Functional identification of activity‐regulated, high‐affinity glutamine transport in hippocampal neurons inhibited by riluzole
Glutamine (Gln) is considered the preferred precursor for the neurotransmitter pool of glutamate (Glu), the major excitatory transmitter in the mammalian CNS. Here, an activity‐regulated, high‐affinity Gln transport system is described in developing and mature neuron‐enriched hippocampal cultures th...
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| Published in | Journal of neurochemistry Vol. 142; no. 1; pp. 29 - 40 |
|---|---|
| Main Author | |
| Format | Journal Article |
| Language | English |
| Published |
England
Blackwell Publishing Ltd
01.07.2017
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| Abstract | Glutamine (Gln) is considered the preferred precursor for the neurotransmitter pool of glutamate (Glu), the major excitatory transmitter in the mammalian CNS. Here, an activity‐regulated, high‐affinity Gln transport system is described in developing and mature neuron‐enriched hippocampal cultures that is potently inhibited by riluzole (IC50 1.3 ± 0.5 μM), an anti‐glutamatergic drug, and is blocked by low concentrations of 2‐(methylamino)isobutyrate (MeAIB), a system A transport inhibitor. K+‐stimulated MeAIB transport displays an affinity (Km) for MeAIB of 37 ± 1.2 μM, saturates at ~ 200 μM, is dependent on extracellular Ca2+, and is blocked by inhibition of voltage‐gated Ca2+ channels. Spontaneous MeAIB transport is also dependent on extracellullar Ca2+ and voltage‐gated calcium channels, but is also blocked by the Na+ channel blocker tetrodotoxin, by Glu receptor antagonists, and by GABA indicating its dependence on intact neural circuits driven by endogenous glutamatergic activity. The transport of MeAIB itself does not rely on Ca2+, but on Na+ ions, and is pH sensitive. Activity‐regulated, riluzole‐sensitive spontaneous and K+‐stimulated transport is minimal at 7–8 days in vitro, coordinately induced during the next 2 weeks and is maximally expressed by days in vitro > 20; the known period for maturation of the Glu/Gln cycle and regulated pre‐synaptic Glu release. Competition analyses with various amino acids indicate that Gln is the most likely physiological substrate. Activity‐regulated Gln/MeAIB transport is not observed in astrocytes. The functional identification of activity‐regulated, high‐affinity, riluzole‐sensitive Gln/MeAIB transport in hippocampal neurons may have important ramifications in the neurobiology of activity‐stimulated pre‐synaptic Glu release, the Glu/Gln cycle between astrocytes and neurons, and neuronal Glu‐induced excitotoxicity.
Cover Image for this issue: doi: 10.1111/jnc.13805.
This report describes a Ca2+‐regulated ‘system A’ glutamine transport system in hippocampal neuron‐enriched primary cultures that is dependent on neural activity in mature synapses, potently inhibited by riluzole (a blocker of synaptic glutamate release), and that is up‐regulated during the critical postnatal period of functional maturation of the glutamate/glutamine cycle between astrocytes and neurons and synaptic glutamate release. The novel high‐affinity system A transporter described here may have physiological and pathological implications in understanding the neurobiology of excitotoxic synaptic glutamate release in acute and chronic neurodegenerative diseases.
Cover Image for this issue: doi: 10.1111/jnc.13805. |
|---|---|
| AbstractList | Abstract
Glutamine (Gln) is considered the preferred precursor for the neurotransmitter pool of glutamate (Glu), the major excitatory transmitter in the mammalian
CNS
. Here, an activity‐regulated, high‐affinity Gln transport system is described in developing and mature neuron‐enriched hippocampal cultures that is potently inhibited by riluzole (
IC
50
1.3 ± 0.5 μM), an anti‐glutamatergic drug, and is blocked by low concentrations of 2‐(methylamino)isobutyrate (Me
AIB
), a system A transport inhibitor. K
+
‐stimulated Me
AIB
transport displays an affinity (
K
m
) for Me
AIB
of 37 ± 1.2 μM, saturates at ~ 200 μM, is dependent on extracellular Ca
2+
, and is blocked by inhibition of voltage‐gated Ca
2+
channels. Spontaneous Me
AIB
transport is also dependent on extracellullar Ca
2+
and voltage‐gated calcium channels, but is also blocked by the Na
+
channel blocker tetrodotoxin, by Glu receptor antagonists, and by
GABA
indicating its dependence on intact neural circuits driven by endogenous glutamatergic activity. The transport of Me
AIB
itself does not rely on Ca
2+
, but on Na
+
ions, and is
pH
sensitive. Activity‐regulated, riluzole‐sensitive spontaneous and K
+
‐stimulated transport is minimal at 7–8 days
in vitro
, coordinately induced during the next 2 weeks and is maximally expressed by days
in vitro
> 20; the known period for maturation of the Glu/Gln cycle and regulated pre‐synaptic Glu release. Competition analyses with various amino acids indicate that Gln is the most likely physiological substrate. Activity‐regulated Gln/Me
AIB
transport is not observed in astrocytes. The functional identification of activity‐regulated, high‐affinity, riluzole‐sensitive Gln/Me
AIB
transport in hippocampal neurons may have important ramifications in the neurobiology of activity‐stimulated pre‐synaptic Glu release, the Glu/Gln cycle between astrocytes and neurons, and neuronal Glu‐induced excitotoxicity.
