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Volume 48 Issue 12
Dec.  2021
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Article Navigation >  Journal of Genetics and Genomics  > 2021  >  48(12): 1045-1056

3D genome organization in the central nervous system, implications for neuropsychological disorders

doi: 10.1016/j.jgg.2021.06.017
  •  

    Institutes of Brain Science, State Key Laboratory of Medical Neurobiology, MOE Frontier Center for Brain Science, Fudan University, Shanghai 200032, China

Funds:

This work was supported by Science and Technology Commission of Shanghai Municipality (19ZR1405400).

  • Received Date: 2021-05-17
  • Accepted Date: 2021-06-17
  • Rev Recd Date: 2021-06-11
  • Publish Date: 2021-12-20
    Abstract
  • Chromosomes in eukaryotic cell nuclei are highly compacted and finely organized into hierarchical three-dimensional (3D) configuration. In recent years, scientists have gained deeper understandings of 3D genome structures and revealed novel evidence linking 3D genome organization to various important cell events on the molecular level. Most importantly, alteration of 3D genome architecture has emerged as an intriguing higher order mechanism that connects disease-related genetic variants in multiple heterogenous and polygenic neuropsychological disorders, delivering novel insights into the etiology. In this review, we provide a brief overview of the hierarchical structures of 3D genome and two proposed regulatory models, loop extrusion and phase separation. We then focus on recent Hi-C data in the central nervous system and discuss 3D genome alterations during normal brain development and in mature neurons. Most importantly, we make a comprehensive review on current knowledge and discuss the role of 3D genome in multiple neuropsychological disorders, including schizophrenia, repeat expansion disorders, 22q11 deletion syndrome, and others.
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  • Alberti, S., Gladfelter, A., Mittag, T., 2019. Considerations and challenges in studying liquid-liquid phase separation and biomolecular condensates. Cell 176, 419-434.
    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., et al., 2018. Enhancer hubs and loop collisions identified from single-allele topologies. Nat. Genet. 50, 1151-1160.
    Andrews, S.J., Fulton-Howard, B., Goate, A., 2020. Interpretation of risk loci from genome-wide association studies of alzheimer's disease. Lancet Neurol. 19, 326-335.
    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., et al., 2017. Complex multienhan cercontacts captured by genome architecture mapping. Nature 543, 519-524.
    Bintu, B., Mateo, L.J., Su, J.H., Sinnott-Armstrong, N.A., Parker, M., Kinrot, S., Yamaya, K., Boettiger, A.N., Zhuang, X., 2018. Super-resolution chromatin tracing reveals domains and cooperative interactions in single cells. Science 362 eaau1783.
    Boehning, M., Dugast-Darzacq, C., Rankovic, M., Hansen, A.S., Yu, T., Marie-Nelly, H., McSwiggen, D.T., Kokic, G., Dailey, G.M., Cramer, P., et al., 2018. RNA polymerase II clustering through carboxy-terminal domain phase separation. Nat. Struct. Mol. Biol. 25, 833-840.
    Bonder, M.J., Luijk, R., Zhernakova, D.V., Moed, M., Deelen, P., Vermaat, M., van Iterson, M., van Dijk, F., van Galen, M., Bot, J., et al., 2017. Disease variants alter transcription factor levels and methylation of their binding sites. Nat. Genet. 49, 131-138.
    Bonev, B., Mendelson Cohen, N., Szabo, Q., Fritsch, L., Papadopoulos, G.L., Lubling, Y., Xu, X., Lv, X., Hugnot, J.P., Tanay, A., et al., 2017. Multiscale 3D genome rewiring during mouse neural development. Cell 171, 557-572.
    Chathoth, K.T., Zabet, N.R., 2019. Chromatin architecture reorganization during neuronal cell differentiation in Drosophila genome. Genome Res. 29, 613-625.
