CTCF/cohesin-mediated DNA looping is required for protocadherin α promoter choice
Open accessAbstract
The closely linked human protocadherin ( Pcdh ) α, β, and γ gene clusters encode 53 distinct protein isoforms, which are expressed in a combinatorial manner to generate enormous diversity on the surface of individual neurons. This diversity is a consequence of stochastic promoter choice and alternative pre-mRNA processing. Here, we show that Pcdhα promoter choice is achieved by DNA looping between two downstream transcriptional enhancers and individual promoters driving the expression of alternate Pcdhα isoforms. In addition, we show that this DNA looping requires specific binding of the CTCF/cohesin complex to two symmetrically aligned binding sites in both the transcriptionally active promoters and in one of the enhancers. These findings have important implications regarding enhancer/promoter interactions in the generation of complex Pcdh cell surface codes for the establishment of neuronal identity and self-avoidance in individual neurons.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the classic scenario, the boundary is presented by CTCF binding to its sequence motifs located in a divergent orientation at either end of the loop.
“In the classic scenario, this boundary is presented by CTCF binding to its sequence motifs located in a divergent orientation at either end of the loop [277, 438–440]”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [438]
In the mammalian protocadherin α (Pcdhα) gene cluster, each promoter contains a CTCF binding site capable of looping with a convergent CTCF binding site on the enhancer.
“In the mammalian protocadherin α (Pcdhα) gene cluster, each promoter contains a CTCF binding site capable of looping with a convergent CTCF binding site on the enhancer.”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [140]
Selective demethylation of the CTCF binding site on a particular Pcdhα promoter allows that promoter to establish contact with the enhancer, resulting in activation of the expression of that particular Pcdhα gene.
“Selective demethylation of the CTCF binding site on a particular promoter allows that promoter to establish contact with the enhancer, resulting in activation of the expression of that particular Pcdhα gene [140,141].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [140]
The CTCF sites on the Pcdhα promoters are methylated, preventing CTCF binding and looping.
“However, the CTCF sites on the promoters are methylated, preventing CTCF binding and looping.”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [140]
Cites
An integrated encyclopedia of DNA elements in the human genome
The ENCODE Project Consortium (2012) · Nature · doi:10.1038/nature11247 · Cited by 18,072 · see citing works
Widespread transcription at neuronal activity-regulated enhancers
Kim, T.-K., Hemberg, M., Gray, J. M., Costa, A. M., Bear, D. M., Wu, J., Harmin, D. A., Laptewicz, M., Barbara-Haley, K., Kuersten, S., et al. (2010) · Nature · doi:10.1038/nature09033 · Cited by 2,450 · see citing works
Mediator and cohesin connect gene expression and chromatin architecture
Kagey, M. H., Newman, J. J., Bilodeau, S., Zhan, Y., Orlando, D. A., van Berkum, N. L., Ebmeier, C. C., Goossens, J., Rahl, P. B., Levine, S. S., et al. (2010) · Nature · doi:10.1038/nature09380 · Cited by 1,939 · see citing works
Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene
Bell, A. C., & Felsenfeld, G. (2000) · Nature · doi:10.1038/35013100 · Cited by 1,746 · see citing works
CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus
Hark, A. T., Schoenherr, C. J., Katz, D. J., Ingram, R. S., Levorse, J. M., & Tilghman, S. M. (2000) · Nature · doi:10.1038/35013106 · Cited by 1,547 · see citing works
CTCF: Master Weaver of the Genome
Phillips‐Cremins, J. E., & Corces, V. G. (2009) · Cell · doi:10.1016/j.cell.2009.06.001 · Cited by 1,540 · see citing works
Cohesin mediates transcriptional insulation by CCCTC-binding factor
Wendt, K. S., Yoshida, K., Itoh, T., Bando, M., Koch, B., Schirghuber, E., Tsutsumi, S., Nagae, G., Ishihara, K., Mishiro, T., et al. (2008) · Nature · doi:10.1038/nature06634 · Cited by 1,193 · see citing works
Cohesin: Its Roles and Mechanisms
Nasmyth, K., & Haering, C. H. (2009) · Annual Review of Genetics · doi:10.1146/annurev-genet-102108-134233 · Cited by 967 · see citing works
Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones.
