Cited by 99Developmental Biology and Gene RegulationNeurogenesis and neuroplasticity mechanismsWnt/β-catenin signaling in development and cancer

Tfap2a and Foxd3 regulate early steps in the development of the neural crest progenitor population

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Wang, Wen-Der, Melville, David B., Montero-Balaguer, Mercedes, Hatzopoulos, Antonis K., Knapik, Ela W.·2011·Developmental Biology

Abstract

The neural crest is a stem cell-like population exclusive to vertebrates that gives rise to many different cell types including chondrocytes, neurons and melanocytes. Arising from the neural plate border at the intersection of Wnt and Bmp signaling pathways, the complexity of neural crest gene regulatory networks has made the earliest steps of induction difficult to elucidate. Here, we report that tfap2a and foxd3 participate in neural crest induction and are necessary and sufficient for this process to proceed. Double mutant tfap2a (mont blanc, mob) and foxd3 (mother superior, mos) mob;mos zebrafish embryos completely lack all neural crest-derived tissues. Moreover, tfap2a and foxd3 are expressed during gastrulation prior to neural crest induction in distinct, complementary, domains; tfap2a is expressed in the ventral non-neural ectoderm and foxd3 in the dorsal mesendoderm and ectoderm. We further show that Bmp signaling is expanded in mob;mos embryos while expression of dkk1, a Wnt signaling inhibitor, is increased and canonical Wnt targets are suppressed. These changes in Bmp and Wnt signaling result in specific perturbations of neural crest induction rather than general defects in neural plate border or dorso-ventral patterning. foxd3 overexpression, on the other hand, enhances the ability of tfap2a to ectopically induce neural crest around the neural plate, overriding the normal neural plate border limit of the early neural crest territory. Although loss of either Tfap2a or Foxd3 alters Bmp and Wnt signaling patterns, only their combined inactivation sufficiently alters these signaling gradients to abort neural crest induction. Collectively, our results indicate that tfap2a and foxd3, in addition to their respective roles in the differentiation of neural crest derivatives, also jointly maintain the balance of Bmp and Wnt signaling in order to delineate the neural crest induction domain.

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Crossref · 10.1016/j.ydbio.2011.09.019

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  • Redundant activities of Tfap2a and Tfap2c are required for NC induction and development of other non-neural ectoderm derivatives in zebrafish embryos.

    “Redundant activities of Tfap2a and Tfap2c are required for NC induction and development of other non-neural ectoderm derivatives in zebrafish embryos [52, 53].”

    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 [53]

    The Discussion reports that Tfap2a and Foxd3 cooperate in neural crest induction in zebrafish embryos. It does not establish redundant activity of Tfap2a and Tfap2c or their requirement for development of other non-neural ectoderm derivatives; a search for Tfap2c found no supporting passage. (LLM, conf=0.84)

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Cited by

Authors
Wang, W.-D., Melville, D. B., Montero-Balaguer, M., Hatzopoulos, A. K., & Knapik, E. W.
Affiliations
  • Vanderbilt University Medical Center (US)
  • University of Freiburg (DE)
Corresponding author
Knapik, Ela W.
Venue
Developmental Biology
Publisher
Elsevier BV
Published
2011-12
Volume
360
Issue
1
Pages
173-185
ISSN
0012-1606 (ISSN-L)
OpenAlex
W2002466559
Cited by
99
References
0
Citations by year
2026: 5 · 2025: 6 · 2024: 8 · 2023: 3 · 2022: 7 · 2021: 7 · 2020: 7 · 2019: 7 · 2018: 9 · 2017: 7 · 2016: 4 · 2015: 6 · 2014: 7 · 2013: 7 · 2012: 8
FWCI
2.80
Type
journal article
Language
en
Open access
Locations
  • Developmental Biology (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • NIH
  • Zebrafish Initiative of the Vanderbilt University Academic Venture Capital Fund
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
Keywords
neural crest induction, TFAP2A, FOXD3, neural plate border, BMP signaling, Wnt signaling, DKK1, neural crest progenitors, zebrafish, Mont Blanc, gene regulatory networks, gastrulation, dorsoventral patterning
MeSH terms
Animals, Base Sequence, Mutation, Neural Crest, Zebrafish, Genes, p53, Cell Death, DNA Primers, Gene Expression Regulation, Developmental, Bone Morphogenetic Proteins, Body Patterning, Zebrafish Proteins, Intercellular Signaling Peptides and Proteins, Transcription Factor AP-2, Forkhead Transcription Factors, Embryonic Stem Cells, Gastrulation, Neurogenesis, Wnt Signaling Pathway

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