Human Genome Sequencing Consortium Initial sequencing and analysis of the human genome Nature, 409 (2001),pp. 860-921
    [66]
    Jasin, M., Rothstein, R. Repair of strand breaks by homologous recombination Cold Spring Harb. Perspect. Biol., 5 (2013),p. a012740
    [67]
    Jia, Z., Guo, Y., Tang, Y. et al. Mol. Cell. Biol., 34 (2014),pp. 3895-3910
    [68]
    Jiang, W., Bikard, D., Cox, D. et al. RNA-guided editing of bacterial genomes using CRISPR-Cas systems Nat. Biotechnol., 31 (2013),pp. 233-239
    [69]
    Jiang, W., Marraffini, L.A. CRISPR-Cas: new tools for genetic manipulations from bacterial immunity systems Annu. Rev. Microbiol., 69 (2015),pp. 209-228
    [70]
    Jinek, M., Chylinski, K., Fonfara, I. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity Science, 337 (2012),pp. 816-821
    [71]
    Jinek, M., East, A., Cheng, A. et al. RNA-programmed genome editing in human cells eLife, 2 (2013),p. e00471
    [72]
    Johnson, D.S., Mortazavi, A., Myers, R.M. et al. Science, 316 (2007),pp. 1497-1502
    [73]
    Kearns, N.A., Pham, H., Tabak, B. et al. Functional annotation of native enhancers with a Cas9-histone demethylase fusion Nat. Methods, 12 (2015),pp. 401-403
    [74]
    Kehayova, P., Monahan, K., Chen, W. et al. Regulatory elements required for the activation and repression of the protocadherin-alpha gene cluster Proc. Natl. Acad. Sci. USA, 108 (2011),pp. 17195-17200
    [75]
    Kim, T.H., Abdullaev, Z.K., Smith, A.D. et al. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome Cell, 128 (2007),pp. 1231-1245
    [76]
    Kim, T.K., Hemberg, M., Gray, J.M. et al. Widespread transcription at neuronal activity-regulated enhancers Nature, 465 (2010),pp. 182-187
    [77]
    Kmita, M., Kondo, T., Duboule, D. Nat. Genet., 26 (2000),pp. 451-454
    [78]
    Kraft, K., Geuer, S., Will, A.J. et al. Deletions, inversions, duplications: engineering of structural variants using CRISPR/Cas in mice Cell Rep., 10 (2015),pp. 833-839
    [79]
    Kungulovski, G., Jeltsch, A. Epigenome editing: state of the art, concepts, and perspectives Trends Genet., 32 (2016),pp. 101-113
    [80]
    Lagha, M., Bothma, J.P., Levine, M. Mechanisms of transcriptional precision in animal development Trends Genet., 28 (2012),pp. 409-416
    [81]
    Lander, E.S. The heroes of CRISPR Cell, 164 (2016),pp. 18-28
    [82]
    Lee, H.J., Kim, E., Kim, J.S. Targeted chromosomal deletions in human cells using zinc finger nucleases Genome Res., 20 (2010),pp. 81-89
    [83]
    Lee, H.J., Kweon, J., Kim, E. et al. Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleases Genome Res., 22 (2012),pp. 539-548
    [84]
    Lefebvre, J.L., Kostadinov, D., Chen, W.V. et al. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system Nature, 488 (2012),pp. 517-521
    [85]
    Levine, M., Cattoglio, C., Tjian, R. Looping back to leap forward: transcription enters a new era Cell, 157 (2014),pp. 13-25
    [86]
    Li, J., Shou, J., Guo, Y. et al. Efficient inversions and duplications of mammalian regulatory DNA elements and gene clusters by CRISPR/Cas9 J. Mol. Cell Biol., 7 (2015),pp. 284-298
    [87]
    Li, J., Shou, J., Wu, Q. DNA fragment editing of genomes by CRISPR/Cas9 Hereditas (Beijing), 37 (2015),pp. 992-1002
    [88]
    Li, L., Lyu, X., Hou, C. et al. Widespread rearrangement of 3D chromatin organization underlies polycomb-mediated stress-induced silencing Mol. Cell, 58 (2015),pp. 216-231
    [89]
    Lieberman-Aiden, E., van Berkum, N.L., Williams, L. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome Science, 326 (2009),pp. 289-293
    [90]
    Lindahl, T. Instability and decay of the primary structure of DNA Nature, 362 (1993),pp. 709-715
    [91]
    Lobanenkov, V.V., Nicolas, R.H., Adler, V.V. et al. Oncogene, 5 (1990),pp. 1743-1753
    [92]
