Surfaceome dynamics reveal proteostasis-independent reorganization of neuronal surface proteins during development and synaptic plasticity

Marc Oostrum, Benjamin Campbell, Charlotte Seng, Maik Müller, Susanne Dieck, Jacqueline Hammer, Patrick G. A. Pedrioli, Csaba Földy, Shiva K. Tyagarajan and Bernd Wollscheid ()
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Marc Oostrum: Neuroscience Center Zurich
Benjamin Campbell: Neuroscience Center Zurich
Charlotte Seng: Neuroscience Center Zurich
Maik Müller: ETH Zurich
Susanne Dieck: Max Planck Institute for Brain Research
Jacqueline Hammer: ETH Zurich
Patrick G. A. Pedrioli: ETH Zurich
Csaba Földy: Neuroscience Center Zurich
Shiva K. Tyagarajan: Neuroscience Center Zurich
Bernd Wollscheid: Neuroscience Center Zurich

Nature Communications, 2020, vol. 11, issue 1, 1-16

Abstract: Abstract Neurons are highly compartmentalized cells with tightly controlled subcellular protein organization. While brain transcriptome, connectome and global proteome maps are being generated, system-wide analysis of temporal protein dynamics at the subcellular level are currently lacking. Here, we perform a temporally-resolved surfaceome analysis of primary neuron cultures and reveal dynamic surface protein clusters that reflect the functional requirements during distinct stages of neuronal development. Direct comparison of surface and total protein pools during development and homeostatic synaptic scaling demonstrates system-wide proteostasis-independent remodeling of the neuronal surface, illustrating widespread regulation on the level of surface trafficking. Finally, quantitative analysis of the neuronal surface during chemical long-term potentiation (cLTP) reveals fast externalization of diverse classes of surface proteins beyond the AMPA receptor, providing avenues to investigate the requirement of exocytosis for LTP. Our resource (neurosurfaceome.ethz.ch) highlights the importance of subcellular resolution for systems-level understanding of cellular processes.

Date: 2020
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DOI: 10.1038/s41467-020-18494-6

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