Unconventional secretory processing diversifies neuronal ion channel properties

Hanus, Cyril; Geptin, Helene; Tushev, Georgi; Garg, Sakshi; Alvarez-Castelao, Beatriz; Sambandan, Sivakumar; Kochen, Lisa; Hafner, Anne-Sophie; Langer, Julian David; Schuman, Erin Margaret

doi:10.7554/eLife.20609

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Unconventional secretory processing diversifies neuronal ion channel properties

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Hanus, Cyril
Synaptic Plasticity Department, Max Planck Institute for Brain Research, Max Planck Society;

Geptin, Helene
Synaptic Plasticity Department, Max Planck Institute for Brain Research, Max Planck Society;

Tushev, Georgi
Synaptic Plasticity Department, Max Planck Institute for Brain Research, Max Planck Society;

Garg, Sakshi
Synaptic Plasticity Department, Max Planck Institute for Brain Research, Max Planck Society;

Alvarez-Castelao, Beatriz
Synaptic Plasticity Department, Max Planck Institute for Brain Research, Max Planck Society;

Sambandan, Sivakumar
Synaptic Plasticity Department, Max Planck Institute for Brain Research, Max Planck Society;

Kochen, Lisa
Synaptic Plasticity Department, Max Planck Institute for Brain Research, Max Planck Society;

Hafner, Anne-Sophie
Synaptic Plasticity Department, Max Planck Institute for Brain Research, Max Planck Society;

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Langer, Julian David
Synaptic Plasticity Department, Max Planck Institute for Brain Research, Max Planck Society;
Department of Molecular Membrane Biology, Max Planck Institute of Biophysics, Max Planck Society;

Schuman, Erin Margaret
Synaptic Plasticity Department, Max Planck Institute for Brain Research, Max Planck Society;

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Citation

Hanus, C., Geptin, H., Tushev, G., Garg, S., Alvarez-Castelao, B., Sambandan, S., et al. (2016). Unconventional secretory processing diversifies neuronal ion channel properties. eLife, 5: e20609. doi:10.7554/eLife.20609.

Cite as: https://hdl.handle.net/21.11116/0000-0007-9074-3

Abstract

N-glycosylation - the sequential addition of complex sugars to adhesion proteins, neurotransmitter receptors, ion channels and secreted trophic factors as they progress through the endoplasmic reticulum and the Golgi apparatus - is one of the most frequent protein modifications. In mammals, most organ-specific N-glycosylation events occur in the brain. Yet, little is known about the nature, function and regulation of N-glycosylation in neurons. Using imaging, quantitative immunoblotting and mass spectrometry, we show that hundreds of neuronal surface membrane proteins are core-glycosylated, resulting in the neuronal membrane displaying surprisingly high levels of glycosylation profiles that are classically associated with immature intracellular proteins. We report that while N-glycosylation is generally required for dendritic development and glutamate receptor surface expression, core-glycosylated proteins are sufficient to sustain these processes, and are thus functional. This atypical glycosylation of surface neuronal proteins can be attributed to a bypass or a hypo-function of the Golgi apparatus. Core-glycosylation is regulated by synaptic activity, modulates synaptic signaling and accelerates the turnover of GluA2-containing glutamate receptors, revealing a novel mechanism that controls the composition and sensing properties of the neuronal membrane.