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Volume 47 Issue 8
Aug.  2020
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Article Contents

Many facades of CTCF unified by its coding for three-dimensional genome architecture

doi: 10.1016/j.jgg.2020.06.008
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  • Corresponding author: E-mail address: qwu123@gmail.com (Qiang Wu)
  • Publish Date: 2020-08-25
  • CCCTC-binding factor (CTCF) is a multifunctional zinc finger protein that is conserved in metazoan species. CTCF is consistently found to play an important role in many diverse biological processes. CTCF/cohesin-mediated active chromatin ‘loop extrusion’ architects three-dimensional (3D) genome folding. The 3D architectural role of CTCF underlies its multifarious functions, including developmental regulation of gene expression, protocadherin (Pcdh) promoter choice in the nervous system, immunoglobulin (Ig) and T-cell receptor (Tcr) V(D)J recombination in the immune system, homeobox (Hox) gene control during limb development, as well as many other aspects of biology. Here, we review the pleiotropic functions of CTCF from the perspective of its essential role in 3D genome architecture and topological promoter/enhancer selection. We envision the 3D genome as an enormous complex architecture, with tens of thousands of CTCF sites as connecting nodes and CTCF proteins as mysterious bonds that glue together genomic building parts with distinct articulation joints. In particular, we focus on the internal mechanisms by which CTCF controls higher order chromatin structures that manifest its many façades of physiological and pathological functions. We also discuss the dichotomic role of CTCF sites as intriguing 3D genome nodes for seemingly contradictory ‘looping bridges’ and ‘topological insulators’ to frame a beautiful magnificent house for a cell's nuclear home.
  • These authors contributed equally to this work.
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  • [1]
    Alipour, E., Marko, J.F., 2012. Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Res. 40, 11202-11212.
    [2]
    Allahyar, A., Vermeulen, C., Bouwman, B.A.M., Krijger, P.H.L., Verstegen, M., Geeven, G., van Kranenburg, M., Pieterse, M., Straver, R., Haarhuis, J.H.I., Jalink, K., Teunissen, H., Renkens, I.J., Kloosterman, W.P., Rowland, B.D., de Wit, E., de Ridder, J., de Laat, W., 2018. Enhancer hubs and loop collisions identified from single-allele topologies. Nat. Genet. 50, 1151-1160.
    [3]
    Almenar-Queralt, A., Merkurjev, D., Kim, H.S., Navarro, M., Ma, Q., Chaves, R.S., Allegue, C., Driscoll, S.P., Chen, A.G., Kohlnhofer, B., Fong, L.K., Woodruff, G., Mackintosh, C., Bohaciakova, D., Hruska-Plochan, M., Tadokoro, T., Young, J.E., El Hajj, N., Dittrich, M., Marsala, M., Goldstein, L.S.B., Garcia-Bassets, I., 2019. Chromatin establishes an immature version of neuronal protocadherin selection during the naive-to-primed conversion of pluripotent stem cells. Nat. Genet. 51, 1691-1701.
    [4]
    Andrey, G., Montavon, T., Mascrez, B., Gonzalez, F., Noordermeer, D., Leleu, M., Trono, D., Spitz, F., Duboule, D., 2013. A switch between topological domains underlies HoxD genes collinearity in mouse limbs. Science 340, 1234167.
    [5]
    Andrey, G., Schopflin, R., Jerkovic, I., Heinrich, V., Ibrahim, D.M., Paliou, C., Hochradel, M., Timmermann, B., Haas, S., Vingron, M., Mundlos, S., 2017. Characterization of hundreds of regulatory landscapes in developing limbs reveals two regimes of chromatin folding. Genome Res. 27, 223-233.
    [6]
    Arzate-Mejia, R.G., Recillas-Targa, F., Corces, V.G., 2018. Developing in 3D: the role of CTCF in cell differentiation. Development 145.
    [7]
    Aulmann, S., Blaker, H., Penzel, R., Rieker, R.J., Otto, H.F., Sinn, H.P., 2003. CTCF gene mutations in invasive ductal breast cancer. Breast Cancer Res. Treat. 80, 347-352.
    [8]
    Ba, Z., Lou, J., Dring, E.W., Ye, A.Y., Lin, S.G., Jain, S., Kieffer-Kwon, K.-R., Casellas, R., Alt, F.W., 2020. CTCF orchestrates long-range cohesin-driven V(D)J recombinational scanning. BioRxiv. DOI: 10.1101/2020.01.01.891473.
    [9]
    Baniahmad, A., Steiner, C., Kohne, A.C., Renkawitz, R., 1990. Modular structure of a chicken lysozyme silencer: involvement of an unusual thyroid hormone receptor binding site. Cell 61, 505-514.
    [10]
    Barajas-Mora, E.M., Kleiman, E., Xu, J., Carrico, N.C., Lu, H., Oltz, E.M., Murre, C., Feeney, A.J., 2019. A B-cell-specific enhancer orchestrates nuclear architecture to generate a diverse antigen receptor repertoire. Mol. Cell 73, 48-60 e45.
    [11]
    Beagrie, R.A., Scialdone, A., Schueler, M., Kraemer, D.C., Chotalia, M., Xie, S.Q., Barbieri, M., de Santiago, I., Lavitas, L.M., Branco, M.R., Fraser, J., Dostie, J., Game, L., Dillon, N., Edwards, P.A., Nicodemi, M., Pombo, A., 2017. Complex multi-enhancer contacts captured by genome architecture mapping. Nature 543, 519-524.
    [12]
    Bell, A.C., Felsenfeld, G., 2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405, 482-485.
    [13]
    Bell, A.C., West, A.G., Felsenfeld, G., 1999. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98, 387-396.
    [14]
    Bickmore, W.A., 2013. The spatial organization of the human genome. Annu. Rev. Genomics Hum. Genet. 14, 67-84.
    [15]
    Bolland, D.J., Koohy, H., Wood, A.L., Matheson, L.S., Krueger, F., Stubbington, M.J., Baizan-Edge, A., Chovanec, P., Stubbs, B.A., Tabbada, K., Andrews, S.R., Spivakov, M., Corcoran, A.E., 2016. Two mutually exclusive local chromatin states drive efficient V(D)J recombination. Cell Rep. 15, 2475-2487.
    [16]
    Bonev, B., Cavalli, G., 2016. Organization and function of the 3D genome. Nat. Rev. Genet. 17, 661-678.
    [17]
    Bonev, B., Mendelson Cohen, N., Szabo, Q., Fritsch, L., Papadopoulos, G.L., Lubling, Y., Xu, X., Lv, X., Hugnot, J.P., Tanay, A., Cavalli, G., 2017. Multiscale 3D genome rewiring during mouse neural development. Cell 171, 557-572 e524.
    [18]
    Bonora, G., Deng, X., Fang, H., Ramani, V., Qiu, R., Berletch, J.B., Filippova, G.N., Duan, Z., Shendure, J., Noble, W.S., Disteche, C.M., 2018. Orientation-dependent Dxz4 contacts shape the 3D structure of the inactive X chromosome. Nat. Commun. 9, 1445.
    [19]
    Boyle, A.P., Song, L., Lee, B.K., London, D., Keefe, D., Birney, E., Iyer, V.R., Crawford, G.E., Furey, T.S., 2011. High-resolution genome-wide in vivo footprinting of diverse transcription factors in human cells. Genome Res. 21, 456-464.
    [20]
    Braccioli, L., de Wit, E., 2019. CTCF: a Swiss-army knife for genome organization and transcription regulation. Essays Biochem. 63, 157-165.
    [21]
    Brasch, J., Goodman, K.M., Noble, A.J., Rapp, M., Mannepalli, S., Bahna, F., Dandey, V.P., Bepler, T., Berger, B., Maniatis, T., Potter, C.S., Carragher, B., Honig, B., Shapiro, L., 2019. Visualization of clustered protocadherin neuronal self-recognition complexes. Nature 569, 280-283.
    [22]
    Burcin, M., Arnold, R., Lutz, M., Kaiser, B., Runge, D., Lottspeich, F., Filippova, G.N., Lobanenkov, V.V., Renkawitz, R., 1997. Negative protein 1, which is required for function of the chicken lysozyme gene silencer in conjunction with hormone receptors, is identical to the multivalent zinc finger repressor CTCF. Mol. Cell. Biol. 17, 1281-1288.
    [23]
    Canzio, D., Nwakeze, C.L., Horta, A., Rajkumar, S.M., Coffey, E.L., Duffy, E.E., Duffie, R., Monahan, K., O'Keeffe, S., Simon, M.D., Lomvardas, S., Maniatis, T., 2019. Antisense lncRNA transcription mediates DNA demethylation to drive stochastic protocadherin alpha promoter choice. Cell 177, 639-653 e615.