image
Cover Image
for this issue: doi:
10.1111/jnc.13805
. Glutamine (Gln) is considered the preferred precursor for the neurotransmitter pool of glutamate (Glu), the major excitatory transmitter in the mammalian CNS. Here, an activity-regulated, high-affinity Gln transport system is described in developing and mature neuron-enriched hippocampal cultures that is potently inhibited by riluzole (IC50 1.3 ± 0.5 μM), an anti-glutamatergic drug, and is blocked by low concentrations of 2-(methylamino)isobutyrate (MeAIB), a system A transport inhibitor. K+ -stimulated MeAIB transport displays an affinity (Km ) for MeAIB of 37 ± 1.2 μM, saturates at ~ 200 μM, is dependent on extracellular Ca2+ , and is blocked by inhibition of voltage-gated Ca2+ channels. Spontaneous MeAIB transport is also dependent on extracellullar Ca2+ and voltage-gated calcium channels, but is also blocked by the Na+ channel blocker tetrodotoxin, by Glu receptor antagonists, and by GABA indicating its dependence on intact neural circuits driven by endogenous glutamatergic activity. The transport of MeAIB itself does not rely on Ca2+ , but on Na+ ions, and is pH sensitive. Activity-regulated, riluzole-sensitive spontaneous and K+ -stimulated transport is minimal at 7-8 days in vitro, coordinately induced during the next 2 weeks and is maximally expressed by days in vitro > 20; the known period for maturation of the Glu/Gln cycle and regulated pre-synaptic Glu release. Competition analyses with various amino acids indicate that Gln is the most likely physiological substrate. Activity-regulated Gln/MeAIB transport is not observed in astrocytes. The functional identification of activity-regulated, high-affinity, riluzole-sensitive Gln/MeAIB transport in hippocampal neurons may have important ramifications in the neurobiology of activity-stimulated pre-synaptic Glu release, the Glu/Gln cycle between astrocytes and neurons, and neuronal Glu-induced excitotoxicity. Cover Image for this issue: doi: 10.1111/jnc.13805. Glutamine (Gln) is considered the preferred precursor for the neurotransmitter pool of glutamate (Glu), the major excitatory transmitter in the mammalian CNS. Here, an activity-regulated, high-affinity Gln transport system is described in developing and mature neuron-enriched hippocampal cultures that is potently inhibited by riluzole (IC 1.3 ± 0.5 μM), an anti-glutamatergic drug, and is blocked by low concentrations of 2-(methylamino)isobutyrate (MeAIB), a system A transport inhibitor. K -stimulated MeAIB transport displays an affinity (K ) for MeAIB of 37 ± 1.2 μM, saturates at ~ 200 μM, is dependent on extracellular Ca , and is blocked by inhibition of voltage-gated Ca channels. Spontaneous MeAIB transport is also dependent on extracellullar Ca and voltage-gated calcium channels, but is also blocked by the Na channel blocker tetrodotoxin, by Glu receptor antagonists, and by GABA indicating its dependence on intact neural circuits driven by endogenous glutamatergic activity. The transport of MeAIB itself does not rely on Ca , but on Na ions, and is pH sensitive. Activity-regulated, riluzole-sensitive spontaneous and K -stimulated transport is minimal at 7-8 days in vitro, coordinately induced during the next 2 weeks and is maximally expressed by days in vitro > 20; the known period for maturation of the Glu/Gln cycle and regulated pre-synaptic Glu release. Competition analyses with various amino acids indicate that Gln is the most likely physiological substrate. Activity-regulated Gln/MeAIB transport is not observed in astrocytes. The functional identification of activity-regulated, high-affinity, riluzole-sensitive Gln/MeAIB transport in hippocampal neurons may have important ramifications in the neurobiology of activity-stimulated pre-synaptic Glu release, the Glu/Gln cycle between astrocytes and neurons, and neuronal Glu-induced excitotoxicity. Cover Image for this issue: doi: 10.1111/jnc.13805. Glutamine (Gln) is considered the preferred precursor for the neurotransmitter pool of glutamate (Glu), the major excitatory transmitter in the mammalian CNS. Here, an activity-regulated, high-affinity Gln transport system is described in developing and mature neuron-enriched hippocampal cultures that is potently inhibited by riluzole (IC 50 1.3 +/− 0.5µM), an anti-glutamatergic drug, and is blocked by low concentrations of 2-(methylamino)isobutyrate (MeAIB), a system A transport inhibitor. K + -stimulated MeAIB transport displays an affinity ( K m ) for MeAIB of 37 +/− 1.2 µM, saturates at ~200 µM, is