Chromatin Loops as Allosteric Modulators of Enhancer-Promoter Interactions
Publication Date
October 23, 2014
Journal
PLOS Computational Biology
Authors
Boryana Doyle, Geoffrey Fudenberg, Maxim Imakaev & Leonid A. Mirny
Volume
10
Issue
10
Pages
e1003867
DOI
https://dx.plos.org/10.1371/journal.pcbi.1003867
Publisher URL
http://journals.plos.org/ploscompbiol/article?id=10.1371%2Fjournal.pcbi.1003867
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/25340767
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4207457
Europe PMC
http://europepmc.org/abstract/MED/25340767
Web of Science
000344547900022
Scopus
84908333387
Mendeley
http://www.mendeley.com/research/chromatin-loops-allosteric-modulators-enhancerpromoter-interactions-1
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Mendeley | Further Information

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CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1728860"], "description"=>"<p><i>Experimental Studies</i>, (<b>A</b>) Illustration of an enhancer (in yellow) spatially interacting with a promoter (blue) along a chromatin fiber. This coloring convention continues throughout the paper. (<b>B</b>) A recent study in Drosophila suggested a 7 kb chromatin loop formed between Su(Hw) insulators (orange) could decrease E-P interactions (red “X”) <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003867#pcbi.1003867-Savitskaya1\" target=\"_blank\">[20]</a>. (<b>C</b>) Conversely, a 3 kb chromatin loop in the region between enhancer and promoter was proposed to increase E-P interactions. (<b>D</b>) Five arrangements for proposed looping interactions from three studies, left to right, <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003867#pcbi.1003867-Kyrchanova1\" target=\"_blank\">[21]</a>, <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003867#pcbi.1003867-Kurukuti1\" target=\"_blank\">[22]</a>, and <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003867#pcbi.1003867-Comet1\" target=\"_blank\">[23]</a>. (<i>left</i>) a single Drosophila <i>gypsy</i> element between an enhancer and a promoter did not change their interactions (<i>top</i>), however an additional <i>gypsy</i> element upstream of the enhancer decreased E-P interactions (<i>bottom</i>) <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003867#pcbi.1003867-Kyrchanova1\" target=\"_blank\">[21]</a>. (<i>center</i>) at the mouse H19 locus, a regulatory element with multiple larger loops (55 kb and 25 kb) was suggested to control multiple E-P contacts; the enhancer can regulate the promoter before the loop, but cannot regulate the promoter within the loop <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003867#pcbi.1003867-Kurukuti1\" target=\"_blank\">[22]</a>. (<i>right</i>) chromatin loops may also modulate spatial interactions between silencing elements (e.g. PRE, black triangles) and their target promoters <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003867#pcbi.1003867-Comet1\" target=\"_blank\">[23]</a>. The promoter within the loop is not silenced (<i>top</i>), whereas the promoter beyond the loop is silenced (<i>bottom</i>). <i>Polymer Simulations</i>, (<b>E</b>) Arrangement 1: polymer conformation where an enhancer is within a chromatin loop and a promoter is beyond the loop. (<b>F</b>) Arrangement 2: polymer conformation where an enhancer is before the loop and a promoter is after the loop. (<b>G</b>) (<i>left</i>) zoom-in on our polymer model of chromatin. The three large circles represent one monomer each; each monomer consists of three nucleosomes (small circles) or 500 bp. (<i>right</i>) full view of a sample polymer conformation showing a 30 kb chromatin loop (black) with highlighted loop-bases (orange) within a 1 Mb region.