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Multiomics of synaptic junctions reveals altered lipid metabolism and signaling following environmental enrichment

M. Borgmeyer, C. Coman, C. Has, HF. Schött, T. Li, P. Westhoff, YFH. Cheung, N. Hoffmann, P. Yuanxiang, T. Behnisch, GM. Gomes, M. Dumenieu, M. Schweizer, M. Chocholoušková, M. Holčapek, M. Mikhaylova, MR. Kreutz, R. Ahrends

. 2021 ; 37 (1) : 109797. [pub] 20211005

Language English Country United States

Document type Journal Article, Research Support, Non-U.S. Gov't

Persistent link   https://www.medvik.cz/link/bmc22012112

Membrane lipids and their metabolism have key functions in neurotransmission. Here we provide a quantitative lipid inventory of mouse and rat synaptic junctions. To this end, we developed a multiomics extraction and analysis workflow to probe the interplay of proteins and lipids in synaptic signal transduction from the same sample. Based on this workflow, we generate hypotheses about novel mechanisms underlying complex changes in synaptic connectivity elicited by environmental stimuli. As a proof of principle, this approach reveals that in mice exposed to an enriched environment, reduced endocannabinoid synthesis and signaling is linked to increased surface expression of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) in a subset of Cannabinoid-receptor 1 positive synapses. This mechanism regulates synaptic strength in an input-specific manner. Thus, we establish a compartment-specific multiomics workflow that is suitable to extract information from complex lipid and protein networks involved in synaptic function and plasticity.

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$a Multiomics of synaptic junctions reveals altered lipid metabolism and signaling following environmental enrichment / $c M. Borgmeyer, C. Coman, C. Has, HF. Schött, T. Li, P. Westhoff, YFH. Cheung, N. Hoffmann, P. Yuanxiang, T. Behnisch, GM. Gomes, M. Dumenieu, M. Schweizer, M. Chocholoušková, M. Holčapek, M. Mikhaylova, MR. Kreutz, R. Ahrends
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$a Membrane lipids and their metabolism have key functions in neurotransmission. Here we provide a quantitative lipid inventory of mouse and rat synaptic junctions. To this end, we developed a multiomics extraction and analysis workflow to probe the interplay of proteins and lipids in synaptic signal transduction from the same sample. Based on this workflow, we generate hypotheses about novel mechanisms underlying complex changes in synaptic connectivity elicited by environmental stimuli. As a proof of principle, this approach reveals that in mice exposed to an enriched environment, reduced endocannabinoid synthesis and signaling is linked to increased surface expression of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) in a subset of Cannabinoid-receptor 1 positive synapses. This mechanism regulates synaptic strength in an input-specific manner. Thus, we establish a compartment-specific multiomics workflow that is suitable to extract information from complex lipid and protein networks involved in synaptic function and plasticity.
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$a Coman, Cristina $u Leibniz-Institut für Analytische Wissenschaften-ISAS-e.V., 44227 Dortmund, Germany; Department of Analytical Chemistry, Faculty of Chemistry, University of Vienna, 1090 Wien, Austria
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$a Has, Canan $u Leibniz-Institut für Analytische Wissenschaften-ISAS-e.V., 44227 Dortmund, Germany
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$a Schött, Hans-Frieder $u Leibniz-Institut für Analytische Wissenschaften-ISAS-e.V., 44227 Dortmund, Germany
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$a Li, Tingting $u Leibniz-Institut für Analytische Wissenschaften-ISAS-e.V., 44227 Dortmund, Germany
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$a Westhoff, Philipp $u Leibniz-Institut für Analytische Wissenschaften-ISAS-e.V., 44227 Dortmund, Germany
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$a Cheung, Yam F H $u Leibniz-Institut für Analytische Wissenschaften-ISAS-e.V., 44227 Dortmund, Germany
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$a Hoffmann, Nils $u Leibniz-Institut für Analytische Wissenschaften-ISAS-e.V., 44227 Dortmund, Germany
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$a Yuanxiang, PingAn $u RG Neuroplasticity, Leibniz Institute for Neurobiology, 39118 Magdeburg, Germany
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$a Behnisch, Thomas $u Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and MOE Frontiers Center for Brain Science, Fudan University, Shanghai 200032, China
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$a Gomes, Guilherme M $u RG Neuroplasticity, Leibniz Institute for Neurobiology, 39118 Magdeburg, Germany
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$a Dumenieu, Mael $u RG Neuroplasticity, Leibniz Institute for Neurobiology, 39118 Magdeburg, Germany
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$a Schweizer, Michaela $u Morphology and Electron Microscopy, University Medical Center Hamburg-Eppendorf, Center for Molecular Neurobiology, ZMNH, 20251 Hamburg, Germany
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$a Chocholoušková, Michaela $u University of Pardubice, Department of Analytical Chemistry, CZ-532 10 Pardubice, Czech Republic
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$a Holčapek, Michal $u University of Pardubice, Department of Analytical Chemistry, CZ-532 10 Pardubice, Czech Republic
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$a Mikhaylova, Marina $u Emmy Noether Group 'Neuronal Protein Transport,' University Medical Center Hamburg-Eppendorf, Center for Molecular Neurobiology, ZMNH, 20251 Hamburg, Germany; AG Optobiology, Institute for Biology, Humboldt Universität zu Berlin, 10115 Berlin, Germany
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$a Kreutz, Michael R $u Leibniz Group 'Dendritic Organelles and Synaptic Function,' University Medical Center Hamburg-Eppendorf, Center for Molecular Neurobiology, ZMNH, 20251 Hamburg, Germany; RG Neuroplasticity, Leibniz Institute for Neurobiology, 39118 Magdeburg, Germany; German Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany; Center for Behavioral Brain Sciences, 30120 Magdeburg, Germany. Electronic address: michael.kreutz@zmnh.uni-hamburg.de
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$a Ahrends, Robert $u Leibniz-Institut für Analytische Wissenschaften-ISAS-e.V., 44227 Dortmund, Germany; Department of Analytical Chemistry, Faculty of Chemistry, University of Vienna, 1090 Wien, Austria. Electronic address: robert.ahrends@univie.ac.at
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