Biedler, J. L., Roffler-Tarlov, S. K., Schachner, M., & Freedman, L. S. (1978) · PubMed · Cited by 759 · see citing works
A Striking Organization of a Large Family of Human Neural Cadherin-like Cell Adhesion Genes
Wu, Q., & Maniatis, T. (1999) · Cell · doi:10.1016/s0092-8674(00)80789-8 · Cited by 714 · see citing works
Self-citationProtocadherins mediate dendritic self-avoidance in the mammalian nervous system
Lefebvre, J. L., Kostadinov, D., Chen, W. V., Maniatis, T., & Sanes, J. R. (2012) · Nature · doi:10.1038/nature11305 · Cited by 444 · see citing works
Self-citationLobanenkov, V. V., Nicolas, R. H., Adler, V., Paterson, H., Klenova, E. M., Polotskaja, A. V., & Goodwin, G. H. (1990) · PubMed · Cited by 376 · see citing works
Promoter Choice Determines Splice Site Selection in Protocadherin α and γ Pre-mRNA Splicing
Tasic, B., Nabholz, C. E., Baldwin, K. K., Kim, Y., Rueckert, E. H., Ribich, S. A., Cramer, P., Wu, Q., Axel, R., & Maniatis, T. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00578-6 · Cited by 278 · see citing works
Self-citationComparative DNA Sequence Analysis of Mouse and Human Protocadherin Gene ClustersPreprint
Wu, Q., Zhang, T., Cheng, J., Kim, Y.-W., Grimwood, J., Schmutz, J., Dickson, M. C., Noonan, J. P., Zhang, M. Q., Myers, R., et al. (2001) · Genome Research · doi:10.1101/gr.167301 · Cited by 251 · see citing works
Self-citationKawauchi, S., Calof, A. L., Santos, R., Lopez‐Burks, M. E., Young, C. M., Hoang, M. P., Chua, A., Lao, T., Lechner, M. S., Daniel, J. A., et al. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000650 · Cited by 239 · see citing works
Wang, X., Su, H., & Bradley, A. (2002) · Genes & Development · doi:10.1101/gad.1004802 · Cited by 183 · see citing works
Xiao, T., Wallace, J., & Felsenfeld, G. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05093-11 · Cited by 182 · see citing works
Kaneko, R., Kato, H., Kawamura, Y., Esumi, S., Hirayama, T., Hirabayashi, T., & Yagi, T. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m605677200 · Cited by 174 · see citing works
Chernukhin, I. V., Shamsuddin, S., Kang, S. Y., Bergström, R., Kwon, Y., Yu, W., Whitehead, J., Mukhopadhyay, R., Docquier, F., Farrar, D., et al. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01993-06 · Cited by 173 · see citing works
Control of embryonic stem cell lineage commitment by core promoter factor, TAF3
Liu, Z., Scannell, D. R., Eisen, M. B., & Tjian, R. (2011) · Cell · doi:10.1016/j.cell.2011.08.005 · Cited by 167 · see citing works
Garrett, A. M., Schreiner, D., Lobas, M. A., & Weiner, J. A. (2012) · Neuron · doi:10.1016/j.neuron.2012.01.028 · Cited by 165 · see citing works
Monahan, K. D., Rudnick, N. D., Kehayova, P. D., Pauli, F., Newberry, K. M., Myers, R., & Maniatis, T. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1205074109 · Cited by 155 · see citing works
Self-citationDallosso, A. R., Hancock, A. L., Szemes, M., Moorwood, K., Chilukamarri, L., Tsai, H.-H., Sarkar, A., Barasch, J. M., Vuononvirta, R., Jones, C., et al. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000745 · Cited by 150 · see citing works
A unique role of cohesin‐SA1 in gene regulation and development
Remeseiro, S., Cuadrado, A., Goméz-López, G., Pisano, D. G., & Losada, A. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.60 · Cited by 138 · see citing works
Protocadherin clusters and cell adhesion kinase regulate dendrite complexity through Rho GTPase
Suo, L., Lu, H., Ying, G., Capecchi, M. R., & Wu, Q. (2012) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjs034 · Cited by 113 · see citing works
Self-citationIdentification of long-range regulatory elements in the protocadherin-α gene cluster
Ribich, S. A., Tasic, B., & Maniatis, T. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609445104 · Cited by 112 · see citing works
Self-citationFunctional Significance of Isoform Diversification in the Protocadherin Gamma Gene Cluster
Chen, W. V., Álvarez, F. J., Lefebvre, J. L., Friedman, B. A., Nwakeze, C. L., Geiman, E. J., Smith, C., Thu, C. A., Tapia, J. C., Tasic, B., et al. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.039 · Cited by 108 · see citing works
Self-citationRegulatory elements required for the activation and repression of the protocadherin-α gene cluster