    Consortium, S.W.G. o. t. P.G., 2014. Biological insights from 108 schizophrenia-associated genetic loci. Nature 511, 421-427.
    Davies, J.O., Telenius, J.M., McGowan, S.J., Roberts, N.A., Taylor, S., Higgs, D.R., Hughes, J.R., 2016. Multiplexed analysis of chromosome conformation at vastly improved sensitivity. Nat. Methods 13, 74-80.
    Deardorff, M.A., Kaur, M., Yaeger, D., Rampuria, A., Korolev, S., Pie, J., Gil-Rodriguez, C., Arnedo, M., Loeys, B., Kline, A.D., et al., 2007. Mutations in cohesin complex members SMC3 and SMC1A cause a mild variant of cornelia de lange syndrome with predominant mental retardation. Am. J. Hum. Genet. 80, 485-494.
    Dekker, J., Rippe, K., Dekker, M., Kleckner, N., 2002. Capturing chromosome conformation. Science 295, 1306-1311.
    Dixon, J.R., Jung, I., Selvaraj, S., Shen, Y., Antosiewicz-Bourget, J.E., Lee, A.Y., Ye, Z., Kim, A., Rajagopal, N., Xie, W., et al., 2015. Chromatin architecture reorganization during stem cell differentiation. Nature 518, 331-336.
    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.
    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., et al., 2006. Chromosome conformation capture carbon copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res. 16, 1299-1309.
    Dryden, N.H., Broome, L.R., Dudbridge, F., Johnson, N., Orr, N., Schoenfelder, S., Nagano, T., Andrews, S., Wingett, S., Kozarewa, I., et al., 2014. Unbiased analysis of potential targets of breast cancer susceptibility loci by capture Hi-C. Genome Res. 24, 1854-1868.
    Espeso-Gil, S., Halene, T., Bendl, J., Kassim, B., Ben Hutta, G., Iskhakova, M., Shokrian, N., Auluck, P., Javidfar, B., Rajarajan, P., et al., 2020. A chromosomal connectome for psychiatric and metabolic risk variants in adult dopaminergic neurons. Genome Med. 12, 19.
    Falk, M., Feodorova, Y., Naumova, N., Imakaev, M., Lajoie, B.R., Leonhardt, H., Joffe, B., Dekker, J., Fudenberg, G., Solovei, I., et al., 2019. Heterochromatin drives compartmentalization of inverted and conventional nuclei. Nature 570, 395-399.
    Fang, R., Yu, M., Li, G., Chee, S., Liu, T., Schmitt, A.D., Ren, B., 2016. Mapping of long-range chromatin interactions by proximity ligation-assisted Chip-seq. Cell Res. 26, 1345-1348.
    Fraser, J., Ferrai, C., Chiariello, A.M., Schueler, M., Rito, T., Laudanno, G., Barbieri, M., Moore, B.L., Kraemer, D.C., Aitken, S., et al., 2015. Hierarchical folding and reorganization of chromosomes are linked to transcriptional changes in cellular differentiation. Mol. Syst. Biol. 11, 852.
    Frost, B., Bardai, F.H., Feany, M.B., 2016. Lamin dysfunction mediates neurodegeneration in tauopathies. Curr. Biol. 26, 129-136.
    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.
    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., et al., 2009. An oestrogen-receptor-α-bound human chromatin interactome. Nature 462, 58-64.
    Gallegos, D.A., Chan, U., Chen, L.F., West, A.E., 2018. Chromatin regulation of neuronal maturation and plasticity. Trends Neurosci. 41, 311-324.
    Garcia, A., Huang, D., Righolt, A., Righolt, C., Kalaw, M.C., Mathur, S., McAvoy, E., Anderson, J., Luedke, A., Itorralba, J., et al., 2017. Super-resolution structure of DNA significantly differs in buccal cells of controls and Alzheimer's patients. J. Cell. Physiol. 232, 2387-2395.
