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GABAergic basket cells expressing cholecystokinin contain vesicular glutamate transporter type 3 (VGLUT3) in their synaptic terminals in hippocampus and isocortex of the rat

Somogyi, Jozsef, Baude, Agnès, Omori, Yuko, Shimizu, Hidemi, Mestikawy, Salah El, Fukaya, Masahiro, Shigemoto, Ryuichi, Watanabe, Masahiko +1 more·2004·European Journal of Neuroscience
DOI 10.1111/j.0953-816x.2003.03091.x
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Abstract

Vesicular glutamate transporter type 3 (VGLUT3) containing neuronal elements were characterized using antibodies to VGLUT3 and molecular cell markers. All VGLUT3-positive somata were immunoreactive for CCK, and very rarely, also for calbindin; none was positive for parvalbumin, calretinin, VIP or somatostatin. In the CA1 area, 26.8 +/- 0.7% of CCK-positive interneuron somata were VGLUT3-positive, a nonoverlapping 22.8 +/- 1.9% were calbindin-positive, 10.7 +/- 2.5% VIP-positive and the rest were only CCK-positive. The patterns of coexpression were similar in the CA3 area, the dentate gyrus and the isocortex. Immunoreactivity for VGLUT3 was undetectable in pyramidal and dentate granule cells. Boutons colabelled for VGLUT3, CCK and GAD were most abundant in the cellular layers of the hippocampus and in layers II-III of the isocortex. Large VGLUT3-labelled boutons at the border of strata radiatum and lacunosum-moleculare in the CA1 area were negative for GAD, but were labelled for vesicular monoamine transporter type 2, plasmalemmal serotonin transporter or serotonin. No colocalization was found in terminals between VGLUT3 and parvalbumin, vesicular acetylcholine transporter and group III (mGluR7a,b; mGluR8a,b) metabotropic glutamate receptors. In stratum radiatum and the isocortex, VGLUT3-positive but GAD-negative boutons heavily innervated the soma and proximal dendrites of some VGLUT3- or calbindin-positive interneurons. The results suggest that boutons coexpressing VGLUT3, CCK and GAD originate from CCK-positive basket cells, which are VIP-immunonegative. Other VGLUT3-positive boutons immunopositive for serotonergic markers but negative for GAD probably originate from the median raphe nucleus and innervate select interneurons. The presumed amino acid substrate of VGLUT3 may act on presynaptic kainate or group II metabotropic glutamate receptors.

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Crossref · 10.1111/j.0953-816x.2003.03091.x

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  • CCKBCs are considered to parse into at least two subtypes: those that coexpress vasoactive intestinal peptide (VIP) and those that coexpress vesicular glutamate transporter 3 (VGluT3), though neither marker is specific on its own for CCKBCs and a substantial proportion of CCKBCs express neither.

    “Molecularly, CCKBCs are considered to parse into at least two subtypes: those that coexpress vasoactive intestinal peptide (VIP) and those that coexpress vesicular glutamate transporter 3 (VGluT3), though again neither of these markers is specific on their own for CCKBCs and a substantial proportion of CCKBCs express neither of them (5, 102, 1031).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1031]

  • VGluT3 expression was originally described as being limited to CCKBCs, it has also been detected in ADIs.

    “While VGluT3 expression was originally described as being limited to CCKBCs (1031), it has also been detected in ADIs (584).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1031]

  • Cells in cluster 6 had the highest incidence of CCK expression (typically in combination with VGluT3 and VIP) and anatomies indicative of CCKBCs and mossy fiber associated cells, with intrinsic features often intermediate to cells in all other clusters.

    “Finally, cells in cluster 6 had the highest incidence of CCK expression (typically in combination with VGluT3 and VIP) and anatomies indicative of CCKBCs (1031, 584) and mossy fiber associated cells (1138) with intrinsic features that were often intermediate to cells in all other clusters (TABLE 1).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1031]

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Authors
Somogyi, J., Baude, A., Omori, Y., Shimizu, H., Mestikawy, S. E., Fukaya, M., Shigemoto, R., Watanabe, M., & Somogyi, P.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Hokkaido University (JP)
  • Inserm (FR)
  • Japan Science and Technology Agency (JP)
ORCID
Venue
European Journal of Neuroscience
Publisher
Wiley
Published
2004-01-30
Volume
19
Issue
3
Pages
552-569
ISSN
  • 0953-816X (ISSN-L)
  • 1460-9568
DOI
10.1111/j.0953-816x.2003.03091.x
OpenAlex
W1974705547
Cited by
207
References
76
Citations by year
2026: 4 · 2025: 7 · 2024: 6 · 2023: 11 · 2022: 5 · 2021: 16 · 2020: 16 · 2019: 11 · 2018: 12 · 2017: 13 · 2016: 6 · 2015: 6 · 2014: 8 · 2013: 6 · 2012: 8
FWCI
3.40
Type
journal article
Language
en
Open access
closed
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • European Journal of Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
Funders
Wellcome Trust
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
  • Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
Keywords
basket cells, cholecystokinin, GABAergic interneurons, hippocampus, neocortex, calbindin, VIP, glutamatergic terminals, serotonergic terminals, median raphe nucleus, kainate receptors, group II metabotropic glutamate receptors, presynaptic glutamate release
MeSH terms
Animals, Carrier Proteins, Cell Count, Cerebral Cortex, Cholecystokinin, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Hippocampus, Immunohistochemistry, Male, Membrane Glycoproteins, Nerve Tissue Proteins, Neuropeptides, Blotting, Western, Rats, Wistar, Presynaptic Terminals, Receptors, Metabotropic Glutamate, Microscopy, Confocal, Membrane Transport Proteins, Amino Acid Transport Systems, Acidic, Serotonin Plasma Membrane Transport Proteins, Vesicular Biogenic Amine Transport Proteins, Vesicular Monoamine Transport Proteins, Vesicular Glutamate Transport Proteins, Rats, Calbindins, S100 Calcium Binding Protein G

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