Evidence map›Paper›PMID 24360275›Full record

ArticleCell2013

Rapid and pervasive changes in genome-wide enhancer usage during mammalian development.

Alex S Nord, Matthew J Blow, Catia Attanasio, Jennifer A Akiyama, Amy Holt, Roya Hosseini, Sengthavy Phouanenavong, Ingrid Plajzer-Frick, Malak Shoukry, Veena Afzal and 4 more

Open access · bronzeAbstract read
In one paragraph

Article in Cell, 2013. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 248 papers.

0numbers the graph read from it
0cells of the map it votes in
248citing papers in PubMed
15.1field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

248 citing papers in PubMed, 400 citations in OpenAlex.

  1. Trial
  2. Review
  3. Article
  4. Chromatin topology control by a muscle-specific ribosomal protein.bioRxiv : the preprint server for biology · 2026
    Article
  5. Article
  6. Cardiac epigenome in heart development and disease.Nature reviews. Cardiology · 2026
    Review
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188 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

14 authors at 3 institutions in 1 country.

Alex S NordGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Matthew J BlowGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; U.S. Department of Energy Joint Genome Institute, Walnut Creek, CA 94598, USA.
Catia AttanasioGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Jennifer A AkiyamaGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Amy HoltGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Roya HosseiniGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Sengthavy PhouanenavongGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Ingrid Plajzer-FrickGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Malak ShoukryGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Veena AfzalGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
John L R RubensteinDepartment of Psychiatry, Rock Hall, University of California, San Francisco, CA 94158-2324, USA.
Edward M RubinGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; U.S. Department of Energy Joint Genome Institute, Walnut Creek, CA 94598, USA.
Len A PennacchioGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; U.S. Department of Energy Joint Genome Institute, Walnut Creek, CA 94598, USA. Electronic address: lapennacchio@lbl.gov.
Axel ViselGenomics Division, MS 84-171, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; U.S. Department of Energy Joint Genome Institute, Walnut Creek, CA 94598, USA; School of Natural Sciences, University of California, Merced, CA 95343, USA. Electronic address: avisel@lbl.gov.
Lawrence Berkeley National Laboratory · USJoint Genome Institute · USUniversity of California, San Francisco · US

Funding

Generation of an In Vivo Human Genome Transcriptional Enhancer DatasetR01HG003988 · NHGRI · UNIVERSITY OF CALIF-LAWRENC BERKELEY LAB · PI Len Alexander Pennacchio · 2006 to 2026
$24.1M
Genetic Control of Basal Telencephalic DevelopmentR01MH081880 · NIMH · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI RUBENSTEIN, JOHN L. R. · 2009 to 2023
$8.1M
Genetic Studies of Cortex Structure and DevelopmentR01NS099099 · NINDS · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI RUBENSTEIN, JOHN L. R. · 2016 to 2025
$6.4M
Genetic Regulation of Telencephalon DevelopmentR37MH049428 · NIMH · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI RUBENSTEIN, JOHN L. R. · 2008 to 2017
$5.9M
GENETIC STUDIES OF CORTEX STRUCTURE AND DEVELOPMENTR01NS034661 · NINDS · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI RUBENSTEIN, JOHN L. R. · 1996 to 2015
$4.6M
Research Project: Genome-Wide Atlas of Craniofacial Transcriptional EnhancersU01DE020060 · NIDCR · UNIVERSITY OF CALIF-LAWRENC BERKELEY LAB · PI VISEL, AXEL · 2009 to 2013
$2.1M
A High-Resolution Enhancer Atlas of the Developing ForebrainR01NS062859 · NINDS · UNIVERSITY OF CALIF-LAWRENC BERKELEY LAB · PI PENNACCHIO, LEN ALEXANDER · 2008 to 2010
$1.7M
Developmental and evolutionary dynamics of tissue-specific mammalian enhancers.F32GM105202 · NIGMS · UNIVERSITY OF CALIF-LAWRENC BERKELEY LAB · PI NORD, ALEXANDER · 2013 to 2014
$60k
NHGRI NIH HHS R01 HG003988NHGRI NIH HHS R01HG003988NIDCR NIH HHS U01 DE020060NIDCR NIH HHS U01DE020060NIGMS NIH HHS F32 GM105202NIGMS NIH HHS GM105202NIMH NIH HHS R01 MH081880NIMH NIH HHS R37 MH049428NIMH NIH HHS R37MH049428NINDS NIH HHS R01 NS034661NINDS NIH HHS R01 NS062859NINDS NIH HHS R01NS062859ANINDS NIH HHS R01 NS099099
6 · The paper itself

Abstract

Enhancers are distal regulatory elements that can activate tissue-specific gene expression and are abundant throughout mammalian genomes. Although substantial progress has been made toward genome-wide annotation of mammalian enhancers, their temporal activity patterns and global contributions in the context of developmental in vivo processes remain poorly explored. Here we used epigenomic profiling for H3K27ac, a mark of active enhancers, coupled to transgenic mouse assays to examine the genome-wide utilization of enhancers in three different mouse tissues across seven developmental stages. The majority of the ∼90,000 enhancers identified exhibited tightly temporally restricted predicted activity windows and were associated with stage-specific biological functions and regulatory pathways in individual tissues. Comparative genomic analysis revealed that evolutionary conservation of enhancers decreases following midgestation across all tissues examined. The dynamic enhancer activities uncovered in this study illuminate rapid and pervasive temporal in vivo changes in enhancer usage that underlie processes central to development and disease.

Indexed as

Enhancer Elements, GeneticGene Expression Regulation, DevelopmentalGenome-Wide Association StudyAcetylationAnimalsEpigenesis, GeneticEvolution, MolecularHistonesMiceMice, TransgenicOrgan SpecificityHistones

Identifiers

PMID24360275
PMCPMC3989111
OpenAlexW2041171293

What OpenQuestion holds

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Read underepoch 390

Registered trials

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.