Developmental regulation of AMPA-receptor properties in CA1 pyramidal neurons of rat hippocampus

Seifert, Gerald; Zhou, Min; Dietrich, Dirk; Schumacher, Thekla B.; Dybek, A.; Weiser, Thomas; Wienrich, M.; Wilhelm, D.; Steinhäuser, Christian

doi:10.1016/s0028-3908(99)00212-9

Cited by 26 publications

(23 citation statements)

References 44 publications

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“…All of the widely used AMPAR agonists, including glutamate and AMPA, evoke strong desensitization of the receptor, with the exception of kainate (Patneau and Mayer, 1991). Importantly, kainate responses in CA1 neurons can also be completely blocked by the AMPA antagonist, GYKI 53655 (Seifert et al, 2000). Therefore, rectification studies were carried out during both ultrarapid application of glutamate and prolonged exposure to kainate with spermine in the micropipette.…”

Section: Methodsmentioning

confidence: 99%

“…Because kainate is the only AMPAR agonist with a minimal capacity to induce desensitization and because at this age (postnatal days 36 -42) more than 95% of kainate-induced currents in CA1 neurons are due to AMPAR activation (Seifert et al, 2000), we applied kainate on CA1 neurons to further characterize the I-V properties of altered AMPA currents. There was a clearly observable (Fig.…”

Section: Synaptic and Extrasynaptic Ampar Function Ismentioning

confidence: 99%

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Benzodiazepine Withdrawal-Induced Glutamatergic Plasticity Involves Up-Regulation of GluR1-Containing α-Amino-3-hydroxy-5-methylisoxazole-4-propionic Acid Receptors in Hippocampal CA1 Neurons

Song

Shen²,

Greenfield³

et al. 2007

J Pharmacol Exp Ther

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Modification of glutamatergic synaptic function, a mechanism central to neuronal plasticity, may also mediate long-term drug effects, including dependence and addiction. Benzodiazepine withdrawal results in increased glutamatergic strength, but whether ␣-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptors (AMPARs) are functionally and structurally remodeled during benzodiazepine withdrawal is uncertain. Whole-cell recordings of rat hippocampal CA1 neurons, either acutely dissociated or in hippocampal slices, revealed that AMPAR function was enhanced up to 50% during flurazepam (FZP) withdrawal, without changes in whole-cell channel kinetic properties. Agonist-elicited AMPA currents showed a negative shift in rectification in the presence of spermine, suggesting augmented membrane incorporation of glutamate receptor (GluR) 2-lacking AMPARs. As GluR1-containing AMPARs are critical for activity-dependent alterations in excitatory strength, we sought to determine whether changes in GluR1 subunit distribution in CA1 neurons occurred during benzodiazepine withdrawal. Confocal image analysis revealed that FZP withdrawal promoted GluR1 subunit incorporation into somatic and proximal dendritic membranes of CA1 neurons without GluR2 subunit alterations. Findings of immunoblot studies were consistent with immunofluorescent studies indicating increased GluR1, but not GluR2, subunit protein levels in cytosolic, crude membrane and postsynaptic density-enriched fractions from CA1 minislices. As with long-term potentiation (LTP), the FZPwithdrawal-induced GluR1 incorporation into CA1 neuron membranes may require the GluR1-trafficking protein, synapse-associated protein 97, which was also elevated in membrane-associated fractions. Together, our findings provide evidence that during FZP withdrawal, increased membrane incorporation of GluR1-containing AMPARs and associated upregulation of AMPAR functions in hippocampal CA1 pyramidal neurons share fundamental similarities with the mechanisms underlying LTP. This implies that glutamatergic neuronal remodeling observed in LTP also subserves physiological adaptations to drug withdrawal.Remodeling of glutamatergic neurotransmission has recently been associated with dependence on and addiction to various drugs of abuse (Nestler, 2005), including the benzodiazepines (Izzo et al., 2001;Van Sickle et al., 2004;Xiang and Tietz, 2007). Benzodiazepines are widely prescribed anxiolytics and hypnotics but have more limited clinical use as anticonvulsants due to the development of tolerance, largely mediated by dysfunction of GABA A receptors, the site of benzodiazepine allosteric actions (Zeng and Tietz, 1999;Bateson, 2002). Abrupt benzodiazepine withdrawal causes anxiety and insomnia, which can lead to drug self-administration and contribute to benzodiazepine misuse and abuse This work was supported by Department of Health and Human Services Grants R01-DA-04075-15 and R01-DA18342-02 from the National Institute on Drug Abuse (to E.I.T.) and predoctoral fellowships from t...