    Giusti-Rodríguez, P., Lu, L., Yang, Y., Crowley, C.A., Liu, X., Juric, I., Martin, J.S., Abnousi, A., Allred, S.C., Ancalade, N., et al., 2019. Using three-dimensional regulatory chromatin interactions from adult and fetal cortex to interpret genetic results for psychiatric disorders and cognitive traits. bioRxiv. https://doi.org/10.1101/406330.
    Golov, A.K., Ulianov, S.V., Luzhin, A.V., Kalabusheva, E.P., Kantidze, O.L., Flyamer, I.M., Razin, S.V., Gavrilov, A.A., 2020. C-TALE, a new cost-effective method for targeted enrichment of Hi-C/3C-seq libraries. Methods 170, 48-60.
    Gregor, A., Oti, M., Kouwenhoven, E.N., Hoyer, J., Sticht, H., Ekici, A.B., Kjaergaard, S., Rauch, A., Stunnenberg, H.G., Uebe, S., et al., 2013. De novo mutations in the genome organizer CTCF cause intellectual disability. Am. J. Hum. Genet. 93, 124-131.
    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 α promoter choice. Proc. Natl. Acad. Sci. U. S. A. 109, 21081-21086.
    Guo, Y., Xu, Q., Canzio, D., Shou, J., Li, J., Gorkin, D.U., Jung, I., Wu, H., Zhai, Y., Tang, Y., et al., 2015. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162, 900-910.
    Hilker, R., Helenius, D., Fagerlund, B., Skytthe, A., Christensen, K., Werge, T.M., Nordentoft, M., Glenthøj, B., 2018. Heritability of schizophrenia and schizophrenia spectrum based on the nationwide Danish twin register. Biol. Psychiatr. 83, 492-498.
    Hirayama, T., Tarusawa, E., Yoshimura, Y., Galjart, N., Yagi, T., 2012. CTCF is required for neural development and stochastic expression of clustered Pcdh genes in neurons. Cell Rep. 2, 345-357.
    Hsieh, T.H., Weiner, A., Lajoie, B., Dekker, J., Friedman, N., Rando, O.J., 2015. Mapping nucleosome resolution chromosome folding in yeast by micro-C. Cell 162, 108-119.
    Hughes, J.R., Roberts, N., McGowan, S., Hay, D., Giannoulatou, E., Lynch, M., De Gobbi, M., Taylor, S., Gibbons, R., Higgs, D.R., 2014. Analysis of hundreds of cis-regulatory landscapes at high resolution in a single, high-throughput experiment. Nat. Genet. 46, 205-212.
    Jain, A., Vale, R.D., 2017. RNA phase transitions in repeat expansion disorders. Nature 546, 243-247.
    Javierre, B.M., Burren, O.S., Wilder, S.P., Kreuzhuber, R., Hill, S.M., Sewitz, S., Cairns, J., Wingett, S.W., Várnai, C., Thiecke, M.J., et al., 2016. Lineage-specific genome architecture links enhancers and non-coding disease variants to target gene promoters. Cell 167, 1369-1384.
    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.
    Jia, Z., Wu, Q., 2020. Clustered protocadherins emerge as novel susceptibility loci for mental disorders. Front. Neurosci. 14, 1191.
    Jiang, Y., Loh, Y.E., Rajarajan, P., Hirayama, T., Liao, W., Kassim, B.S., Javidfar, B., Hartley, B.J., Kleofas, L., Park, R.B., et al., 2017. The methyltransferase SETDB1 regulates a large neuron-specific topological chromatin domain. Nat. Genet. 49, 1239-1250.
    Joo, J.Y., Schaukowitch, K., Farbiak, L., Kilaru, G., Kim, T.K., 2016. Stimulus-specific combinatorial functionality of neuronal c-fos enhancers. Nat. Neurosci. 19, 75-83.
