mGluR1/5-Dependent Long-Term Depression Requires the Regulated Ectodomain Cleavage of Neuronal Pentraxin NPR by TACE
Open accessAbstract
Matrix metalloproteases (MMPs) play a role in remodeling the extracellular matrix during brain development and have been implicated in synaptic plasticity. Here, we report that a member of the neuronal pentraxin (NP) family, neuronal pentraxin receptor (NPR), undergoes regulated cleavage by the MMP tumor necrosis factor-alpha converting enzyme (TACE). NPR is enriched at excitatory synapses where it associates with AMPA-type glutamate receptors (AMPAR) and enhances synaptogenesis. However, in response to activation of group 1 mGluRs (mGluR1/5), TACE cleaves NPR and releases the pentraxin domain from its N-terminal transmembrane domain. Cleaved NPR rapidly accumulates in endosomes where it colocalizes with AMPAR. This process is necessary for mGluR1/5-dependent LTD in hippocampal and cerebellar synapses. These observations suggest that cleaved NPR functions to "capture" AMPAR for endocytosis and reveal a bifunctional role of NPs in both synapse strengthening and weakening.
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The three NPTXs interact, directly or indirectly, with the N-terminal extracellular domain of AMPAR subunits (GluA1, GluA2, GluA3, and GluA4), via their conserved pentraxin domain.
“The three NPTXs interact, directly or indirectly, with the N-terminal extracellular domain of AMPAR subunits (GluA1, GluA2, GluA3 and GluA4), via their conserved pentraxin domain (Chang et al. 2010; Cho et al. 2008; Lee et al. 2017; Sia et al. 2007; Suzuki et al. 2020).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Cho et al. 2008
The NPTX complex acts as a trans-synaptic signalling molecule, regulating the activity of neurotransmitter receptors at excitatory synapses.
“The NPTX complex acts as trans-synaptic signalling molecule, regulating the activity of neurotransmitter receptors at excitatory synapses.”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Cho et al. 2008
In response to activation of group 1 mGluR1/5, TACE cleaves NPTXR, releasing it from its N-terminal transmembrane domain.
“In vitro studies revealed that, in response to the activation of group 1 metabotropic receptor (mGluR1/5), the metalloprotease tumour necrosis factor-alpha converting enzyme (TACE)—implicated in shedding of proteins (Black 2002)—cleaves NPTXR, releasing it from its N-terminal transmembrane domain.”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Cho et al. 2008
NPTX heterocomplex plays a dual role in synapse formation and depression.
“In addition, NPTX heterocomplex play a dual role in synapse formation and depression.”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Cho et al. 2008
This mechanism is necessary for long-term depression in hippocampus and cerebellum.
“This mechanism is necessary for LTD in hippocampus and cerebellum (Cho et al. 2008).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Cho et al. 2008
Internalisation of AMPAR receptors upon TACE action may serve as a protective mechanism against excess glutamate.
“The internalisation of AMPAR receptors upon TACE action (Cho et al. 2008) may serve as a protective mechanism against the excess of glutamate (Schwarz et al. 2002).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Cho et al. 2008
NPTXs modulate long-term depression in synapses formed in hippocampus (Schaffer collateral-CA1 synapses) and cerebellum (Purkinje cells).
“Moreover, they modulate LTD in synapses formed in hippocampus (Schaffer collateral—CA1 synapses), and cerebellum (Purkinje cells) (Cho et al. 2008).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Cho et al. 2008
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- Authors
- Cho, R. W., Park, J. M., Wolff, S. B. E., Xu, D., Hopf, C., Kim, J.-A., Reddy, R. C., Petralia, R. S., Perin, M. S., Linden, D. J., & Worley, P. F.
- Affiliations
- Johns Hopkins University (US)
- National Institutes of Health (US)
- Cleveland Clinic (US)
- Corresponding author
- Worley, Paul F.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2008-03
- Volume
- 57
- Issue
- 6
- Pages
- 858-871
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC2701195
- OpenAlex
- W1965208860
- Cited by
- 125
- References
- 67
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 7 · 2023: 7 · 2022: 7 · 2021: 10 · 2020: 7 · 2019: 3 · 2018: 6 · 2017: 7 · 2016: 3 · 2015: 5 · 2014: 9 · 2013: 2 · 2012: 5
- FWCI
- 5.33
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2000 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- U.S. Public Health Service (R37MM51106)
- National Eye Institute
- National Institute on Deafness and Other Communication Disorders
- National Institute of Neurological Disorders and Stroke (R01NS039156)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- transarterial chemoembolization, matrix metalloproteinases, long-term depression, AMPA receptors, ectodomain shedding, endosomal trafficking, synaptic plasticity, synaptogenesis, hippocampus, cerebellum, excitatory synapses
- MeSH terms
- ADAM17 Protein, Pentraxins, Animals, Animals, Newborn, C-Reactive Protein, Cells, Cultured, Cerebellum, Embryo, Mammalian, Hippocampus, Humans, Nerve Tissue Proteins, Neuronal Plasticity, Neurons, Receptors, Cell Surface, Transfection, Protein Structure, Tertiary, Receptors, Metabotropic Glutamate, Mice, Knockout, Patch-Clamp Techniques, Excitatory Amino Acid Agents, RNA, Small Interfering, Mice, ADAM Proteins, Inhibitory Postsynaptic Potentials
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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