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Cited by 40Developmental Biology and Gene RegulationZebrafish Biomedical Research ApplicationsCongenital gastrointestinal and neural anomalies

The gene regulatory basis of genetic compensation during neural crest induction

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Dooley, Christopher M., Wali, Neha, Sealy, Ian M., White, Richard J., Stemple, Derek L., Collins, John E., Busch-Nentwich, Elisabeth M.·2019·PLOS Genetics
DOI 10.1371/journal.pgen.1008213PMC PMC6594659

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Abstract

The neural crest (NC) is a vertebrate-specific cell type that contributes to a wide range of different tissues across all three germ layers. The gene regulatory network (GRN) responsible for the formation of neural crest is conserved across vertebrates. Central to the induction of the NC GRN are AP-2 and SoxE transcription factors. NC induction robustness is ensured through the ability of some of these transcription factors to compensate loss of function of gene family members. However the gene regulatory events underlying compensation are poorly understood. We have used gene knockout and RNA sequencing strategies to dissect NC induction and compensation in zebrafish. We genetically ablate the NC using double mutants of tfap2a;tfap2c or remove specific subsets of the NC with sox10 and mitfa knockouts and characterise genome-wide gene expression levels across multiple time points. We find that compensation through a single wild-type allele of tfap2c is capable of maintaining early NC induction and differentiation in the absence of tfap2a function, but many target genes have abnormal expression levels and therefore show sensitivity to the reduced tfap2 dosage. This separation of morphological and molecular phenotypes identifies a core set of genes required for early NC development. We also identify the 15 somites stage as the peak of the molecular phenotype which strongly diminishes at 24 hpf even as the morphological phenotype becomes more apparent. Using gene knockouts, we associate previously uncharacterised genes with pigment cell development and establish a role for maternal Hippo signalling in melanocyte differentiation. This work extends and refines the NC GRN while also uncovering the transcriptional basis of genetic compensation via paralogues.

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  • tfec was recently identified as a likely direct target of Tfap2a/2c, through analysis of gene expression changes in mutants combining different numbers of tfap2a and tfap2c mutant alleles.

    “In this context, it is interesting that tfec was recently identified as a likely direct target of Tfap2a/2c, through analysis of gene expression changes in mutants combining different numbers of tfap2a and tfap2c mutant alleles [54].”

    From The MITF paralog tfec is required in neural crest development for fate specification of the iridophore lineage from a multipotent pigment cell progenitor (2021) · cites this paper as [54]

    The Results section on neural crest rescue (Fig. 4; page unavailable) compares gene expression across mutants with different numbers of tfap2a and tfap2c alleles and identifies a set enriched for possible AP-2 targets. The passages in our copy do not identify tfec as a likely direct target; a search for “tfec” found no passage that does so. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

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Authors
Dooley, C. M., Wali, N., Sealy, I. M., White, R. J., Stemple, D. L., Collins, J. E., & Busch-Nentwich, E. M.
Affiliations
  • Wellcome Sanger Institute (GB)
  • University of Cambridge (GB)
ORCID
Venue
PLOS Genetics
Publisher
Public Library of Science (PLoS)
Published
2019-06-14
Volume
15
Issue
6
Pages
e1008213
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1008213
PMC
PMC6594659
OpenAlex
W2951612984
Cited by
40
References
5
Citations by year
2026: 6 · 2025: 2 · 2024: 5 · 2023: 4 · 2022: 7 · 2021: 8 · 2020: 6 · 2019: 2
FWCI
1.89
Type
journal article
Language
en
Update notices
new_version (2019-06-26)
Open access
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Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • Apollo (cc-by)
Funders
  • Wellcome Trust (098051 and 206194, 206194, 098051)
  • Russian Science Foundation
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
  • Health Sciences › Medicine › Surgery › Congenital gastrointestinal and neural anomalies
Keywords
neural crest induction, genetic compensation, gene regulatory networks, AP2 transcription factor, TFAP2A, TFAP2C, SOX10, mitfa, dosage sensitivity, melanocyte differentiation, pigment cell development, Hippo signaling pathway, maternal effect genes, zebrafish, somite stage
MeSH terms
Serine-Threonine Kinase 3, Hippo Kinases, Animals, Cell Differentiation, Embryo, Nonmammalian, Melanocytes, Neural Crest, Pigmentation, Zebrafish, Protein Serine-Threonine Kinases, Gene Expression Regulation, Developmental, Cell Lineage, Zebrafish Proteins, Embryonic Development, Transcription Factor AP-2, Microphthalmia-Associated Transcription Factor, Gene Regulatory Networks, SOXE Transcription Factors

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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