    Kim, S., Yu, N.K., Shim, K.W., Kim, J.I., Kim, H., Han, D.H., Choi, J.E., Lee, S.W., Choi, D.I., Kim, M.W., et al., 2018. Remote memory and cortical synaptic plasticity require neuronal CCCTC-binding factor (CTCF). J. Neurosci. 38, 5042-5052.
    La Spada, A.R., Taylor, J.P., 2010. Repeat expansion disease: progress and puzzles in disease pathogenesis. Nat. Rev. Genet. 11, 247-258.
    Larson, A.G., Elnatan, D., Keenen, M.M., Trnka, M.J., Johnston, J.B., Burlingame, A.L., Agard, D.A., Redding, S., Narlikar, G.J., 2017. Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin. Nature 547, 236-240.
    Lee, D.S., Luo, C., Zhou, J., Chandran, S., Rivkin, A., Bartlett, A., Nery, J.R., Fitzpatrick, C., O'Connor, C., Dixon, J.R., et al., 2019. Simultaneous profiling of 3D genome structure and DNA methylation in single human cells. Nat. Methods 16, 999-1006.
    Li, G., Liu, Y., Zhang, Y., Kubo, N., Yu, M., Fang, R., Kellis, M., Ren, B., 2019. Joint profiling of DNA methylation and chromatin architecture in single cells. Nat. Methods 16, 991-993.
    Liang, Z., Li, G., Wang, Z., Djekidel, M.N., Li, Y., Qian, M.P., Zhang, M.Q., Chen, Y., 2017. BL-Hi-C is an efficient and sensitive approach for capturing structural and regulatory chromatin interactions. Nat. Commun. 8, 1622.
    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., et al., 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293.
    Liu, J., Krantz, I.D., 2008. Cohesin and human disease. Annu. Rev. Genom. Hum. Genet. 9, 303-320.
    Lu, H., Yu, D., Hansen, A.S., Ganguly, S., Liu, R., Heckert, A., Darzacq, X., Zhou, Q., 2018. Phase-separation mechanism for C-terminal hyperphosphorylation of RNA polymerase II. Nature 558, 318-323.
    Ma, W., Ay, F., Lee, C., Gulsoy, G., Deng, X., Cook, S., Hesson, J., Cavanaugh, C., Ware, C.B., Krumm, A., et al., 2015. Fine-scale chromatin interaction maps reveal the cis-regulatory landscape of human lincrna genes. Nat. Methods 12, 71-78.
    Meguro-Horike, M., Yasui, D.H., Powell, W., Schroeder, D.I., Oshimura, M., Lasalle, J.M., Horike, S., 2011. Neuron-specific impairment of inter-chromosomal pairing and transcription in a novel model of human 15q-duplication syndrome. Hum. Mol. Genet. 20, 3798-3810.
    Monahan, K., Horta, A., Lomvardas, S., 2019. LHX2-and LDB1-mediated trans interactions regulate olfactory receptor choice. Nature 565, 448-453.
    Mumbach, M.R., Rubin, A.J., Flynn, R.A., Dai, C., Khavari, P.A., Greenleaf, W.J., Chang, H.Y., 2016. HiChIP: efficient and sensitive analysis of protein-directed genome architecture. Nat. Methods 13, 919-922.
    Nasmyth, K., 2011. Cohesin: a catenase with separate entry and exit gates? Nat. Cell Biol. 13, 1170-1177.
    Niu, L., Shen, W., Huang, Y., He, N., Zhang, Y., Sun, J., Wan, J., Jiang, D., Yang, M., Tse, Y.C., et al., 2019. Amplification-free library preparation with SAFE Hi-C uses ligation products for deep sequencing to improve traditional Hi-C analysis. Commun. Biol. 2, 267.
    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., et al., 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381-385.
    Nott, A., Holtman, I.R., Coufal, N.G., Schlachetzki, J.C.M., Yu, M., Hu, R., Han, C.Z., Pena, M., Xiao, J., Wu, Y., et al., 2019. Brain cell type-specific enhancer-promoter interactome maps and disease-risk association. Science 366, 1134-1139.
