Evidence map›Paper›PMID 35179181›Full record

ArticleDevelopment (Cambridge, England)2022

Identification of enhancer regulatory elements that direct epicardial gene expression during zebrafish heart regeneration.

Yingxi Cao, Yu Xia, Joseph J Balowski, Jianhong Ou, Lingyun Song, Alexias Safi, Timothy Curtis, Gregory E Crawford, Kenneth D Poss, Jingli Cao

Open access · bronzeAbstract read
In one paragraph

Article in Development (Cambridge, England), 2022. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 22 papers.

0numbers the graph read from it
0cells of the map it votes in
22citing papers in PubMed
3.1field-weighted citation impact, top 7% 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

22 citing papers in PubMed, 38 citations in OpenAlex.

  1. Article
  2. Enhancer-directed gene delivery for digit regeneration based on conserved epidermal factors.Proceedings of the National Academy of Sciences of the United States of America · 2026
    Article
  3. Article
  4. Zebrafish: A Versatile and Powerful Model for Biomedical Research.BioEssays : news and reviews in molecular, cellular and developmental biology · 2025
    Review
  5. Article
  6. Article
  7. Article
  8. Review
  9. Review
  10. Article
  11. Article
  12. Review
  13. Review
  14. Article
  15. Article
  16. Animal models to study cardiac regeneration.Nature reviews. Cardiology · 2024
    Review
  17. leptin b and its regeneration enhancer illustrate the regenerative features of zebrafish hearts.Developmental dynamics : an official publication of the American Association of Anatomists · 2024
    Article
  18. Article
  19. Article
  20. Article
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

10 authors at 3 institutions in 1 country.

Yingxi CaoCardiovascular Research Institute, Weill Cornell Medicine, 1300 York Avenue, New York, NY 10021, USA.ORCID 0000-0001-5938-6604
Yu XiaCardiovascular Research Institute, Weill Cornell Medicine, 1300 York Avenue, New York, NY 10021, USA.
Joseph J BalowskiDepartment of Cell Biology, Duke University Medical Center, Durham, NC 27710, USA.
Jianhong OuDepartment of Cell Biology, Duke University Medical Center, Durham, NC 27710, USA.ORCID 0000-0002-8652-2488
Lingyun SongCenter for Genomic and Computational Biology, Duke University Medical Center, Durham, NC 27710, USA.
Alexias SafiCenter for Genomic and Computational Biology, Duke University Medical Center, Durham, NC 27710, USA.
Timothy CurtisDepartment of Cell Biology, Duke University Medical Center, Durham, NC 27710, USA.
Gregory E CrawfordCenter for Genomic and Computational Biology, Duke University Medical Center, Durham, NC 27710, USA.
Kenneth D PossDepartment of Cell Biology, Duke University Medical Center, Durham, NC 27710, USA.
Jingli CaoCardiovascular Research Institute, Weill Cornell Medicine, 1300 York Avenue, New York, NY 10021, USA.
Duke University · USCornell University · USDuke Medical Center · US

Funding

Leveraging zebrafish models to dissect and enhance heart regenerationR35HL150713 · NHLBI · MORGRIDGE INSTITUTE FOR RESEARCH, INC. · PI KENNETH D POSS · 2020 to 2026
$6.9M
Mechanisms controlling epicardial-dependent promotion of heart regeneration in zebrafish.R01HL155607 · NHLBI · WEILL MEDICAL COLL OF CORNELL UNIV · PI Jingli Cao · 2021 to 2026
$2.9M
Regulation of the Epicardial Injury Response During Heart Regeneration in ZebrafishR01HL131319 · NHLBI · DUKE UNIVERSITY · PI POSS, KENNETH D · 2016 to 2019
$1.6M
American Heart Association-American Stroke Association 18CDA34110108NHLBI NIH HHS R01 HL131319NHLBI NIH HHS R01 HL155607NHLBI NIH HHS R35 HL150713
6 · The paper itself

Abstract

The epicardium is a mesothelial tissue layer that envelops the heart. Cardiac injury activates dynamic gene expression programs in epicardial tissue, which in zebrafish enables subsequent regeneration through paracrine and vascularizing effects. To identify tissue regeneration enhancer elements (TREEs) that control injury-induced epicardial gene expression during heart regeneration, we profiled transcriptomes and chromatin accessibility in epicardial cells purified from regenerating zebrafish hearts. We identified hundreds of candidate TREEs, which are defined by increased chromatin accessibility of non-coding elements near genes with increased expression during regeneration. Several of these candidate TREEs were incorporated into stable transgenic lines, with five out of six elements directing injury-induced epicardial expression but not ontogenetic epicardial expression in larval hearts. Whereas two independent TREEs linked to the gene gnai3 showed similar functional features of gene regulation in transgenic lines, two independent ncam1a-linked TREEs directed distinct spatiotemporal domains of epicardial gene expression. Thus, multiple TREEs linked to a regeneration gene can possess either matching or complementary regulatory controls. Our study provides a new resource and principles for understanding the regulation of epicardial genetic programs during heart regeneration. This article has an associated 'The people behind the papers' interview.

Indexed as

AnimalsAnimals, Genetically ModifiedChromatinEnhancer Elements, GeneticGene Expression RegulationGTP-Binding Protein alpha Subunits, Gi-GoHeartLarvaNerve Tissue ProteinsNeural Cell Adhesion MoleculesPericardiumRegenerationZebrafishZebrafish ProteinsChromatinGTP-Binding Protein alpha Subunits, Gi-Goncam1a protein, zebrafishNerve Tissue ProteinsNeural Cell Adhesion MoleculesZebrafish ProteinsATAC-seqEnhancerEpicardiumHeart regenerationTREEZebrafish

Identifiers

PMID35179181
PMCPMC8918790
OpenAlexW4225852965

What OpenQuestion holds

Textmetadata
Read underepoch 390

Registered trials

None linked

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.