Interactions with iridophores and the tissue environment required for patterning melanophores and xanthophores during zebrafish adult pigment stripe formation
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Skin pigment patterns of vertebrates are a classic system for understanding fundamental mechanisms of morphogenesis, differentiation, and pattern formation, and recent studies of zebrafish have started to elucidate the cellular interactions and molecular mechanisms underlying these processes. In this species, horizontal dark stripes of melanophores alternate with light interstripes of yellow or orange xanthophores and iridescent iridophores. We showed previously that the highly conserved zinc finger protein Basonuclin-2 (Bnc2) is required in the environment in which pigment cells reside to promote the development and maintenance of all three classes of pigment cells; bnc2 mutants lack body stripes and interstripes. Previous studies also revealed that interactions between melanophores and xanthophores are necessary for organizing stripes and interstripes. Here we show that bnc2 promotes melanophore and xanthophore development by regulating expression of the growth factors Kit ligand a (Kitlga) and Colony stimulating factor-1 (Csf1), respectively. Yet, we found that rescue of melanophores and xanthophores was insufficient for the recovery of stripes in the bnc2 mutant. We therefore asked whether bnc2-dependent iridophores might contribute to stripe and interstripe patterning as well. We found that iridophores themselves express Csf1, and by ablating iridophores in wild-type and mutant backgrounds, we showed that iridophores contribute to organizing both melanophores and xanthophores during the development of stripes and interstripes. Our results reveal an important role for the cellular environment in promoting adult pigment pattern formation and identify new components of a pigment-cell autonomous pattern-generating system likely to have broad implications for understanding how pigment patterns develop and evolve.
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Genetically or experimentally induced deficiencies in iridophores cause pattern defects, including alterations in primary stripe positioning and boundary formation, and also lead to reductions or losses of secondary interstripes and stripes.
“The iridophore’s importance in skin patterning has been demonstrated in experiments showing that genetically or experimentally induced deficiencies in iridophores cause pattern defects, including alterations in primary stripe positioning and boundary formation, and also lead to reductions or losses of secondary interstripes and stripes13–17.”
From In situ differentiation of iridophore crystallotypes underlies zebrafish stripe patterning (2020) · cites this paper as [15]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredStromal cells of the hypodermis and iridophores regulate melanophore and xanthophore numbers during adult pigment pattern formation.
“stromal cells of the hypodermis (Lang et al., 2009) and also iridophores (Frohnhöfer et al., 2013; Patterson and Parichy, 2013) regulate melanophore and xanthophore numbers during adult pigment pattern formation”
From Thyroid hormone regulates distinct paths to maturation in pigment cell lineages (2019) · cites this paper as Patterson and Parichy, 2013
The authors' data, together with those of others, suggest that some of these signals depend on melanophores, promoting differentiation of iridoblasts toward a state having ordered reflecting crystal platelets that are physiologically responsive (blue ⟷ yellow) in stripes, and away from an alternative state of disordered-crystal platelets lacking physiological responsiveness (silvery-yellow) in the
“Our data, together with those of others, suggest that some of these signals depend on melanophores14,15,25,47, promoting differentiation of iridoblasts toward a state having ordered reflecting crystal platelets that are physiologically responsive (blue ⟷ yellow) in stripes, and away from an alternative state of disordered-crystal platelets lacking physiological responsiveness (silvery-yellow) in”
From In situ differentiation of iridophore crystallotypes underlies zebrafish stripe patterning (2020) · cites this paper as [15]
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Advancing biology through a deeper understanding of zebrafish ecology and evolution.
Parichy, D. M. (2015) · eLife · doi:10.7554/elife.05635 · Cited by 203 · see citing works
Self-citationThyroid hormone regulates distinct paths to maturation in pigment cell lineages
Saunders, L. M., Mishra, A. K., Aman, A. J., Lewis, V. M., Toomey, M. B., Packer, J. S., Qiu, X., McFaline-Figueroa, J. L., Corbo, J. C., Trapnell, C., et al. (2019) · eLife · doi:10.7554/elife.45181 · Cited by 170 · see citing works
Self-citationIn situ differentiation of iridophore crystallotypes underlies zebrafish stripe patterning
Gur, D., Bain, E. J., Johnson, K. R., Aman, A. J., Pasolli, H. A., Flynn, J. D., Allen, M. C., Deheyn, D. D., Lee, J. C., Lippincott-Schwartz, J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-20088-1 · Cited by 69 · see citing works
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- Authors
- Patterson, L. B., & Parichy, D. M.
- Affiliations
- University of Washington (US)
- Corresponding author
- Parichy, David M.
- ORCID
- Parichy, David M.
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-05-30
- Volume
- 9
- Issue
- 5
- Pages
- e1003561
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3667786
- OpenAlex
- W1997183853
- Cited by
- 170
- References
- 0
- Citations by year
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- FWCI
- 6.61
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, 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)
- Funders
- National Science Foundation
- National Institutes of Health (NIH-R01)
- National Institute of General Medical Sciences (R01GM096906, R01GM062182)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD007183)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › melanin and skin pigmentation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- zebrafish, melanophores, xanthophores, iridophores, BNC2, zinc finger proteins, CSF-1, tissue environment, pigment pattern formation, cell ablation
- MeSH terms
- Animals, Carrier Proteins, Cell Differentiation, Embryo, Nonmammalian, Genotype, Melanophores, Morphogenesis, Neural Crest, Phenotype, Skin Pigmentation, Zebrafish, Macrophage Colony-Stimulating Factor, Gene Expression Regulation, Developmental, Stem Cell Factor, Zebrafish Proteins
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