    Olivares-Chauvet, P., Mukamel, Z., Lifshitz, A., Schwartzman, O., Elkayam, N.O., Lubling, Y., Deikus, G., Sebra, R.P., Tanay, A., 2016. Capturing pairwise and multi-way chromosomal conformations using chromosomal walks. Nature 540, 296-300.
    Pardiñas, A.F., Holmans, P., Pocklington, A.J., Escott-Price, V., Ripke, S., Carrera, N., Legge, S.E., Bishop, S., Cameron, D., Hamshere, M.L., et al., 2018. Common schizophrenia alleles are enriched in mutation-intolerant genes and in regions under strong background selection. Nat. Genet. 50, 381-389.
    Paulsen, J., Liyakat Ali, T.M., Nekrasov, M., Delbarre, E., Baudement, M.O., Kurscheid, S., Tremethick, D., Collas, P., 2019. Long-range interactions between topologically associating domains shape the four-dimensional genome during differentiation. Nat. Genet. 51, 835-843.
    Pessina, F., Giavazzi, F., Yin, Y., Gioia, U., Vitelli, V., Galbiati, A., Barozzi, S., Garre, M., Oldani, A., Flaus, A., et al., 2019. Functional transcription promoters at DNA double-strand breaks mediate RNA-driven phase separation of damageresponse factors. Nat. Cell Biol. 21, 1286-1299.
    Philibert, R.A., Bohle, P., Secrest, D., Deaderick, J., Sandhu, H., Crowe, R., Black, D.W., 2007. The association of the HOPA12bppolymorphism with schizophrenia in the NIMH Genetics Initiative for Schizophrenia sample. Am. J. Med. Genet. 144b, 743-747.
    Quinodoz, S.A., Ollikainen, N., Tabak, B., Palla, A., Schmidt, J.M., Detmar, E., Lai, M.M., Shishkin, A.A., Bhat, P., Takei, Y., et al., 2018. Higher-order interchromosomal hubs shape 3D genome organization in the nucleus. Cell 174, 744-757.
    Rajarajan, P., Borrman, T., Liao, W., Schrode, N., Flaherty, E., Casiño, C., Powell, S., Yashaswini, C., LaMarca, E.A., Kassim, B., et al., 2018. Neuron-specific signatures in the chromosomal connectome associated with schizophrenia risk. Science 362, eaat4311.
    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., et al., 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665-1680.
    Ramani, V., Deng, X., Qiu, R., Gunderson, K.L., Steemers, F.J., Disteche, C.M., Noble, W.S., Duan, Z., Shendure, J., 2017. Massively multiplex single-cell Hi-C. Nat. Methods 14, 263-266.
    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., et al., 2017. Cohesin loss eliminates all loop domains. Cell 171, 305-320.
    Remeseiro, S., Cuadrado, A., Losada, A., 2013. Cohesin in development and disease. Development 140, 3715-3718.
    Risheg, H., Graham Jr., J.M., Clark, R.D., Rogers, R.C., Opitz, J.M., Moeschler, J.B., Peiffer, A.P., May, M., Joseph, S.M., Jones, J.R., et al., 2007. A recurrent mutation in MED12 leading to R961W causes Opitz-Kaveggia syndrome. Nat. Genet. 39, 451-453.
    Sams, D.S., Nardone, S., Getselter, D., Raz, D., Tal, M., Rayi, P.R., Kaphzan, H., Hakim, O., Elliott, E., 2016. Neuronal CTCF is necessary for basal and experience-dependent gene regulation, memory formation, and genomic structure of BDNF and Arc. Cell Rep. 17, 2418-2430.
    Sanulli, S., Trnka, M.J., Dharmarajan, V., Tibble, R.W., Pascal, B.D., Burlingame, A.L., Griffin, P.R., Gross, J.D., Narlikar, G.J., 2019. HP1 reshapes nucleosome core to promote heterochromatin phase separation. Nature 575, 390-394.
