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PMID:17229826

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Citation

Qiu, S and Weeber, EJ (2007) Reelin signaling facilitates maturation of CA1 glutamatergic synapses. J. Neurophysiol. 97:2312-21

Abstract

Reelin signaling through the low-density lipoprotein receptor family members, apoliproprotein E receptor 2 (apoER2) and very-low-density lipoprotein receptor (VLDLR), plays a pivotal role in dictating neuronal lamination during embryonic brain development. Recent evidence suggests that this signaling system also plays a role in the postnatal brain to modulate synaptic transmission, plasticity, and cognitive behavior, mostly likely due to a functional coupling with N-methyl-d-aspartate (NMDA) receptors. In this study, we investigated the effects of reelin on the maturation of CA1 glutamatergic function using electrophysiological and biochemical approaches. In cultured hippocampal slices, reelin treatment increased the amplitude of AMPAR-mediated miniature excitatory postsynaptic currents and the evoked AMPA/NMDA receptor current ratios. In addition, reelin treatment also reduced the number of silent synapses, facilitated a developmental switch from NR2B to NR2A of NMDARs, and increased surface expression of AMPARs in CA1 tissue. In cultured hippocampal neurons from reeler embryos, reduced numbers of AMPAR subunit GluR1 and NMDAR subunit NR1 clustering were observed compared with those obtained from wild-type embryos. Supplementing reelin in the reeler culture obliterated these genotypic differences. These results demonstrate that reelin- and lipoprotein receptor-mediated signaling may operate during developmental maturation of hippocampal glutamatergic function and thus represent a potential important mechanism for controlling synaptic strength and plasticity in the postnatal hippocampus.

Links

PubMed Online version:10.1152/jn.00869.2006

Keywords

2-Amino-5-phosphonovalerate/pharmacology; 6-Cyano-7-nitroquinoxaline-2,3-dione/pharmacology; Analysis of Variance; Animals; Animals, Newborn; Cell Adhesion Molecules, Neuronal/genetics; Cell Adhesion Molecules, Neuronal/metabolism; Cells, Cultured; Dose-Response Relationship, Radiation; Electric Stimulation/methods; Excitatory Amino Acid Antagonists/pharmacology; Excitatory Postsynaptic Potentials/drug effects; Excitatory Postsynaptic Potentials/physiology; Excitatory Postsynaptic Potentials/radiation effects; Extracellular Matrix Proteins/genetics; Extracellular Matrix Proteins/metabolism; Gene Expression Regulation, Developmental/drug effects; Gene Expression Regulation, Developmental/physiology; Glutamic Acid/metabolism; Hippocampus/cytology; Hippocampus/growth & development; Hippocampus/metabolism; Humans; Mice; Mice, Transgenic; Nerve Tissue Proteins/genetics; Nerve Tissue Proteins/metabolism; Pyramidal Cells/cytology; Pyramidal Cells/drug effects; Pyramidal Cells/physiology; Pyramidal Cells/radiation effects; Serine Endopeptidases/genetics; Serine Endopeptidases/metabolism; Signal Transduction/physiology; Synapses/drug effects; Synapses/physiology; Transfection/methods

Significance

Annotations

Gene product Qualifier GO Term Evidence Code with/from Aspect Extension Notes Status

MOUSE:GRIA1

located_in

GO:0009986: cell surface

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NMDE1

located_in

GO:0009986: cell surface

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NMDZ1

located_in

GO:0009986: cell surface

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NMDE2

located_in

GO:0009986: cell surface

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:RELN

involved_in

GO:2000463: positive regulation of excitatory postsynaptic potential

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

MOUSE:RELN

involved_in

GO:2000969: positive regulation of AMPA receptor activity

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

MOUSE:RELN

involved_in

GO:0051968: positive regulation of synaptic transmission, glutamatergic

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

MOUSE:RELN

involved_in

GO:0090129: positive regulation of synapse maturation

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

MOUSE:RELN

involved_in

GO:2000969: positive regulation of AMPA receptor activity

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

MOUSE:RELN

involved_in

GO:0051968: positive regulation of synaptic transmission, glutamatergic

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

MOUSE:RELN

involved_in

GO:0090129: positive regulation of synapse maturation

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

MOUSE:RELN

GO:2000463 : positive regulation of excitatory postsynaptic membrane potential

ECO:0000315:

