Puckered and JNK signaling in pioneer neurons coordinates the motor activity of the Drosophila embryo
Abstract Central nervous system organogenesis is a complex process that obeys precise architectural rules. The impact that nervous system architecture may have on its functionality remains, however, relatively unexplored. To clarify this problem, we analyze the development of the Drosophila embryoni...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-12-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-43783-1 |
| _version_ | 1797388224875724800 |
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| author | Katerina Karkali Samuel W. Vernon Richard A. Baines George Panayotou Enrique Martín-Blanco |
| author_facet | Katerina Karkali Samuel W. Vernon Richard A. Baines George Panayotou Enrique Martín-Blanco |
| author_sort | Katerina Karkali |
| collection | DOAJ |
| description | Abstract Central nervous system organogenesis is a complex process that obeys precise architectural rules. The impact that nervous system architecture may have on its functionality remains, however, relatively unexplored. To clarify this problem, we analyze the development of the Drosophila embryonic Ventral Nerve Cord (VNC). VNC morphogenesis requires the tight control of Jun kinase (JNK) signaling in a subset of pioneer neurons, exerted in part via a negative feedback loop mediated by the dual specificity phosphatase Puckered. Here we show that the JNK pathway autonomously regulates neuronal electrophysiological properties without affecting synaptic vesicle transport. Manipulating JNK signaling activity in pioneer neurons during early embryogenesis directly influences their function as organizers of VNC architecture and, moreover, uncovers a role in the coordination of the embryonic motor circuitry that is required for hatching. Together, our data reveal critical links, mediated by the control of the JNK signaling cascade by Puckered, between the structural organization of the VNC and its functional optimization. |
| first_indexed | 2024-03-08T22:36:42Z |
| format | Article |
| id | doaj.art-b866f92b75464a13a267f89280a79503 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-08T22:36:42Z |
| publishDate | 2023-12-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-b866f92b75464a13a267f89280a795032023-12-17T12:24:16ZengNature PortfolioNature Communications2041-17232023-12-0114111310.1038/s41467-023-43783-1Puckered and JNK signaling in pioneer neurons coordinates the motor activity of the Drosophila embryoKaterina Karkali0Samuel W. Vernon1Richard A. Baines2George Panayotou3Enrique Martín-Blanco4Instituto de Biología Molecular de Barcelona (CSIC), Parc Cientific de Barcelona, Baldiri Reixac 10-12Division of Neuroscience, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science CentreDivision of Neuroscience, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science CentreBSRC “Alexander Fleming”Instituto de Biología Molecular de Barcelona (CSIC), Parc Cientific de Barcelona, Baldiri Reixac 10-12Abstract Central nervous system organogenesis is a complex process that obeys precise architectural rules. The impact that nervous system architecture may have on its functionality remains, however, relatively unexplored. To clarify this problem, we analyze the development of the Drosophila embryonic Ventral Nerve Cord (VNC). VNC morphogenesis requires the tight control of Jun kinase (JNK) signaling in a subset of pioneer neurons, exerted in part via a negative feedback loop mediated by the dual specificity phosphatase Puckered. Here we show that the JNK pathway autonomously regulates neuronal electrophysiological properties without affecting synaptic vesicle transport. Manipulating JNK signaling activity in pioneer neurons during early embryogenesis directly influences their function as organizers of VNC architecture and, moreover, uncovers a role in the coordination of the embryonic motor circuitry that is required for hatching. Together, our data reveal critical links, mediated by the control of the JNK signaling cascade by Puckered, between the structural organization of the VNC and its functional optimization.https://doi.org/10.1038/s41467-023-43783-1 |
| spellingShingle | Katerina Karkali Samuel W. Vernon Richard A. Baines George Panayotou Enrique Martín-Blanco Puckered and JNK signaling in pioneer neurons coordinates the motor activity of the Drosophila embryo Nature Communications |
| title | Puckered and JNK signaling in pioneer neurons coordinates the motor activity of the Drosophila embryo |
| title_full | Puckered and JNK signaling in pioneer neurons coordinates the motor activity of the Drosophila embryo |
| title_fullStr | Puckered and JNK signaling in pioneer neurons coordinates the motor activity of the Drosophila embryo |
| title_full_unstemmed | Puckered and JNK signaling in pioneer neurons coordinates the motor activity of the Drosophila embryo |
| title_short | Puckered and JNK signaling in pioneer neurons coordinates the motor activity of the Drosophila embryo |
| title_sort | puckered and jnk signaling in pioneer neurons coordinates the motor activity of the drosophila embryo |
| url | https://doi.org/10.1038/s41467-023-43783-1 |
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