Reelin mobilizes a VAMP7-dependent synaptic vesicle pool and selectively augments spontaneous neurotransmission
Open accessAbstract
Reelin is a glycoprotein that is critical for proper layering of neocortex during development as well as dynamic regulation of glutamatergic postsynaptic signaling in mature synapses. Here, we show that Reelin also acts presynaptically, resulting in robust rapid enhancement of spontaneous neurotransmitter release without affecting properties of evoked neurotransmission. This effect of Reelin requires a modest but significant increase in presynaptic Ca(2+) initiated via ApoER2 signaling. The specificity of Reelin action on spontaneous neurotransmitter release is encoded at the level of vesicular SNARE machinery as it requires VAMP7 and SNAP-25 but not synaptobrevin2, VAMP4, or vti1a. These results uncover a presynaptic regulatory pathway that utilizes the heterogeneity of synaptic vesicle-associated SNAREs and selectively augments action potential-independent neurotransmission.
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Reelin signaling through Apoer2 and Vldlr receptors on the presynaptic membrane leads to transient elevations of intracellular Ca2+.
“Reelin signaling through Apoer2 and Vldlr receptors on the presynaptic membrane leads to transient elevations of intracellular Ca2+ [73].”
From ApoE, ApoE Receptors, and the Synapse in Alzheimer's Disease (2017) · cites this paper as [73]
Emerging data indicate that ApoE receptors have a similarly important role in regulating presynaptic vesicle release.
“emerging data indicate that ApoE receptors have a similarly important role in regulating presynaptic vesicle release [73].”
From ApoE, ApoE Receptors, and the Synapse in Alzheimer's Disease (2017) · cites this paper as [73]
Reelin acts presynaptically.
“Reelin also acts presynaptically (25,26).”
From Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses (2017) · cites this paper as [25]
This increase in VAMP7-containing mobilization of presynaptic vesicles requires release of Ca2+ from intracellular compartments, both ApoER2 and VLDLR, and PI3K.
“This increase in VAMP7-containing mobilization of presynaptic vesicles requires release of Ca 2ϩ from intracellular compartments, both ApoER2 and VLDLR, and PI3K (25).”
From Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses (2017) · cites this paper as [25]
Acute application of Reelin increases spontaneous fusion of VAMP7-containing presynaptic vesicles in hippocampal cultures, rapid within 5 min and robust as early as 6 days in vitro.
“Acute application of Reelin increases the spontaneous fusion of vesicle-associated membrane protein 7 (VAMP7)-containing presynaptic vesicles in hippocampal cultures, and this effect is rapid (within 5 min) and robust as early as 6 days in vitro when spontaneous fusion is minimal (25).”
From Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses (2017) · cites this paper as [25]
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“For example, in mature nerve terminals, a series of v-SNARE proteins including Vti1a, VAMP4 and VAMP7 all appear to bias neurotransmitter release towards spontaneous SV fusion when overexpressed in primary neuronal cultures (Bal et al. 2013; Lin et al. 2020; Ramirez et al. 2012).”
- Authors
- Bal, M., Leitz, J., Reese, A. L., Ramirez, D. M. O., Durakoglugil, M., Herz, J., Monteggia, L. M., & Kavalali, E. T.
- Affiliations
- The University of Texas Southwestern Medical Center (US)
- Corresponding author
- Kavalali, Ege T.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2013-11
- Volume
- 80
- Issue
- 4
- Pages
- 934-946
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3840105
- OpenAlex
- W1997090186
- Cited by
- 131
- References
- 76
- Citations by year
- 2026: 8 · 2025: 6 · 2024: 7 · 2023: 4 · 2022: 8 · 2021: 8 · 2020: 13 · 2019: 10 · 2018: 9 · 2017: 20 · 2016: 16 · 2015: 12 · 2014: 10
- FWCI
- 6.21
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Heart, Lung, and Blood Institute (R01HL063762, R37HL063762, HL063762)
- National Institute of Mental Health (MH 070727, R01MH066198, MH-066198, R01MH070727)
- National Institute of Neurological Disorders and Stroke (R21NS075499, T32NS069562)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- reelin, VAMP7, SNAP-25, synaptic vesicle pools, spontaneous neurotransmission, presynaptic modulation, SNARE proteins, vti1a, VAMP4, glutamatergic synapses, neocortex development
- MeSH terms
- Reelin Protein, Animals, Apolipoproteins E, Cells, Cultured, Female, Male, Nerve Tissue Proteins, Synaptic Transmission, Serine Endopeptidases, Synaptic Vesicles, Tetrodotoxin, Cell Adhesion Molecules, Neuronal, Lentivirus, Extracellular Matrix Proteins, Rats, Sprague-Dawley, Patch-Clamp Techniques, Excitatory Postsynaptic Potentials, Phosphatidylinositol 3-Kinases, Calcium Signaling, SNARE Proteins, R-SNARE Proteins, Synaptosomal-Associated Protein 25, Mice, Rats, Electrophysiological Phenomena
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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