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Identification of a rudimentary neural crest in a non-vertebrate chordate.

Abitua PB, Wagner E, Navarrete IA, Levine M - Nature (2012)

Bottom Line: Neural crest arises at the neural plate border, expresses a core set of regulatory genes and produces a diverse array of cell types, including ectomesenchyme derivatives that elaborate the vertebrate head.Our results suggest that the neural crest melanocyte regulatory network pre-dated the divergence of tunicates and vertebrates.We propose that the co-option of mesenchyme determinants, such as Twist, into the neural plate ectoderm was crucial to the emergence of the vertebrate 'new head'.

View Article: PubMed Central - PubMed

Affiliation: Center for Integrative Genomics, Division of Genetics, Genomics and Development, Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, USA.

ABSTRACT
Neural crest arises at the neural plate border, expresses a core set of regulatory genes and produces a diverse array of cell types, including ectomesenchyme derivatives that elaborate the vertebrate head. The evolution of neural crest has been proposed to be a key event leading to the appearance of new cell types that fostered the transition from filter feeding to active predation in ancestral vertebrates. However, the origin of neural crest remains controversial, as homologous cell types have not been unambiguously identified in non-vertebrate chordates. Here we show that the tunicate Ciona intestinalis possesses a cephalic melanocyte lineage (a9.49) similar to neural crest that can be reprogrammed into migrating 'ectomesenchyme' by the targeted misexpression of Twist (also known as twist-like 2). Our results suggest that the neural crest melanocyte regulatory network pre-dated the divergence of tunicates and vertebrates. We propose that the co-option of mesenchyme determinants, such as Twist, into the neural plate ectoderm was crucial to the emergence of the vertebrate 'new head'.

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Wnt signaling promotes ocellus formationa, Gastrula stage schematic indicates the lineage specific expression of enhancers in this study. b, Tailbud electroporated with Mitf>LacZ detected with an antibody (green), and hybridized with a Wnt7 probe (red). c-f, Larvae electroporated with βγ-crystallin>GFP marks the otolith and anterior palps. c, Co-electroporated with Mitf>LacZ (166/196 had an otolith and ocellus). d, Co-electroporated with Mitf>Wnt7 (172/205 had two ocelli). e, Co-electroporated with Mitf>stable β-catenin (189/205 had two ocelli). f, Coelectroporated with Mitf>dnTCF (100/205 had two otoliths). g,h, Larvae electroporated with Zicl>Ets:VP16 and βγ-crystallin>GFP. g, Co-electroporated with Mitf>LacZ (75/100 had extra otoliths). h, Co-electroporated with Mitf>Wnt7 (only 11/100 had extra otoliths). Scale bars, 50 μm.
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Figure 1: Wnt signaling promotes ocellus formationa, Gastrula stage schematic indicates the lineage specific expression of enhancers in this study. b, Tailbud electroporated with Mitf>LacZ detected with an antibody (green), and hybridized with a Wnt7 probe (red). c-f, Larvae electroporated with βγ-crystallin>GFP marks the otolith and anterior palps. c, Co-electroporated with Mitf>LacZ (166/196 had an otolith and ocellus). d, Co-electroporated with Mitf>Wnt7 (172/205 had two ocelli). e, Co-electroporated with Mitf>stable β-catenin (189/205 had two ocelli). f, Coelectroporated with Mitf>dnTCF (100/205 had two otoliths). g,h, Larvae electroporated with Zicl>Ets:VP16 and βγ-crystallin>GFP. g, Co-electroporated with Mitf>LacZ (75/100 had extra otoliths). h, Co-electroporated with Mitf>Wnt7 (only 11/100 had extra otoliths). Scale bars, 50 μm.

Mentions: We present evidence that the a9.49 cell lineage of Ciona embryos represents a rudimentary neural crest. It arises at the neural plate border and expresses several neural plate border genes, as well as a number of neural crest specification genes, including Id, Snail, Ets, and FoxD8-13 (Fig. 1a, Supplementary Fig. 1). In vertebrates, Mitf directly activates several target genes required for melanogenesis of neural crest-derived melanocytes, including Tyr and TRP14. In tunicates, Mitf is expressed in the a9.49 lineage15, which can be labeled via electroporation of a Mitf reporter plasmid (Mitf>GFP) (Fig. 1b). The posterior daughters of the lineage (a10.97) intercalate at the dorsal midline and form the gravity-sensing otolith and melanocyte of the light detecting ocellus (Fig. 1c)16. We sought to understand the basis for the differential specification of these pigmented cells.