    Lupiáñez, D.G., Kraft, K., Heinrich, V. et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions Cell, 161 (2015),pp. 1012-1025
    [93]
    Ma, H., Naseri, A., Reyes-Gutierrez, P. et al. Multicolor CRISPR labeling of chromosomal loci in human cells Proc. Natl. Acad. Sci. USA, 112 (2015),pp. 3002-3007
    [94]
    Maddalo, D., Manchado, E., Concepcion, C.P. et al. Nature, 516 (2014),pp. 423-427
    [95]
    Makarova, K.S., Wolf, Y.I., Alkhnbashi, O.S. et al. An updated evolutionary classification of CRISPR-Cas systems Nat. Rev. Microbiol., 13 (2015),pp. 722-736
    [96]
    Mali, P., Esvelt, K.M., Church, G.M. Cas9 as a versatile tool for engineering biology Nat. Methods, 10 (2013),pp. 957-963
    [97]
    Mali, P., Yang, L., Esvelt, K.M. et al. Science, 339 (2013),pp. 823-826
    [98]
    Maston, G.A., Evans, S.K., Green, M.R. Transcriptional regulatory elements in the human genome Annu. Rev. Genomics Hum. Genet., 7 (2006),pp. 29-59
    [99]
    Maurano, M.T., Humbert, R., Rynes, E. et al. Systematic localization of common disease-associated variation in regulatory DNA Science, 337 (2012),pp. 1190-1195
    [100]
    McVey, M., Lee, S.E. MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings Trends Genet., 24 (2008),pp. 529-538
    [101]
    Meyer, C.A., Liu, X.S. Identifying and mitigating bias in next-generation sequencing methods for chromatin biology Nat. Rev. Genet., 15 (2014),pp. 709-721
    [102]
    Mills, A.A., Bradley, A. From mouse to man: generating megabase chromosome rearrangements Trends Genet., 17 (2001),pp. 331-339
    [103]
    Monahan, K., Rudnick, N.D., Kehayova, P.D. et al. Role of CCCTC binding factor (CTCF) and cohesin in the generation of single-cell diversity of protocadherin-alpha gene expression Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 9125-9130
    [104]
    Nakahashi, H., Kwon, K.R., Resch, W. et al. A genome-wide map of CTCF multivalency redefines the CTCF code Cell Rep., 3 (2013),pp. 1678-1689
    [105]
    Narendra, V., Rocha, P.P., An, D. et al. Science, 347 (2015),pp. 1017-1021
    [106]
    Nichols, M.H., Corces, V.G. A CTCF code for 3D genome architecture Cell, 162 (2015),pp. 703-705
    [107]
    Noonan, J.P., McCallion, A.S. Genomics of long-range regulatory elements Annu. Rev. Genomics Hum. Genet., 11 (2010),pp. 1-23
    [108]
    Nora, E.P., Lajoie, B.R., Schulz, E.G. et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre Nature, 485 (2012),pp. 381-385
    [109]
    Ong, C.T., Corces, V.G. CTCF: an architectural protein bridging genome topology and function Nat. Rev. Genet., 15 (2014),pp. 234-246
    [110]
    Orkin, S.H. Globin gene regulation and switching: circa 1990 Cell, 63 (1990),pp. 665-672
    [111]
    Orr-Weaver, T.L., Szostak, J.W., Rothstein, R.J. Yeast transformation: a model system for the study of recombination Proc. Natl. Acad. Sci. USA, 78 (1981),pp. 6354-6358
    [112]
    Parelho, V., Hadjur, S., Spivakov, M. et al. Cohesins functionally associate with CTCF on mammalian chromosome arms Cell, 132 (2008),pp. 422-433
    [113]
    Phillips-Cremins, J.E., Sauria, M.E., Sanyal, A. et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment Cell, 153 (2013),pp. 1281-1295
    [114]
    Quitschke, W.W., Taheny, M.J., Fochtmann, L.J. et al. Differential effect of zinc finger deletions on the binding of CTCF to the promoter of the amyloid precursor protein gene Nucleic Acids Res., 28 (2000),pp. 3370-3378
    [115]
    Rada-Iglesias, A., Bajpai, R., Swigut, T. et al. A unique chromatin signature uncovers early developmental enhancers in humans Nature, 470 (2011),pp. 279-283
    [116]
    Rao, S.S., Huntley, M.H., Durand, N.C. et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping Cell, 159 (2014),pp. 1665-1680
    [117]