Kehayova, P. D., Monahan, K. D., Chen, W., & Maniatis, T. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114357108 · Cited by 102 · see citing works
Self-citationWu, Q. (2005) · Genetics · doi:10.1534/genetics.104.037606 · Cited by 98 · see citing works
Self-citationYokota, S., Hirayama, T., Hirano, K., Kaneko, R., Toyoda, S., Kawamura, Y., Hirabayashi, M., Hirabayashi, T., & Yagi, T. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.245605 · Cited by 81 · see citing works
Kawaguchi, M., Toyama, T., Kaneko, R., Hirayama, T., Kawamura, Y., & Yagi, T. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m709648200 · Cited by 63 · see citing works
Identification of CTCF as a master regulator of the clustered protocadherin genes
Golan‐Mashiach, M., Grunspan, M., Emmanuel, R., Gibbs-Bar, L., Dikstein, R., & Shapiro, E. Y. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1260 · Cited by 62 · see citing works
Sequence analysis and expression mapping of the rat clustered protocadherin gene repertoires
Zou, C., Huang, W. M., Ying, G., & Wu, Q. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.10.011 · Cited by 55 · see citing works
Self-citation
Flagged first, then by citations
2 of the 35 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
CTCF: an architectural protein bridging genome topology and function
Ong, C., & Corces, V. G. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3663 · Cited by 1,044 · see citing works
CRISPR Inversion of CTCF Sites Alters Genome Topology and Enhancer/Promoter Function
Guo, Y., Xu, Q., Canzio, D., Shou, J., Li, J., Gorkin, D. U., Jung, I., Wu, H., Zhai, Y., Tang, Y., et al. (2015) · Cell · doi:10.1016/j.cell.2015.07.038 · Cited by 958 · see citing works
Self-citationThree-dimensional genome architecture: players and mechanisms
Pombo, A., & Dillon, N. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3965 · Cited by 571 · see citing works
Genome folding through loop extrusion by SMC complexes
Davidson, I. F., & Peters, J. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00349-7 · Cited by 507 · see citing works
Looping Back to Leap Forward: Transcription Enters a New Era
Levine, M., Cattoglio, C., & Tjian, R. (2014) · Cell · doi:10.1016/j.cell.2014.02.009 · Cited by 481 · see citing works
Integrated genomics and proteomics define huntingtin CAG length-dependent networks in mice
Langfelder, P., Cantle, J. P., Chatzopoulou, D., Wang, N., Gao, F., Al-Ramahi, I., Lu, X.-H., Ramos, E. M., El-Zein, K., Zhao, Y., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4256 · Cited by 385 · see citing works
CTCF: making the right connectionsPreprint
Ghirlando, R., & Felsenfeld, G. (2016) · Genes & Development · doi:10.1101/gad.277863.116 · Cited by 292 · see citing works
YY1 and CTCF orchestrate a 3D chromatin looping switch during early neural lineage commitment
Beagan, J. A., Duong, M. T., Titus, K. R., Zhou, L., Cao, Z., Ma, J., Lachanski, C. V., Gillis, D. R., & Phillips-Cremins, J. E. (2017) · Genome Research · doi:10.1101/gr.215160.116 · Cited by 299 · see citing works
“Finally, CTCF binding is also required for the differential expression of protocadherin ( Pcdh) isoforms that enable branching neurites to self-recognize (Guo et al. 2012).”
Molecular mechanisms driving transcriptional stress responses
Vihervaara, A., Duarte, F. M., & Lis, J. T. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0001-6 · Cited by 273 · see citing works
Two major mechanisms of chromosome organization
Mirny, L. A., Imakaev, M., & Abdennur, N. A. (2019) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.05.001 · Cited by 222 · see citing works
Enhancer hubs and loop collisions identified from single-allele topologies
Allahyar, A., Vermeulen, C., Bouwman, B. A. M., Krijger, P. H. L., Verstegen, M. J. A. M., Geeven, G., van Kranenburg, M., Pieterse, M., Straver, R., Haarhuis, J. H. I., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0161-5 · Cited by 227 · see citing works
Chromatin Insulators: Linking Genome Organization to Cellular Function
Phillips‐Cremins, J. E., & Corces, V. G. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.04.018 · Cited by 213 · see citing works