</p>", "links"=>[], "tags"=>["enhancer", "eukaryotic gene expression", "silico 3 C", "looping interactions", "equilibrium polymer simulations show", "promoter"], "article_id"=>1213608, "categories"=>["Uncategorised"], "users"=>["Boryana Doyle", "Geoffrey Fudenberg", "Maxim Imakaev", "Leonid A. Mirny"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003867.g001", "stats"=>{"downloads"=>2, "page_views"=>32, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Enhancer_promoter_pairs_in_the_context_of_other_interactions_/1213608", "title"=>"Enhancer-promoter pairs in the context of other interactions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-23 03:30:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1728884", "https://ndownloader.figshare.com/files/1728885", "https://ndownloader.figshare.com/files/1728886", "https://ndownloader.figshare.com/files/1728887", "https://ndownloader.figshare.com/files/1728888", "https://ndownloader.figshare.com/files/1728889", "https://ndownloader.figshare.com/files/1728890", "https://ndownloader.figshare.com/files/1728891", "https://ndownloader.figshare.com/files/1728892"], "description"=>"<div><p>The classic model of eukaryotic gene expression requires direct spatial contact between a distal enhancer and a proximal promoter. Recent Chromosome Conformation Capture (3C) studies show that enhancers and promoters are embedded in a complex network of looping interactions. Here we use a polymer model of chromatin fiber to investigate whether, and to what extent, looping interactions between elements in the vicinity of an enhancer-promoter pair can influence their contact frequency. Our equilibrium polymer simulations show that a chromatin loop, formed by elements flanking either an enhancer or a promoter, suppresses enhancer-promoter interactions, working as an insulator. A loop formed by elements located in the region between an enhancer and a promoter, on the contrary, facilitates their interactions. We find that different mechanisms underlie insulation and facilitation; insulation occurs due to steric exclusion by the loop, and is a global effect, while facilitation occurs due to an effective shortening of the enhancer-promoter genomic distance, and is a local effect. Consistently, we find that these effects manifest quite differently for <i>in silico</i> 3C and microscopy. Our results show that looping interactions that do not directly involve an enhancer-promoter pair can nevertheless significantly modulate their interactions. This phenomenon is analogous to allosteric regulation in proteins, where a conformational change triggered by binding of a regulatory molecule to one site affects the state of another site.</p></div>", "links"=>[], "tags"=>["enhancer", "eukaryotic gene expression", "silico 3 C", "looping interactions", "equilibrium polymer simulations show", "promoter"], "article_id"=>1213629, "categories"=>["Uncategorised"], "users"=>["Boryana Doyle", "Geoffrey Fudenberg", "Maxim Imakaev", "Leonid A. Mirny"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1003867.s001", "https://dx.doi.org/10.1371/journal.pcbi.1003867.s002", "https://dx.doi.org/10.1371/journal.pcbi.1003867.s003", "https://dx.doi.org/10.1371/journal.pcbi.1003867.s004", "https://dx.doi.org/10.1371/journal.pcbi.1003867.s005", "https://dx.doi.org/10.1371/journal.pcbi.1003867.s006", "https://dx.doi.org/10.1371/journal.pcbi.1003867.s007", "https://dx.doi.org/10.1371/journal.pcbi.1003867.s008", "https://dx.doi.org/10.1371/journal.pcbi.1003867.s009"], "stats"=>{"downloads"=>47, "page_views"=>32, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chromatin_Loops_as_Allosteric_Modulators_of_Enhancer_Promoter_Interactions_/1213629", "title"=>"Chromatin Loops as Allosteric Modulators of Enhancer-Promoter Interactions", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-10-23 03:30:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1728863"], "description"=>"<p>(<b>A</b>) (<i>top</i>) Illustration of the insulation mechanism: strong dynamic steric exclusion by a chromatin loop is shown by a superposition of loops in multiple conformations (grey, with enhancer and promoter) and their sterically excluded region (dashed lines), surrounded by other distal regions of chromatin (grey). (<i>bottom</i>) Density of distal monomers (i.e. outside the loop and>10 kb from the loop base) as a function of radial distance from the center of mass of the loop. The loop-free control exactly repeats this procedure for an equivalent region without a loop. Both are normalized using respective radial-position dependent spatial density (<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003867#s4\" target=\"_blank\">Methods</a>). (<b>B</b>) (<i>top</i>) Illustration of facilitation mechanism: an E-P pair flanking a loop has an effectively shorter genomic distance; here an E-P pair with 50 kb separation and a 30 kb loop behaves similarly to an E-P pair separated by 20 kb in a region without a loop. (<i>bottom</i>) Comparison of contact frequency ratios for the above situations, as a function of E-P distance. (<b>C</b>) Simulated cumulative distribution of spatial distances (<i>in silico</i> FISH) for an E-P pair with a genomic distance of 90 kb.