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Section: Methodsmentioning

confidence: 99%

Section: Synaptic and Extrasynaptic Ampar Function Ismentioning

confidence: 99%

Benzodiazepine Withdrawal-Induced Glutamatergic Plasticity Involves Up-Regulation of GluR1-Containing α-Amino-3-hydroxy-5-methylisoxazole-4-propionic Acid Receptors in Hippocampal CA1 Neurons

Song

Shen²,

Greenfield³

et al. 2007

J Pharmacol Exp Ther

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“…Acute Isolation of Hippocampal Neurons-Hippocampal neurons were freshly isolated as previously reported (34,35). Briefly, FVB mice or Wistar rats (1-4 days old or 2 months old) were anesthetized and decapitated, and frontal brain slices of 300-m thickness were cut with a vibratome (FTB, Plano, Marburg, Germany) in a solution containing 90 mM NaCl, 3 mM KCl, 2 mM MgSO 4 , 2 mM CaCl 2 , 1 mM sodium pyruvate, 10 mM glucose, 10 mM HEPES, 90 mM sucrose (4°C, pH 7.4).…”

Section: Methodsmentioning

confidence: 99%

“…Incubation time varied between 5 and 6 min at 35°C (juvenile mice) and 20 min at 35°C plus 10 min at room temperature (21-24°C, adult). After wash, the stratum pyramidale of the CA1 region of the hippocampus was dissected, and cells were isolated as described (35).…”

Section: Methodsmentioning

confidence: 99%

“…This may happen due to a bias in receptor composition possibly introduced by the purification procedure, for instance by selecting for particular glycan structures by lectin column chromatography. This bias may mask developmental changes in splicing or subunit composition of AMPA-Rs in neural cells (35,55) possibly underlying the age-dependent differences in PSA-mediated modulation. Alternatively, removal of AMPA-R-associated molecules during the purification has to be considered (i.e.…”

Section: Mechanisms Of Interaction Between Polysialicmentioning

confidence: 99%

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Neural Cell Adhesion Molecule-associated Polysialic Acid Potentiates α-Amino-3-hydroxy-5-methylisoxazole-4-propionic Acid Receptor Currents

Vaithianathan

Matthias

Bahr

et al. 2004

Journal of Biological Chemistry

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The highly negatively charged polysialic acid (PSA) is a carbohydrate predominantly carried by the neural cell adhesion molecule (NCAM) in mammals. NCAM and, in particular, PSA play important roles in cellular and synaptic plasticity. Here we investigated whether PSA modulates the activity of the ␣-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) subtype of glutamate receptors (AMPA-Rs). Single channel recordings of affinity-purified AMPA-Rs reconstituted in lipid bilayers revealed that bacterially derived PSA, called colominic acid, prolonged the open channel time of AMPA-R-mediated currents by severalfold and altered the bursting pattern of the receptor channels but did not modify AMPA-R single channel conductance. This effect was reversible, concentration-dependent, and specific, since monomers of sialic acid and another negatively charged carbohydrate, chondroitin sulfate, did not potentiate single channel AMPA-R currents. Recombinant PSA-NCAM also potentiated currents mediated by reconstituted AMPA-Rs. In pyramidal neurons acutely isolated from the CA1 region of the early postnatal hippocampus, L-glutamate or AMPA (applied in the presence of antagonists blocking voltage-gated Na ؉ and K ؉ currents and N-methyl-D-aspartate and metabotropic glutamate receptors) induced inward currents, which were significantly increased by co-application of colominic acid. Chondroitin sulfate did not affect AMPA-R-mediated currents in CA1 neurons. The effect of colominic acid was age-dependent, since in pyramidal neurons from adult hippocampus, colominic acid failed to potentiate glutamate responses. Thus, our study demonstrates agedependent potentiation of AMPA receptors by PSA via a mechanism probably involving direct PSA-AMPA-R interactions. This mechanism might amplify AMPA-R-mediated signaling in immature cells, thereby affecting their development.

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Structure-Function Analyses of Single Cells by Combining Patch-Clamp Techniques with Reverse Transcription-Polymerase Chain Reaction

Seifert

Steinhäuser

2007

Neuromethods

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Developmental regulation of AMPA-receptor properties in CA1 pyramidal neurons of rat hippocampus

Cited by 26 publications

References 44 publications

Benzodiazepine Withdrawal-Induced Glutamatergic Plasticity Involves Up-Regulation of GluR1-Containing α-Amino-3-hydroxy-5-methylisoxazole-4-propionic Acid Receptors in Hippocampal CA1 Neurons

Benzodiazepine Withdrawal-Induced Glutamatergic Plasticity Involves Up-Regulation of GluR1-Containing α-Amino-3-hydroxy-5-methylisoxazole-4-propionic Acid Receptors in Hippocampal CA1 Neurons

Neural Cell Adhesion Molecule-associated Polysialic Acid Potentiates α-Amino-3-hydroxy-5-methylisoxazole-4-propionic Acid Receptor Currents

Structure-Function Analyses of Single Cells by Combining Patch-Clamp Techniques with Reverse Transcription-Polymerase Chain Reaction

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