    Ren, B., Dixon, J.R. A CRISPR connection between chromatin topology and genetic disorders Cell, 161 (2015),pp. 955-957
    [118]
    Renda, M., Baglivo, I., Burgess-Beusse, B. et al. Critical DNA binding interactions of the insulator protein CTCF: a small number of zinc fingers mediate strong binding, and a single finger-DNA interaction controls binding at imprinted loci J. Biol. Chem., 282 (2007),pp. 33336-33345
    [119]
    Rhee, H.S., Pugh, B.F. Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution Cell, 147 (2011),pp. 1408-1419
    [120]
    Ribich, S., Tasic, B., Maniatis, T. Identification of long-range regulatory elements in the protocadherin-alpha gene cluster Proc. Natl. Acad. Sci. USA, 103 (2006),pp. 19719-19724
    [121]
    Saitoh, N., Bell, A.C., Recillas-Targa, F. et al. Structural and functional conservation at the boundaries of the chicken beta-globin domain EMBO J., 19 (2000),pp. 2315-2322
    [122]
    Sanborn, A.L., Rao, S.S., Huang, S.C. et al. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes Proc. Natl. Acad. Sci. USA, 112 (2015),pp. E6456-E6465
    [123]
    Sancar, A., Rupp, W.D. Cell, 33 (1983),pp. 249-260
    [124]
    Sander, J.D., Joung, J.K. CRISPR-Cas systems for editing, regulating and targeting genomes Nat. Biotechnol., 32 (2014),pp. 347-355
    [125]
    Sanyal, A., Lajoie, B.R., Jain, G. et al. The long-range interaction landscape of gene promoters Nature, 489 (2012),pp. 109-113
    [126]
    Schmidt, D., Schwalie, P.C., Wilson, M.D. et al. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages Cell, 148 (2012),pp. 335-348
    [127]
    Schoenherr, C.J., Anderson, D.J. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes Science, 267 (1995),pp. 1360-1363
    [128]
    Sexton, T., Cavalli, G. The role of chromosome domains in shaping the functional genome Cell, 160 (2015),pp. 1049-1059
    [129]
    Shen, Y., Yue, F., McCleary, D.F. et al. Nature, 488 (2012),pp. 116-120
    [130]
    Simonis, M., Klous, P., Splinter, E. et al. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C) Nat. Genet., 38 (2006),pp. 1348-1354
    [131]
    Spitz, F., Herkenne, C., Morris, M.A. et al. Nat. Genet., 37 (2005),pp. 889-893
    [132]
    Splinter, E., Heath, H., Kooren, J. et al. Genes Dev., 20 (2006),pp. 2349-2354
    [133]
    Suo, L., Lu, H., Ying, G. et al. Protocadherin clusters and cell adhesion kinase regulate dendrite complexity through Rho GTPase J. Mol. Cell Biol., 4 (2012),pp. 362-376
    [134]
    Tai, D.J., Ragavendran, A., Manavalan, P. et al. Engineering microdeletions and microduplications by targeting segmental duplications with CRISPR Nat. Neurosci., 19 (2016),pp. 517-522
    [135]
    Tang, Z., Luo, O.J., Li, X. et al. CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription Cell, 163 (2015),pp. 1611-1627
    [136]
    Tanimoto, K., Liu, Q., Bungert, J. et al. Nature, 398 (1999),pp. 344-348
    [137]
    Thakore, P.I., D'Ippolito, A.M., Song, L. et al. Highly specific epigenome editing by CRISPR-Cas9 repressors for silencing of distal regulatory elements Nat. Methods, 12 (2015),pp. 1143-1149
    [138]
    Thu, C.A., Chen, W.V., Rubinstein, R. et al. Single-cell identity generated by combinatorial homophilic interactions between alpha, beta, and gamma protocadherins Cell, 158 (2014),pp. 1045-1059
    [139]
    Thurman, R.E., Rynes, E., Humbert, R. et al. The accessible chromatin landscape of the human genome Nature, 489 (2012),pp. 75-82
    [140]
    Tjian, R., Maniatis, T. Transcriptional activation: a complex puzzle with few easy pieces Cell, 77 (1994),pp. 5-8
    [141]
    Torres, R., Martin, M.C., Garcia, A. et al. Engineering human tumour-associated chromosomal translocations with the RNA-guided CRISPR-Cas9 system Nat. Commun., 5 (2014),p. 3964
    [142]