    [24]
    Capecchi, M.R., 1997. Hox genes and mammalian development. Cold Spring Harb. Symp. Quant. Biol. 62, 273-281.
    [25]
    Chen, B., Brinkmann, K., Chen, Z., Pak, C.W., Liao, Y., Shi, S., Henry, L., Grishin, N.V., Bogdan, S., Rosen, M.K., 2014. The WAVE regulatory complex links diverse receptors to the actin cytoskeleton. Cell 156, 195-207.
    [26]
    Chen, L., Carico, Z., Shih, H.Y., Krangel, M.S., 2015. A discrete chromatin loop in the mouse Tcra-Tcrd locus shapes the TCRdelta and TCRalpha repertoires. Nat. Immunol. 16, 1085-1093.
    [27]
    Chen, W.V., Nwakeze, C.L., Denny, C.A., O'Keeffe, S., Rieger, M.A., Mountoufaris, G., Kirner, A., Dougherty, J.D., Hen, R., Wu, Q., Maniatis, T., 2017. Pcdhalphac2 is required for axonal tiling and assembly of serotonergic circuitries in mice. Science 356, 406-411.
    [28]
    Chen, X., Ke, Y., Wu, K., Zhao, H., Sun, Y., Gao, L., Liu, Z., Zhang, J., Tao, W., Hou, Z., Liu, H., Liu, J., Chen, Z.J., 2019. Key role for CTCF in establishing chromatin structure in human embryos. Nature 576, 306-310.
    [29]
    Chen, H., Tian, Y., Shu, W., Bo, X., Wang, S., 2012. Comprehensive identification and annotation of cell type-specific and ubiquitous CTCF-binding sites in the human genome. PLoS One 7, e41374.
    [30]
    Chung, J.H., Whiteley, M., Felsenfeld, G., 1993. A 5' element of the chicken beta-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell 74, 505-514.
    [31]
    Ciccone, D.N., Namiki, Y., Chen, C., Morshead, K.B., Wood, A.L., Johnston, C.M., Morris, J.W., Wang, Y., Sadreyev, R., Corcoran, A.E., Matthews, A.G.W., Oettinger, M.A., 2019. The murine IgH locus contains a distinct DNA sequence motif for the chromatin regulatory factor CTCF. J. Biol. Chem. 294, 13580-13592.
    [32]
    Cremer, T., Cremer, C., 2001. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2, 292-301.
    [33]
    Cuddapah, S., Jothi, R., Schones, D.E., Roh, T.Y., Cui, K., Zhao, K., 2009. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res. 19, 24-32.
    [34]
    Dai, J., Zhu, M., Wang, C., Shen, W., Zhou, W., Sun, J., Liu, J., Jin, G., Ma, H., Hu, Z., Lin, D., Shen, H., 2015. Systematical analyses of variants in CTCF-binding sites identified a novel lung cancer susceptibility locus among Chinese population. Sci. Rep. 5, 7833.
    [35]
    Darrow, E.M., Huntley, M.H., Dudchenko, O., Stamenova, E.K., Durand, N.C., Sun, Z., Huang, S.C., Sanborn, A.L., Machol, I., Shamim, M., Seberg, A.P., Lander, E.S., Chadwick, B.P., Aiden, E.L., 2016. Deletion of DXZ4 on the human inactive X chromosome alters higher-order genome architecture. Proc. Natl. Acad. Sci. U. S. A. 113, E4504-4512.
    [36]
    Davidson, I.F., Bauer, B., Goetz, D., Tang, W., Wutz, G., Peters, J.M., 2019. DNA loop extrusion by human cohesin. Science 366, 1338-1345.
    [37]
    Davis, A.P., Witte, D.P., Hsieh-Li, H.M., Potter, S.S., Capecchi, M.R., 1995. Absence of radius and ulna in mice lacking hoxa-11 and hoxd-11. Nature 375, 791-795.
    [38]
    De Wit, E., Vos, E.S., Holwerda, S.J., Valdes-Quezada, C., Verstegen, M.J., Teunissen, H., Splinter, E., Wijchers, P.J., Krijger, P.H., de Laat, W., 2015. CTCF binding polarity determines chromatin looping. Mol. Cell 60, 676-684.
    [39]
    Degner, S.C., Wong, T.P., Jankevicius, G., Feeney, A.J., 2009. Cutting edge: developmental stage-specific recruitment of cohesin to CTCF sites throughout immunoglobulin loci during B lymphocyte development. J. Immunol. 182, 44-48.
    [40]
    Dekker, J., 2012. CTCF and cohesin help neurons raise their self-awareness. Proc. Natl. Acad. Sci. U. S. A. 109, 8799-8800.
    [41]
    Dekker, J., Mirny, L., 2016. The 3D genome as moderator of chromosomal communication. Cell 164, 1110-1121.
    [42]
    Dekker, J., Rippe, K., Dekker, M., Kleckner, N., 2002. Capturing chromosome conformation. Science 295, 1306-1311.
    [43]
    Dixon, J.R., Gorkin, D.U., Ren, B., 2016. Chromatin domains: the unit of chromosome organization. Mol. Cell 62, 668-680.
    [44]
    Dixon, J.R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J.S., Ren, B., 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376-380.
    [45]
    Dostie, J., Richmond, T.A., Arnaout, R.A., Selzer, R.R., Lee, W.L., Honan, T.A., Rubio, E.D., Krumm, A., Lamb, J., Nusbaum, C., Green, R.D., Dekker, J., 2006. Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res. 16, 1299-1309.
    [46]
    Dowen, J.M., Fan, Z.P., Hnisz, D., Ren, G., Abraham, B.J., Zhang, L.N., Weintraub, A.S., Schujiers, J., Lee, T.I., Zhao, K., Young, R.A., 2014. Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell 159, 374-387.
    [47]
    Du, Z., Zheng, H., Huang, B., Ma, R., Wu, J., Zhang, X., He, J., Xiang, Y., Wang, Q., Li, Y., Ma, J., Zhang, X., Zhang, K., Wang, Y., Zhang, M.Q., Gao, J., Dixon, J.R., Wang, X., Zeng, J., Xie, W., 2017. Allelic reprogramming of 3D chromatin architecture during early mammalian development. Nature 547, 232-235.
    [48]
    Ebert, A., Hill, L., Busslinger, M., 2015. Spatial regulation of V-(D)J recombination at antigen receptor loci. Adv. Immunol. 128, 93-121.
    [49]
    El-Kady, A., Klenova, E., 2005. Regulation of the transcription factor, CTCF, by phosphorylation with protein kinase CK2. FEBS Lett. 579, 1424-1434.
    [50]
    Englesberg, E., Squires, C., Meronk, F., Jr., 1969. The L-arabinose operon in Escherichia coli B-r: a genetic demonstration of two functional states of the product of a regulator gene. Proc. Natl. Acad. Sci. U. S. A. 62, 1100-1107.
    [51]
    Esumi, S., Kakazu, N., Taguchi, Y., Hirayama, T., Sasaki, A., Hirabayashi, T., Koide, T., Kitsukawa, T., Hamada, S., Yagi, T., 2005. Monoallelic yet combinatorial expression of variable exons of the protocadherin-alpha gene cluster in single neurons. Nat. Genet. 37, 171-176.
    [52]
    Fan, L., Lu, Y., Shen, X., Shao, H., Suo, L., Wu, Q., 2018. Alpha protocadherins and Pyk2 kinase regulate cortical neuron migration and cytoskeletal dynamics via Rac1 GTPase and WAVE complex in mice. eLife 7.
    [53]
    Fang, R., Wang, C., Skogerbo, G., Zhang, Z., 2015. Functional diversity of CTCFs is encoded in their binding motifs. BMC Genomics 16, 649.
    [54]
    Filippova, G.N., Fagerlie, S., Klenova, E.M., Myers, C., Dehner, Y., Goodwin, G., Neiman, P.E., Collins, S.J., Lobanenkov, V.V., 1996. An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol. Cell. Biol. 16, 2802-2813.
    [55]
    Filippova, G.N., Lindblom, A., Meincke, L.J., Klenova, E.M., Neiman, P.E., Collins, S.J., Doggett, N.A., Lobanenkov, V.V., 1998. A widely expressed transcription factor with multiple DNA sequence specificity, CTCF, is localized at chromosome segment 16q22.1 within one of the smallest regions of overlap for common deletions in breast and prostate cancers. Genes Chromosomes Cancer 22, 26-36.
    [56]
    Flavahan, W.A., Drier, Y., Liau, B.B., Gillespie, S.M., Venteicher, A.S., Stemmer-Rachamimov, A.O., Suva, M.L., Bernstein, B.E., 2016. Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature 529, 110-114.
    [57]
    Fritsch, E.F., Lawn, R.M., Maniatis, T., 1980. Molecular cloning and characterization of the human beta-like globin gene cluster. Cell 19, 959-972.