Enhancer Interaction Networks as a Means for Singular Olfactory Receptor Expression
Markenscoff-Papadimitriou, E., Allen, W. E., Colquitt, B. M., Goh, T., Murphy, K. K., Monahan, K., Mosley, C. P., Ahituv, N., & Lomvardas, S. (2014) · Cell · doi:10.1016/j.cell.2014.09.033 · Cited by 214 · see citing works
Self-citationMechanisms of Interplay between Transcription Factors and the 3D Genome
Kim, S., & Shendure, J. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.08.010 · Cited by 204 · see citing works
Shou, J., Li, J., Liu, Y., & Wu, Q. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.06.021 · Cited by 187 · see citing works
Self-citationProtocadherins at the Crossroad of Signaling Pathways
Pancho, A., Aerts, T., Mitsogiannis, M. D., & Seuntjens, E. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00117 · Cited by 189 · see citing works
Huang, H., Zhu, Q., Jussila, A., Han, Y., Bintu, B., Kern, C., Conte, M., Zhang, Y., Bianco, S., Chiariello, A. M., et al. (2021) · Nature Genetics · doi:10.1038/s41588-021-00863-6 · Cited by 187 · see citing works
An atlas of gene regulatory elements in adult mouse cerebrum
Li, Y. E., Preissl, S., Hou, X., Zhang, Z., Zhang, K., Qiu, Y., Poirion, O. B., Li, B., Chiou, J., Liu, H., et al. (2021) · Nature · doi:10.1038/s41586-021-03604-1 · Cited by 185 · see citing works
CTCF-mediated topological boundaries during development foster appropriate gene regulationPreprint
Narendra, V. K., Bulajić, M., Dekker, J., Mazzoni, E. O., & Reinberg, D. (2016) · Genes & Development · doi:10.1101/gad.288324.116 · Cited by 172 · see citing works
Canzio, D., Nwakeze, C. L., Horta, A., Rajkumar, S. M., Coffey, E. L., Duffy, E. E., Duffié, R., Monahan, K., O’Keeffe, S., Simon, M. D., et al. (2019) · Cell · doi:10.1016/j.cell.2019.03.008 · Cited by 175 · see citing works
Self-citationChen, W. V., & Maniatis, T. (2013) · Development · doi:10.1242/dev.090621 · Cited by 174 · see citing works
Self-citationKmt1e regulates a large neuron-specific topological chromatin domain
Jiang, Y., Loh, Y., Rajarajan, P., Hirayama, T., Liao, W., Kassim, B. S., Javidfar, B., Hartley, B., Kleofas, L., Park, R. B., et al. (2017) · Nature Genetics · doi:10.1038/ng.3906 · Cited by 128 · see citing works
Li, J.-H., Shou, J., Guo, Y., Tang, Y.-X., Wu, Y.-H., Jia, Z.-L., Zhai, Y.-N., Chen, Z.-F., Xu, Q., & Wu, Q. (2015) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjv016 · Cited by 139 · see citing works
Self-citationDeveloping in 3D: the role of CTCF in cell differentiation
Arzate‐Mejía, R. G., Targa, F. R., & Corces, V. G. (2018) · Development · doi:10.1242/dev.137729 · Cited by 139 · see citing works
Toyoda, S., Kawaguchi, M., Kobayashi, T., Tarusawa, E., Toyama, T., Okano, M., Oda, M., Nakauchi, H., Yoshimura, Y., Sanbo, M., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.005 · Cited by 134 · see citing works
Diehl, A. G., Ouyang, N., & Boyle, A. P. (2020) · Nature Communications · doi:10.1038/s41467-020-15520-5 · Cited by 134 · see citing works
Loop stacking organizes genome folding from TADs to chromosomes
Hafner, A., Park, M., Berger, S. E., Murphy, S. E., Nora, E. P., & Boettiger, A. N. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.04.008 · Cited by 120 · see citing works
Molecular mechanism of directional CTCF recognition of a diverse range of genomic sites
Yin, M., Wang, J., Wang, M., Li, X., Zhang, M., Wu, Q., & Wang, Y. (2017) · Cell Research · doi:10.1038/cr.2017.131 · Cited by 115 · see citing works
Self-citationRegulation of neural circuit formation by protocadherins
Peek, S. L., Mah, K. M., & Weiner, J. A. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2572-3 · Cited by 119 · see citing works
Epigenetic Functions of Smchd1 Repress Gene Clusters on the Inactive X Chromosome and on Autosomes
Gendrel, A.-V., Tang, A., Suzuki, M., Godwin, J., Nesterova, T. B., Greally, J. M., Heard, É., & Brockdorff, N. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.00145-13 · Cited by 110 · see citing works
Three-dimensional genome structures of single sensory neurons in mouse visual and olfactory systems
Tan, L., Xing, D., Daley, N., & Xie, X. S. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0205-2 · Cited by 115 · see citing works