</p>", "links"=>[], "tags"=>["enhancer", "eukaryotic gene expression", "silico 3 C", "looping interactions", "equilibrium polymer simulations show", "promoter"], "article_id"=>1213611, "categories"=>["Uncategorised"], "users"=>["Boryana Doyle", "Geoffrey Fudenberg", "Maxim Imakaev", "Leonid A. Mirny"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003867.g004", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mechanisms_of_insulation_and_facilitation_/1213611", "title"=>"Mechanisms of insulation and facilitation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-23 03:30:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1728861"], "description"=>"<p>(<b>A</b>) Five sample conformations from polymer simulations with a 30 kb permanent loop (black) formed between two loop bases (orange) in a 1 Mb region of fiber. (<b>B</b>) Average heatmap (300 kb by 300 kb) for polymer simulations of the permanent, one-loop system, with a 30 kb loop (aggregated over 800,000 simulated conformations). Top and left edges show positions of the enhancer (yellow), promoter (blue), and loop bases (orange) for insulation and facilitation arrangements. (<b>C</b>) Schematics of E-P arrangements. (<i>top</i>) chromatin fiber without a fixed loop and with E-P genomic distance of 50 kb, as used to calculate expected (no-loop) contact frequencies (<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003867#s4\" target=\"_blank\">Methods</a>). (<i>middle</i>) arrangement where insulation is observed, represented by the red “X”. (<i>bottom</i>) arrangement where facilitation is observed. (<b>D</b>) Contact frequency ratios (<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003867#s4\" target=\"_blank\">Methods</a>) for insulation and facilitation arrangements with a 30 kb loop and 50 kb E-P genomic distance. Here and below, error bars indicate one standard deviation about the mean.</p>", "links"=>[], "tags"=>["enhancer", "eukaryotic gene expression", "silico 3 C", "looping interactions", "equilibrium polymer simulations show", "promoter"], "article_id"=>1213609, "categories"=>["Uncategorised"], "users"=>["Boryana Doyle", "Geoffrey Fudenberg", "Maxim Imakaev", "Leonid A. Mirny"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003867.g002", "stats"=>{"downloads"=>0, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_chromatin_loop_alters_the_frequency_of_enhancer_promoter_interactions_/1213609", "title"=>"A chromatin loop alters the frequency of enhancer-promoter interactions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-23 03:30:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1728862"], "description"=>"<p>(<b>A</b>) Insulation (<i>left</i>) and facilitation (<i>right</i>) as a function of E-P genomic distance. For insulation, enhancer position remains fixed. For facilitation, an E-P pair is positioned symmetrically around the loop at each genomic distance. (<b>B</b>) Insulation for different positions of the enhancer within the loop with a constant genomic distance of 50 kb.</p>", "links"=>[], "tags"=>["enhancer", "eukaryotic gene expression", "silico 3 C", "looping interactions", "equilibrium polymer simulations show", "promoter"], "article_id"=>1213610, "categories"=>["Uncategorised"], "users"=>["Boryana Doyle", "Geoffrey Fudenberg", "Maxim Imakaev", "Leonid A. Mirny"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003867.g003", "stats"=>{"downloads"=>0, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Insulation_and_facilitation_strength_depends_on_enhancer_promoter_positions_/1213610", "title"=>"Insulation and facilitation strength depends on enhancer-promoter positions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-23 03:30:21"}

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Relative Metric

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