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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

Delta-Notch gene expression and patterning consequences.(A) Delta genes dlc and delta-like 4 (dll4) are expressed by isolated xanthophores of zebrafish and pearl danio. csf1r, xanthophore lineage marker; actb1, actin b1. notch1a is expressed by melanophores of both species. pmela, melanophore lineage marker. Fins containing numerous cell types are positive controls. Preliminary surveys also revealed a variety of additional Delta-Notch ligands and receptors expressed by cells in skin and other tissues in the environment of pigment cells that were not expressed detectably in xanthophores or melanophores (data not shown). (B) Zebrafish expressing constitutively active Notch intracellular domain (NICD) in the melanophore lineage exhibited wider stripes (t8=5.4, p<0.001) yet ~30% fewer melanophores (t8=6.9, p<0.0001) than non-transgenic siblings. Dashed yellow lines, approximate dorsal- and ventral-most stripe boundaries. (C) Zebrafish dlc mutants have more interstripe melanophores than wild-type siblings (t9=4.8, p<0.001), though total melanophore numbers were not different (P=0.6). Dashed lines, approximate location boundaries of interstripe as determined for wild-type fish (see Materials and methods). Scale bar: 200 µm (in B, for A and B).DOI:http://dx.doi.org/10.7554/eLife.12401.031
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fig5s1: Delta-Notch gene expression and patterning consequences.(A) Delta genes dlc and delta-like 4 (dll4) are expressed by isolated xanthophores of zebrafish and pearl danio. csf1r, xanthophore lineage marker; actb1, actin b1. notch1a is expressed by melanophores of both species. pmela, melanophore lineage marker. Fins containing numerous cell types are positive controls. Preliminary surveys also revealed a variety of additional Delta-Notch ligands and receptors expressed by cells in skin and other tissues in the environment of pigment cells that were not expressed detectably in xanthophores or melanophores (data not shown). (B) Zebrafish expressing constitutively active Notch intracellular domain (NICD) in the melanophore lineage exhibited wider stripes (t8=5.4, p<0.001) yet ~30% fewer melanophores (t8=6.9, p<0.0001) than non-transgenic siblings. Dashed yellow lines, approximate dorsal- and ventral-most stripe boundaries. (C) Zebrafish dlc mutants have more interstripe melanophores than wild-type siblings (t9=4.8, p<0.001), though total melanophore numbers were not different (P=0.6). Dashed lines, approximate location boundaries of interstripe as determined for wild-type fish (see Materials and methods). Scale bar: 200 µm (in B, for A and B).DOI:http://dx.doi.org/10.7554/eLife.12401.031

Mentions: We sought to understand molecular bases for aox5+ airineme effects on melanophore patterning in zebrafish. A good candidate for mediating such interactions is Delta-Notch signaling. In amniotes, Notch promotes melanocyte migration and survival and also regulates differentiation (Moriyama et al., 2006; Schouwey et al., 2007; Aubin-Houzelstein et al., 2008; Kumano et al., 2008; Pinnix et al., 2009). In zebrafish as well as pearl danio, xanthophores express Delta genes whereas melanophores express Notch genes (Hamada et al., 2014) (Figure 5—figure supplement 1A). Consistent with a role for Notch in promoting melanophore migration, we found that expressing the constitutively active Notch1a intracellular domain in melanophores, using a promoter derived from the microphthalmia a (mitfa) gene (Lister et al., 1999), resulted in stripes that were significantly broader than in wild type (Figure 5—figure supplement 1B). Conversely, delta c (dlc) mutants exhibited melanophores ectopically in the interstripe, similar to the aox5:Tet:dnCdc42 phenotype (Figure 5—figure supplement 1C).


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)

Delta-Notch gene expression and patterning consequences.(A) Delta genes dlc and delta-like 4 (dll4) are expressed by isolated xanthophores of zebrafish and pearl danio. csf1r, xanthophore lineage marker; actb1, actin b1. notch1a is expressed by melanophores of both species. pmela, melanophore lineage marker. Fins containing numerous cell types are positive controls. Preliminary surveys also revealed a variety of additional Delta-Notch ligands and receptors expressed by cells in skin and other tissues in the environment of pigment cells that were not expressed detectably in xanthophores or melanophores (data not shown). (B) Zebrafish expressing constitutively active Notch intracellular domain (NICD) in the melanophore lineage exhibited wider stripes (t8=5.4, p<0.001) yet ~30% fewer melanophores (t8=6.9, p<0.0001) than non-transgenic siblings. Dashed yellow lines, approximate dorsal- and ventral-most stripe boundaries. (C) Zebrafish dlc mutants have more interstripe melanophores than wild-type siblings (t9=4.8, p<0.001), though total melanophore numbers were not different (P=0.6). Dashed lines, approximate location boundaries of interstripe as determined for wild-type fish (see Materials and methods). Scale bar: 200 µm (in B, for A and B).DOI:http://dx.doi.org/10.7554/eLife.12401.031
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Related In: Results  -  Collection

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fig5s1: Delta-Notch gene expression and patterning consequences.(A) Delta genes dlc and delta-like 4 (dll4) are expressed by isolated xanthophores of zebrafish and pearl danio. csf1r, xanthophore lineage marker; actb1, actin b1. notch1a is expressed by melanophores of both species. pmela, melanophore lineage marker. Fins containing numerous cell types are positive controls. Preliminary surveys also revealed a variety of additional Delta-Notch ligands and receptors expressed by cells in skin and other tissues in the environment of pigment cells that were not expressed detectably in xanthophores or melanophores (data not shown). (B) Zebrafish expressing constitutively active Notch intracellular domain (NICD) in the melanophore lineage exhibited wider stripes (t8=5.4, p<0.001) yet ~30% fewer melanophores (t8=6.9, p<0.0001) than non-transgenic siblings. Dashed yellow lines, approximate dorsal- and ventral-most stripe boundaries. (C) Zebrafish dlc mutants have more interstripe melanophores than wild-type siblings (t9=4.8, p<0.001), though total melanophore numbers were not different (P=0.6). Dashed lines, approximate location boundaries of interstripe as determined for wild-type fish (see Materials and methods). Scale bar: 200 µm (in B, for A and B).DOI:http://dx.doi.org/10.7554/eLife.12401.031
Mentions: We sought to understand molecular bases for aox5+ airineme effects on melanophore patterning in zebrafish. A good candidate for mediating such interactions is Delta-Notch signaling. In amniotes, Notch promotes melanocyte migration and survival and also regulates differentiation (Moriyama et al., 2006; Schouwey et al., 2007; Aubin-Houzelstein et al., 2008; Kumano et al., 2008; Pinnix et al., 2009). In zebrafish as well as pearl danio, xanthophores express Delta genes whereas melanophores express Notch genes (Hamada et al., 2014) (Figure 5—figure supplement 1A). Consistent with a role for Notch in promoting melanophore migration, we found that expressing the constitutively active Notch1a intracellular domain in melanophores, using a promoter derived from the microphthalmia a (mitfa) gene (Lister et al., 1999), resulted in stripes that were significantly broader than in wild type (Figure 5—figure supplement 1B). Conversely, delta c (dlc) mutants exhibited melanophores ectopically in the interstripe, similar to the aox5:Tet:dnCdc42 phenotype (Figure 5—figure supplement 1C).

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