The genomic landscape of cohesin-associated chromatin interactions
DeMare, L. E., Leng, J., Cotney, J., Reilly, S. K., Yin, J., Sarro, R., & Noonan, J. P. (2013) · Genome Research · doi:10.1101/gr.156570.113 · Cited by 114 · see citing works
Carleton, J. B., Berrett, K. C., & Gertz, J. (2017) · Cell Systems · doi:10.1016/j.cels.2017.08.011 · Cited by 113 · see citing works
Self-citationMechanisms of Chromosome Folding and Nuclear Organization: Their Interplay and Open QuestionsPreprint
Mirny, L. A., & Dekker, J. (2021) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a040147 · Cited by 102 · see citing works
Genome-wide binding and mechanistic analyses of Smchd1-mediated epigenetic regulation
Chen, K.-L., Hu, J., Moore, D. L., Liu, R., Kessans, S. A., Breslin, K., Lucet, I., Keniry, A., Leong, H. S., Parish, C., et al. (2015) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1504232112 · Cited by 105 · see citing works
Cohesin subunit RAD21: From biology to disease
Cheng, H., Zhang, N., & Pati, D. (2020) · Gene · doi:10.1016/j.gene.2020.144966 · Cited by 103 · see citing works
Architectural proteins: regulators of 3D genome organization in cell fate
Gómez‐Díaz, E., & Corces, V. G. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2014.08.003 · Cited by 100 · see citing works
Smchd1 regulates long-range chromatin interactions on the inactive X chromosome and at Hox clusters
Jansz, N., Keniry, A., Trussart, M., Bildsoe, H., Beck, T. J., Tonks, I. D., Mould, A. W., Hickey, P. F., Breslin, K. A., Iminitoff, M., et al. (2018) · Nature Structural & Molecular Biology · doi:10.1038/s41594-018-0111-z · Cited by 97 · see citing works
Associative DNA Methylation Changes in Children with Prenatal Alcohol Exposure
Laufer, B. I., Kapalanga, J., Castellani, C. A., Chater‐Diehl, E., Yan, L., & Singh, S. M. (2015) · Epigenomics · doi:10.2217/epi.15.60 · Cited by 97 · see citing works
Landscape of monoallelic DNA accessibility in mouse embryonic stem cells and neural progenitor cells
Xu, J., Carter, A. C., Gendrel, A.-V., Attia, M., Loftus, J. R., Greenleaf, W. J., Tibshirani, R. J., Heard, É., & Chang, H. Y. (2017) · Nature Genetics · doi:10.1038/ng.3769 · Cited by 97 · see citing works
Mountoufaris, G., Canzio, D., Nwakeze, C. L., Chen, W. V., & Maniatis, T. (2018) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100616-060701 · Cited by 91 · see citing works
Self-citationRibosomal DNA and the Nucleolus as Keystones of Nuclear Architecture, Organization, and Function
Cerqueira, A. V., & Lemos, B. (2019) · Trends in Genetics · doi:10.1016/j.tig.2019.07.011 · Cited by 89 · see citing works
Wu, Q., Guo, Y., Lu, Y., Li, J., Guo, Y., & Jia, Z. (2020) · Genome biology · doi:10.1186/s13059-020-01984-7 · Cited by 81 · see citing works
Self-citationTranscriptional enhancers and their communication with gene promoters
Ray-Jones, H., & Spivakov, M. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03903-w · Cited by 81 · see citing works
Stochastic gene expression in mammals: lessons from olfaction
Magklara, A., & Lomvardas, S. (2013) · Trends in Cell Biology · doi:10.1016/j.tcb.2013.04.005 · Cited by 81 · see citing works
Epigenetic dysregulation of protocadherins in human disease
Hajj, N. E., Dittrich, M. T., & Haaf, T. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.07.007 · Cited by 76 · see citing works
Chatterjee, A., Stockwell, P. A., Rodger, E. J., Duncan, E. J., Parry, M. F., Weeks, R. J., & Morison, I. M. (2015) · Scientific Reports · doi:10.1038/srep17328 · Cited by 75 · see citing works
Kwon, S. Y., Grisan, V., Jang, B., Herbert, J. M. J., & Badenhorst, P. W. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1005969 · Cited by 71 · see citing works
Poly(ADP-ribosyl)ation regulates insulator function and intrachromosomal interactions in Drosophila
Ong, C.-T., Van Bortle, K., Ramos, E., & Corces, V. G. (2013) · Cell · doi:10.1016/j.cell.2013.08.052 · Cited by 70 · see citing works
“…communication and block transcription (Guo et al., 2011; Wood et al., 2011), whereas interactions between two insulator sites that bring an enhancer in close proximity to a promoter facilitate activation of transcription (Guo et al., 2012; Liu et al., 2011; Monahan et al., 2012; Xu et al., 2011).”