P

Mouse CA1 pyramidal neurons used to record spontaneous miniature activities and whole cell response. Cells treated with Reelin increased spontaneous mEPSC amplitude which was blocked by a antagonist (figure 1A-C)

Figure 6F shows a reduced amplitude of AMPA receptor mediated mEPSC when not treated with reelin. Therefore treatment with reelin rescues mutant reelin (reeler) mice.

complete
CACAO 2385

MOUSE:RELN

GO:0051968: positive regulation of synaptic transmission, glutamatergic

ECO:0000315:

P

Mouse CA1 pyramidal neurons used to record spontaneous miniature activities and whole cell response. Cells treated with reelin increased spontaneous mEPSC amplitude which was not seen when blocked by a antagonist (figure 1A-C). In addition figure 2B shows current ratio of AMPA/NMDA. Cells treated with reelin showed high ratio compared to cell not treated with Reelin.

complete
CACAO 2386

MOUSE:RELN

GO:2000969: positive regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate selective glutamate receptor activity

ECO:0000315:

P

Mouse CA1 pyramidal neurons used to record spontaneous miniature activities and whole cell response. Cells treated with reelin increased spontaneous mEPSC amplitude which was not seen when blocked by a antagonist (figure 1A-C). In addition figure 2B shows current ratio of AMPA/NMDA. Cells treated with eeelin showed high ratio compared to cell not treated with reelin. Therefore enhances AMPA receptor function.

complete
CACAO 2387

MOUSE:RELN

GO:0097113: alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor clustering

ECO:0000315:

P

Figure 3 (A-C) cells treated with reelin showed increase levels of surface GluR1 compared to control.

complete
CACAO 2388

MOUSE:RELN

GO:0090129: positive regulation of synapse maturation

ECO:0000315:

P

Figure 5A used antagonist to block Reelin activity, which increase the failure rate of functional synapse in CA1 hippocampus region of mice.

complete
CACAO 2390

MOUSE:RELN

GO:0010976: positive regulation of neuron projection development

ECO:0000315:

P

In mice with mutation in the reelin gene there was stunted neurite growth but when treated with reelin the growth was corrected, figure 6A-C.

complete
CACAO 2391

MOUSE:RELN

involved_in

GO:0010976: positive regulation of neuron projection development

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

MOUSE:RELN

involved_in

GO:0021766: hippocampus development

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

MOUSE:RELN

involved_in

GO:2000463: positive regulation of excitatory postsynaptic potential

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

MOUSE:NMDE1

GO:0009986: cell surface

ECO:0000315:

C

Cell surface protein biotinylation and Western blotting was used. Figure 3 A-C, cells treated with reelin showed increase levels of surface NR2A compared to control.

complete
CACAO 2396

MOUSE:NMDE1

part_of

GO:0009986: cell surface

ECO:0000315: mutant phenotype evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NMDE1

part_of

GO:0009986: cell surface

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NMDE2

GO:0009986: cell surface

ECO:0000315:

C

Cell surface protein biotinylation and Western blotting was used, figure 3 A-C

complete
CACAO 2398

MOUSE:NMDE2

part_of

GO:0009986: cell surface

ECO:0000315: mutant phenotype evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NMDE2

part_of

GO:0009986: cell surface

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:GRIA1

part_of

GO:0009986: cell surface

ECO:0000315: mutant phenotype evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:GRIA1

GO:0009986: cell surface

ECO:0000315:

C

Cell surface protein biotinylation and Western blotting was used. Figure 3 A-C, cells treated with Reelin showed increase levels of surface GluR1 compared to control.

complete
CACAO 2392

MOUSE:GRIA1

part_of

GO:0009986: cell surface

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NMDZ1

part_of

GO:0009986: cell surface

ECO:0000315: mutant phenotype evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NMDZ1

part_of

GO:0030425: dendrite

ECO:0000315: mutant phenotype evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NMDZ1

part_of

GO:0009986: cell surface

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NMDZ1

GO:0030425: dendrite

ECO:0000315:

C

Wild type primary dendrites show labelling of NR1 by using immunofluorescence techniques, figure 6A. Figure 6B in reelin mutant mice showed decrease NR1 which was corrected by treating with reelin, figure 6C.

complete
CACAO 2394

MOUSE:NMDZ1

GO:0009986: cell surface

ECO:0000315:

C

Cell surface protein biotinylation and Western blotting was used, figure 3 A-C.

complete
CACAO 2397


See also

References

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