    [58]
    Fromental-Ramain, C., Warot, X., Messadecq, N., LeMeur, M., Dolle, P., Chambon, P., 1996. Hoxa-13 and Hoxd-13 play a crucial role in the patterning of the limb autopod. Development 122, 2997-3011.
    [59]
    Fu, Y., Sinha, M., Peterson, C.L., Weng, Z., 2008. The insulator binding protein CTCF positions 20 nucleosomes around its binding sites across the human genome. PLoS Genet. 4, e1000138.
    [60]
    Fudenberg, G., Imakaev, M., Lu, C., Goloborodko, A., Abdennur, N., Mirny, L.A., 2016. Formation of chromosomal domains by loop extrusion. Cell Rep. 15, 2038-2049.
    [61]
    Fujimoto, A., Furuta, M., Totoki, Y., Tsunoda, T., Kato, M., Shiraishi, Y., Tanaka, H., Taniguchi, H., Kawakami, Y., Ueno, M., Gotoh, K., Ariizumi, S., Wardell, C.P., Hayami, S., Nakamura, T., Aikata, H., Arihiro, K., Boroevich, K.A., Abe, T., Nakano, K., Maejima, K., Sasaki-Oku, A., Ohsawa, A., Shibuya, T., Nakamura, H., Hama, N., Hosoda, F., Arai, Y., Ohashi, S., Urushidate, T., Nagae, G., Yamamoto, S., Ueda, H., Tatsuno, K., Ojima, H., Hiraoka, N., Okusaka, T., Kubo, M., Marubashi, S., Yamada, T., Hirano, S., Yamamoto, M., Ohdan, H., Shimada, K., Ishikawa, O., Yamaue, H., Chayama, K., Miyano, S., Aburatani, H., Shibata, T., Nakagawa, H., 2016. Whole-genome mutational landscape and characterization of noncoding and structural mutations in liver cancer. Nat. Genet. 48, 500-509.
    [62]
    Fullwood, M.J., Liu, M.H., Pan, Y.F., Liu, J., Xu, H., Mohamed, Y.B., Orlov, Y.L., Velkov, S., Ho, A., Mei, P.H., Chew, E.G., Huang, P.Y., Welboren, W.J., Han, Y., Ooi, H.S., Ariyaratne, P.N., Vega, V.B., Luo, Y., Tan, P.Y., Choy, P.Y., Wansa, K.D., Zhao, B., Lim, K.S., Leow, S.C., Yow, J.S., Joseph, R., Li, H., Desai, K.V., Thomsen, J.S., Lee, Y.K., Karuturi, R.K., Herve, T., Bourque, G., Stunnenberg, H.G., Ruan, X., Cacheux-Rataboul, V., Sung, W.K., Liu, E.T., Wei, C.L., Cheung, E., Ruan, Y., 2009. An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 462, 58-64.
    [63]
    Garrett, A.M., Schreiner, D., Lobas, M.A., Weiner, J.A., 2012. Gamma-protocadherins control cortical dendrite arborization by regulating the activity of a FAK/PKC/MARCKS signaling pathway. Neuron 74, 269-276.
    [64]
    Gerasimova, T.I., Corces, V.G., 2001. Chromatin insulators and boundaries: effects on transcription and nuclear organization. Annu. Rev. Genet. 35, 193-208.
    [65]
    Ghirlando, R., Felsenfeld, G., 2016. CTCF: making the right connections. Genes Dev. 30, 881-891.
    [66]
    Giorgetti, L., Lajoie, B.R., Carter, A.C., Attia, M., Zhan, Y., Xu, J., Chen, C.J., Kaplan, N., Chang, H.Y., Heard, E., Dekker, J., 2016. Structural organization of the inactive X chromosome in the mouse. Nature 535, 575-579.
    [67]
    Gray, C.E., Coates, C.J., 2005. Cloning and characterization of cDNAs encoding putative CTCFs in the mosquitoes, Aedes aegypti and Anopheles gambiae. BMC Mol. Biol. 6, 16.
    [68]
    Guibert, S., Zhao, Z., Sjolinder, M., Gondor, A., Fernandez, A., Pant, V., Ohlsson, R., 2012. CTCF-binding sites within the H19 ICR differentially regulate local chromatin structures and cis-acting functions. Epigenetics 7, 361-369.
    [69]
    Guo, C., Yoon, H.S., Franklin, A., Jain, S., Ebert, A., Cheng, H.L., Hansen, E., Despo, O., Bossen, C., Vettermann, C., Bates, J.G., Richards, N., Myers, D., Patel, H., Gallagher, M., Schlissel, M.S., Murre, C., Busslinger, M., Giallourakis, C.C., Alt, F.W., 2011. CTCF-binding elements mediate control of V(D)J recombination. Nature 477, 424-430.
    [70]
    Guo, Y., Monahan, K., Wu, H., Gertz, J., Varley, K.E., Li, W., Myers, R.M., Maniatis, T., Wu, Q., 2012. CTCF/cohesin-mediated DNA looping is required for protocadherin alpha promoter choice. Proc. Natl. Acad. Sci. U. S. A. 109, 21081-21086.
    [71]
    Guo, Y., Xu, Q., Canzio, D., Shou, J., Li, J., Gorkin, D.U., Jung, I., Wu, H., Zhai, Y., Tang, Y., Lu, Y., Wu, Y., Jia, Z., Li, W., Zhang, M.Q., Ren, B., Krainer, A.R., Maniatis, T., Wu, Q., 2015. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162, 900-910.
    [72]
    Guo, Y.A., Chang, M.M., Huang, W., Ooi, W.F., Xing, M., Tan, P., Skanderup, A.J., 2018. Mutation hotspots at CTCF binding sites coupled to chromosomal instability in gastrointestinal cancers. Nat. Commun. 9, 1520.
    [73]
    Hadjur, S., Williams, L.M., Ryan, N.K., Cobb, B.S., Sexton, T., Fraser, P., Fisher, A.G., Merkenschlager, M., 2009. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 460, 410-413.
    [74]
    Handoko, L., Xu, H., Li, G., Ngan, C.Y., Chew, E., Schnapp, M., Lee, C.W., Ye, C., Ping, J.L., Mulawadi, F., Wong, E., Sheng, J., Zhang, Y., Poh, T., Chan, C.S., Kunarso, G., Shahab, A., Bourque, G., Cacheux-Rataboul, V., Sung, W.K., Ruan, Y., Wei, C.L., 2011. CTCF-mediated functional chromatin interactome in pluripotent cells. Nat. Genet. 43, 630-638.
    [75]
    Hansen, A.S., Hsieh, T.S., Cattoglio, C., Pustova, I., Saldana-Meyer, R., Reinberg, D., Darzacq, X., Tjian, R., 2019. Distinct classes of chromatin loops revealed by deletion of an RNA-binding region in CTCF. Mol. Cell 76, 395-411 e313.
    [76]
    Hansen, A.S., Pustova, I., Cattoglio, C., Tjian, R., Darzacq, X., 2017. CTCF and cohesin regulate chromatin loop stability with distinct dynamics. eLife 6.
    [77]
    Hark, A.T., Schoenherr, C.J., Katz, D.J., Ingram, R.S., Levorse, J.M., Tilghman, S.M., 2000. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405, 486-489.
    [78]
    Hashimoto, H., Wang, D., Horton, J.R., Zhang, X., Corces, V.G., Cheng, X., 2017. Structural basis for the versatile and methylation-dependent binding of CTCF to DNA. Mol. Cell 66, 711-720 e713.
    [79]
    Heger, P., Marin, B., Bartkuhn, M., Schierenberg, E., Wiehe, T., 2012. The chromatin insulator CTCF and the emergence of metazoan diversity. Proc. Natl. Acad. Sci. U. S. A. 109, 17507-17512.
    [80]
    Hirano, T., Mitchison, T.J., 1994. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 79, 449-458.
    [81]
    Hirano, T., Mitchison, T.J., Swedlow, J.R., 1995. The SMC family: from chromosome condensation to dosage compensation. Curr. Opin. cell biol. 7, 329-336.
    [82]
    Hnisz, D., Shrinivas, K., Young, R.A., Chakraborty, A.K., Sharp, P.A., 2017. A phase separation model for transcriptional control. Cell 169, 13-23.
    [83]
    Holohan, E.E., Kwong, C., Adryan, B., Bartkuhn, M., Herold, M., Renkawitz, R., Russell, S., White, R., 2007. CTCF genomic binding sites in Drosophila and the organisation of the bithorax complex. PLoS Genet. 3, e112.
    [84]
    Hou, C., Zhao, H., Tanimoto, K., Dean, A., 2008. CTCF-dependent enhancer-blocking by alternative chromatin loop formation. Proc. Natl. Acad. Sci. U. S. A. 105, 20398-20403.
