ATG9 resides on a unique population of small vesicles in presynaptic nerve 
terminals

Binotti, Beyenech; Ninov, Momchil; Cepeda, Andreia P.; Ganzella, Marcelo; Matti, U.; Riedel, Dietmar; Urlaub, Henning; Sambandan, Sivakumar; Jahn, Reinhard

doi:10.1080/15548627.2023.2274204

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ATG9 resides on a unique population of small vesicles in presynaptic nerve terminals

MPG-Autoren

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Binotti, Beyenech
Emeritus Group Laboratory of Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Ninov, Momchil
Emeritus Group Laboratory of Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;
Research Group of Bioanalytical Mass Spectrometry, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Cepeda, Andreia P.
Research Group of Bioanalytical Mass Spectrometry, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Ganzella, Marcelo
Emeritus Group Laboratory of Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Riedel, Dietmar
Facility for Transmission Electron Microscopy Fassberg Campus, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Urlaub, Henning
Research Group of Bioanalytical Mass Spectrometry, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Sambandan, Sivakumar
Emeritus Group Laboratory of Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Jahn, Reinhard
Emeritus Group Laboratory of Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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https://doi.org/10.1080/15548627.2023.2274204
(Verlagsversion)

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Zitation

Binotti, B., Ninov, M., Cepeda, A. P., Ganzella, M., Matti, U., Riedel, D., et al. (2024). ATG9 resides on a unique population of small vesicles in presynaptic nerve terminals. Autophagy, 20(4), 883-901. doi:10.1080/15548627.2023.2274204.

Zitierlink: https://hdl.handle.net/21.11116/0000-000E-2C72-1

Zusammenfassung

In neurons, autophagosome biogenesis occurs mainly in distal axons, followed by maturation during retrograde transport. Autophagosomal growth depends on the supply of membrane lipids which requires small vesicles containing ATG9, a lipid scramblase essential for macroautophagy/autophagy. Here, we show that ATG9-containing vesicles are enriched in synapses and resemble synaptic vesicles in size and density. The proteome of ATG9-containing vesicles immuno-isolated from nerve terminals showed conspicuously low levels of trafficking proteins except of the AP2-complex and some enzymes involved in endosomal phosphatidylinositol metabolism. Super resolution microscopy of nerve terminals and isolated vesicles revealed that ATG9-containing vesicles represent a distinct vesicle population with limited overlap not only with synaptic vesicles but also other membranes of the secretory pathway, uncovering a surprising heterogeneity in their membrane composition. Our results are compatible with the view that ATG9-containing vesicles function as lipid shuttles that scavenge membrane lipids from various intracellular membranes to support autophagosome biogenesis.