dependent on extracellular Ca 2+ , and is blocked by inhibition of voltage gated Ca 2+ -channels (VGCCs). Spontaneous MeAIB transport is also dependent on extracellullar Ca 2+ and VGCCs, but is also blocked by the Na + channel blocker tetrodotoxin, by Glu receptor antagonists, and by GABA indicating its dependence on intact neural circuits driven by endogenous glutamatergic activity. The transport of MeAIB itself does not rely on Ca 2+ , but on Na + ions, and is pH-sensitive. Activity-regulated, riluzole-sensitive spontaneous and K + -stimulated transport is minimal at 7–8 days in vitro (DIV), coordinantly induced during the next two weeks, and is maximally expressed by DIV>20; the known period for maturation of the Glu/Gln cycle and regulated presynaptic Glu release. Competition analyses with various amino acids indicate that Gln is the most likely physiological substrate. Activity-regulated Gln/MeAIB transport is not observed in astrocytes. The functional identification of activity-regulated, high-affinity, riluzole-sensitive Gln/MeAIB transport in hippocampal neurons may have important ramifications in the neurobiology of activity stimulated presynaptic Glu release, the Glu/Gln cycle between astrocytes and neurons, and neuronal Glu-induced excitotoxicity. This report describes a Ca 2+ -regulated ‘system A’ glutamine transport system in hippocampal neuron-enriched primary cultures that is dependent on neural activity in mature synapses, potently inhibited by riluzole (a blocker of synaptic glutamate release), and that is up-regulated during the critical postnatal period of functional maturation of the glutamate/glutamine cycle between astrocytes and neurons and synaptic glutamate release. The novel high-affinity system A transporter described here may have physiological and pathological implications in understanding the neurobiology of excitotoxic synaptic glutamate release in acute and chronic neurodegenerative diseases. Glutamine (Gln) is considered the preferred precursor for the neurotransmitter pool of glutamate (Glu), the major excitatory transmitter in the mammalian CNS. Here, an activity‐regulated, high‐affinity Gln transport system is described in developing and mature neuron‐enriched hippocampal cultures that is potently inhibited by riluzole (IC50 1.3 ± 0.5 μM), an anti‐glutamatergic drug, and is blocked by low concentrations of 2‐(methylamino)isobutyrate (MeAIB), a system A transport inhibitor. K+‐stimulated MeAIB transport displays an affinity (Km) for MeAIB of 37 ± 1.2 μM, saturates at ~ 200 μM, is dependent on extracellular Ca2+, and is blocked by inhibition of voltage‐gated Ca2+ channels. Spontaneous MeAIB transport is also dependent on extracellullar Ca2+ and voltage‐gated calcium channels, but is also blocked by the Na+ channel blocker tetrodotoxin, by Glu receptor antagonists, and by GABA indicating its dependence on intact neural circuits driven by endogenous glutamatergic activity. The transport of MeAIB itself does not rely on Ca2+, but on Na+ ions, and is pH sensitive. Activity‐regulated, riluzole‐sensitive spontaneous and K+‐stimulated transport is minimal at 7–8 days in vitro, coordinately induced during the next 2 weeks and is maximally expressed by days in vitro > 20; the known period for maturation of the Glu/Gln cycle and regulated pre‐synaptic Glu release. Competition analyses with various amino acids indicate that Gln is the most likely physiological substrate. Activity‐regulated Gln/MeAIB transport is not observed in astrocytes. The functional identification of activity‐regulated, high‐affinity, riluzole‐sensitive Gln/MeAIB transport in hippocampal neurons may have important ramifications in the neurobiology of activity‐stimulated pre‐synaptic Glu release, the Glu/Gln cycle between astrocytes and neurons, and neuronal Glu‐induced excitotoxicity. Cover Image for this issue: doi: 10.1111/jnc.13805. This report describes a Ca2+‐regulated ‘system A’ glutamine transport system in hippocampal neuron‐enriched primary cultures that is dependent on neural activity in mature synapses, potently inhibited by riluzole (a blocker of synaptic glutamate release), and that is up‐regulated during the critical postnatal period of functional maturation of the glutamate/glutamine cycle between astrocytes and neurons and synaptic glutamate release. The novel high‐affinity system A transporter described here may have physiological and pathological implications in understanding the neurobiology of excitotoxic synaptic glutamate release in acute and chronic