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PMID: 9405697 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Glutamate transporter currents in bergmann glial cells follow the time course of extrasynaptic glutamate.

Bergles DE, Dzubay JA, Jahr CE

Abstract

Glutamate transporters in the central nervous system are expressed in both neurons and glia, they mediate high affinity, electrogenic uptake of glutamate, and they are associated with an anion conductance that is stoichiometrically uncoupled from glutamate flux. Although a complete cycle of transport may require 50-100 ms, previous studies suggest that transporters can alter synaptic currents on a much faster time scale. We find that application of L-glutamate to outside-out patches from cerebellar Bergmann glia activates anion-potentiated glutamate transporter currents that activate in <1 ms, suggesting an efficient mechanism for the capture of extrasynaptic glutamate. Stimulation in the granule cell layer in cerebellar slices elicits all or none alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptor and glutamate transporter currents in Bergmann glia that have a rapid onset, suggesting that glutamate released from climbing fiber terminals escapes synaptic clefts and reaches glial membranes shortly after release. Comparison of the concentration dependence of both alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptor and glutamate transporter kinetics in patches with the time course of climbing fiber-evoked responses indicates that the glutamate transient at Bergmann glial membranes reaches a lower concentration than attained in the synaptic cleft and remains elevated in the extrasynaptic space for many milliseconds.

MeSH Terms
Animals Biological Transport Carrier Proteins/physiology Cells, Cultured Glutamic Acid/physiology Neuroglia/physiology Patch-Clamp Techniques Rats
Chemicals
Carrier Proteins Glutamic Acid
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Bergles D E
Vollum Institute L474, Oregon Health Sciences University, 3181 S.W. Sam Jackson Park Road, Portland, OR 97201-3098, USA.
Dzubay J A
Jahr C E
References (36)
36 references, click to expand
  1. Three-dimensional analysis of dendritic spines. III. Glial sheath.
    Anat Embryol (Berl). 1985;171(2):245-52 PMID: 3985373
  2. L-glutamate and L-glutamine uptake in adult rat cerebellum: an autoradiographic study.
    Neuroscience. 1982 May;7(5):1289-97 PMID: 6125917
  3. Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices.
    Neuron. 1990 Sep;5(3):247-53 PMID: 1976014
  4. The release and uptake of excitatory amino acids.
    Trends Pharmacol Sci. 1990 Nov;11(11):462-8 PMID: 1980041
  5. The time course of glutamate in the synaptic cleft.
    Science. 1992 Nov 27;258(5087):1498-501 PMID: 1359647
  6. Glutamate receptor channels in isolated patches from CA1 and CA3 pyramidal cells of rat hippocampal slices.
    J Physiol. 1992 Sep;455:143-71 PMID: 1282929
  7. A fast activating presynaptic reuptake current during serotonergic transmission in identified neurons of Hirudo.
    Neuron. 1993 Apr;10(4):559-72 PMID: 8386524
  8. Glutamate uptake from the synaptic cleft does not shape the decay of the non-NMDA component of the synaptic current.
    Neuron. 1993 Sep;11(3):541-9 PMID: 7691104
  9. The uptake inhibitor L-trans-PDC enhances responses to glutamate but fails to alter the kinetics of excitatory synaptic currents in the hippocampus.
    J Neurophysiol. 1993 Nov;70(5):2187-91 PMID: 7905032
  10. Glial contributions to excitatory neurotransmission in cultured hippocampal cells.
    Nature. 1994 Mar 3;368(6466):59-62 PMID: 7906399
  11. Synaptic and nonsynaptic localization of the GluR1 subunit of the AMPA-type excitatory amino acid receptor in the rat cerebellum.
    J Neurosci. 1994 May;14(5 Pt 1):2830-43 PMID: 8182442
  12. Prolonged presence of glutamate during excitatory synaptic transmission to cerebellar Purkinje cells.
    Neuron. 1994 Jun;12(6):1331-43 PMID: 7912092
  13. Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex.
    J Neurosci. 1994 Sep;14(9):5559-69 PMID: 7521911
  14. Localization of neuronal and glial glutamate transporters.
    Neuron. 1994 Sep;13(3):713-25 PMID: 7917301
  15. Mechanisms shaping glutamate-mediated excitatory postsynaptic currents in the CNS.
    Curr Opin Neurobiol. 1994 Jun;4(3):366-72 PMID: 7522678
  16. Functional properties and substrate specificity of the cloned L-glutamate/L-aspartate transporter GLAST-1 from rat brain expressed in Xenopus oocytes.
    J Neurosci. 1994 Oct;14(10):5759-65 PMID: 7523627
  17. Block of glutamate transporters potentiates postsynaptic excitation.
    Neuron. 1994 Nov;13(5):1195-203 PMID: 7946356
  18. A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis.
    J Neurophysiol. 1994 Aug;72(2):705-18 PMID: 7983529
  19. Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations.
    J Neurosci. 1995 Mar;15(3 Pt 1):1835-53 PMID: 7891138
  20. Kinetics of a human glutamate transporter.
    Neuron. 1995 May;14(5):1019-27 PMID: 7748550
  21. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry.
    Neuron. 1995 Sep;15(3):711-20 PMID: 7546749
  22. Ion fluxes associated with excitatory amino acid transport.
    Neuron. 1995 Sep;15(3):721-8 PMID: 7546750
  23. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate.
    Neuron. 1996 Mar;16(3):675-86 PMID: 8785064
  24. Dynamic changes in expression of glutamate transporter mRNAs in developing brain.
    Neuroreport. 1996 Feb 29;7(3):705-9 PMID: 8733726
  25. Monte Carlo simulation of fast excitatory synaptic transmission at a hippocampal synapse.
    J Neurophysiol. 1996 Feb;75(2):597-608 PMID: 8714637
  26. Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites.
    J Neurosci. 1996 Mar 1;16(5):1634-44 PMID: 8774432
  27. Flux coupling in a neuronal glutamate transporter.
    Nature. 1996 Oct 17;383(6601):634-7 PMID: 8857541
  28. Heterogeneity and functional properties of subtypes of sodium-dependent glutamate transporters in the mammalian central nervous system.
    Adv Pharmacol. 1997;37:69-115 PMID: 8891100
  29. Postsynaptic glutamate uptake in rat cerebellar Purkinje cells.
    J Physiol. 1996 Dec 1;497 ( Pt 2):523-30 PMID: 8961192
  30. Mutation of an amino acid residue influencing potassium coupling in the glutamate transporter GLT-1 induces obligate exchange.
    J Biol Chem. 1997 Jan 17;272(3):1703-8 PMID: 8999849
  31. Transporters buffer synaptically released glutamate on a submillisecond time scale.
    J Neurosci. 1997 Jun 15;17(12):4672-87 PMID: 9169528
  32. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1.
    Science. 1997 Jun 13;276(5319):1699-702 PMID: 9180080
  33. Long-term potentiation of glial synaptic currents in cerebellar culture.
    Neuron. 1997 Jun;18(6):983-94 PMID: 9208865
  34. Currents evoked in Bergmann glial cells by parallel fibre stimulation in rat cerebellar slices.
    J Physiol. 1997 Jul 15;502 ( Pt 2):335-50 PMID: 9263914
  35. Postsynaptic glutamate transport at the climbing fiber-Purkinje cell synapse.
    Science. 1997 Sep 5;277(5331):1515-8 PMID: 9278516
  36. Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors.
    J Neurosci. 1990 Jul;10(7):2385-99 PMID: 2165523
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1997-12-23
Pages
14821-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC25121
Subset
IM
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