Glutamate-, kainate- and NMDA-evoked membrane currents in identified glial cells in rat spinal cord slice.

The effect of L-glutamate, kainate and N-methyl-D-aspartate (NMDA) on membrane currents of astrocytes, oligodendrocytes and their respective precursors was studied in acute spinal cord slices of rats between the ages of postnatal days 5 and 13 using the whole-cell patch-clamp technique. L-glutamate (10(-3) M), kainate (10(-3) M), and NMDA (2x10(-3) M) evoked inward currents in all glial cells. Kainate evoked larger currents in precursors than in astrocytes and oligodendrocytes, while NMDA induced larger currents in astrocytes and oligodendrocytes than in precursors. Kainate-evoked currents were blocked by the AMPA/kainate receptor antagonist CNQX (10(-4) M) and were, with the exception of the precursors, larger in dorsal than in ventral horns, as were NMDA-evoked currents. Currents evoked by NMDA were unaffected by CNQX and, in contrast to those seen in neurones, were not sensitive to Mg2+. In addition, they significantly decreased during development and were present when synaptic transmission was blocked in a Ca2+-free solution. NMDA-evoked currents were not abolished during the block of K+ inward currents in glial cells by Ba2+; thus they are unlikely to be mediated by an increase in extracellular K+ during neuronal activity. We provide evidence that spinal cord glial cells are sensitive to the application of L-glutamate, kainate and transiently, during postnatal development, to NMDA.

[1]  Christian Steinhäuser,et al.  News on glutamate receptors in glial cells , 1996, Trends in Neurosciences.

[2]  I. Holopainen,et al.  Glutamate receptor‐linked changes in membrane potential and intracellular Ca2+ in primary rat astrocytes , 1989, Glia.

[3]  K. Sakimura,et al.  Molecular diversity of the NMDA receptor channel , 1992, Nature.

[4]  G. Rougon,et al.  Functional N-methyl-D-aspartate receptors in O-2A glial precursor cells: a critical role in regulating polysialic acid-neural cell adhesion molecule expression and cell migration , 1996, The Journal of cell biology.

[5]  S. Chiu,et al.  The role of potassium channels in Schwann cell proliferation in Wallerian degeneration of explant rabbit sciatic nerves. , 1989, The Journal of physiology.

[6]  H. Kettenmann,et al.  Properties of GABA and glutamate responses in identified glial cells of the mouse hippocampal slice , 1994, Hippocampus.

[7]  K. McCarthy,et al.  GFAP‐positive hippocampal astrocytes in situ respond to glutamatergic neuroligands with increases in [Ca2+]i , 1995, Glia.

[8]  A. Mathie,et al.  Activation of glutamate receptors and glutamate uptake in identified macroglial cells in rat cerebellar cultures. , 1991, The Journal of physiology.

[9]  V. Gallo,et al.  Oligodendrocyte progenitor cell proliferation and lineage progression are regulated by glutamate receptor-mediated K+ channel block , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  M. Mayer,et al.  Permeation and block of N‐methyl‐D‐aspartic acid receptor channels by divalent cations in mouse cultured central neurones. , 1987, The Journal of physiology.

[11]  R J Miller,et al.  Glutamate receptors activate Ca2+ mobilization and Ca2+ influx into astrocytes. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[12]  D. Puro,et al.  Glutamate as a neuron-to-glial signal for mitogenesis: role of glialN-methyl-d-aspartate receptors , 1993, Brain Research.

[13]  H. Kettenmann,et al.  Gamma-aminobutyric acid and glutamate receptors , 1995 .

[14]  T. Berger,et al.  Calcium entry through kainate receptors and resulting potassium-channel blockade in Bergmann glial cells. , 1992, Science.

[15]  F. Conti,et al.  Expression of NR1 and NR2A/B subunits of the NMDA receptor in cortical astrocytes , 1996, Glia.

[16]  K. Borges,et al.  Blockade of K+ channels induced by AMPA/kainate receptor activation in mouse oligodendrocyte precursor cells is mediated by NA+ entry , 1995, Journal of neuroscience research.

[17]  C. Polosa,et al.  Fast excitatory postsynaptic potentials and the responses to excitant amino acids of sympathetic preganglionic neurons in the slice of the cat spinal cord , 1992, Neuroscience.

[18]  H. Kettenmann,et al.  Glycine‐ and GABA‐activated Currents in Identified Glial Cells of the Developing Rat Spinal Cord Slice , 1995, The European journal of neuroscience.

[19]  T. Berger,et al.  Developmental regulation of ion channels and receptors on glial cells. , 1995, Perspectives on developmental neurobiology.

[20]  H. Marrero,et al.  Nerve impulses increase glial intercellular permeability , 1996, Glia.

[21]  C. Tang,et al.  Membrane properties of neuroglia in the optic nerve of Necturus. , 1981, The Journal of experimental biology.

[22]  R. Kalb,et al.  Quantitative and qualitative changes in AMPA receptor expression during spinal cord development , 1995, Neuroscience.

[23]  C. Steinhäuser,et al.  Glial Cells in the Mouse Hippocampus Express AMPA Receptors with an Intermediate Ca2+ Permeability , 1995, The European journal of neuroscience.

[24]  V. Gallo,et al.  Excitatory amino acid receptors in glia: Different subtypes for distinct functions? , 1995, Journal of neuroscience research.

[25]  K. Chandy,et al.  Voltage-gated K+ channels in human T lymphocytes: a role in mitogenesis? , 1984, Nature.

[26]  S. Heinemann,et al.  Cloned glutamate receptors. , 1994, Annual review of neuroscience.

[27]  T. Berger,et al.  GABA‐ and glutamate‐activated currents in glial cells of the mouse corpus callosum slice , 1992, Journal of neuroscience research.

[28]  A. Cornell-Bell,et al.  Glutamate‐induced calcium signaling in astrocytes , 1994, Glia.

[29]  J. Grosche,et al.  NMDA-activated currents in Bergmann glial cells. , 1993, Neuroreport.

[30]  K. McCarthy,et al.  Hippocampal Astrocytes In Situ Respond to Glutamate Released from Synaptic Terminals , 1996, The Journal of Neuroscience.

[31]  T. Berger.  AMPA‐type glutamate receptors in glial precursor cells of the rat corpus callosum: Ionic and pharmacological properties , 1995, Glia.

[32]  H. Kettenmann,et al.  Distinct Populations of Identified Glial Cells in the Developing Rat Spinal Cord Slice: Ion Channel Properties and Cell Morphology , 1995, The European journal of neuroscience.

[33]  J. Beal,et al.  Axonal and dendritic development of substantia gelatinosa neurons in the lumbosacral spinal cord of the rat , 1984, The Journal of comparative neurology.

[34]  M. Droge,et al.  Distribution of NMDA receptor binding in developing mouse spinal cord , 1993, Neuroscience Letters.

[35]  M J Halsted,et al.  N-methyl-D-aspartate receptors are transiently expressed in the developing spinal cord ventral horn. , 1992, Proceedings of the National Academy of Sciences of the United States of America.