neurodegenerative diseases. Cover Image for this issue: doi: 10.1111/jnc.13805. Glutamine (Gln) is considered the preferred precursor for the neurotransmitter pool of glutamate (Glu), the major excitatory transmitter in the mammalian CNS. Here, an activity-regulated, high-affinity Gln transport system is described in developing and mature neuron-enriched hippocampal cultures that is potently inhibited by riluzole (IC50 1.3 ± 0.5 µM), an anti-glutamatergic drug, and is blocked by low concentrations of 2-(methylamino)isobutyrate (MeAIB), a system A transport inhibitor. K+-stimulated MeAIB transport displays an affinity (Km) for MeAIB of 37 ± 1.2 µM, saturates at ~ 200 µM, is dependent on extracellular Ca2+, and is blocked by inhibition of voltage-gated Ca2+ channels. Spontaneous MeAIB transport is also dependent on extracellullar Ca2+ and voltage-gated calcium channels, but is also blocked by the Na+ channel blocker tetrodotoxin, by Glu receptor antagonists, and by GABA indicating its dependence on intact neural circuits driven by endogenous glutamatergic activity. The transport of MeAIB itself does not rely on Ca2+, but on Na+ ions, and is pH sensitive. Activity-regulated, riluzole-sensitive spontaneous and K+-stimulated transport is minimal at 7-8 days in vitro, coordinately induced during the next 2 weeks and is maximally expressed by days in vitro > 20; the known period for maturation of the Glu/Gln cycle and regulated pre-synaptic Glu release. Competition analyses with various amino acids indicate that Gln is the most likely physiological substrate. Activity-regulated Gln/MeAIB transport is not observed in astrocytes. The functional identification of activity-regulated, high-affinity, riluzole-sensitive Gln/MeAIB transport in hippocampal neurons may have important ramifications in the neurobiology of activity-stimulated pre-synaptic Glu release, the Glu/Gln cycle between astrocytes and neurons, and neuronal Glu-induced excitotoxicity. Cover Image for this issue: doi: 10.1111/jnc.13805. |
| Author | Erickson, Jeffrey D. |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28423185$$D View this record in MEDLINE/PubMed |
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| Copyright | 2017 International Society for Neurochemistry 2017 International Society for Neurochemistry. Copyright © 2017 International Society for Neurochemistry |
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| Keywords | neurotransmitter cycling neuronal glutamine transporter glutamate/glutamine cycle excitotoxicity activity-dependent regulation neuroprotection |
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| Publisher | Blackwell Publishing Ltd |
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| Snippet | Glutamine (Gln) is considered the preferred precursor for the neurotransmitter pool of glutamate (Glu), the major excitatory transmitter in the mammalian CNS.... Abstract Glutamine (Gln) is considered the preferred precursor for the neurotransmitter pool of glutamate (Glu), the major excitatory transmitter in the... |
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| SubjectTerms | activity‐dependent regulation Affinity Amino Acid Transport System X-AG - drug effects Amino acids Animals Astrocytes Astrocytes - drug effects Astrocytes - metabolism Axonal transport beta-Alanine - analogs & derivatives beta-Alanine - metabolism Calcium Calcium (extracellular) Calcium - metabolism Calcium Channel Blockers - pharmacology Calcium channels Calcium channels (voltage-gated) Calcium transport Central nervous system Channels Circuits Competition Displays Enrichment Excitatory Amino Acid Antagonists - pharmacology Excitotoxicity Female Functional anatomy glutamate/glutamine cycle Glutamatergic transmission Glutamic acid Glutamine Glutamine - metabolism Hippocampus Hippocampus - cytology Hippocampus - drug effects Hippocampus - metabolism In vitro methods and tests Inhibition Inhibitors Ions Low concentrations Mammals Maturation Nervous system Neural networks neuronal glutamine transporter Neurons Neurons - drug effects Neurons - metabolism neuroprotection Neuroprotective Agents - pharmacology Neurosciences neurotransmitter cycling Physiology Potassium - pharmacology Pregnancy Rats Rats, Sprague-Dawley Riluzole - pharmacology Sodium channels (voltage-gated) Tetrodotoxin Transport γ-Aminobutyric acid |
| Title | Functional identification of activity‐regulated, high‐affinity glutamine transport in hippocampal neurons inhibited by riluzole |
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