Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus

Nature Neuroscience

Volumn 7, Issue 1, 2004, Pages 24-32

  Lin, Shih Chun ^a   Bergles, Dwight E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; AMPA RECEPTOR; NEUROTRANSMITTER;

ANIMAL TISSUE; ARTICLE; ELECTRON MICROSCOPY; HIPPOCAMPUS; IMMUNOFLUORESCENCE; INTERNEURON; MEMBRANE CURRENT; NEUROTRANSMISSION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; STEM CELL; SYNAPTIC TRANSMISSION;

ANIMALS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; INTERNEURONS; OLIGODENDROGLIA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; STEM CELLS; SYNAPSES;

EID: 0346102454     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1162     Document Type: Article

References (47)

1. Barres, B.A., Chun, L.L. & Corey, D.P. Ion channels in vertebrate glia. Annu. Rev. Neurosci. 13, 441-474 (1990).
2. Yuan, X., Eisen, A.M., McBain, C.J. & Gallo, V. A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 125, 2901-2914 (1998).
3. Stevens, B., Porta, S., Haak, L.L., Gallo, V. & Fields, R.D. Adenosine: a neuron-glia transmitter promoting myelination in the CNS in response to action potentials. Neuron 36, 855-868 (2002).
4. 2+-permeable AMPA receptors in Bergmann glia. Science 292, 926-929 (2001).
5. Kang, J., Jiang, L., Goldman, S.A. & Nedergaard, M. Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat. Neurosci. 1, 683-692 (1998).
6. Takano, T. et al. Glutamate release promotes growth of malignant gliomas. Nat. Med. 7, 1010-1015 (2001).
7. Follett, P.L., Rosenberg, P.A., Volpe, J.J. & Jensen, F.E. NBQX attenuates excitotoxic injury in developing white matter. J. Neurosci. 20, 9235-9241 (2000).
8. Barres, B.A. & Raff, M.C. Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361, 258-260 (1993).
9. + channel block. J Neurosci. 16, 2659-2670 (1996).
10. Raff, M.C., Miller, R.H. & Noble, M. A glia progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303, 390-396 (1983).
11. Barres, B.A., Koroshetz, W.J., Swartz, K.J., Chun, L.L. & Corey, D.P. Ion channel expression by white matter glia: the O-2A glia progenitor cell. Neuron 4, 507-524 (1990).
12. Patneau, D.K., Wright, P.W., Winters, C., Mayer, M.L. & Gallo, V. Glial cells of the oligodendrocyte lineage express both kainate- and AMPA-preferring subtypes of glutamate receptor. Neuron 12, 357-371 (1994).
13. A receptor in cultured murine cells of the oligodendrocyte lineage. Eur. J. Neurosci. 3, 310-316 (1991).
14. A receptors in cultured rat oligodendrocyte progenitor cells. Neuropharmacology 37, 859-873 (1998).
15. Levison, S.W., Young, G.M. & Goldman, J.E. Cycling cells in the adult rat neocortex preferentially generate oligodendroglia. J. Neurosci. Res. 57, 435-446 (1999).
16. Chang, A., Nishiyama, A., Peterson, J., Prineas, J. & Trapp, B.D. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J. Neurosci. 20, 6404-6412 (2000).
17. Isaacson, J.S., Solis, J.M. & Nicoll, R.A. Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10, 165-175 (1993).
18. Clark, B.A. & Cull-Candy, S.G. Activity-dependent recruitment of extrasynaptic NMDA receptor activation at an AMPA receptor-only synapse. J. Neurosci. 22, 4428-4436 (2002).
19. Bergles, D.E., Dzubay, J.A. & Jahr, C.E. Glutamate transporter currents in bergmann glial cells follow the time course of extrasynaptic glutamate. Proc. Natl. Acad. Sci. USA 94, 14821-14825 (1997).
20. Porter, J.T. & McCarthy, K.D. Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J. Neurosci. 16, 5073-5081 (1996).
