Evidence map›Paper›PMID 39481376›Full record

ArticleDevelopmental cell2025

Combinatorial transcription factor binding encodes cis-regulatory wiring of mouse forebrain GABAergic neurogenesis.

Rinaldo Catta-Preta, Susan Lindtner, Athena Ypsilanti, Nicolas Seban, James D Price, Armen Abnousi, Linda Su-Feher, Yurong Wang, Karol Cichewicz, Sally A Boerma and 10 more

Abstract read
In one paragraph

Article in Developmental cell, 2025. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 14 papers.

0numbers the graph read from it
0cells of the map it votes in
14citing papers in PubMed
–field-weighted citation impact
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

14 citing papers in PubMed.

  1. Article
  2. Article
  3. Review
  4. Article
  5. Article
  6. Article
  7. Article
  8. Article
  9. Review
  10. Article
  11. Article
  12. Assessing candidate DLX-regulated genes in the first pharyngeal arch of chick embryos.Developmental dynamics : an official publication of the American Association of Anatomists · 2025
    Article
  13. Proceedings of the National Academy of Sciences of the United States of America · 2024
    Article
  14. DLX genes and proteins in mammalian forebrain development.Development (Cambridge, England) · 2024
    Review
4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

20 authors.

Rinaldo Catta-PretaDepartment of Neurobiology, Physiology and Behavior, and Department of Psychiatry and Behavioral Sciences, University of California, Davis, Davis, CA 95618, USA.
Susan LindtnerNina Ireland Laboratory of Developmental Neurobiology, Department of Psychiatry and Behavioral Sciences, UCSF Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA 94143, USA.
Athena YpsilantiNina Ireland Laboratory of Developmental Neurobiology, Department of Psychiatry and Behavioral Sciences, UCSF Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA 94143, USA.
Nicolas SebanDepartment of Neurobiology, Physiology and Behavior, and Department of Psychiatry and Behavioral Sciences, University of California, Davis, Davis, CA 95618, USA.
James D PriceNina Ireland Laboratory of Developmental Neurobiology, Department of Psychiatry and Behavioral Sciences, UCSF Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA 94143, USA.
Armen AbnousiDepartment of Quantitative Health Sciences, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, OH 44106, USA.
Linda Su-FeherDepartment of Neurobiology, Physiology and Behavior, and Department of Psychiatry and Behavioral Sciences, University of California, Davis, Davis, CA 95618, USA.
Yurong WangDepartment of Neurobiology, Physiology and Behavior, and Department of Psychiatry and Behavioral Sciences, University of California, Davis, Davis, CA 95618, USA.
Karol CichewiczDepartment of Neurobiology, Physiology and Behavior, and Department of Psychiatry and Behavioral Sciences, University of California, Davis, Davis, CA 95618, USA.
Sally A BoermaDepartment of Neurobiology, Physiology and Behavior, and Department of Psychiatry and Behavioral Sciences, University of California, Davis, Davis, CA 95618, USA.
Ivan JuricDepartment of Quantitative Health Sciences, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, OH 44106, USA.
Ian R JonesInstitute for Human Genetics, Department of Neurology, University of California, San Francisco, San Francisco, CA 94143, USA; Department of Neurology, University of California, San Francisco, San Francisco, CA 94143, USA.
Jennifer A AkiyamaEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Ming HuDepartment of Quantitative Health Sciences, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, OH 44106, USA.
Yin ShenInstitute for Human Genetics, Department of Neurology, University of California, San Francisco, San Francisco, CA 94143, USA; Department of Neurology, University of California, San Francisco, San Francisco, CA 94143, USA.
Axel ViselEnvironmental Genomics and Systems Biology Division, 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, Merced, CA 95343, USA.
Len A PennacchioEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; U.S. Department of Energy Joint Genome Institute, Walnut Creek, CA 94598, USA; Comparative Biochemistry Program, University of California, Berkeley, Berkeley, CA 94720, USA.
Diane E DickelEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
John L R RubensteinNina Ireland Laboratory of Developmental Neurobiology, Department of Psychiatry and Behavioral Sciences, UCSF Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA 94143, USA. Electronic address: john.rubenstein@ucsf.edu.
Alex S NordDepartment of Neurobiology, Physiology and Behavior, and Department of Psychiatry and Behavioral Sciences, University of California, Davis, Davis, CA 95618, USA. Electronic address: asnord@ucdavis.edu.

