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Puckered and JNK signaling in pioneer neurons coordinates the motor activity of the Drosophila embryo

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  • Katerina Karkali

    (Instituto de Biología Molecular de Barcelona (CSIC), Parc Cientific de Barcelona, Baldiri Reixac 10-12
    BSRC “Alexander Fleming”)

  • Samuel W. Vernon

    (University of Manchester, Manchester Academic Health Science Centre
    Brain Mind Institute, EPFL – Swiss Federal Institute of Technology)

  • Richard A. Baines

    (University of Manchester, Manchester Academic Health Science Centre)

  • George Panayotou

    (BSRC “Alexander Fleming”)

  • Enrique Martín-Blanco

    (Instituto de Biología Molecular de Barcelona (CSIC), Parc Cientific de Barcelona, Baldiri Reixac 10-12)

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.

Suggested Citation

  • Katerina Karkali & Samuel W. Vernon & Richard A. Baines & George Panayotou & Enrique Martín-Blanco, 2023. "Puckered and JNK signaling in pioneer neurons coordinates the motor activity of the Drosophila embryo," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43783-1
    DOI: 10.1038/s41467-023-43783-1
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    References listed on IDEAS

    as
    1. Maximiliano L. Suster & Michael Bate, 2002. "Embryonic assembly of a central pattern generator without sensory input," Nature, Nature, vol. 416(6877), pages 174-178, March.
    2. Subhabrata Sanyal & David J. Sandstrom & Charles A. Hoeffer & Mani Ramaswami, 2002. "AP-1 functions upstream of CREB to control synaptic plasticity in Drosophila," Nature, Nature, vol. 416(6883), pages 870-874, April.
    3. Katerina Karkali & Timothy E. Saunders & George Panayotou & Enrique Martín-Blanco, 2023. "JNK signaling in pioneer neurons organizes ventral nerve cord architecture in Drosophila embryos," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Graeme W. Davis & Corey S. Goodman, 1998. "Synapse-specific control of synaptic efficacy at the terminals of a single neuron," Nature, Nature, vol. 392(6671), pages 82-86, March.
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