Identification of a rudimentary neural crest in a non-vertebrate chordate.

Abitua PB, Wagner E, Navarrete IA, Levine M - Nature (2012)

Wnt signaling promotes ocellus formationa, Gastrula stage schematic indicates the lineage specific expression of enhancers in this study. b, Tailbud electroporated with Mitf>LacZ detected with an antibody (green), and hybridized with a Wnt7 probe (red). c-f, Larvae electroporated with βγ-crystallin>GFP marks the otolith and anterior palps. c, Co-electroporated with Mitf>LacZ (166/196 had an otolith and ocellus). d, Co-electroporated with Mitf>Wnt7 (172/205 had two ocelli). e, Co-electroporated with Mitf>stable β-catenin (189/205 had two ocelli). f, Coelectroporated with Mitf>dnTCF (100/205 had two otoliths). g,h, Larvae electroporated with Zicl>Ets:VP16 and βγ-crystallin>GFP. g, Co-electroporated with Mitf>LacZ (75/100 had extra otoliths). h, Co-electroporated with Mitf>Wnt7 (only 11/100 had extra otoliths). Scale bars, 50 μm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4257486&req=5

Figure 1: Wnt signaling promotes ocellus formationa, Gastrula stage schematic indicates the lineage specific expression of enhancers in this study. b, Tailbud electroporated with Mitf>LacZ detected with an antibody (green), and hybridized with a Wnt7 probe (red). c-f, Larvae electroporated with βγ-crystallin>GFP marks the otolith and anterior palps. c, Co-electroporated with Mitf>LacZ (166/196 had an otolith and ocellus). d, Co-electroporated with Mitf>Wnt7 (172/205 had two ocelli). e, Co-electroporated with Mitf>stable β-catenin (189/205 had two ocelli). f, Coelectroporated with Mitf>dnTCF (100/205 had two otoliths). g,h, Larvae electroporated with Zicl>Ets:VP16 and βγ-crystallin>GFP. g, Co-electroporated with Mitf>LacZ (75/100 had extra otoliths). h, Co-electroporated with Mitf>Wnt7 (only 11/100 had extra otoliths). Scale bars, 50 μm.
Mentions: We present evidence that the a9.49 cell lineage of Ciona embryos represents a rudimentary neural crest. It arises at the neural plate border and expresses several neural plate border genes, as well as a number of neural crest specification genes, including Id, Snail, Ets, and FoxD8-13 (Fig. 1a, Supplementary Fig. 1). In vertebrates, Mitf directly activates several target genes required for melanogenesis of neural crest-derived melanocytes, including Tyr and TRP14. In tunicates, Mitf is expressed in the a9.49 lineage15, which can be labeled via electroporation of a Mitf reporter plasmid (Mitf>GFP) (Fig. 1b). The posterior daughters of the lineage (a10.97) intercalate at the dorsal midline and form the gravity-sensing otolith and melanocyte of the light detecting ocellus (Fig. 1c)16. We sought to understand the basis for the differential specification of these pigmented cells.

Bottom Line: Neural crest arises at the neural plate border, expresses a core set of regulatory genes and produces a diverse array of cell types, including ectomesenchyme derivatives that elaborate the vertebrate head.Our results suggest that the neural crest melanocyte regulatory network pre-dated the divergence of tunicates and vertebrates.We propose that the co-option of mesenchyme determinants, such as Twist, into the neural plate ectoderm was crucial to the emergence of the vertebrate 'new head'.

View Article: PubMed Central - PubMed

Affiliation: Center for Integrative Genomics, Division of Genetics, Genomics and Development, Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, USA.

ABSTRACT
Neural crest arises at the neural plate border, expresses a core set of regulatory genes and produces a diverse array of cell types, including ectomesenchyme derivatives that elaborate the vertebrate head. The evolution of neural crest has been proposed to be a key event leading to the appearance of new cell types that fostered the transition from filter feeding to active predation in ancestral vertebrates. However, the origin of neural crest remains controversial, as homologous cell types have not been unambiguously identified in non-vertebrate chordates. Here we show that the tunicate Ciona intestinalis possesses a cephalic melanocyte lineage (a9.49) similar to neural crest that can be reprogrammed into migrating 'ectomesenchyme' by the targeted misexpression of Twist (also known as twist-like 2). Our results suggest that the neural crest melanocyte regulatory network pre-dated the divergence of tunicates and vertebrates. We propose that the co-option of mesenchyme determinants, such as Twist, into the neural plate ectoderm was crucial to the emergence of the vertebrate 'new head'.

Show MeSH
Related in: MedlinePlus