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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

Dependence of melanophore kita expression on airinemes and Notch signaling.(A) kita heterozygosity sensitized melanophores (means ± SE) for reduced Notch signaling [dnSu(H); t7=4.0, p<0.005] or airineme production (dnCdc42; t6=4.0, p<0.005). (B) Excess interstripe melanophores in kita heterozygotes compared to fish homozygous wild type for kita when Notch signaling or airinemes are inhibited. (C) kita expression (means ± SE) was reduced upon depletion of xanthophore lineage, Notch signaling or airinemes (one-tailed, paired t2=9.9, 7.6, 5.0; all p<0.05). (D) In pearl melanophores, Notch signaling (her6; Figure 5—figure supplement 1C) and kita expression (means ± SE) were reduced in comparison to zebrafish melanophores (one-tailed, paired t2=3.4, 3.4; p<0.05). Scale: 200 µm (B).DOI:http://dx.doi.org/10.7554/eLife.12401.035
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fig5s5: Dependence of melanophore kita expression on airinemes and Notch signaling.(A) kita heterozygosity sensitized melanophores (means ± SE) for reduced Notch signaling [dnSu(H); t7=4.0, p<0.005] or airineme production (dnCdc42; t6=4.0, p<0.005). (B) Excess interstripe melanophores in kita heterozygotes compared to fish homozygous wild type for kita when Notch signaling or airinemes are inhibited. (C) kita expression (means ± SE) was reduced upon depletion of xanthophore lineage, Notch signaling or airinemes (one-tailed, paired t2=9.9, 7.6, 5.0; all p<0.05). (D) In pearl melanophores, Notch signaling (her6; Figure 5—figure supplement 1C) and kita expression (means ± SE) were reduced in comparison to zebrafish melanophores (one-tailed, paired t2=3.4, 3.4; p<0.05). Scale: 200 µm (B).DOI:http://dx.doi.org/10.7554/eLife.12401.035

Mentions: Because amniote melanocytes and most melanophores require the Kit (Kita) receptor tyrosine kinase for migration and survival (Tan et al., 1990; Parichy et al., 1999; Rawls and Johnson, 2003; Wehrle-Haller, 2003; Budi et al., 2011), we further speculated that airineme-dependent Notch signaling might act through Kita to promote melanophore clearance. Consistent with this idea, we found that melanophores of fish heterozygous for a kita allele were sensitized to very low level induction of mitfa:Tet:dnSu(H) and aox5:Tet:dnCdc42 (Figure 5—figure supplement 5A,B). Abundances of kita transcript were also moderately reduced in melanophores, both in the absence of xanthophores and after inducing mitfa:Tet:dnSu(H) or aox5:Tet:dnCdc42 transgenes (Figure 5—figure supplement 5C). Indeed, melanophores of pearl danio, which migrate less than zebrafish (Quigley et al., 2005), exhibited similar reductions in Notch-responsive her6 and kita transcripts (Figure 5—figure supplement 5D).


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)

Dependence of melanophore kita expression on airinemes and Notch signaling.(A) kita heterozygosity sensitized melanophores (means ± SE) for reduced Notch signaling [dnSu(H); t7=4.0, p<0.005] or airineme production (dnCdc42; t6=4.0, p<0.005). (B) Excess interstripe melanophores in kita heterozygotes compared to fish homozygous wild type for kita when Notch signaling or airinemes are inhibited. (C) kita expression (means ± SE) was reduced upon depletion of xanthophore lineage, Notch signaling or airinemes (one-tailed, paired t2=9.9, 7.6, 5.0; all p<0.05). (D) In pearl melanophores, Notch signaling (her6; Figure 5—figure supplement 1C) and kita expression (means ± SE) were reduced in comparison to zebrafish melanophores (one-tailed, paired t2=3.4, 3.4; p<0.05). Scale: 200 µm (B).DOI:http://dx.doi.org/10.7554/eLife.12401.035
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4764569&req=5

fig5s5: Dependence of melanophore kita expression on airinemes and Notch signaling.(A) kita heterozygosity sensitized melanophores (means ± SE) for reduced Notch signaling [dnSu(H); t7=4.0, p<0.005] or airineme production (dnCdc42; t6=4.0, p<0.005). (B) Excess interstripe melanophores in kita heterozygotes compared to fish homozygous wild type for kita when Notch signaling or airinemes are inhibited. (C) kita expression (means ± SE) was reduced upon depletion of xanthophore lineage, Notch signaling or airinemes (one-tailed, paired t2=9.9, 7.6, 5.0; all p<0.05). (D) In pearl melanophores, Notch signaling (her6; Figure 5—figure supplement 1C) and kita expression (means ± SE) were reduced in comparison to zebrafish melanophores (one-tailed, paired t2=3.4, 3.4; p<0.05). Scale: 200 µm (B).DOI:http://dx.doi.org/10.7554/eLife.12401.035
Mentions: Because amniote melanocytes and most melanophores require the Kit (Kita) receptor tyrosine kinase for migration and survival (Tan et al., 1990; Parichy et al., 1999; Rawls and Johnson, 2003; Wehrle-Haller, 2003; Budi et al., 2011), we further speculated that airineme-dependent Notch signaling might act through Kita to promote melanophore clearance. Consistent with this idea, we found that melanophores of fish heterozygous for a kita allele were sensitized to very low level induction of mitfa:Tet:dnSu(H) and aox5:Tet:dnCdc42 (Figure 5—figure supplement 5A,B). Abundances of kita transcript were also moderately reduced in melanophores, both in the absence of xanthophores and after inducing mitfa:Tet:dnSu(H) or aox5:Tet:dnCdc42 transgenes (Figure 5—figure supplement 5C). Indeed, melanophores of pearl danio, which migrate less than zebrafish (Quigley et al., 2005), exhibited similar reductions in Notch-responsive her6 and kita transcripts (Figure 5—figure supplement 5D).

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