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SUSD4 controls GLUA2 degradation, synaptic plasticity and motor learning

View ORCID ProfileI. González-Calvo, K. Iyer, M. Carquin, A. Khayachi, View ORCID ProfileF.A. Giuliani, J. Vincent, M. Séveno, S.M. Sigoillot, View ORCID ProfileM. Veleanu, S. Tahraoui, M. Albert, O. Vigy, C. Bosso-Lefèvre, Y. Nadjar, A. Dumoulin, View ORCID ProfileA. Triller, View ORCID ProfileJ.-L. Bessereau, View ORCID ProfileL. Rondi-Reig, P. Isope, View ORCID ProfileF. Selimi
doi: https://doi.org/10.1101/859587
I. González-Calvo
1Center for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France
2Institut de Neurosciences Cellulaires et Intégratives (INCI), CNRS, Université de Strasbourg, Strasbourg, France
8Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297, F-33000 Bordeaux, France
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K. Iyer
1Center for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France
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M. Carquin
1Center for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France
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A. Khayachi
1Center for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France
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F.A. Giuliani
2Institut de Neurosciences Cellulaires et Intégratives (INCI), CNRS, Université de Strasbourg, Strasbourg, France
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J. Vincent
3Institut Biology Paris Seine (IBPS), Neuroscience Paris Seine (NPS), CeZaMe, CNRS, Sorbonne University, INSERM, Paris, France
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M. Séveno
4BioCampus Montpellier, CNRS, INSERM, Université de Montpellier, Montpellier, France
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S.M. Sigoillot
1Center for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France
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M. Veleanu
1Center for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France
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S. Tahraoui
1Center for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France
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M. Albert
1Center for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France
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O. Vigy
5Institut de Génomique Fonctionnelle, CNRS, INSERM, Université de Montpellier, Montpellier, France
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C. Bosso-Lefèvre
1Center for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France
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Y. Nadjar
6École Normale Supérieure, Institut de Biologie de l’ENS, INSERM, CNRS, PSL Research University, Paris, France
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A. Dumoulin
6École Normale Supérieure, Institut de Biologie de l’ENS, INSERM, CNRS, PSL Research University, Paris, France
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A. Triller
6École Normale Supérieure, Institut de Biologie de l’ENS, INSERM, CNRS, PSL Research University, Paris, France
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J.-L. Bessereau
7Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5310, INSERM U 1217, Institut Neuromyogène, 69008, Lyon, France
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L. Rondi-Reig
3Institut Biology Paris Seine (IBPS), Neuroscience Paris Seine (NPS), CeZaMe, CNRS, Sorbonne University, INSERM, Paris, France
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P. Isope
2Institut de Neurosciences Cellulaires et Intégratives (INCI), CNRS, Université de Strasbourg, Strasbourg, France
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F. Selimi
1Center for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France
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  • For correspondence: fekrije.selimi@college-de-france.fr
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Summary

Fine control of protein stoichiometry at synapses underlies brain function and plasticity. How proteostasis is controlled independently for each type of synaptic protein in a synapse-specific and activity-dependent manner remains unclear. Here we show that SUSD4, a complement-related transmembrane protein, binds the AMPA receptor subunit GLUA2 and controls its activity-dependent degradation. Several proteins with known roles in the regulation of AMPA receptor turnover, in particular ubiquitin ligases of the NEDD4 subfamily, are identified as SUSD4 binding partners. SUSD4 is expressed by many neuronal populations starting at the time of synapse formation. Loss-of-function of Susd4 in the mouse prevents long-term depression at cerebellar synapses, and leads to impairment in motor coordination adaptation and learning. Our findings reveal that activity-dependent synaptic plasticity relies on a transmembrane CCP domain-containing protein that regulates the degradation of specific substrates. This mechanism potentially accounts for the role of SUSD4 mutations in neurodevelopmental diseases.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted December 16, 2020.
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SUSD4 controls GLUA2 degradation, synaptic plasticity and motor learning
I. González-Calvo, K. Iyer, M. Carquin, A. Khayachi, F.A. Giuliani, J. Vincent, M. Séveno, S.M. Sigoillot, M. Veleanu, S. Tahraoui, M. Albert, O. Vigy, C. Bosso-Lefèvre, Y. Nadjar, A. Dumoulin, A. Triller, J.-L. Bessereau, L. Rondi-Reig, P. Isope, F. Selimi
bioRxiv 859587; doi: https://doi.org/10.1101/859587
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SUSD4 controls GLUA2 degradation, synaptic plasticity and motor learning
I. González-Calvo, K. Iyer, M. Carquin, A. Khayachi, F.A. Giuliani, J. Vincent, M. Séveno, S.M. Sigoillot, M. Veleanu, S. Tahraoui, M. Albert, O. Vigy, C. Bosso-Lefèvre, Y. Nadjar, A. Dumoulin, A. Triller, J.-L. Bessereau, L. Rondi-Reig, P. Isope, F. Selimi
bioRxiv 859587; doi: https://doi.org/10.1101/859587

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