    [85]
    Huang, H., Wu, Q., 2016. CRISPR double cutting through the labyrinthine architecture of 3D genomes. J. Genet. Genomics 43, 273-288.
    [86]
    Huang, K., Jia, J., Wu, C., Yao, M., Li, M., Jin, J., Jiang, C., Cai, Y., Pei, D., Pan, G., Yao, H., 2013. Ribosomal RNA gene transcription mediated by the master genome regulator protein CCCTC-binding factor (CTCF) is negatively regulated by the condensin complex. J. Biol. Chem. 288, 26067-26077.
    [87]
    Hug, C.B., Grimaldi, A.G., Kruse, K., Vaquerizas, J.M., 2017. Chromatin architecture emerges during zygotic genome activation independent of transcription. Cell 169, 216-228 e219.
    [88]
    Hug, C.B., Vaquerizas, J.M., 2018. The birth of the 3D genome during early embryonic development. Trends Genet. 34, 903-914.
    [89]
    Hyle, J., Zhang, Y., Wright, S., Xu, B., Shao, Y., Easton, J., Tian, L., Feng, R., Xu, P., Li, C., 2019. Acute depletion of CTCF directly affects MYC regulation through loss of enhancer-promoter looping. Nucleic Acids Res. 47, 6699-6713.
    [90]
    Ing-Esteves, S., Kostadinov, D., Marocha, J., Sing, A.D., Joseph, K.S., Laboulaye, M.A., Sanes, J.R., Lefebvre, J.L., 2018. Combinatorial effects of alpha- and gamma-protocadherins on neuronal survival and dendritic self-avoidance. J. Neurosci. 38, 2713-2729.
    [91]
    Jain, S., Ba, Z., Zhang, Y., Dai, H.Q., Alt, F.W., 2018. CTCF-binding elements mediate accessibility of RAG substrates during chromatin scanning. Cell 174, 102-116 e114.
    [92]
    Jia, Z., Guo, Y., Tang, Y., Xu, Q., Li, B., Wu, Q., 2014. Regulation of the protocadherin Celsr3 gene and its role in globus pallidus development and connectivity. Mol. Cell. Biol. 34, 3895-3910.
    [93]
    Jia, Z., Li, J., Ge, X., Wu, Y., Guo, Y., Wu, Q., 2020. Tandem CTCF sites function as insulators to balance spatial chromatin contacts and topological enhancer-promoter selection. Genome Biol. 21, 75.
    [94]
    Johnson, D.S., Mortazavi, A., Myers, R.M., Wold, B., 2007. Genome-wide mapping of in vivo protein-DNA interactions. Science 316, 1497-1502.
    [95]
    Jothi, R., Cuddapah, S., Barski, A., Cui, K., Zhao, K., 2008. Genome-wide identification of in vivo protein-DNA binding sites from ChIP-Seq data. Nucleic Acids Res. 36, 5221-5231.
    [96]
    Kanduri, C., Pant, V., Loukinov, D., Pugacheva, E., Qi, C.F., Wolffe, A., Ohlsson, R., Lobanenkov, V.V., 2000. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr. Biol. 10, 853-856.
    [97]
    Kang, K., Chung, J.H., Kim, J., 2009. Evolutionary Conserved Motif Finder (ECMFinder) for genome-wide identification of clustered YY1- and CTCF-binding sites. Nucleic Acids Res. 37, 2003-2013.
    [98]
    Katainen, R., Dave, K., Pitkanen, E., Palin, K., Kivioja, T., Valimaki, N., Gylfe, A.E., Ristolainen, H., Hanninen, U.A., Cajuso, T., Kondelin, J., Tanskanen, T., Mecklin, J.P., Jarvinen, H., Renkonen-Sinisalo, L., Lepisto, A., Kaasinen, E., Kilpivaara, O., Tuupanen, S., Enge, M., Taipale, J., Aaltonen, L.A., 2015. CTCF/cohesin-binding sites are frequently mutated in cancer. Nat. Genet. 47, 818-821.
    [99]
    Ke, Y., Xu, Y., Chen, X., Feng, S., Liu, Z., Sun, Y., Yao, X., Li, F., Zhu, W., Gao, L., Chen, H., Du, Z., Xie, W., Xu, X., Huang, X., Liu, J., 2017. 3D chromatin structures of mature gametes and structural reprogramming during mammalian embryogenesis. Cell 170, 367-381 e320.
    [100]
    Kempfer, R., Pombo, A., 2020. Methods for mapping 3D chromosome architecture. Nat. Rev. Genet. 21, 207-226.
    [101]
    Khoury, A., Achinger-Kawecka, J., Bert, S.A., Smith, G.C., French, H.J., Luu, P.L., Peters, T.J., Du, Q., Parry, A.J., Valdes-Mora, F., Taberlay, P.C., Stirzaker, C., Statham, A.L., Clark, S.J., 2020. Constitutively bound CTCF sites maintain 3D chromatin architecture and long-range epigenetically regulated domains. Nat. Commun. 11, 54.
    [102]
    Kim, T.H., Abdullaev, Z.K., Smith, A.D., Ching, K.A., Loukinov, D.I., Green, R.D., Zhang, M.Q., Lobanenkov, V.V., Ren, B., 2007. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 128, 1231-1245.
    [103]
    Kim, Y., Shi, Z., Zhang, H., Finkelstein, I.J., Yu, H., 2019. Human cohesin compacts DNA by loop extrusion. Science 366, 1345-1349.
    [104]
    Klenova, E.M., Nicolas, R.H., Paterson, H.F., Carne, A.F., Heath, C.M., Goodwin, G.H., Neiman, P.E., Lobanenkov, V.V., 1993. CTCF, a conserved nuclear factor required for optimal transcriptional activity of the chicken c-myc gene, is an 11-Zn-finger protein differentially expressed in multiple forms. Mol. Cell. Biol. 13, 7612-7624.
    [105]
    Klenova, E.M., Nicolas, R.H., U, S., Carne, A.F., Lee, R.E., Lobanenkov, V.V., Goodwin, G.H., 1997. Molecular weight abnormalities of the CTCF transcription factor: CTCF migrates aberrantly in SDS-PAGE and the size of the expressed protein is affected by the UTRs and sequences within the coding region of the CTCF gene. Nucleic Acids Res. 25, 466-474.
    [106]
    Kloetgen, A., Thandapani, P., Tsirigos, A., Aifantis, I., 2019. 3D chromosomal landscapes in hematopoiesis and immunity. Trends Immunol. 40, 809-824.
    [107]
    Kraft, K., Magg, A., Heinrich, V., Riemenschneider, C., Schopflin, R., Markowski, J., Ibrahim, D.M., Acuna-Hidalgo, R., Despang, A., Andrey, G., Wittler, L., Timmermann, B., Vingron, M., Mundlos, S., 2019. Serial genomic inversions induce tissue-specific architectural stripes, gene misexpression and congenital malformations. Nat. Cell Biol. 21, 305-310.
    [108]
    Kubo, N., Ishii, H., Gorkin, D., Meitinger, F., Xiong, X., Fang, R., Liu, T., Ye, Z., Li, B., Dixon, J., Desai, A., Zhao, H., Ren, B., 2017. Preservation of chromatin organization after acute loss of CTCF in mouse embryonic stem cells. BioRxiv. DOI: 10.1101/118737.
    [109]
    Kubo, N., Ishii, H., Xiong, X., Bianco, S., Meitinger, F., Hu, R., Hocker, J.D., Conte, M., Gorkin, D., Yu, M., Li, B., Dixon, J.R., Hu, M., Nicodemi, M., Zhao, H., Ren, B., 2020. CTCF promotes long-range enhancer-promoter interactions and lineage-specific gene expression in mammalian cells. BioRxiv. DOI: 10.1101/2020.03.21.001693.
    [110]
    Kurukuti, S., Tiwari, V.K., Tavoosidana, G., Pugacheva, E., Murrell, A., Zhao, Z., Lobanenkov, V., Reik, W., Ohlsson, R., 2006. CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2. Proc. Natl. Acad. Sci. U. S. A. 103, 10684-10689.
    [111]
    Lefebvre, J.L., Kostadinov, D., Chen, W.V., Maniatis, T., Sanes, J.R., 2012. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488, 517-521.
    [112]
    Levine, M., Cattoglio, C., Tjian, R., 2014. Looping back to leap forward: transcription enters a new era. Cell 157, 13-25.
    [113]
    Li, R., Liu, Y., Li, T., Li, C., 2016. 3Disease Browser: A Web server for integrating 3D genome and disease-associated chromosome rearrangement data. Sci. Rep. 6, 34651.
    [114]
    Li, Y., Haarhuis, J.H.I., Sedeno Cacciatore, A., Oldenkamp, R., van Ruiten, M.S., Willems, L., Teunissen, H., Muir, K.W., de Wit, E., Rowland, B.D., Panne, D., 2020. The structural basis for cohesin-CTCF-anchored loops. Nature 578, 472-476.