Mapping the zebrafish brain methylome using reduced representation bisulfite sequencing
Chatterjee, A., Ozaki, Y., Stockwell, P. A., Horsfield, J. A., Morison, I. M., & Nakagawa, S. (2013) · Epigenetics · doi:10.4161/epi.25797 · Cited by 70 · see citing works
Gene regulation and chromatin organization: relevance of cohesin mutations to human disease
Watrin, E., Kaiser, F. J., & Wendt, K. S. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2015.12.004 · Cited by 69 · see citing works
The generation of a protocadherin cell-surface recognition code for neural circuit assembly
Canzio, D., & Maniatis, T. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.10.001 · Cited by 70 · see citing works
Self-citationThe role of clustered protocadherins in neurodevelopment and neuropsychiatric diseases
Flaherty, E. K., & Maniatis, T. (2020) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.05.041 · Cited by 66 · see citing works
Self-citationProtocadherins branch out: Multiple roles in dendrite development
Keeler, A. B., Molumby, M. J., & Weiner, J. A. (2015) · Cell Adhesion & Migration · doi:10.1080/19336918.2014.1000069 · Cited by 70 · see citing works
The Epigenetic Regulator SMCHD1 in Development and Disease
Jansz, N., Chen, K., Murphy, J. M., & Blewitt, M. E. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.01.007 · Cited by 68 · see citing works
CTCF as a regulator of alternative splicing: new tricks for an old player
Alharbi, A. B., Schmitz, U., Bailey, C. G., & Rasko, J. E. J. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab520 · Cited by 66 · see citing works
Fan, L., Lu, Y., Shen, X., Shao, H., Suo, L., & Wu, Q. (2018) · eLife · doi:10.7554/elife.35242 · Cited by 67 · see citing works
Self-citationHung, T.-C., Kingsley, D. M., & Boettiger, A. N. (2024) · Nature Genetics · doi:10.1038/s41588-023-01641-2 · Cited by 61 · see citing works
Clustered protocadherins methylation alterations in cancer
Vega-Benedetti, A. F., Loi, E., Moi, L., Blois, S., Fadda, A., Antonelli, M., Arcella, A., Badiali, M., Giangaspero, F., Morra, I., et al. (2019) · Clinical Epigenetics · doi:10.1186/s13148-019-0695-0 · Cited by 64 · see citing works
Epigenetic Regulation of Alternative Splicing: How LncRNAs Tailor the Message
Pisignano, G., & Ladomery, M. (2021) · Non-Coding RNA · doi:10.3390/ncrna7010021 · Cited by 63 · see citing works
Plasschaert, R. N., Vigneau, S., Tempera, I., Gupta, R., Maksimoska, J., Everett, L. J., Davuluri, R. V., Mamorstein, R., Lieberman, P. M., Schultz, D., et al. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt910 · Cited by 60 · see citing works
Huang, W.-C., Ferris, E., Cheng, T., Hörndli, C. S., Gleason, K., Tamminga, C. A., Wagner, J. D., Boucher, K. M., Christian, J. L., & Gregg, C. J. (2017) · Neuron · doi:10.1016/j.neuron.2017.01.033 · Cited by 59 · see citing works
Molecular architecture of enhancer–promoter interaction
Hamamoto, K., & Fukaya, T. (2022) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2022.01.003 · Cited by 55 · see citing works
WAPL functions as a rheostat of Protocadherin isoform diversity that controls neural wiring
Kiefer, L., Chiosso, A., Langen, J., Buckley, A., Gaudin, S., Rajkumar, S. M., Servito, G., Cha, E. S., Vijay, A., Yeung, A. K. W., et al. (2023) · Science · doi:10.1126/science.adf8440 · Cited by 59 · see citing works
Mechanisms of cohesin-mediated gene regulation and lessons learned from cohesinopathies
Ball, A. R., Chen, Y.-Y., & Yokomori, K. (2013) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2013.11.002 · Cited by 56 · see citing works
Juraeva, D., Haenisch, B., Zapatka, M., Frank, J., GROUP Investigators, PSYCH-GEMS SCZ working group, Witt, S. H., Mühleisen, T. W., Treutlein, J., Strohmaier, J., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004345 · Cited by 57 · see citing works
CTCF-mediated chromatin loops enclose inducible gene regulatory domains
Oti, M., Falck, J., Huynen, M. A., & Zhou, H. (2016) · BMC Genomics · doi:10.1186/s12864-016-2516-6 · Cited by 57 · see citing works
