Functional similarities and differences of AMPA and kainate receptors expressed by cultured rat sensory neurons

Changjoon Lee, C. Labrakakis, D. J. Joseph, A. B. MacDermott

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

Dorsal root ganglion neurons express functional AMPA and kainate receptors near their central terminals. Activation of these receptors causes a decrease in glutamate release during action potential evoked synaptic transmission. Due to differences in kinetic properties and expression patterns of these two families of glutamate receptors in subpopulations of sensory neurons, AMPA and kainate receptors are expected to function differently. We used embryonic dorsal root ganglion (DRG) neurons maintained in culture to compare functional properties of kainate and AMPA receptors. Most DRG neurons in culture expressed kainate receptors and about half also expressed AMPA receptors. Most AMPA and kainate receptor-expressing DRG neurons were sensitive to capsaicin, suggesting involvement of these glutamate receptors in nociception. When activated by kainate, AMPA receptors were capable of driving a sustained train of action potentials while kainate receptors tended to activate action potential firing more transiently. Glutamate elicited more action potentials and a larger steady-state depolarization in neurons expressing both AMPA and kainate receptors than in neurons expressing only kainate receptors. Adding to their more potent activation properties, AMPA receptors recovered from desensitization much more quickly than kainate receptors. Activation of presynaptic receptors by low concentrations of kainate, but not ATPA, caused a tetrodotoxin-sensitive increase in the frequency of spontaneous EPSCs recorded in dorsal horn neurons. By recording synaptic pairs of DRG and dorsal horn neurons, we found that activation of presynaptic kainate and AMPA receptors decreased evoked glutamate release from terminals of DRG neurons in culture. Our data suggest that the endogenous ligand, glutamate, will cause a different physiological impact when activating these two types of non-NMDA glutamate receptors at central or peripheral nerve endings of sensory neurons.

Original languageEnglish
Pages (from-to)35-48
Number of pages14
JournalNeuroscience
Volume129
Issue number1
DOIs
Publication statusPublished - 2004 Oct 25
Externally publishedYes

Fingerprint

Kainic Acid Receptors
AMPA Receptors
Sensory Receptor Cells
Spinal Ganglia
Neurons
Action Potentials
Glutamic Acid
Glutamate Receptors
Presynaptic Receptors
Posterior Horn Cells
Nociception
Nerve Endings
Kainic Acid
Capsaicin
Tetrodotoxin
Peripheral Nerves
Synaptic Transmission

Keywords

  • action potential
  • capsaicin
  • dorsal root ganglion
  • presynaptic receptors
  • spontaneous EPSCs
  • synaptic transmission

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Functional similarities and differences of AMPA and kainate receptors expressed by cultured rat sensory neurons. / Lee, Changjoon; Labrakakis, C.; Joseph, D. J.; MacDermott, A. B.

In: Neuroscience, Vol. 129, No. 1, 25.10.2004, p. 35-48.

Research output: Contribution to journalArticle

Lee, Changjoon ; Labrakakis, C. ; Joseph, D. J. ; MacDermott, A. B. / Functional similarities and differences of AMPA and kainate receptors expressed by cultured rat sensory neurons. In: Neuroscience. 2004 ; Vol. 129, No. 1. pp. 35-48.
@article{e2736f7679c040f09af6574abde26fc6,
title = "Functional similarities and differences of AMPA and kainate receptors expressed by cultured rat sensory neurons",
abstract = "Dorsal root ganglion neurons express functional AMPA and kainate receptors near their central terminals. Activation of these receptors causes a decrease in glutamate release during action potential evoked synaptic transmission. Due to differences in kinetic properties and expression patterns of these two families of glutamate receptors in subpopulations of sensory neurons, AMPA and kainate receptors are expected to function differently. We used embryonic dorsal root ganglion (DRG) neurons maintained in culture to compare functional properties of kainate and AMPA receptors. Most DRG neurons in culture expressed kainate receptors and about half also expressed AMPA receptors. Most AMPA and kainate receptor-expressing DRG neurons were sensitive to capsaicin, suggesting involvement of these glutamate receptors in nociception. When activated by kainate, AMPA receptors were capable of driving a sustained train of action potentials while kainate receptors tended to activate action potential firing more transiently. Glutamate elicited more action potentials and a larger steady-state depolarization in neurons expressing both AMPA and kainate receptors than in neurons expressing only kainate receptors. Adding to their more potent activation properties, AMPA receptors recovered from desensitization much more quickly than kainate receptors. Activation of presynaptic receptors by low concentrations of kainate, but not ATPA, caused a tetrodotoxin-sensitive increase in the frequency of spontaneous EPSCs recorded in dorsal horn neurons. By recording synaptic pairs of DRG and dorsal horn neurons, we found that activation of presynaptic kainate and AMPA receptors decreased evoked glutamate release from terminals of DRG neurons in culture. Our data suggest that the endogenous ligand, glutamate, will cause a different physiological impact when activating these two types of non-NMDA glutamate receptors at central or peripheral nerve endings of sensory neurons.",
keywords = "action potential, capsaicin, dorsal root ganglion, presynaptic receptors, spontaneous EPSCs, synaptic transmission",
author = "Changjoon Lee and C. Labrakakis and Joseph, {D. J.} and MacDermott, {A. B.}",
year = "2004",
month = "10",
day = "25",
doi = "10.1016/j.neuroscience.2004.07.015",
language = "English",
volume = "129",
pages = "35--48",
journal = "Neuroscience",
issn = "0306-4522",
publisher = "Elsevier Limited",
number = "1",