    [115]
    Lieberman-Aiden, E., van Berkum, N.L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B.R., Sabo, P.J., Dorschner, M.O., Sandstrom, R., Bernstein, B., Bender, M.A., Groudine, M., Gnirke, A., Stamatoyannopoulos, J., Mirny, L.A., Lander, E.S., Dekker, J., 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293.
    [116]
    Lin, S.G., Ba, Z., Alt, F.W., Zhang, Y., 2018. RAG chromatin scanning during V(D)J recombination and chromatin loop extrusion are related processes. Adv. Immunol. 139, 93-135.
    [117]
    Lobanenkov, V.V., Nicolas, R.H., Adler, V.V., Paterson, H., Klenova, E.M., Polotskaja, A.V., Goodwin, G.H., 1990. A novel sequence-specific DNA binding protein which interacts with three regularly spaced direct repeats of the CCCTC-motif in the 5'-flanking sequence of the chicken c-myc gene. Oncogene 5, 1743-1753.
    [118]
    Lu, Y., Shou, J., Jia, Z., Wu, Y., Li, J., Guo, Y., Wu, Q., 2019. Genetic evidence for asymmetric blocking of higher-order chromatin structure by CTCF/cohesin. Protein Cell 10, 914-920.
    [119]
    Luo, H., Wang, F., Zha, J., Li, H., Yan, B., Du, Q., Yang, F., Sobh, A., Vulpe, C., Drusbosky, L., Cogle, C., Chepelev, I., Xu, B., Nimer, S.D., Licht, J., Qiu, Y., Chen, B., Xu, M., Huang, S., 2018. CTCF boundary remodels chromatin domain and drives aberrant HOX gene transcription in acute myeloid leukemia. Blood 132, 837-848.
    [120]
    Luo, H., Yu, Q., Liu, Y., Tang, M., Liang, M., Zhang, D., Xiao, T.S., Wu, L., Tan, M., Ruan, Y., Bungert, J., Lu, J., 2020. LATS kinase-mediated CTCF phosphorylation and selective loss of genomic binding. Sci. Adv. 6, eaaw4651.
    [121]
    Lyu, X., Rowley, M.J., Corces, V.G., 2018. Architectural proteins and pluripotency factors cooperate to orchestrate the transcriptional response of hESCs to temperature stress. Mol. Cell 71, 940-955 e947.
    [122]
    MacDonald, W.A., Menon, D., Bartlett, N.J., Sperry, G.E., Rasheva, V., Meller, V., Lloyd, V.K., 2010. The Drosophila homolog of the mammalian imprint regulator, CTCF, maintains the maternal genomic imprint in Drosophila melanogaster. BMC Biol. 8, 105.
    [123]
    Mackenzie, P.I., Gregory, P.A., Lewinsky, R.H., Yasmin, S.N., Height, T., McKinnon, R.A., Gardner-Stephen, D.A., 2005. Polymorphic variations in the expression of the chemical detoxifying UDP glucuronosyltransferases. Toxicology and applied pharmacology 207, 77-83.
    [124]
    Maeshima, K., Eltsov, M., Laemmli, U.K., 2005. Chromosome structure: improved immunolabeling for electron microscopy. Chromosoma 114, 365-375.
    [125]
    Majumder, K., Koues, O.I., Chan, E.A., Kyle, K.E., Horowitz, J.E., Yang-Iott, K., Bassing, C.H., Taniuchi, I., Krangel, M.S., Oltz, E.M., 2015. Lineage-specific compaction of Tcrb requires a chromatin barrier to protect the function of a long-range tethering element. J. Exp. Med. 212, 107-120.
    [126]
    Mallo, M., Wellik, D.M., Deschamps, J., 2010. Hox genes and regional patterning of the vertebrate body plan. Developmental biology 344, 7-15.
    [127]
    Marko, J.F., Siggia, E.D., 1997. Polymer models of meiotic and mitotic chromosomes. Molecular biology of the cell 8, 2217-2231.
    [128]
    Marsden, M.P., Laemmli, U.K., 1979. Metaphase chromosome structure: evidence for a radial loop model. Cell 17, 849-858.
    [129]
    Martin, D., Pantoja, C., Fernandez Minan, A., Valdes-Quezada, C., Molto, E., Matesanz, F., Bogdanovic, O., de la Calle-Mustienes, E., Dominguez, O., Taher, L., Furlan-Magaril, M., Alcina, A., Canon, S., Fedetz, M., Blasco, M.A., Pereira, P.S., Ovcharenko, I., Recillas-Targa, F., Montoliu, L., Manzanares, M., Guigo, R., Serrano, M., Casares, F., Gomez-Skarmeta, J.L., 2011. Genome-wide CTCF distribution in vertebrates defines equivalent sites that aid the identification of disease-associated genes. Nat. Struct. Mol. Biol. 18, 708-714.
    [130]
    Martin, K., Huo, L., Schleif, R.F., 1986. The DNA loop model for ara repression: AraC protein occupies the proposed loop sites in vivo and repression-negative mutations lie in these same sites. Proc. Natl. Acad. Sci. U. S. A. 83, 3654-3658.
    [131]
    Martinez, S.R., Miranda, J.L., 2010. CTCF terminal segments are unstructured. Protein Sci. 19, 1110-1116.
    [132]
    Merkenschlager, M., Nora, E.P., 2016. CTCF and Cohesin in genome folding and transcriptional gene regulation. Annu. Rev. Genomics Hum. Genet. 17, 17-43.
    [133]
    Michaelis, C., Ciosk, R., Nasmyth, K., 1997. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35-45.
    [134]
    Miguel-Escalada, I., Bonas-Guarch, S., Cebola, I., Ponsa-Cobas, J., Mendieta-Esteban, J., Atla, G., Javierre, B.M., Rolando, D.M.Y., Farabella, I., Morgan, C.C., Garcia-Hurtado, J., Beucher, A., Moran, I., Pasquali, L., Ramos-Rodriguez, M., Appel, E.V.R., Linneberg, A., Gjesing, A.P., Witte, D.R., Pedersen, O., Grarup, N., Ravassard, P., Torrents, D., Mercader, J.M., Piemonti, L., Berney, T., de Koning, E.J.P., Kerr-Conte, J., Pattou, F., Fedko, I.O., Groop, L., Prokopenko, I., Hansen, T., Marti-Renom, M.A., Fraser, P., Ferrer, J., 2019. Human pancreatic islet three-dimensional chromatin architecture provides insights into the genetics of type 2 diabetes. Nat. Genet. 51, 1137-1148.
    [135]
    Misteli, T., 2007. Beyond the sequence: cellular organization of genome function. Cell 128, 787-800.
    [136]
    Monahan, K., Rudnick, N.D., Kehayova, P.D., Pauli, F., Newberry, K.M., Myers, R.M., Maniatis, T., 2012. Role of CCCTC binding factor (CTCF) and cohesin in the generation of single-cell diversity of protocadherin-alpha gene expression. Proc. Natl. Acad. Sci. U. S. A. 109, 9125-9130.
    [137]
    Montavon, T., Le Garrec, J.F., Kerszberg, M., Duboule, D., 2008. Modeling Hox gene regulation in digits: reverse collinearity and the molecular origin of thumbness. Genes & development 22, 346-359.
    [138]
    Moon, H., Filippova, G., Loukinov, D., Pugacheva, E., Chen, Q., Smith, S.T., Munhall, A., Grewe, B., Bartkuhn, M., Arnold, R., Burke, L.J., Renkawitz-Pohl, R., Ohlsson, R., Zhou, J., Renkawitz, R., Lobanenkov, V., 2005. CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator. EMBO Rep. 6, 165-170.
    [139]
    Mountoufaris, G., Canzio, D., Nwakeze, C.L., Chen, W.V., Maniatis, T., 2018. Writing, reading, and translating the clustered protocadherin cell surface recognition code for neural circuit assembly. Annu. Rev. Cell Dev. Biol. 34, 471-493.
    [140]
    Mueller-Storm, H.P., Sogo, J.M., Schaffner, W., 1989. An enhancer stimulates transcription in trans when attached to the promoter via a protein bridge. Cell 58, 767-777.
    [141]
    Muller, H.P., Matthias, P., Schaffner, W., 1990. A transcriptional terminator between enhancer and promoter does not affect remote transcriptional control. Somatic cell and molecular genetics 16, 351-360.
    [142]
    Nagy, G., Czipa, E., Steiner, L., Nagy, T., Pongor, S., Nagy, L., Barta, E., 2016. Motif oriented high-resolution analysis of ChIP-seq data reveals the topological order of CTCF and cohesin proteins on DNA. BMC Genomics 17, 637.