Eldholm, V., Haugen, A., & Zienolddiny, S. (2013) · International Journal of Cancer · doi:10.1002/ijc.28570 · Cited by 56 · see citing works
Martinez, F. W. P., Cruz, R., Lu, F. Y., Plasschaert, R. N., Deng, Z., Rivera-Molina, Y. A., Bartolomei, M. S., Lieberman, P. M., & Tang, Q. (2014) · Journal of Virology · doi:10.1128/jvi.00845-14 · Cited by 55 · see citing works
Histone and DNA Modifications as Regulators of Neuronal Development and FunctionPreprint
Lomvardas, S., & Maniatis, T. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a024208 · Cited by 54 · see citing works
Self-citationRole of primary aging hallmarks in Alzheimer´s disease
Zhao, J., & Huai, J. (2022) · Theranostics · doi:10.7150/thno.79535 · Cited by 53 · see citing works
Wiring the Brain by Clustered Protocadherin Neural Codes
Wu, Q., & Jia, Z. (2020) · Neuroscience Bulletin · doi:10.1007/s12264-020-00578-4 · Cited by 49 · see citing works
Self-citationChovanec, P., Collier, A. J., Krueger, C., Várnai, C., Semprich, C. I., Schoenfelder, S., Corcoran, A. E., & Rugg‐Gunn, P. J. (2021) · Nature Communications · doi:10.1038/s41467-021-22201-4 · Cited by 48 · see citing works
Regulation of clustered protocadherin genes in individual neurons
Hirayama, T., & Yagi, T. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.05.026 · Cited by 50 · see citing works
Amândio, A. R., Beccari, L. L., Lopez‐Delisle, L., Mascrez, B., Zákány, J., Gitto, S., & Duboule, D. (2021) · Genes & Development · doi:10.1101/gad.348934.121 · Cited by 49 · see citing works
Laufer, B. I., Chater-Diehl, E. J., Kapalanga, J., & Singh, S. M. (2017) · Alcohol · doi:10.1016/j.alcohol.2016.11.009 · Cited by 46 · see citing works
Remote Memory and Cortical Synaptic Plasticity Require Neuronal CCCTC-Binding Factor (CTCF)
Kim, S., Yu, N., Shim, K.-W., Kim, J., Kim, H., Han, D. H., Choi, J. E., Lee, S.-W., Choi, D. I., Kim, M. W., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2738-17.2018 · Cited by 47 · see citing works
Abnormal neocortex arealization and Sotos-like syndrome–associated behavior in Setd2 mutant mice
Xu, L., Zheng, Y., Li, X., Wang, A., Huo, D., Li, Q., Wang, S., Luo, Z., Liu, Y., Xu, F., et al. (2021) · Science Advances · doi:10.1126/sciadv.aba1180 · Cited by 45 · see citing works
Surviving an identity crisis: A revised view of chromatin insulators in the genomics era
Matzat, L. H., & Lei, E. P. (2013) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2013.10.007 · Cited by 44 · see citing works
DeBoer, E., Kraushar, M. L., Hart, R. P., & Rašin, M. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.05.042 · Cited by 45 · see citing works
Iacono, G. L., Dubos, A., Méziane, H., Benevento, M., Habibi, E., Mandoli, A., Riet, F., Selloum, M., Feil, R., Zhou, H., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky196 · Cited by 45 · see citing works
SMC1B is present in mammalian somatic cells and interacts with mitotic cohesin proteins
Mannini, L., Cucco, F., Quarantotti, V., Amato, C., Tinti, M., Tana, L., Frattini, A., Delia, D., Krantz, I. D., Jessberger, R., et al. (2015) · Scientific Reports · doi:10.1038/srep18472 · Cited by 43 · see citing works
Gene Positioning Effects on Expression in Eukaryotes
Nguyen, H. Q., & Bosco, G. (2015) · Annual Review of Genetics · doi:10.1146/annurev-genet-112414-055008 · Cited by 41 · see citing works
SMCHD1 regulates a limited set of gene clusters on autosomal chromosomes
Mason, A. G., Slieker, R. C., Balog, J., Lemmers, R. J. L. F., Wong, C.-J., Yao, Z., Lim, J.-W., Filippova, G. N., Ne, E., Tawil, R., et al. (2017) · Skeletal Muscle · doi:10.1186/s13395-017-0129-7 · Cited by 43 · see citing works
Clustered Protocadherins Emerge as Novel Susceptibility Loci for Mental Disorders
Jia, Z., & Wu, Q. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.587819 · Cited by 43 · see citing works
Self-citationCommunication of genome regulatory elements in a folded chromosome
Razin, S. V., Gavrilov, A. A., Ioudinkova, E. S., & Iarovaia, O. V. (2013) · FEBS Letters · doi:10.1016/j.febslet.2013.04.027 · Cited by 42 · see citing works
How many roads lead to cohesinopathies?