    Vietri Rudan, M., Barrington, C., Henderson, S. et al. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture Cell Rep., 10 (2015),pp. 1297-1309
    [143]
    Visel, A., Blow, M.J., Li, Z. et al. ChIP-seq accurately predicts tissue-specific activity of enhancers Nature, 457 (2009),pp. 854-858
    [144]
    Wang, H., Maurano, M.T., Qu, H. et al. Widespread plasticity in CTCF occupancy linked to DNA methylation Genome Res., 22 (2012),pp. 1680-1688
    [145]
    Wang, H., Yang, H., Shivalila, C.S. et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering Cell, 153 (2013),pp. 910-918
    [146]
    Weckselblatt, B., Rudd, M.K. Human structural variation: mechanisms of chromosome rearrangements Trends Genet., 31 (2015),pp. 587-599
    [147]
    Wei, C., Liu, J., Yu, Z. et al. TALEN or Cas9-rapid, efficient and specific choices for genome modifications J. Genet. Genomics, 40 (2013),pp. 281-289
    [148]
    Wendt, K.S., Yoshida, K., Itoh, T. et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor Nature, 451 (2008),pp. 796-801
    [149]
    Whyte, W.A., Orlando, D.A., Hnisz, D. et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes Cell, 153 (2013),pp. 307-319
    [150]
    Wright, A.V., Nunez, J.K., Doudna, J.A. Biology and applications of CRISPR systems: harnessing nature's toolbox for genome engineering Cell, 164 (2016),pp. 29-44
    [151]
    Wu, Q. Comparative genomics and diversifying selection of the clustered vertebrate protocadherin genes Genetics, 169 (2005),pp. 2179-2188
    [152]
    Wu, Q., Maniatis, T. A striking organization of a large family of human neural cadherin-like cell adhesion genes Cell, 97 (1999),pp. 779-790
    [153]
    Wu, Q., Zhang, T., Cheng, J.F. et al. Comparative DNA sequence analysis of mouse and human protocadherin gene clusters Genome Res., 11 (2001),pp. 389-404
    [154]
    Wu, S., Ying, G., Wu, Q. et al. Toward simpler and faster genome-wide mutagenesis in mice Nat. Genet., 39 (2007),pp. 922-930
    [155]
    Xi, H., Shulha, H.P., Lin, J.M. et al. Identification and characterization of cell type-specific and ubiquitous chromatin regulatory structures in the human genome PLoS Genet., 3 (2007),p. e136
    [156]
    Xiao, A., Wang, Z., Hu, Y. et al. Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish Nucleic Acids Res., 41 (2013),p. e141
    [157]
    Xie, X., Mikkelsen, T.S., Gnirke, A. et al. Systematic discovery of regulatory motifs in conserved regions of the human genome, including thousands of CTCF insulator sites Proc. Natl. Acad. Sci. USA, 104 (2007),pp. 7145-7150
    [158]
    Xu, C., Corces, V.G. Towards a predictive model of chromatin 3D organization Semin. Cell Dev. Biol. (2015)
    [159]
    Yokota, S., Hirayama, T., Hirano, K. et al. Identification of the cluster control region for the protocadherin-beta genes located beyond the protocadherin-gamma cluster J. Biol. Chem., 286 (2011),pp. 31885-31895
    [160]
    Zetsche, B., Gootenberg, J.S., Abudayyeh, O.O. et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system Cell, 163 (2015),pp. 759-771
    [161]
    Zhang, T., Haws, P., Wu, Q. Multiple variable first exons: a mechanism for cell- and tissue-specific gene regulation Genome Res., 14 (2004),pp. 79-89
    [162]
    Zhang, Y., McCord, R.P., Ho, Y.J. et al. Spatial organization of the mouse genome and its role in recurrent chromosomal translocations Cell, 148 (2012),pp. 908-921
    [163]
    Zhao, Z., Tavoosidana, G., Sjolinder, M. et al. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions Nat. Genet., 38 (2006),pp. 1341-1347
    [164]
    Zou, C., Huang, W., Ying, G. et al. Sequence analysis and expression mapping of the rat clustered protocadherin gene repertoires Neuroscience, 144 (2007),pp. 579-603
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (74) PDF downloads (3) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return