}

TY - JOUR

T1 - Functional similarities and differences of AMPA and kainate receptors expressed by cultured rat sensory neurons

AU - Lee, Changjoon

AU - Labrakakis, C.

AU - Joseph, D. J.

AU - MacDermott, A. B.

PY - 2004/10/25

Y1 - 2004/10/25

N2 - Dorsal root ganglion neurons express functional AMPA and kainate receptors near their central terminals. Activation of these receptors causes a decrease in glutamate release during action potential evoked synaptic transmission. Due to differences in kinetic properties and expression patterns of these two families of glutamate receptors in subpopulations of sensory neurons, AMPA and kainate receptors are expected to function differently. We used embryonic dorsal root ganglion (DRG) neurons maintained in culture to compare functional properties of kainate and AMPA receptors. Most DRG neurons in culture expressed kainate receptors and about half also expressed AMPA receptors. Most AMPA and kainate receptor-expressing DRG neurons were sensitive to capsaicin, suggesting involvement of these glutamate receptors in nociception. When activated by kainate, AMPA receptors were capable of driving a sustained train of action potentials while kainate receptors tended to activate action potential firing more transiently. Glutamate elicited more action potentials and a larger steady-state depolarization in neurons expressing both AMPA and kainate receptors than in neurons expressing only kainate receptors. Adding to their more potent activation properties, AMPA receptors recovered from desensitization much more quickly than kainate receptors. Activation of presynaptic receptors by low concentrations of kainate, but not ATPA, caused a tetrodotoxin-sensitive increase in the frequency of spontaneous EPSCs recorded in dorsal horn neurons. By recording synaptic pairs of DRG and dorsal horn neurons, we found that activation of presynaptic kainate and AMPA receptors decreased evoked glutamate release from terminals of DRG neurons in culture. Our data suggest that the endogenous ligand, glutamate, will cause a different physiological impact when activating these two types of non-NMDA glutamate receptors at central or peripheral nerve endings of sensory neurons.

AB - Dorsal root ganglion neurons express functional AMPA and kainate receptors near their central terminals. Activation of these receptors causes a decrease in glutamate release during action potential evoked synaptic transmission. Due to differences in kinetic properties and expression patterns of these two families of glutamate receptors in subpopulations of sensory neurons, AMPA and kainate receptors are expected to function differently. We used embryonic dorsal root ganglion (DRG) neurons maintained in culture to compare functional properties of kainate and AMPA receptors. Most DRG neurons in culture expressed kainate receptors and about half also expressed AMPA receptors. Most AMPA and kainate receptor-expressing DRG neurons were sensitive to capsaicin, suggesting involvement of these glutamate receptors in nociception. When activated by kainate, AMPA receptors were capable of driving a sustained train of action potentials while kainate receptors tended to activate action potential firing more transiently. Glutamate elicited more action potentials and a larger steady-state depolarization in neurons expressing both AMPA and kainate receptors than in neurons expressing only kainate receptors. Adding to their more potent activation properties, AMPA receptors recovered from desensitization much more quickly than kainate receptors. Activation of presynaptic receptors by low concentrations of kainate, but not ATPA, caused a tetrodotoxin-sensitive increase in the frequency of spontaneous EPSCs recorded in dorsal horn neurons. By recording synaptic pairs of DRG and dorsal horn neurons, we found that activation of presynaptic kainate and AMPA receptors decreased evoked glutamate release from terminals of DRG neurons in culture. Our data suggest that the endogenous ligand, glutamate, will cause a different physiological impact when activating these two types of non-NMDA glutamate receptors at central or peripheral nerve endings of sensory neurons.

KW - action potential

KW - capsaicin

KW - dorsal root ganglion

KW - presynaptic receptors

KW - spontaneous EPSCs

KW - synaptic transmission

UR - http://www.scopus.com/inward/record.url?scp=5444270687&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=5444270687&partnerID=8YFLogxK

U2 - 10.1016/j.neuroscience.2004.07.015

DO - 10.1016/j.neuroscience.2004.07.015

M3 - Article

VL - 129

SP - 35

EP - 48

JO - Neuroscience

JF - Neuroscience

SN - 0306-4522

IS - 1

ER -