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Cited by 85melanin and skin pigmentationMelanoma and MAPK PathwaysDevelopmental Biology and Gene Regulation

TFAP2 paralogs regulate melanocyte differentiation in parallel with MITF

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Seberg, Hannah E., Van Otterloo, Eric, Loftus, Stacie K., Liu, Huan, Bonde, Greg, Sompallae, Ramakrishna, Gildea, Derek E., Santana, Juan F. +4 more·2017·PLOS Genetics
DOI 10.1371/journal.pgen.1006636PMC PMC5352137
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Abstract

Mutations in the gene encoding transcription factor TFAP2A result in pigmentation anomalies in model organisms and premature hair graying in humans. However, the pleiotropic functions of TFAP2A and its redundantly-acting paralogs have made the precise contribution of TFAP2-type activity to melanocyte differentiation unclear. Defining this contribution may help to explain why TFAP2A expression is reduced in advanced-stage melanoma compared to benign nevi. To identify genes with TFAP2A-dependent expression in melanocytes, we profile zebrafish tissue and mouse melanocytes deficient in Tfap2a, and find that expression of a small subset of genes underlying pigmentation phenotypes is TFAP2A-dependent, including Dct, Mc1r, Mlph, and Pmel. We then conduct TFAP2A ChIP-seq in mouse and human melanocytes and find that a much larger subset of pigmentation genes is associated with active regulatory elements bound by TFAP2A. These elements are also frequently bound by MITF, which is considered the "master regulator" of melanocyte development. For example, the promoter of TRPM1 is bound by both TFAP2A and MITF, and we show that the activity of a minimal TRPM1 promoter is lost upon deletion of the TFAP2A binding sites. However, the expression of Trpm1 is not TFAP2A-dependent, implying that additional TFAP2 paralogs function redundantly to drive melanocyte differentiation, which is consistent with previous results from zebrafish. Paralogs Tfap2a and Tfap2b are both expressed in mouse melanocytes, and we show that mouse embryos with Wnt1-Cre-mediated deletion of Tfap2a and Tfap2b in the neural crest almost completely lack melanocytes but retain neural crest-derived sensory ganglia. These results suggest that TFAP2 paralogs, like MITF, are also necessary for induction of the melanocyte lineage. Finally, we observe a genetic interaction between tfap2a and mitfa in zebrafish, but find that artificially elevating expression of tfap2a does not increase levels of melanin in mitfa hypomorphic or loss-of-function mutants. Collectively, these results show that TFAP2 paralogs, operating alongside lineage-specific transcription factors such as MITF, directly regulate effectors of terminal differentiation in melanocytes. In addition, they suggest that TFAP2A activity, like MITF activity, has the potential to modulate the phenotype of melanoma cells.

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Cited by

Sorted by citations

Authors
Seberg, H. E., Van Otterloo, E., Loftus, S. K., Liu, H., Bonde, G., Sompallae, R., Gildea, D. E., Santana, J. F., Manak, J. R., Pavan, W. J., Williams, T., & Cornell, R. A.
Affiliations
  • University of Iowa (US)
  • National Institutes of Health (US)
  • University of Colorado Anschutz (US)
Corresponding author
Cornell, Robert A.
ORCID
Venue
PLOS Genetics
Publisher
Public Library of Science (PLoS)
Published
2017-03-01
Volume
13
Issue
3
Pages
e1006636
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1006636
PMC
PMC5352137
OpenAlex
W2592875818
Cited by
85
References
6
Citations by year
2026: 5 · 2025: 12 · 2024: 6 · 2023: 9 · 2022: 10 · 2021: 14 · 2020: 7 · 2019: 14 · 2018: 2 · 2017: 6
FWCI
4.13
Type
journal article
Language
en
Update notices
new_version (2017-03-15)
Open access
Licence
Locations
  • PLoS Genetics (publishedVersion, public-domain)
  • PubMed Central (publishedVersion, public-domain)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR062547)
  • National Institute of Dental and Craniofacial Research (DE12728)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › melanin and skin pigmentation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Melanoma and MAPK Pathways
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
TFAP2A, melanocyte differentiation, MITF, pigmentation, melanoma, TRPM1, discrete cosine transform, MC1R, PMEL, melanophilin, neural crest, transcriptional regulation, genetic interactions
MeSH terms
Animals, Base Sequence, Binding Sites, Cell Differentiation, Cell Line, Cells, Cultured, Embryo, Mammalian, Embryo, Nonmammalian, Humans, Melanocytes, Mutation, Pigmentation, Sequence Homology, Nucleic Acid, Zebrafish, Mice, Knockout, Gene Expression Regulation, Developmental, Microscopy, Confocal, Reverse Transcriptase Polymerase Chain Reaction, Gene Expression Profiling, Zebrafish Proteins, RNA Interference, Cell Line, Tumor, Transcription Factor AP-2, Microphthalmia-Associated Transcription Factor

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