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Glial Draper signaling triggers cross-neuron plasticity in bystander neurons after neuronal cell death in Drosophila

Author

Listed:
  • Yupu Wang

    (University of Chicago
    University of Chicago
    Janelia Research Campus)

  • Ruiling Zhang

    (University of Chicago
    University of Chicago
    University of Chicago)

  • Sihao Huang

    (University of Chicago)

  • Parisa Tajalli Tehrani Valverde

    (University of Chicago
    University of Chicago
    University of Chicago)

  • Meike Lobb-Rabe

    (University of Chicago
    University of Chicago
    University of Chicago)

  • James Ashley

    (University of Chicago
    University of Chicago)

  • Lalanti Venkatasubramanian

    (University of Cambridge)

  • Robert A. Carrillo

    (University of Chicago
    University of Chicago
    University of Chicago
    University of Chicago)

Abstract

Neuronal cell death and subsequent brain dysfunction are hallmarks of aging and neurodegeneration, but how the nearby healthy neurons (bystanders) respond to the death of their neighbors is not fully understood. In the Drosophila larval neuromuscular system, bystander motor neurons can structurally and functionally compensate for the loss of their neighbors by increasing their terminal bouton number and activity. We term this compensation as cross-neuron plasticity, and in this study, we demonstrate that the Drosophila engulfment receptor, Draper, and the associated kinase, Shark, are required for cross-neuron plasticity. Overexpression of the Draper-I isoform boosts cross-neuron plasticity, implying that the strength of plasticity correlates with Draper signaling. In addition, we find that functional cross-neuron plasticity can be induced at different developmental stages. Our work uncovers a role for Draper signaling in cross-neuron plasticity and provides insights into how healthy bystander neurons respond to the loss of their neighboring neurons.

Suggested Citation

  • Yupu Wang & Ruiling Zhang & Sihao Huang & Parisa Tajalli Tehrani Valverde & Meike Lobb-Rabe & James Ashley & Lalanti Venkatasubramanian & Robert A. Carrillo, 2023. "Glial Draper signaling triggers cross-neuron plasticity in bystander neurons after neuronal cell death in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40142-y
    DOI: 10.1038/s41467-023-40142-y
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    References listed on IDEAS

    as
    1. Jennifer S. Ziegenfuss & Romi Biswas & Michelle A. Avery & Kyoungja Hong & Amy E. Sheehan & Yee-Guide Yeung & E. Richard Stanley & Marc R. Freeman, 2008. "Draper-dependent glial phagocytic activity is mediated by Src and Syk family kinase signalling," Nature, Nature, vol. 453(7197), pages 935-939, June.
    2. Johnna Doherty & Amy E Sheehan & Rachel Bradshaw & A Nicole Fox & Tsai-Yi Lu & Marc R Freeman, 2014. "PI3K Signaling and Stat92E Converge to Modulate Glial Responsiveness to Axonal Injury," PLOS Biology, Public Library of Science, vol. 12(11), pages 1-16, November.
    3. Tsai-Yi Lu & Jennifer M. MacDonald & Lukas J. Neukomm & Amy E. Sheehan & Rachel Bradshaw & Mary A. Logan & Marc R. Freeman, 2017. "Axon degeneration induces glial responses through Draper-TRAF4-JNK signalling," Nature Communications, Nature, vol. 8(1), pages 1-9, April.
    4. Maria D. Purice & Sean D. Speese & Mary A. Logan, 2016. "Delayed glial clearance of degenerating axons in aged Drosophila is due to reduced PI3K/Draper activity," Nature Communications, Nature, vol. 7(1), pages 1-13, November.
    5. Sarah D. Ackerman & Nelson A. Perez-Catalan & Marc R. Freeman & Chris Q. Doe, 2021. "Astrocytes close a motor circuit critical period," Nature, Nature, vol. 592(7854), pages 414-420, April.
    6. Pragya Goel & Dion Dickman, 2018. "Distinct homeostatic modulations stabilize reduced postsynaptic receptivity in response to presynaptic DLK signaling," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
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