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LC3-associated phagocytosis promotes glial degradation of axon debris after injury in Drosophila models

Author

Listed:
  • Áron Szabó

    (Institute of Genetics, Eötvös Loránd Research Network (ELKH))

  • Virág Vincze

    (Institute of Genetics, Eötvös Loránd Research Network (ELKH))

  • Aishwarya Sanjay Chhatre

    (Institute of Genetics, Eötvös Loránd Research Network (ELKH)
    University of Szeged)

  • András Jipa

    (Institute of Genetics, Eötvös Loránd Research Network (ELKH))

  • Sarolta Bognár

    (Institute of Genetics, Eötvös Loránd Research Network (ELKH))

  • Katalin Eszter Varga

    (Institute of Genetics, Eötvös Loránd Research Network (ELKH))

  • Poulami Banik

    (Institute of Genetics, Eötvös Loránd Research Network (ELKH))

  • Adél Harmatos-Ürmösi

    (Institute of Genetics, Eötvös Loránd Research Network (ELKH))

  • Lukas J. Neukomm

    (University of Lausanne)

  • Gábor Juhász

    (Institute of Genetics, Eötvös Loránd Research Network (ELKH)
    Eötvös Loránd University)

Abstract

Glial engulfment of neuron-derived debris after trauma, during development, and in neurodegenerative diseases supports nervous system functions. However, mechanisms governing the efficiency of debris degradation in glia have remained largely unexplored. Here we show that LC3-associated phagocytosis (LAP), an engulfment pathway assisted by certain autophagy factors, promotes glial phagosome maturation in the Drosophila wing nerve. A LAP-specific subset of autophagy-related genes is required in glia for axon debris clearance, encoding members of the Atg8a (LC3) conjugation system and the Vps34 lipid kinase complex including UVRAG and Rubicon. Phagosomal Rubicon and Atg16 WD40 domain-dependent conjugation of Atg8a mediate proper breakdown of internalized axon fragments, and Rubicon overexpression in glia accelerates debris elimination. Finally, LAP promotes survival following traumatic brain injury. Our results reveal a role of glial LAP in the clearance of neuronal debris in vivo, with potential implications for the recovery of the injured nervous system.

Suggested Citation

  • Áron Szabó & Virág Vincze & Aishwarya Sanjay Chhatre & András Jipa & Sarolta Bognár & Katalin Eszter Varga & Poulami Banik & Adél Harmatos-Ürmösi & Lukas J. Neukomm & Gábor Juhász, 2023. "LC3-associated phagocytosis promotes glial degradation of axon debris after injury in Drosophila models," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38755-4
    DOI: 10.1038/s41467-023-38755-4
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    References listed on IDEAS

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    1. Shuhei Nakamura & Masaki Oba & Mari Suzuki & Atsushi Takahashi & Tadashi Yamamuro & Mari Fujiwara & Kensuke Ikenaka & Satoshi Minami & Namine Tabata & Kenichi Yamamoto & Sayaka Kubo & Ayaka Tokumura &, 2019. "Suppression of autophagic activity by Rubicon is a signature of aging," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    2. 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.
    3. Tian Zhou & Yuxin Li & Xiaoyu Li & Fanzhuo Zeng & Yanxia Rao & Yang He & Yafei Wang & Meizhen Liu & Dali Li & Zhen Xu & Xin Zhou & Siling Du & Fugui Niu & Jiyun Peng & Xifan Mei & Sheng-Jian Ji & Yous, 2022. "Microglial debris is cleared by astrocytes via C4b-facilitated phagocytosis and degraded via RUBICON-dependent noncanonical autophagy in mice," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    4. Anuradha Bhukel & Christine Brigitte Beuschel & Marta Maglione & Martin Lehmann & Gabor Juhász & Frank Madeo & Stephan J. Sigrist, 2019. "Autophagy within the mushroom body protects from synapse aging in a non-cell autonomous manner," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
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