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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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Twist reprograms the a9.49 lineagea, Neurula hybridized with a Twist probe. b, Tailbud during mesenchyme migration (arrows) co-electroporated with Twist>GFP and Twist>H2B mCherry.c,d, Larvae electroporated with Mitf>GFP, and Mitf>H2B mCherry. Insets show lineage marked with Tyr>mCherry, and Tyr>H2B YFP.c, Co-electroporated with Mitf>LacZ. # and * mark the otolith and ocellus, respectively. d, Co-electroporated with Mitf>Twist. Arrowheads indicate ectopic position of a9.49 derivatives. e,f, Juveniles electroporated Tyr>mCherry, and Tyr>H2B YFP. Arrows indentify the position of a9.49 derivatives. e, Co-electroporated with Mitf>LacZ.f, Coelectroporated with Mitf>Twist. Scale bars, 50 μm.
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Figure 3: Twist reprograms the a9.49 lineagea, Neurula hybridized with a Twist probe. b, Tailbud during mesenchyme migration (arrows) co-electroporated with Twist>GFP and Twist>H2B mCherry.c,d, Larvae electroporated with Mitf>GFP, and Mitf>H2B mCherry. Insets show lineage marked with Tyr>mCherry, and Tyr>H2B YFP.c, Co-electroporated with Mitf>LacZ. # and * mark the otolith and ocellus, respectively. d, Co-electroporated with Mitf>Twist. Arrowheads indicate ectopic position of a9.49 derivatives. e,f, Juveniles electroporated Tyr>mCherry, and Tyr>H2B YFP. Arrows indentify the position of a9.49 derivatives. e, Co-electroporated with Mitf>LacZ.f, Coelectroporated with Mitf>Twist. Scale bars, 50 μm.

Mentions: There are three Twist-related genes in Ciona. In this study we focused on the one most similar to Twist1 in vertebrates (Supplementary Fig. 5). In Ciona, Twist is expressed solely in mesoderm-derived mesenchyme (Fig. 3a). It is not expressed in any region of the neural plate, including the a9.49 lineage. Twist-expressing mesoderm undergoes long-range migration (Fig. 3b) and produces a number of diverse tissues in juveniles and adults, including body wall muscles, tunic cells (which populate the protective covering of the adult), and blood cells25. The migration and differentiation of these mesoderm tissues are inhibited when Twist expression is reduced25.


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

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

Twist reprograms the a9.49 lineagea, Neurula hybridized with a Twist probe. b, Tailbud during mesenchyme migration (arrows) co-electroporated with Twist>GFP and Twist>H2B mCherry.c,d, Larvae electroporated with Mitf>GFP, and Mitf>H2B mCherry. Insets show lineage marked with Tyr>mCherry, and Tyr>H2B YFP.c, Co-electroporated with Mitf>LacZ. # and * mark the otolith and ocellus, respectively. d, Co-electroporated with Mitf>Twist. Arrowheads indicate ectopic position of a9.49 derivatives. e,f, Juveniles electroporated Tyr>mCherry, and Tyr>H2B YFP. Arrows indentify the position of a9.49 derivatives. e, Co-electroporated with Mitf>LacZ.f, Coelectroporated with Mitf>Twist. Scale bars, 50 μm.
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Figure 3: Twist reprograms the a9.49 lineagea, Neurula hybridized with a Twist probe. b, Tailbud during mesenchyme migration (arrows) co-electroporated with Twist>GFP and Twist>H2B mCherry.c,d, Larvae electroporated with Mitf>GFP, and Mitf>H2B mCherry. Insets show lineage marked with Tyr>mCherry, and Tyr>H2B YFP.c, Co-electroporated with Mitf>LacZ. # and * mark the otolith and ocellus, respectively. d, Co-electroporated with Mitf>Twist. Arrowheads indicate ectopic position of a9.49 derivatives. e,f, Juveniles electroporated Tyr>mCherry, and Tyr>H2B YFP. Arrows indentify the position of a9.49 derivatives. e, Co-electroporated with Mitf>LacZ.f, Coelectroporated with Mitf>Twist. Scale bars, 50 μm.
Mentions: There are three Twist-related genes in Ciona. In this study we focused on the one most similar to Twist1 in vertebrates (Supplementary Fig. 5). In Ciona, Twist is expressed solely in mesoderm-derived mesenchyme (Fig. 3a). It is not expressed in any region of the neural plate, including the a9.49 lineage. Twist-expressing mesoderm undergoes long-range migration (Fig. 3b) and produces a number of diverse tissues in juveniles and adults, including body wall muscles, tunic cells (which populate the protective covering of the adult), and blood cells25. The migration and differentiation of these mesoderm tissues are inhibited when Twist expression is reduced25.

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