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Enhancer sharing promotes neighborhoods of transcriptional regulation across eukaryotes

Quintero-Cadena, Porfirio and Sternberg, Paul W. (2016) Enhancer sharing promotes neighborhoods of transcriptional regulation across eukaryotes. G3, 6 (12). pp. 4167-4174. ISSN 2160-1836 . PMCID PMC5144984. http://resolver.caltech.edu/CaltechAUTHORS:20160801-083326464

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Abstract

Enhancers physically interact with transcriptional promoters, looping over distances that can span multiple regulatory elements. Given that enhancer–promoter (EP) interactions generally occur via common protein complexes, it is unclear whether EP pairing is predominantly deterministic or proximity guided. Here, we present cross-organismic evidence suggesting that most EP pairs are compatible, largely determined by physical proximity rather than specific interactions. By reanalyzing transcriptome datasets, we find that the transcription of gene neighbors is correlated over distances that scale with genome size. We experimentally show that nonspecific EP interactions can explain such correlation, and that EP distance acts as a scaling factor for the transcriptional influence of an enhancer. We propose that enhancer sharing is commonplace among eukaryotes, and that EP distance is an important layer of information in gene regulation.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1534/g3.116.036228DOIArticle
http://www.g3journal.org/content/6/12/4167.shortPublisherArticle
https://doi.org/10.1101/061218DOIDiscussion Paper
http://www.g3journal.org/content/6/12/4167/suppl/DC1PublisherSupplemental Material
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5144984/PubMed CentralArticle
ORCID:
AuthorORCID
Sternberg, Paul W.0000-0002-7699-0173
Additional Information:© 2016 Quintero-Cadena, Sternberg. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Received June 28, 2016. Accepted October 15, 2016. Early Online October 31, 2016. We thank Zhiping Wang and Yishi Jin for plasmids for CRISPR-Cas9 single-copy insertion; Carmie Robinson for discussions, experimental suggestions, and comments on the manuscript; Han Wang for discussions, technical advice, and comments on the manuscript; Hillel Schwartz, Mitchell Guttman, Mihoko Kato, David Angeles-Albores, Jonathan Liu, Barbara Wold, Isabelle Peter, and Angelike Stathopoulos for discussions and comments on the manuscript; the Encode and ModEncode consortiums, FlyBase, WormBase, and Ensembl databases, the Wold Lab, and the Guigo Lab for data accessibility. Our work was supported by the Howard Hughes Medical Institute, of which P.W.S. is an investigator. Author contributions: P.Q.C. performed the experiments and analyzed the data. P.Q.C. and P.W.S. designed the experiments and wrote the paper. The authors declare no competing financial interests.
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:enhancer sharing; gene coexpression; gene neighbors; enhancer specificity; transcriptional domains
PubMed Central ID:PMC5144984
Record Number:CaltechAUTHORS:20160801-083326464
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20160801-083326464
Official Citation:Enhancer Sharing Promotes Neighborhoods of Transcriptional Regulation Across Eukaryotes Porfirio Quintero-Cadena and Paul W. Sternberg G3 December 2016 6:4167-4174; Early Online October 31, 2016, doi:10.1534/g3.116.036228
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:69342
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:01 Aug 2016 18:26
Last Modified:26 Oct 2018 23:50

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