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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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FoxD represses Mitf in the ocellusa, Tailbud electroporated with TRP>LacZ detected with an antibody (green) marking the precursors of the otolith and ocellus, and hybridized with a FoxD probe (red). b, FoxD is expressed in the posterior a10.97 cell. c-d, Tailbuds electroporated with FoxD>mCherry and Mitf>GFP. Arrowheads mark the presumptive ocellus. c, Co-electroporated with Mitf>LacZ (126/180 expressed mCherry). d, Co-electroporated with Mitf>dnTCF (only 30/180 expressed mCherry). e-f, Tailbuds electroporated with Msx>H2B mCherry, and Mitf>GFP. Arrowhead shows GFP expression in a9.49 derivatives. e, Co-electroporated with Msx>LacZ.f, Co-electroporated with Msx>FoxD N-term. Scale bars 50 μm (a, c-f); 25 μm (b).
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Figure 2: FoxD represses Mitf in the ocellusa, Tailbud electroporated with TRP>LacZ detected with an antibody (green) marking the precursors of the otolith and ocellus, and hybridized with a FoxD probe (red). b, FoxD is expressed in the posterior a10.97 cell. c-d, Tailbuds electroporated with FoxD>mCherry and Mitf>GFP. Arrowheads mark the presumptive ocellus. c, Co-electroporated with Mitf>LacZ (126/180 expressed mCherry). d, Co-electroporated with Mitf>dnTCF (only 30/180 expressed mCherry). e-f, Tailbuds electroporated with Msx>H2B mCherry, and Mitf>GFP. Arrowhead shows GFP expression in a9.49 derivatives. e, Co-electroporated with Msx>LacZ.f, Co-electroporated with Msx>FoxD N-term. Scale bars 50 μm (a, c-f); 25 μm (b).

Mentions: In vertebrates, Foxd3 has been shown to repress melanogenesis of neural crest cells via downregulation of Mitf14,18. In Ciona, FoxD is directly activated by the accumulation of nuclear β-catenin in the early embryo, indicating a potential link between Wnt signaling and FoxD expression19. We found that FoxD is selectively expressed in the presumptive ocellus, (Fig. 2a, b) adjacent to the expression of Wnt7 in the dorsal midline (Fig. 1b). A FoxD enhancer recapitulates this expression in the presumptive ocellus (Fig. 2c), and is dependent on Wnt signaling, as expression is lost in the presence of dnTCF (Fig. 2d).


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

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

FoxD represses Mitf in the ocellusa, Tailbud electroporated with TRP>LacZ detected with an antibody (green) marking the precursors of the otolith and ocellus, and hybridized with a FoxD probe (red). b, FoxD is expressed in the posterior a10.97 cell. c-d, Tailbuds electroporated with FoxD>mCherry and Mitf>GFP. Arrowheads mark the presumptive ocellus. c, Co-electroporated with Mitf>LacZ (126/180 expressed mCherry). d, Co-electroporated with Mitf>dnTCF (only 30/180 expressed mCherry). e-f, Tailbuds electroporated with Msx>H2B mCherry, and Mitf>GFP. Arrowhead shows GFP expression in a9.49 derivatives. e, Co-electroporated with Msx>LacZ.f, Co-electroporated with Msx>FoxD N-term. Scale bars 50 μm (a, c-f); 25 μm (b).
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Related In: Results  -  Collection

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

Figure 2: FoxD represses Mitf in the ocellusa, Tailbud electroporated with TRP>LacZ detected with an antibody (green) marking the precursors of the otolith and ocellus, and hybridized with a FoxD probe (red). b, FoxD is expressed in the posterior a10.97 cell. c-d, Tailbuds electroporated with FoxD>mCherry and Mitf>GFP. Arrowheads mark the presumptive ocellus. c, Co-electroporated with Mitf>LacZ (126/180 expressed mCherry). d, Co-electroporated with Mitf>dnTCF (only 30/180 expressed mCherry). e-f, Tailbuds electroporated with Msx>H2B mCherry, and Mitf>GFP. Arrowhead shows GFP expression in a9.49 derivatives. e, Co-electroporated with Msx>LacZ.f, Co-electroporated with Msx>FoxD N-term. Scale bars 50 μm (a, c-f); 25 μm (b).
Mentions: In vertebrates, Foxd3 has been shown to repress melanogenesis of neural crest cells via downregulation of Mitf14,18. In Ciona, FoxD is directly activated by the accumulation of nuclear β-catenin in the early embryo, indicating a potential link between Wnt signaling and FoxD expression19. We found that FoxD is selectively expressed in the presumptive ocellus, (Fig. 2a, b) adjacent to the expression of Wnt7 in the dorsal midline (Fig. 1b). A FoxD enhancer recapitulates this expression in the presumptive ocellus (Fig. 2c), and is dependent on Wnt signaling, as expression is lost in the presence of dnTCF (Fig. 2d).

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