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 Regulation of Telencephalon DevelopmentR37MH049428 · NIMH · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI RUBENSTEIN, JOHN L. R. · 2008 to 2017
$5.9M
STRUCTURE, EXPRESSION &FUNCTION OF THE DLX GENE FAMILYR01MH049428 · NIMH · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI RUBENSTEIN, JOHN L. R. · 1992 to 2022
$5.8M
A Single-Cell Resolution Enhancer Atlas of Craniofacial DevelopmentR01DE028599 · NIDCR · UNIVERSITY OF CALIF-LAWRENC BERKELEY LAB · PI VISEL, AXEL · 2019 to 2023
$4.2M
Functional Elucidation of the Sequence-Encoded Regulatory Activity of Enhancers in Vivo in the BrainR35GM119831 · NIGMS · UNIVERSITY OF CALIFORNIA AT DAVIS · PI Alexander Nord · 2016 to 2026
$3.9M
Linking Psychiatric Genetics to Cell-Type Specific Enhancer FunctionR01MH117106 · NIMH · UNIVERSITY OF CALIF-LAWRENC BERKELEY LAB · PI VISEL, AXEL · 2018 to 2022
$3.6M
Charting the 3D epigenome in human brain development and diseasesU01DA052713 · NIDA · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI KRIEGSTEIN, ARNOLD, SHEN, YIN · 2020 to 2024
$3.4M
Training Program in Biomolecular TechnologyT32GM008799 · NIGMS · UNIVERSITY OF CALIFORNIA DAVIS · PI LEACH, J. KENT · 2002 to 2016
$2.4M
Learning, Memory, and Plasticity (LaMP) Training ProgramT32MH112507 · NIMH · UNIVERSITY OF CALIFORNIA AT DAVIS · PI Karen Zito · 2017 to 2026
$2.4M
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
NHGRI NIH HHS R01 HG003988NIDA NIH HHS U01 DA052713NIDCR NIH HHS R01 DE028599NIGMS NIH HHS R35 GM119831NIGMS NIH HHS T32 GM008799NIMH NIH HHS R01 MH049428NIMH NIH HHS R01 MH081880NIMH NIH HHS R01 MH117106NIMH NIH HHS R37 MH049428NIMH NIH HHS T32 MH112507NINDS NIH HHS R01 NS062859
6 · The paper itself

Abstract

Transcription factors (TFs) bind combinatorially to cis-regulatory elements, orchestrating transcriptional programs. Although studies of chromatin state and chromosomal interactions have demonstrated dynamic neurodevelopmental cis-regulatory landscapes, parallel understanding of TF interactions lags. To elucidate combinatorial TF binding driving mouse basal ganglia development, we integrated chromatin immunoprecipitation sequencing (ChIP-seq) for twelve TFs, H3K4me3-associated enhancer-promoter interactions, chromatin and gene expression data, and functional enhancer assays. We identified sets of putative regulatory elements with shared TF binding (TF-pRE modules) that orchestrate distinct processes of GABAergic neurogenesis and suppress other cell fates. The majority of pREs were bound by one or two TFs; however, a small proportion were extensively bound. These sequences had exceptional evolutionary conservation and motif density, complex chromosomal interactions, and activity as in vivo enhancers. Our results provide insights into the combinatorial TF-pRE interactions that activate and repress expression programs during telencephalon neurogenesis and demonstrate the value of TF binding toward modeling developmental transcriptional wiring.

Indexed as

GABAergic NeuronsNeurogenesisProsencephalonTranscription FactorsAnimalsBinding SitesChromatinChromatin Immunoprecipitation SequencingEnhancer Elements, GeneticGene Expression Regulation, DevelopmentalHistonesMicePromoter Regions, GeneticProtein BindingChromatinHistonesTranscription Factorschromatin conformationcombinatorial TF bindingevolutionary conservationGABAergic cortical interneuronsgene regulatory networkneurogenesistranscription factors

Identifiers

PMID39481376
PMCPMC11753952

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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.