    [143]
    Nakahashi, H., Kieffer Kwon, K.R., Resch, W., Vian, L., Dose, M., Stavreva, D., Hakim, O., Pruett, N., Nelson, S., Yamane, A., Qian, J., Dubois, W., Welsh, S., Phair, R.D., Pugh, B.F., Lobanenkov, V., Hager, G.L., Casellas, R., 2013. A genome-wide map of CTCF multivalency redefines the CTCF code. Cell Rep. 3, 1678-1689.
    [144]
    Narendra, V., Rocha, P.P., An, D., Raviram, R., Skok, J.A., Mazzoni, E.O., Reinberg, D., 2015. CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science 347, 1017-1021.
    [145]
    Nasmyth, K., 2001. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 35, 673-745.
    [146]
    Nativio, R., Wendt, K.S., Ito, Y., Huddleston, J.E., Uribe-Lewis, S., Woodfine, K., Krueger, C., Reik, W., Peters, J.M., Murrell, A., 2009. Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. PLoS Genet. 5, e1000739.
    [147]
    Naumova, N., Imakaev, M., Fudenberg, G., Zhan, Y., Lajoie, B.R., Mirny, L.A., Dekker, J., 2013. Organization of the mitotic chromosome. Science 342, 948-953.
    [148]
    Ni, X., Zhang, Y.E., Negre, N., Chen, S., Long, M., White, K.P., 2012. Adaptive evolution and the birth of CTCF binding sites in the Drosophila genome. PLoS Biol. 10, e1001420.
    [149]
    Nichols, M.H., Corces, V.G., 2015. A CTCF code for 3D genome architecture. Cell 162, 703-705.
    [150]
    Nicoludis, J.M., Green, A.G., Walujkar, S., May, E.J., Sotomayor, M., Marks, D.S., Gaudet, R., 2019. Interaction specificity of clustered protocadherins inferred from sequence covariation and structural analysis. Proc. Natl. Acad. Sci. U. S. A. 116, 17825-17830.
    [151]
    Nora, E.P., Goloborodko, A., Valton, A.L., Gibcus, J.H., Uebersohn, A., Abdennur, N., Dekker, J., Mirny, L.A., Bruneau, B.G., 2017. Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. Cell 169, 930-944 e922.
    [152]
    Nora, E.P., Lajoie, B.R., Schulz, E.G., Giorgetti, L., Okamoto, I., Servant, N., Piolot, T., van Berkum, N.L., Meisig, J., Sedat, J., Gribnau, J., Barillot, E., Bluthgen, N., Dekker, J., Heard, E., 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381-385.
    [153]
    Nuebler, J., Fudenberg, G., Imakaev, M., Abdennur, N., Mirny, L.A., 2018. Chromatin organization by an interplay of loop extrusion and compartmental segregation. Proc. Natl. Acad. Sci. U. S. A. 115, E6697-E6706.
    [154]
    Ong, C.T., Corces, V.G., 2014. CTCF: an architectural protein bridging genome topology and function. Nat. Rev. Genet. 15, 234-246.
    [155]
    Ong, C.T., Van Bortle, K., Ramos, E., Corces, V.G., 2013. Poly(ADP-ribosyl)ation regulates insulator function and intrachromosomal interactions in Drosophila. Cell 155, 148-159.
    [156]
    Oomen, M.E., Hansen, A.S., Liu, Y., Darzacq, X., Dekker, J., 2019. CTCF sites display cell cycle-dependent dynamics in factor binding and nucleosome positioning. Genome Res. 29, 236-249.
    [157]
    Parelho, V., Hadjur, S., Spivakov, M., Leleu, M., Sauer, S., Gregson, H.C., Jarmuz, A., Canzonetta, C., Webster, Z., Nesterova, T., Cobb, B.S., Yokomori, K., Dillon, N., Aragon, L., Fisher, A.G., Merkenschlager, M., 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132, 422-433.
    [158]
    Pauli, A., Althoff, F., Oliveira, R.A., Heidmann, S., Schuldiner, O., Lehner, C.F., Dickson, B.J., Nasmyth, K., 2008. Cell-type-specific TEV protease cleavage reveals cohesin functions in Drosophila neurons. Developmental cell 14, 239-251.
    [159]
    Phillips-Cremins, J.E., Corces, V.G., 2013. Chromatin insulators: linking genome organization to cellular function. Mol. Cell 50, 461-474.
    [160]
    Proudhon, C., Hao, B., Raviram, R., Chaumeil, J., Skok, J.A., 2015. Long-range regulation of V(D)J recombination. Adv. Immunol. 128, 123-182.
    [161]
    Pugacheva, E.M., Kubo, N., Loukinov, D., Tajmul, M., Kang, S., Kovalchuk, A.L., Strunnikov, A.V., Zentner, G.E., Ren, B., Lobanenkov, V.V., 2020. CTCF mediates chromatin looping via N-terminal domain-dependent cohesin retention. Proc. Natl. Acad. Sci. U. S. A. 117, 2020-2031.
    [162]
    Pugacheva, E.M., Kwon, Y.W., Hukriede, N.A., Pack, S., Flanagan, P.T., Ahn, J.C., Park, J.A., Choi, K.S., Kim, K.W., Loukinov, D., Dawid, I.B., Lobanenkov, V.V., 2006. Cloning and characterization of zebrafish CTCF: Developmental expression patterns, regulation of the promoter region, and evolutionary aspects of gene organization. Gene 375, 26-36.
    [163]
    Qiu, X., Kumari, G., Gerasimova, T., Du, H., Labaran, L., Singh, A., De, S., Wood, W.H., 3rd, Becker, K.G., Zhou, W., Ji, H., Sen, R., 2018. Sequential enhancer sequestration dysregulates recombination center formation at the IgH locus. Mol. Cell 70, 21-33 e26.
    [164]
    Rao, S.S., Huntley, M.H., Durand, N.C., Stamenova, E.K., Bochkov, I.D., Robinson, J.T., Sanborn, A.L., Machol, I., Omer, A.D., Lander, E.S., Aiden, E.L., 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665-1680.
    [165]
    Rao, S.S.P., Huang, S.C., Glenn St Hilaire, B., Engreitz, J.M., Perez, E.M., Kieffer-Kwon, K.R., Sanborn, A.L., Johnstone, S.E., Bascom, G.D., Bochkov, I.D., Huang, X., Shamim, M.S., Shin, J., Turner, D., Ye, Z., Omer, A.D., Robinson, J.T., Schlick, T., Bernstein, B.E., Casellas, R., Lander, E.S., Aiden, E.L., 2017. Cohesin loss eliminates all loop domains. Cell 171, 305-320 e324.
    [166]
    Rasko, J.E., Klenova, E.M., Leon, J., Filippova, G.N., Loukinov, D.I., Vatolin, S., Robinson, A.F., Hu, Y.J., Ulmer, J., Ward, M.D., Pugacheva, E.M., Neiman, P.E., Morse, H.C., 3rd, Collins, S.J., Lobanenkov, V.V., 2001. Cell growth inhibition by the multifunctional multivalent zinc-finger factor CTCF. Cancer Res. 61, 6002-6007.
    [167]
    Remeseiro, S., Cuadrado, A., Gomez-Lopez, G., Pisano, D.G., Losada, A., 2012. A unique role of cohesin-SA1 in gene regulation and development. The EMBO journal 31, 2090-2102.
    [168]
    Ren, G., Jin, W., Cui, K., Rodrigez, J., Hu, G., Zhang, Z., Larson, D.R., Zhao, K., 2017. CTCF-mediated enhancer-promoter interaction is a critical regulator of cell-to-cell variation of gene expression. Mol. Cell 67, 1049-1058 e1046.
    [169]
    Rhee, H.S., Pugh, B.F., 2011. Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution. Cell 147, 1408-1419.
    [170]
    Rodriguez-Carballo, E., Lopez-Delisle, L., Zhan, Y., Fabre, P.J., Beccari, L., El-Idrissi, I., Huynh, T.H.N., Ozadam, H., Dekker, J., Duboule, D., 2017. The HoxD cluster is a dynamic and resilient TAD boundary controlling the segregation of antagonistic regulatory landscapes. Genes & development 31, 2264-2281.
    [171]
    Rowley, M.J., Corces, V.G., 2018. Organizational principles of 3D genome architecture. Nat. Rev. Genet. 19, 789-800.
    [172]
    Rowley, M.J., Nichols, M.H., Lyu, X., Ando-Kuri, M., Rivera, I.S.M., Hermetz, K., Wang, P., Ruan, Y., Corces, V.G., 2017. Evolutionarily conserved principles predict 3D chromatin organization. Mol. Cell 67, 837-852 e837.
    [173]
    Saitoh, N., Bell, A.C., Recillas-Targa, F., West, A.G., Simpson, M., Pikaart, M., Felsenfeld, G., 2000. Structural and functional conservation at the boundaries of the chicken beta-globin domain. The EMBO journal 19, 2315-2322.
