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Cited by 47Neuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on BehaviorProtease and Inhibitor Mechanisms

Dopamine Receptor Activation Modulates the Integrity of the Perisynaptic Extracellular Matrix at Excitatory Synapses

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Mitlöhner, Jessica, Kaushik, Rahul, Niekisch, Hartmut, Blondiaux, Armand, Gee, Christine E., Happel, Max F. K., Gundelfinger, Eckart, Dityatev, Alexander +2 more·2020·Cells
DOI 10.3390/cells9020260PMC PMC7073179
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Abstract

In the brain, Hebbian-type and homeostatic forms of plasticity are affected by neuromodulators like dopamine (DA). Modifications of the perisynaptic extracellular matrix (ECM), which control the functions and mobility of synaptic receptors as well as the diffusion of transmitters and neuromodulators in the extracellular space, are crucial for the manifestation of plasticity. Mechanistic links between synaptic activation and ECM modifications are largely unknown. Here, we report that neuromodulation via D1-type DA receptors can induce targeted ECM proteolysis specifically at excitatory synapses of rat cortical neurons via proteases ADAMTS-4 and -5. We showed that receptor activation induces increased proteolysis of brevican (BC) and aggrecan, two major constituents of the adult ECM both in vivo and in vitro. ADAMTS immunoreactivity was detected near synapses, and shRNA-mediated knockdown reduced BC cleavage. We have outlined a molecular scenario of how synaptic activity and neuromodulation are linked to ECM rearrangements via increased cAMP levels, NMDA receptor activation, and intracellular calcium signaling.

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  • The ECM can be modified rapidly by the release of proteases, by microglial action and by internalization, all of which can be activated by memory events.

    “The ECM can be modified rapidly by the release of proteases [36], by microglial action and by internalization, all of which can be activated by memory events [37–39].”

    From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [38]

    The Results (§3.7) show rapid perisynaptic ECM cleavage after experimentally increasing neuronal cAMP, and the Discussion (§4) attributes dopamine-induced ECM restructuring to extracellular proteases. The paper does not show ECM modification by microglia or internalization, or demonstrate that memory events activate these mechanisms; its mention of learning in Results (§3.1) describes a separate study. (LLM, conf=0.87)

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  • Modification of the CNS ECM by activity-related release of metalloproteinases can cause rapid changes in PNNs in region of synapses, enabling local changes in synaptic properties.

    “An important mechanism of plasticity is modification of the CNS ECM by activity-related release of metalloproteinases, which can cause rapid changes in PNNs in region of synapses, enabling local changes in synaptic properties [38, 58].”

    From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [38]

    The Abstract and Discussion report activity-dependent, ADAMTS-mediated cleavage of ECM components specifically around excitatory synapses, and Discussion §4.2 links synaptic ECM remodeling to changes in synaptic properties. But the paper distinguishes diffuse perisynaptic ECM from condensed perineuronal nets (Introduction); it does not establish rapid changes in PNNs or demonstrate that activity-related release, rather than activation, of these metalloproteinases causes the observed cleavage. (LLM, conf=0.87)

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Cited by

Sorted by citations

Authors
Mitlöhner, J., Kaushik, R., Niekisch, H., Blondiaux, A., Gee, C. E., Happel, M. F. K., Gundelfinger, E., Dityatev, A., Frischknecht, R., & Seidenbecher, C.
Affiliations
  • Leibniz Institute for Neurobiology (DE)
  • German Center for Neurodegenerative Diseases (DE)
  • Center for Molecular Neurobiology Hamburg (ZMNH), Institute for Synaptic Physiology, 20251 Hamburg, Germany
  • Center for Behavioral Brain Sciences (DE)
Corresponding author
  • Dityatev, Alexander
  • Frischknecht, Renato
  • Seidenbecher, Constanze
ORCID
Venue
Cells
Publisher
MDPI AG
Published
2020-01-21
Volume
9
Issue
2
Pages
260
ISSN
2073-4409 (ISSN-L)
DOI
10.3390/cells9020260
PMC
PMC7073179
OpenAlex
W3002314302
Cited by
47
References
8
Citations by year
2026: 2 · 2025: 8 · 2024: 6 · 2023: 8 · 2022: 10 · 2021: 6 · 2020: 5 · 2019: 2
FWCI
3.32
Type
journal article
Language
en
Open access
Licence
Locations
  • Cells (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Informationszentrum Lebenswissenschaften (ZB MED) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • DZNE Pub (submittedVersion, cc-by)
Funders
  • Deutsche Forschungsgemeinschaft (SFB779 TPB14, SFB779 TPB16N, SFB779 TPB09)
  • H2020 Marie Skłodowska-Curie Actions (Marie Curie ITN ECMED)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
Keywords
dopamine D1 receptor, excitatory synapses, ADAMTS-4, ADAMTS5, brevican, aggrecan, matrix proteolysis, neuromodulation, synaptic plasticity, cAMP signaling, NMDA receptor, intracellular calcium signaling, cortical neurons
MeSH terms
ADAMTS Proteins, Homer Scaffolding Proteins, Cyclic AMP, Animals, Cells, Cultured, Extracellular Matrix, Male, Receptors, Dopamine, Synapses, Ion Channel Gating, Receptors, N-Methyl-D-Aspartate, Rats, Wistar, Prefrontal Cortex, Presynaptic Terminals, Cyclic AMP-Dependent Protein Kinases, Calcium Channels, L-Type, Furin, Calcium-Calmodulin-Dependent Protein Kinase Type 2, Brevican

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