    Schaukowitch, K., Joo, J.Y., Liu, X., Watts, J.K., Martinez, C., Kim, T.K., 2014. Enhancer RNA facilitates NELF release from immediate early genes. Mol. Cell. 56, 29-42.
    Schuurmans, C., Guillemot, F., 2002. Molecular mechanisms underlying cell fate specification in the developing telencephalon. Curr. Opin. Neurobiol. 12, 26-34.
    Schwartz, C.E., Tarpey, P.S., Lubs, H.A., Verloes, A., May, M.M., Risheg, H., Friez, M.J., Futreal, P.A., Edkins, S., Teague, J., et al., 2007. The original Lujan syndrome family has a novel missense mutation (p. N1007s) in the MED12 gene. J. Med. Genet. 44, 472-477.
    Sexton, T., Yaffe, E., Kenigsberg, E., Bantignies, F., Leblanc, B., Hoichman, M., Parrinello, H., Tanay, A., Cavalli, G., 2012. Three-dimensional folding and functional organization principles of the drosophila genome. Cell 148, 458-472.
    Shin, Y., Chang, Y.C., Lee, D.S.W., Berry, J., Sanders, D.W., Ronceray, P., Wingreen, N.S., Haataja, M., Brangwynne, C.P., 2019. Liquid nuclear condensates mechanically sense and restructure the genome. Cell 176, 1518.
    Song, M., Pebworth, M.P., Yang, X., Abnousi, A., Fan, C., Wen, J., Rosen, J.D., Choudhary, M.N.K., Cui, X., Jones, I.R., et al., 2020. Cell-type-specific 3D epigenomes in the developing human cortex. Nature 587, 644-649.
    Song, M., Yang, X., Ren, X., Maliskova, L., Li, B., Jones, I.R., Wang, C., Jacob, F., Wu, K., Traglia, M., et al., 2019. Mapping cis-regulatory chromatin contacts in neural cells links neuropsychiatric disorder risk variants to target genes. Nat. Genet. 51, 1252-1262.
    Soutourina, J., 2018. Transcription regulation by the mediator complex. Nat. Rev. Mol. Cell Biol. 19, 262-274.
    Stevens, T.J., Lando, D., Basu, S., Atkinson, L.P., Cao, Y., Lee, S.F., Leeb, M., Wohlfahrt, K.J., Boucher, W., O'Shaughnessy-Kirwan, A., et al., 2017. 3D structures of individual mammalian genomes studied by single-cell Hi-C. Nature 544, 59-64.
    Stuhlmüller, M., Schwarz-Finsterle, J., Fey, E., Lux, J., Bach, M., Cremer, C., Hinderhofer, K., Hausmann, M., Hildenbrand, G., 2015. In situ optical sequencing and structure analysis of a trinucleotide repeat genome region by localization microscopy after specific COMBO-FISH nano-probing. Nanoscale 7, 17938-17946.
    Sun, J.H., Zhou, L., Emerson, D.J., Phyo, S.A., Titus, K.R., Gong, W., Gilgenast, T.G., Beagan, J.A., Davidson, B.L., Tassone, F., et al., 2018. Disease-associated short tandem repeats co-localize with chromatin domain boundaries. Cell 175, 224-238.
    Swinnen, B., Robberecht, W., Van Den Bosch, L., 2020. RNA toxicity in non-coding repeat expansion disorders. EMBO J. 39, e101112.
    Takeuchi, H., Sakano, H., 2014. Neural map formation in the mouse olfactory system. Cell. Mol. Life Sci. 71, 3049-3057.
    Tan, L., Ma, W., Wu, H., Zheng, Y., Xing, D., Chen, R., Li, X., Daley, N., Deisseroth, K., Xie, X.S., 2021. Changes in genome architecture and transcriptional dynamics progress independently of sensory experience during post-natal brain development. Cell 184, 741-758.
