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A synaptomic analysis reveals dopamine hub synapses in the mouse striatum

Author

Listed:
  • Vincent Paget-Blanc

    (Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297)

  • Marlene E. Pfeffer

    (Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297)

  • Marie Pronot

    (Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297)

  • Paul Lapios

    (Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297)

  • Maria-Florencia Angelo

    (Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297)

  • Roman Walle

    (Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286)

  • Fabrice P. Cordelières

    (Univ. Bordeaux, CNRS, INSERM, Bordeaux Imaging Center, BIC, UAR 3420, US 4)

  • Florian Levet

    (Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297
    Univ. Bordeaux, CNRS, INSERM, Bordeaux Imaging Center, BIC, UAR 3420, US 4)

  • Stéphane Claverol

    (Univ. Bordeaux, Plateforme Proteome)

  • Sabrina Lacomme

    (Univ. Bordeaux, CNRS, INSERM, Bordeaux Imaging Center, BIC, UAR 3420, US 4)

  • Mélina Petrel

    (Univ. Bordeaux, CNRS, INSERM, Bordeaux Imaging Center, BIC, UAR 3420, US 4)

  • Christelle Martin

    (Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297)

  • Vincent Pitard

    (UB’FACSility CNRS UMS 3427, INSERM US 005, Univ. Bordeaux)

  • Véronique De Smedt Peyrusse

    (Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286)

  • Thomas Biederer

    (Yale School of Medicine)

  • David Perrais

    (Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297)

  • Pierre Trifilieff

    (Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286)

  • Etienne Herzog

    (Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297)

Abstract

Dopamine transmission is involved in reward processing and motor control, and its impairment plays a central role in numerous neurological disorders. Despite its strong pathophysiological relevance, the molecular and structural organization of the dopaminergic synapse remains to be established. Here, we used targeted labelling and fluorescence activated sorting to purify striatal dopaminergic synaptosomes. We provide the proteome of dopaminergic synapses with 57 proteins specifically enriched. Beyond canonical markers of dopamine neurotransmission such as dopamine biosynthetic enzymes and cognate receptors, we validated 6 proteins not previously described as enriched. Moreover, our data reveal the adhesion of dopaminergic synapses to glutamatergic, GABAergic or cholinergic synapses in structures we named “dopamine hub synapses”. At glutamatergic synapses, pre- and postsynaptic markers are significantly increased upon association with dopamine synapses. Dopamine hub synapses may thus support local dopaminergic signalling, complementing volume transmission thought to be the major mechanism by which monoamines modulate network activity.

Suggested Citation

  • Vincent Paget-Blanc & Marlene E. Pfeffer & Marie Pronot & Paul Lapios & Maria-Florencia Angelo & Roman Walle & Fabrice P. Cordelières & Florian Levet & Stéphane Claverol & Sabrina Lacomme & Mélina Pet, 2022. "A synaptomic analysis reveals dopamine hub synapses in the mouse striatum," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30776-9
    DOI: 10.1038/s41467-022-30776-9
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    References listed on IDEAS

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    1. Alexandros Poulopoulos & Alexander J. Murphy & Abdulkadir Ozkan & Patrick Davis & John Hatch & Rory Kirchner & Jeffrey D. Macklis, 2019. "Subcellular transcriptomes and proteomes of developing axon projections in the cerebral cortex," Nature, Nature, vol. 565(7739), pages 356-360, January.
    2. Troels Rahbek-Clemmensen & Matthew D. Lycas & Simon Erlendsson & Jacob Eriksen & Mia Apuschkin & Frederik Vilhardt & Trine N. Jørgensen & Freja H. Hansen & Ulrik Gether, 2017. "Super-resolution microscopy reveals functional organization of dopamine transporters into cholesterol and neuronal activity-dependent nanodomains," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    3. M. W. Howe & D. A. Dombeck, 2016. "Rapid signalling in distinct dopaminergic axons during locomotion and reward," Nature, Nature, vol. 535(7613), pages 505-510, July.
    4. Seung Wook Oh & Julie A. Harris & Lydia Ng & Brent Winslow & Nicholas Cain & Stefan Mihalas & Quanxin Wang & Chris Lau & Leonard Kuan & Alex M. Henry & Marty T. Mortrud & Benjamin Ouellette & Thuc Ngh, 2014. "A mesoscale connectome of the mouse brain," Nature, Nature, vol. 508(7495), pages 207-214, April.
    5. Nicolas X. Tritsch & Jun B. Ding & Bernardo L. Sabatini, 2012. "Dopaminergic neurons inhibit striatal output through non-canonical release of GABA," Nature, Nature, vol. 490(7419), pages 262-266, October.
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