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Long-distance communication by specialized cellular projections during pigment pattern development and evolution.

Eom DS, Bain EJ, Patterson LB, Grout ME, Parichy DM - Elife (2015)

Bottom Line: Changes in gene activity are essential for evolutionary diversification.Projections depended on microfilaments and microtubules, exhibited meandering trajectories, and stabilized on target cells to which they delivered membraneous vesicles.By contrast, the uniformly patterned pearl danio lacked such projections, concomitant with Colony stimulating factor 1-dependent changes in xanthophore differentiation that likely curtail signaling available to melanophores.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Washington, Seattle, United States.

ABSTRACT
Changes in gene activity are essential for evolutionary diversification. Yet, elucidating the cellular behaviors that underlie modifications to adult form remains a profound challenge. We use neural crest-derived adult pigmentation of zebrafish and pearl danio to uncover cellular bases for alternative pattern states. We show that stripes in zebrafish require a novel class of thin, fast cellular projection to promote Delta-Notch signaling over long distances from cells of the xanthophore lineage to melanophores. Projections depended on microfilaments and microtubules, exhibited meandering trajectories, and stabilized on target cells to which they delivered membraneous vesicles. By contrast, the uniformly patterned pearl danio lacked such projections, concomitant with Colony stimulating factor 1-dependent changes in xanthophore differentiation that likely curtail signaling available to melanophores. Our study reveals a novel mechanism of cellular communication, roles for differentiation state heterogeneity in pigment cell interactions, and an unanticipated morphogenetic behavior contributing to a striking difference in adult form.

No MeSH data available.


Related in: MedlinePlus

Connexin dependence of airineme production.(A) Phenotypes of wild-type and cx41.8 mutant zebrafish. (B) Stage-specificity of airineme production and numbers of airinemes produced per cell differed between wild-type and cx41.8 mutant zebrafish (left, genotype x stage interaction: χ2=94.2, d.f.=1, p<0.0001, N=639 cells; right, χ2=51.1, d.f.=7, p<0.0001, N=428 cells). Scale bar: 1 mm (A).DOI:http://dx.doi.org/10.7554/eLife.12401.022
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fig4s4: Connexin dependence of airineme production.(A) Phenotypes of wild-type and cx41.8 mutant zebrafish. (B) Stage-specificity of airineme production and numbers of airinemes produced per cell differed between wild-type and cx41.8 mutant zebrafish (left, genotype x stage interaction: χ2=94.2, d.f.=1, p<0.0001, N=639 cells; right, χ2=51.1, d.f.=7, p<0.0001, N=428 cells). Scale bar: 1 mm (A).DOI:http://dx.doi.org/10.7554/eLife.12401.022

Mentions: To test whether aox5+ airineme targeting is genetically labile, we screened zebrafish pigment pattern mutants and also re-examined the very few airinemes produced in pearl danio. As compared to wild-type zebrafish, we found that airinemes in spotted connexin41.8 (cx41.8; leopard) mutants (Maderspacher and Nusslein-Volhard, 2003; Watanabe et al., 2006) were later-appearing and more promiscuous, stabilizing as extensively on aox5+ cells as on melanophores (Figure 4D-right, 4F; Figure 4—figure supplement 4A,B; Video 15). Such differences could reflect acute morphogenetic interactions, perhaps dependent on connexin hemichannels, or chronic defects in differentiation, as xanthophores of presumptive cx41.8 mutants are reported to contain melanin and melanosome-like vesicles (Kirschbaum, 1975). Interestingly, the rare airinemes of pearl danio also stabilized on xanthophores though inspection cx41.8 sequence and expression did not reveal gross differences between zebrafish and pearl (Figure 4D-right; Video 16; and data not shown).Video 15.Altered airineme targeting altered by connexin mutation.


Long-distance communication by specialized cellular projections during pigment pattern development and evolution.

Eom DS, Bain EJ, Patterson LB, Grout ME, Parichy DM - Elife (2015)

Connexin dependence of airineme production.(A) Phenotypes of wild-type and cx41.8 mutant zebrafish. (B) Stage-specificity of airineme production and numbers of airinemes produced per cell differed between wild-type and cx41.8 mutant zebrafish (left, genotype x stage interaction: χ2=94.2, d.f.=1, p<0.0001, N=639 cells; right, χ2=51.1, d.f.=7, p<0.0001, N=428 cells). Scale bar: 1 mm (A).DOI:http://dx.doi.org/10.7554/eLife.12401.022
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Related In: Results  -  Collection

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fig4s4: Connexin dependence of airineme production.(A) Phenotypes of wild-type and cx41.8 mutant zebrafish. (B) Stage-specificity of airineme production and numbers of airinemes produced per cell differed between wild-type and cx41.8 mutant zebrafish (left, genotype x stage interaction: χ2=94.2, d.f.=1, p<0.0001, N=639 cells; right, χ2=51.1, d.f.=7, p<0.0001, N=428 cells). Scale bar: 1 mm (A).DOI:http://dx.doi.org/10.7554/eLife.12401.022
Mentions: To test whether aox5+ airineme targeting is genetically labile, we screened zebrafish pigment pattern mutants and also re-examined the very few airinemes produced in pearl danio. As compared to wild-type zebrafish, we found that airinemes in spotted connexin41.8 (cx41.8; leopard) mutants (Maderspacher and Nusslein-Volhard, 2003; Watanabe et al., 2006) were later-appearing and more promiscuous, stabilizing as extensively on aox5+ cells as on melanophores (Figure 4D-right, 4F; Figure 4—figure supplement 4A,B; Video 15). Such differences could reflect acute morphogenetic interactions, perhaps dependent on connexin hemichannels, or chronic defects in differentiation, as xanthophores of presumptive cx41.8 mutants are reported to contain melanin and melanosome-like vesicles (Kirschbaum, 1975). Interestingly, the rare airinemes of pearl danio also stabilized on xanthophores though inspection cx41.8 sequence and expression did not reveal gross differences between zebrafish and pearl (Figure 4D-right; Video 16; and data not shown).Video 15.Altered airineme targeting altered by connexin mutation.

Bottom Line: Changes in gene activity are essential for evolutionary diversification.Projections depended on microfilaments and microtubules, exhibited meandering trajectories, and stabilized on target cells to which they delivered membraneous vesicles.By contrast, the uniformly patterned pearl danio lacked such projections, concomitant with Colony stimulating factor 1-dependent changes in xanthophore differentiation that likely curtail signaling available to melanophores.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Washington, Seattle, United States.

ABSTRACT
Changes in gene activity are essential for evolutionary diversification. Yet, elucidating the cellular behaviors that underlie modifications to adult form remains a profound challenge. We use neural crest-derived adult pigmentation of zebrafish and pearl danio to uncover cellular bases for alternative pattern states. We show that stripes in zebrafish require a novel class of thin, fast cellular projection to promote Delta-Notch signaling over long distances from cells of the xanthophore lineage to melanophores. Projections depended on microfilaments and microtubules, exhibited meandering trajectories, and stabilized on target cells to which they delivered membraneous vesicles. By contrast, the uniformly patterned pearl danio lacked such projections, concomitant with Colony stimulating factor 1-dependent changes in xanthophore differentiation that likely curtail signaling available to melanophores. Our study reveals a novel mechanism of cellular communication, roles for differentiation state heterogeneity in pigment cell interactions, and an unanticipated morphogenetic behavior contributing to a striking difference in adult form.

No MeSH data available.


Related in: MedlinePlus