    [174]
    Saldana-Meyer, R., Gonzalez-Buendia, E., Guerrero, G., Narendra, V., Bonasio, R., Recillas-Targa, F., Reinberg, D., 2014. CTCF regulates the human p53 gene through direct interaction with its natural antisense transcript, Wrap53. Genes & development 28, 723-734.
    [175]
    Saldana-Meyer, R., Rodriguez-Hernaez, J., Escobar, T., Nishana, M., Jacome-Lopez, K., Nora, E.P., Bruneau, B.G., Tsirigos, A., Furlan-Magaril, M., Skok, J., Reinberg, D., 2019. RNA interactions are essential for CTCF-mediated genome organization. Mol. Cell 76, 412-422 e415.
    [176]
    Sanborn, A.L., Rao, S.S., Huang, S.C., Durand, N.C., Huntley, M.H., Jewett, A.I., Bochkov, I.D., Chinnappan, D., Cutkosky, A., Li, J., Geeting, K.P., Gnirke, A., Melnikov, A., McKenna, D., Stamenova, E.K., Lander, E.S., Aiden, E.L., 2015. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proc. Natl. Acad. Sci. U. S. A. 112, E6456-6465.
    [177]
    Satou, Y., Miyazato, P., Ishihara, K., Yaguchi, H., Melamed, A., Miura, M., Fukuda, A., Nosaka, K., Watanabe, T., Rowan, A.G., Nakao, M., Bangham, C.R., 2016. The retrovirus HTLV-1 inserts an ectopic CTCF-binding site into the human genome. Proc. Natl. Acad. Sci. U. S. A. 113, 3054-3059.
    [178]
    Schmidt, D., Schwalie, P.C., Wilson, M.D., Ballester, B., Goncalves, A., Kutter, C., Brown, G.D., Marshall, A., Flicek, P., Odom, D.T., 2012. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148, 335-348.
    [179]
    Schuldiner, O., Berdnik, D., Levy, J.M., Wu, J.S., Luginbuhl, D., Gontang, A.C., Luo, L., 2008. piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. Developmental cell 14, 227-238.
    [180]
    Schwarzer, W., Abdennur, N., Goloborodko, A., Pekowska, A., Fudenberg, G., Loe-Mie, Y., Fonseca, N.A., Huber, W., Haering, C.H., Mirny, L., Spitz, F., 2017. Two independent modes of chromatin organization revealed by cohesin removal. Nature 551, 51-56.
    [181]
    Shen, Y., Yue, F., McCleary, D.F., Ye, Z., Edsall, L., Kuan, S., Wagner, U., Dixon, J., Lee, L., Lobanenkov, V.V., Ren, B., 2012. A map of the cis-regulatory sequences in the mouse genome. Nature 488, 116-120.
    [182]
    Simonis, M., Klous, P., Splinter, E., Moshkin, Y., Willemsen, R., de Wit, E., van Steensel, B., de Laat, W., 2006. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat. Genet. 38, 1348-1354.
    [183]
    Sofueva, S., Yaffe, E., Chan, W.C., Georgopoulou, D., Vietri Rudan, M., Mira-Bontenbal, H., Pollard, S.M., Schroth, G.P., Tanay, A., Hadjur, S., 2013. Cohesin-mediated interactions organize chromosomal domain architecture. The EMBO journal 32, 3119-3129.
    [184]
    Strunnikov, A.V., Larionov, V.L., Koshland, D., 1993. SMC1: an essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous protein family. The Journal of cell biology 123, 1635-1648.
    [185]
    Sun, S., Del Rosario, B.C., Szanto, A., Ogawa, Y., Jeon, Y., Lee, J.T., 2013. Jpx RNA activates Xist by evicting CTCF. Cell 153, 1537-1551.
    [186]
    Suo, L., Lu, H., Ying, G., Capecchi, M.R., Wu, Q., 2012. Protocadherin clusters and cell adhesion kinase regulate dendrite complexity through Rho GTPase. J. Mol. Cell Biol. 4, 362-376.
    [187]
    Szabo, Q., Bantignies, F., Cavalli, G., 2019. Principles of genome folding into topologically associating domains. Sci. Adv. 5, eaaw1668.
    [188]
    Tang, Z., Luo, O.J., Li, X., Zheng, M., Zhu, J.J., Szalaj, P., Trzaskoma, P., Magalska, A., Wlodarczyk, J., Ruszczycki, B., Michalski, P., Piecuch, E., Wang, P., Wang, D., Tian, S.Z., Penrad-Mobayed, M., Sachs, L.M., Ruan, X., Wei, C.L., Liu, E.T., Wilczynski, G.M., Plewczynski, D., Li, G., Ruan, Y., 2015. CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell 163, 1611-1627.
    [189]
    Tanwar, V.S., Jose, C.C., Cuddapah, S., 2019. Role of CTCF in DNA damage response. Mutat. Res. 780, 61-68.
    [190]
    Torrano, V., Navascues, J., Docquier, F., Zhang, R., Burke, L.J., Chernukhin, I., Farrar, D., Leon, J., Berciano, M.T., Renkawitz, R., Klenova, E., Lafarga, M., Delgado, M.D., 2006. Targeting of CTCF to the nucleolus inhibits nucleolar transcription through a poly(ADP-ribosyl)ation-dependent mechanism. J. Cell Sci. 119, 1746-1759.
    [191]
    Toyoda, S., Kawaguchi, M., Kobayashi, T., Tarusawa, E., Toyama, T., Okano, M., Oda, M., Nakauchi, H., Yoshimura, Y., Sanbo, M., Hirabayashi, M., Hirayama, T., Hirabayashi, T., Yagi, T., 2014. Developmental epigenetic modification regulates stochastic expression of clustered protocadherin genes, generating single neuron diversity. Neuron 82, 94-108.
    [192]
    Umer, H.M., Cavalli, M., Dabrowski, M.J., Diamanti, K., Kruczyk, M., Pan, G., Komorowski, J., Wadelius, C., 2016. A significant regulatory mutation burden at a high-affinity position of the CTCF motif in gastrointestinal cancers. Hum. Mutat. 37, 904-913.
    [193]
    Vian, L., Pekowska, A., Rao, S.S.P., Kieffer-Kwon, K.R., Jung, S., Baranello, L., Huang, S.C., El Khattabi, L., Dose, M., Pruett, N., Sanborn, A.L., Canela, A., Maman, Y., Oksanen, A., Resch, W., Li, X., Lee, B., Kovalchuk, A.L., Tang, Z., Nelson, S., Di Pierro, M., Cheng, R.R., Machol, I., St Hilaire, B.G., Durand, N.C., Shamim, M.S., Stamenova, E.K., Onuchic, J.N., Ruan, Y., Nussenzweig, A., Levens, D., Aiden, E.L., Casellas, R., 2018. The energetics and physiological impact of cohesin extrusion. Cell 173, 1165-1178 e1120.
    [194]
    Volpi, E.V., Chevret, E., Jones, T., Vatcheva, R., Williamson, J., Beck, S., Campbell, R.D., Goldsworthy, M., Powis, S.H., Ragoussis, J., Trowsdale, J., Sheer, D., 2000. Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J. Cell Sci. 113 ( Pt 9), 1565-1576.
    [195]
    Vostrov, A.A., Taheny, M.J., Quitschke, W.W., 2002. A region to the N-terminal side of the CTCF zinc finger domain is essential for activating transcription from the amyloid precursor protein promoter. J. Biol. Chem. 277, 1619-1627.
    [196]
    Wada, T., Wallerich, S., Becskei, A., 2018. Stochastic gene choice during cellular differentiation. Cell Rep. 24, 3503-3512.
    [197]
    Wallace, J.A., Felsenfeld, G., 2007. We gather together: insulators and genome organization. Curr. Opin. Genet. Dev. 17, 400-407.
    [198]
    Wang, H., Maurano, M.T., Qu, H., Varley, K.E., Gertz, J., Pauli, F., Lee, K., Canfield, T., Weaver, M., Sandstrom, R., Thurman, R.E., Kaul, R., Myers, R.M., Stamatoyannopoulos, J.A., 2012. Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res. 22, 1680-1688.
    [199]
    Wang, Y., Fan, C., Zheng, Y., Li, C., 2017. Dynamic chromatin accessibility modeled by Markov process of randomly-moving molecules in the 3D genome. Nucleic Acids Res. 45, e85.
    [200]
    Wang, W., Ren, G., Hong, N., Jin, W., 2019a. Exploring the changing landscape of cell-to-cell variation after CTCF knockdown via single cell RNA-seq. BMC Genomics 20, 1015.