Banerji, R., Skibbens, R. V., & Iovine, M. K. (2017) · Developmental Dynamics · doi:10.1002/dvdy.24510 · Cited by 40 · see citing works
Gassó, P., Rodríguez, N., Blázquez, A., Monteagudo, A., Boloc, D., Plana, M. T., Lafuente, A., Lázaro, L., Arnáiz, J. A., & Mas, S. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.12.003 · Cited by 39 · see citing works
Marsman, J., O’Neill, A. C., Kao, B., Rhodes, J. M., Meier, M., Antony, J., Mönnich, M., & Horsfield, J. A. (2013) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2013.11.007 · Cited by 38 · see citing works
Nolen, L. D., Boyle, S., Ansari, M., Pritchard, E., & Bickmore, W. A. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt265 · Cited by 38 · see citing works
Mills, J. A., Herrera, P. S., Kaur, M., Leo, L., McEldrew, D., Tintos-Hernández, J. A., Rajagopalan, R., Gagne, A. L., Zhang, Z., Ortiz-Gonzalez, X. R., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-19173-9 · Cited by 39 · see citing works
Guo, Y., & Gifford, D. K. (2017) · BMC Genomics · doi:10.1186/s12864-016-3434-3 · Cited by 37 · see citing works
Self-citationThe contribution of cohesin-SA1 to gene expression and chromatin architecture in two murine tissues
Cuadrado, A., Remeseiro, S., Graña‐Castro, O., Pisano, D. G., & Losada, A. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv144 · Cited by 36 · see citing works
High-throughput characterization of genetic effects on DNA–protein binding and gene transcriptionPreprint
Kalita, C. A., Brown, C. D., Freiman, A., Isherwood, J., Wen, X., Piqué-Regi, R., & Luca, F. (2018) · Genome Research · doi:10.1101/gr.237354.118 · Cited by 35 · see citing works
Nuclear Compartments, Genome Folding, and Enhancer-Promoter Communication
Ulianov, S. V., Gavrilov, A. A., & Razin, S. V. (2015) · International review of cytology · doi:10.1016/bs.ircmb.2014.11.004 · Cited by 36 · see citing works
Neuronal territory formation by the atypical cadherins and clustered protocadherins
Lefebvre, J. L. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.07.040 · Cited by 36 · see citing works
Regulation of Wnt signaling by protocadherins
Mah, K. M., & Weiner, J. A. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.07.043 · Cited by 36 · see citing works
Lmx1b is required at multiple stages to build expansive serotonergic axon architectures
Donovan, L. J., Spencer, W. C., Kitt, M. M., Eastman, B., Lobur, K. J., Jiao, K., Silver, J., & Deneris, E. S. (2019) · eLife · doi:10.7554/elife.48788 · Cited by 37 · see citing works
Enhancer reprogramming in tumor progression: a new route towards cancer cell plasticity
Fagnocchi, L., Poli, V., & Zippo, A. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2820-1 · Cited by 35 · see citing works
How DNA loop extrusion mediated by cohesin enables V(D)J recombination
Peters, J. (2021) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2020.11.007 · Cited by 34 · see citing works
- Authors
- Guo, Y., Monahan, K., Wu, H., Gertz, J., Varley, K. E., Li, W., Myers, R. M., Maniatis, T., & Wu, Q.
- Affiliations
- Shanghai Jiao Tong University (CN)
- Columbia University (US)
- HudsonAlpha Institute for Biotechnology (US)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-11-30
- Volume
- 109
- Issue
- 51
- Pages
- 21081-21086
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3529044
- OpenAlex
- W2013934108
- Cited by
- 258
- References
- 35
- Citations by year
- 2026: 13 · 2025: 13 · 2024: 24 · 2023: 16 · 2022: 11 · 2021: 21 · 2020: 17 · 2019: 21 · 2018: 21 · 2017: 23 · 2016: 19 · 2015: 20 · 2014: 16 · 2013: 23
- FWCI
- 7.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS043915)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- DNA looping, CTCF, cohesin, enhancer-promoter interactions, alternative splicing, isoform diversity, neuronal identity, self-avoidance, enhancers
- MeSH terms
- CCCTC-Binding Factor, Cohesins, Cell Line, Chromatin, Chromosomal Proteins, Non-Histone, DNA, DNA-Binding Proteins, Gene Expression Regulation, Humans, Models, Biological, Models, Genetic, Neurons, Nuclear Proteins, Phosphoproteins, Promoter Regions, Genetic, Repressor Proteins, Stochastic Processes, Transcription, Genetic, Cadherins, Cell Cycle Proteins, CpG Islands, Protein Isoforms, Epigenesis, Genetic
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review