    Tan, L., Xing, D., Chang, C.H., Li, H., Xie, X.S., 2018. Three-dimensional genome structures of single diploid human cells. Science 361, 924-928.
    van de Werken, H.J., Landan, G., Holwerda, S.J., Hoichman, M., Klous, P., Chachik, R., Splinter, E., Valdes-Quezada, C., Oz, Y., Bouwman, B.A., et al., 2012. Robust 4C-seq data analysis to screen for regulatory DNA interactions. Nat. Methods 9, 969-972.
    Tatavosian, R., Kent, S., Brown, K., Yao, T., Duc, H.N., Huynh, T.N., Zhen, C.Y., Ma, B., Wang, H., Ren, X., 2019. Nuclear condensates of the polycomb protein chromobox 2 (CBX2) assemble through phase separation. J. Biol. Chem. 294, 1451-1463.
    van de Werken, H.J.G., Haan, J.C., Feodorova, Y., Bijos, D., Weuts, A., Theunis, K., Holwerda, S.J.B., Meuleman, W., Pagie, L., Thanisch, K., et al., 2017. Small chromosomal regions position themselves autonomously according to their chromatin class. Genome Res. 27, 922-933.
    Wang, L., Hu, M., Zuo, M.Q., Zhao, J., Wu, D., Huang, L., Wen, Y., Li, Y., Chen, P., Bao, X., et al., 2020. Rett syndrome-causing mutations compromise MeCP2-mediated liquid-liquid phase separation of chromatin. Cell Res. 30, 393-407.
    Wang, D., Liu, S., Warrell, J., Won, H., Shi, X., Navarro, F.C.P., Clarke, D., Gu, M., Emani, P., Yang, Y.T., et al., 2018. Comprehensive functional genomic resource and integrative model for the human brain. Science 362, eaat8464.
    Wendt, K.S., Yoshida, K., Itoh, T., Bando, M., Koch, B., Schirghuber, E., Tsutsumi, S., Nagae, G., Ishihara, K., Mishiro, T., et al., 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451, 796-801.
    Wittmann, M., Queisser, G., Eder, A., Wiegert, J.S., Bengtson, C.P., Hellwig, A., Wittum, G., Bading, H., 2009. Synaptic activity induces dramatic changes in the geometry of the cell nucleus: interplay between nuclear structure, histone H3 phosphorylation, and nuclear calcium signaling. J. Neurosci. 29, 14687-14700.
    Won, H., de la Torre-Ubieta, L., Stein, J.L., Parikshak, N.N., Huang, J., Opland, C.K., Gandal, M.J., Sutton, G.J., Hormozdiari, F., Lu, D., et al., 2016. Chromosome conformation elucidates regulatory relationships in developing human brain. Nature 538, 523-527.
    Wu, Q., Jia, Z., 2020. Wiring the brain by clustered protocadherin neural codes. Neurosci. Bull. 37, 117-131.
    Xiao, J.F., Sun, Q.Y., Ding, L.W., Chien, W., Liu, X.Y., Mayakanda, A., Jiang, Y.Y., Loh, X.Y., Ran, X.B., Doan, N.B., et al., 2018. The c-MYC/BMI1 axis is essential for SETDB1-mediated breast tumorigenesis. J. Pathol. 246, 89-102.
    Zhang, F., Gu, W., Hurles, M.E., Lupski, J.R., 2009. Copy number variation in human health, disease, and evolution. Annu. Rev. Genom. Hum. Genet. 10, 451-481.
    Zhang, X., Zhang, Y., Zhu, X., Purmann, C., Haney, M.S., Ward, T., Khechaduri, A., Yao, J., Weissman, S.M., Urban, A.E., 2018. Local and global chromatin interactions are altered by large genomic deletions associated with human brain development. Nat. Commun. 9, 5356.
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