    [201]
    Wang, W., Zhang, L., Wang, X., Zeng, Y., 2019b. The advances in CRISPR technology and 3D genome. Semin. Cell Dev. Biol. 90, 54-61.
    [202]
    Wendt, K.S., Yoshida, K., Itoh, T., Bando, M., Koch, B., Schirghuber, E., Tsutsumi, S., Nagae, G., Ishihara, K., Mishiro, T., Yahata, K., Imamoto, F., Aburatani, H., Nakao, M., Imamoto, N., Maeshima, K., Shirahige, K., Peters, J.M., 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451, 796-801.
    [203]
    Wu, Q., 2005. Comparative genomics and diversifying selection of the clustered vertebrate protocadherin genes. Genetics 169, 2179-2188.
    [204]
    Wu, Q., Guo, Y., Lu, Y., Li, J., Wu, Y., Jia, Z., 2019. Tandem directional CTCF sites balance protocadherin promoter usage. BioRxiv. DOI: 10.1101/525543.
    [205]
    Wu, Q., Jia, Z., 2020. Wiring the brain by clustered protocadherin neural codes. Neuroscience Bull. DOI: 10.1007/s12264-020-00578-4.
    [206]
    Wu, Q., Maniatis, T., 1999. A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97, 779-790.
    [207]
    Wu, Q., Zhang, T., Cheng, J.F., Kim, Y., Grimwood, J., Schmutz, J., Dickson, M., Noonan, J.P., Zhang, M.Q., Myers, R.M., Maniatis, T., 2001. Comparative DNA sequence analysis of mouse and human protocadherin gene clusters. Genome Res. 11, 389-404.
    [208]
    Wu, Y., Jia, Z., Ge, X., Wu, Q., 2020. Three-dimensional genome architectural CCCTC-binding factor makes choice in duplicated enhancers at Pcdhα locus. Science China Life Sciences. 10.1007/s11427-019-1598-4.
    [209]
    Xiang, Y., Zhou, X., Hewitt, S.L., Skok, J.A., Garrard, W.T., 2011. A multifunctional element in the mouse Igkappa locus that specifies repertoire and Ig loci subnuclear location. J. Immunol. 186, 5356-5366.
    [210]
    Xiao, T., Wallace, J., Felsenfeld, G., 2011. Specific sites in the C terminus of CTCF interact with the SA2 subunit of the cohesin complex and are required for cohesin-dependent insulation activity. Mol. Cell. Biol. 31, 2174-2183.
    [211]
    Xie, X., Mikkelsen, T.S., Gnirke, A., Lindblad-Toh, K., Kellis, M., Lander, E.S., 2007. Systematic discovery of regulatory motifs in conserved regions of the human genome, including thousands of CTCF insulator sites. Proc. Natl. Acad. Sci. U. S. A. 104, 7145-7150.
    [212]
    Xu, D., Ma, R., Zhang, J., Liu, Z., Wu, B., Peng, J., Zhai, Y., Gong, Q., Shi, Y., Wu, J., Wu, Q., Zhang, Z., Ruan, K., 2018. Dynamic nature of CTCF tandem 11 zinc fingers in multivalent recognition of DNA as revealed by NMR spectroscopy. J. Phys. Chem. Lett. 9, 4020-4028.
    [213]
    Xu, W., Yang, H., Liu, Y., Yang, Y., Wang, P., Kim, S.H., Ito, S., Yang, C., Wang, P., Xiao, M.T., Liu, L.X., Jiang, W.Q., Liu, J., Zhang, J.Y., Wang, B., Frye, S., Zhang, Y., Xu, Y.H., Lei, Q.Y., Guan, K.L., Zhao, S.M., Xiong, Y., 2011. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 19, 17-30.
    [214]
    Yatskevich, S., Rhodes, J., Nasmyth, K., 2019. Organization of chromosomal DNA by SMC complexes. Annu. Rev. Genet. 53, 445-482.
    [215]
    Yin, M., Wang, J., Wang, M., Li, X., Zhang, M., Wu, Q., Wang, Y., 2017. Molecular mechanism of directional CTCF recognition of a diverse range of genomic sites. Cell Res. 27, 1365-1377.
    [216]
    Yokota, S., Hirayama, T., Hirano, K., Kaneko, R., Toyoda, S., Kawamura, Y., Hirabayashi, M., Hirabayashi, T., Yagi, T., 2011. Identification of the cluster control region for the protocadherin-beta genes located beyond the protocadherin-gamma cluster. J. Biol. Chem. 286, 31885-31895.
    [217]
    Yu, W., Ginjala, V., Pant, V., Chernukhin, I., Whitehead, J., Docquier, F., Farrar, D., Tavoosidana, G., Mukhopadhyay, R., Kanduri, C., Oshimura, M., Feinberg, A.P., Lobanenkov, V., Klenova, E., Ohlsson, R., 2004. Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation. Nat. Genet. 36, 1105-1110.
    [218]
    Yusufzai, T.M., Tagami, H., Nakatani, Y., Felsenfeld, G., 2004. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol. Cell 13, 291-298.
    [219]
    Zakany, J., Duboule, D., 2007. The role of Hox genes during vertebrate limb development. Curr. Opin. Genet. Dev. 17, 359-366.
    [220]
    Zakany, J., Kmita, M., Duboule, D., 2004. A dual role for Hox genes in limb anterior-posterior asymmetry. Science 304, 1669-1672.
    [221]
    Zhai, Y., Xu, Q., Guo, Y., Wu, Q., 2016. Characterization of a cluster of CTCF-binding sites in a protocadherin regulatory region. Yi chuan = Hereditas 38, 323-336 (in Chinese).
    [222]
    Zhang, R., Burke, L.J., Rasko, J.E., Lobanenkov, V., Renkawitz, R., 2004. Dynamic association of the mammalian insulator protein CTCF with centrosomes and the midbody. Exp. Cell Res. 294, 86-93.
    [223]
    Zhang, Y., Heermann, D.W., 2011. Loops determine the mechanical properties of mitotic chromosomes. PLoS One 6, e29225.
    [224]
    Zhang, X., Zhang, Y., Ba, Z., Kyritsis, N., Casellas, R., Alt, F.W., 2019a. Fundamental roles of chromatin loop extrusion in antibody class switching. Nature 575, 385-389.
    [225]
    Zhang, Y., Zhang, X., Ba, Z., Liang, Z., Dring, E.W., Hu, H., Lou, J., Kyritsis, N., Zurita, J., Shamim, M.S., Presser Aiden, A., Lieberman Aiden, E., Alt, F.W., 2019b. The fundamental role of chromatin loop extrusion in physiological V(D)J recombination. Nature 573, 600-604.
    [226]
    Zhao, Z., Tavoosidana, G., Sjolinder, M., Gondor, A., Mariano, P., Wang, S., Kanduri, C., Lezcano, M., Sandhu, K.S., Singh, U., Pant, V., Tiwari, V., Kurukuti, S., Ohlsson, R., 2006. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat. Genet. 38, 1341-1347.
    [227]
    Zheng, X.F., Huang, H.Y., Wu, Q., 2019. Chromatin architectural protein CTCF regulates gene expression of the UGT1 cluster. Yi chuan = Hereditas 41, 509-523 (in Chinese).
    [228]
    Zheng, H., Xie, W., 2019. The role of 3D genome organization in development and cell differentiation. Nat. Rev. Mol. Cell Biol. 9,535-550.
    [229]
    Zirkel, A., Nikolic, M., Sofiadis, K., Mallm, J.P., Brackley, C.A., Gothe, H., Drechsel, O., Becker, C., Altmuller, J., Josipovic, N., Georgomanolis, T., Brant, L., Franzen, J., Koker, M., Gusmao, E.G., Costa, I.G., Ullrich, R.T., Wagner, W., Roukos, V., Nurnberg, P., Marenduzzo, D., Rippe, K., Papantonis, A., 2018. HMGB2 loss upon senescence entry disrupts genomic organization and induces CTCF clustering across cell types. Mol. Cell 70, 730-744.
    [230]
    Zlatanova, J., Caiafa, P., 2009. CTCF and its protein partners: divide and rule? J. Cell Sci. 122, 1275-1284.
    [231]
    Zuin, J., Dixon, J.R., van der Reijden, M.I., Ye, Z., Kolovos, P., Brouwer, R.W., van de Corput, M.P., van de Werken, H.J., Knoch, T.A., van, I.W.F., Grosveld, F.G., Ren, B., Wendt, K.S., 2014. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. Proc. Natl. Acad. Sci. U. S. A. 111, 996-1001.
    [232]
    Zylicz, J.J., Bousard, A., Zumer, K., Dossin, F., Mohammad, E., da Rocha, S.T., Schwalb, B., Syx, L., Dingli, F., Loew, D., Cramer, P., Heard, E., 2019. The implication of early chromatin changes in X chromosome inactivation. Cell 176, 182-197 e123.
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