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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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Lineage tracing of reprogrammed a9.49 cellsa-f, Ciona electroporated with Mitf>Twist and Tyr>Kaede. a,b, Non-UV treated tailbud shows only green fluorescence c, Embryo never exposed to UV results in a juvenile with only green ectopic cells (arrows). d,e, UV treated tailbud shows green and red fluorescence respectively. f, UV treated embryo results in a juvenile with green and red ectopic cells (arrows). g, Time-lapse frames of Supplemental Movie 2 (minutes indicated) shows the migration of reprogrammed a9.49 cell labeled with Tyr>mCherry (arrowhead). Scale bars, 50 μm.
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Figure 4: Lineage tracing of reprogrammed a9.49 cellsa-f, Ciona electroporated with Mitf>Twist and Tyr>Kaede. a,b, Non-UV treated tailbud shows only green fluorescence c, Embryo never exposed to UV results in a juvenile with only green ectopic cells (arrows). d,e, UV treated tailbud shows green and red fluorescence respectively. f, UV treated embryo results in a juvenile with green and red ectopic cells (arrows). g, Time-lapse frames of Supplemental Movie 2 (minutes indicated) shows the migration of reprogrammed a9.49 cell labeled with Tyr>mCherry (arrowhead). Scale bars, 50 μm.

Mentions: Additional evidence for the reprogramming of the a9.49 lineage was obtained with Kaede, a photoconvertible fluorescent protein that was previously used in Ciona to trace the formation of the CNS27. Here, embryos were co-electroporated with Mitf>Twist and Tyr>Kaede, which mediate expression in the a9.49 lineage (Fig. 4a). Tailbud embryos that were not exposed to UV light show no red fluorescence (Fig. 4b) and result in juveniles that have only green a9.49 descendants (Fig. 4c). In contrast, tailbud embryos treated with UV (Fig. 4d, e) develop into juveniles that display red cells throughout the body. Control juveniles lacking Mitf>Twist exhibit the expected expression solely in the CNS (Supplementary Fig. 10). Finally, time-lapse microscopy was used to examine the Mitf>Twist expressing cells in juveniles. Some of these cells migrate like the normal tunic cells derived from the mesenchyme (Fig. 4g, Supplementary Movie 2). Thus, the misexpression of Twist appears to be sufficient, in part, to reprogram the a9.49 lineage into ectomesenchyme.


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

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

Lineage tracing of reprogrammed a9.49 cellsa-f, Ciona electroporated with Mitf>Twist and Tyr>Kaede. a,b, Non-UV treated tailbud shows only green fluorescence c, Embryo never exposed to UV results in a juvenile with only green ectopic cells (arrows). d,e, UV treated tailbud shows green and red fluorescence respectively. f, UV treated embryo results in a juvenile with green and red ectopic cells (arrows). g, Time-lapse frames of Supplemental Movie 2 (minutes indicated) shows the migration of reprogrammed a9.49 cell labeled with Tyr>mCherry (arrowhead). Scale bars, 50 μm.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 4: Lineage tracing of reprogrammed a9.49 cellsa-f, Ciona electroporated with Mitf>Twist and Tyr>Kaede. a,b, Non-UV treated tailbud shows only green fluorescence c, Embryo never exposed to UV results in a juvenile with only green ectopic cells (arrows). d,e, UV treated tailbud shows green and red fluorescence respectively. f, UV treated embryo results in a juvenile with green and red ectopic cells (arrows). g, Time-lapse frames of Supplemental Movie 2 (minutes indicated) shows the migration of reprogrammed a9.49 cell labeled with Tyr>mCherry (arrowhead). Scale bars, 50 μm.
Mentions: Additional evidence for the reprogramming of the a9.49 lineage was obtained with Kaede, a photoconvertible fluorescent protein that was previously used in Ciona to trace the formation of the CNS27. Here, embryos were co-electroporated with Mitf>Twist and Tyr>Kaede, which mediate expression in the a9.49 lineage (Fig. 4a). Tailbud embryos that were not exposed to UV light show no red fluorescence (Fig. 4b) and result in juveniles that have only green a9.49 descendants (Fig. 4c). In contrast, tailbud embryos treated with UV (Fig. 4d, e) develop into juveniles that display red cells throughout the body. Control juveniles lacking Mitf>Twist exhibit the expected expression solely in the CNS (Supplementary Fig. 10). Finally, time-lapse microscopy was used to examine the Mitf>Twist expressing cells in juveniles. Some of these cells migrate like the normal tunic cells derived from the mesenchyme (Fig. 4g, Supplementary Movie 2). Thus, the misexpression of Twist appears to be sufficient, in part, to reprogram the a9.49 lineage into ectomesenchyme.

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