21. Dzubay, J.A. & Jahr, C.E. The concentration of synaptically released glutamate outside of the climbing fiber-Purkinje cell synaptic cleft. J. Neurosci. 19, 5265-5274 (1999).
22. Bergles, D.E., Roberts, J.D., Somogyi, P. & Jahr, C.E. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405, 187-191 (2000).
23. Steinhauser, C., Berger, T., Frotscher, M. & Kettenmann, H. Heterogeneity in the membrane current pattern of identified glial cells in the hippocampal slice. Eur. J. Neurosci. 4, 472-484 (1992).
24. Levine, J.M., Reynolds, R. & Fawcett, J.W. The oligodendrocyte precursor cell in health and disease. Trends Neurosci. 24, 39-47 (2001).
25. Pitler, T.A. & Alger, B.E. Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J. Physiol. 450, 127-142 (1992).
26. Sciancalepore, M., Savic, N., Gyori, J. & Cherubini, E. Facilitation of miniature GABAergic currents by ruthenium red in neonatal rat hippocampal neurons. J. Neurophysiol. 80, 2316-2322 (1998).
27. A receptors. J. Neurosci. 20, 7914-7921 (2000).
28. A receptors in central synapses. J. Neurosci. 19, 578-588 (1999).
29. A receptor occupancy. Eur. J. Neurosci. 12, 810-818 (2000).
30. A receptor microscopic affinity. Neuropharmacology 35, 1383-1392 (1996).
31. Frerking, M., Borges, S. & Wilson, M. Variation in GABA mini amplitude is the consequence of variation in transmitter concentration. Neuron 15, 885-895 (1995).
32. Owens, D.F., Boyce, L.H., Davis, M.B. & Kriegstein, A.R. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforatedpatch recordings and calcium imaging. J. Neurosci. 16, 6414-6423 (1996).
33. Gilbert, P., Kettenmann, H. & Schachner, M. Gamma-aminobutyric acid directly depolarizes cultured oligodendrocytes. J. Neurosci. 4, 561-569 (1984).
34. Ebihara, S., Shirato, K., Harata, N. & Akaike, N. Gramicidin-perforated patch recording: GABA response in mammalian neurones with intact intracellular chloride. J. Physiol. 484, 77-86 (1995).
35. 2+-dependent AMPA receptor-mediated motoneuron death. J. Neurosci. 23, 4942-4950 (2003).
36. A receptors responsible for tonic and phasic conductances. Neurochem. Res. 26, 907-913 (2001).
37. Cohen, A.S., Lin, D.D. & Coulter, D.A. Protracted postnatal development of inhibitory synaptic transmission in rat hippocampal area CA1 neurons. J. Neurophysiol. 84, 2465-2476 (2000).
38. A receptor alphal subunit. J. Neurophysiol. 88, 3208-3217 (2002).
39. Burgard, E.C., Tietz, E.I., Neelands, T.R. & Macdonald, R.L. Properties of recombinant gamma-aminobutyric acid A receptor isoforms containing the alpha 5 subunit subtype. Mol. Pharmacol. 50, 119-127 (1996).
40. Brunig, I., Scotti, E., Sidler, C. & Fritschy, J.M. Intact sorting, targeting, and clustering of gamma-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J. Comp. Neurol. 443, 43-55 (2002).
41. A receptor. J. Neurosci. 22, 5572-5580 (2002).
42. Pastor, A., Chvatal, A., Sykova, E. & Kettenmann, H. Glycine- and GABA-activated currents in identified glial cells of the developing rat spinal cord slice. Eur. J. Neurosci. 7, 1188-1198 (1995).
43. Mudrick-Donnon, L.A., Williams, P.J., Pittman, Q.J. & MacVicar, B.A. Postsynaptic potentials mediated by GABA and dopamine evoked in stellate glial cells of the pituitary pars intermedia. J. Neurosci. 13, 4660-4668 (1993).
44. Theodosis, D.T. & MacVicar, B. Neurone-glia interactions in the hypothalamus and pituitary. Trends Neurosci. 19, 363-367 (1996).
45. Ganguly, K., Schinder, A.F., Wong, S.T. & Poo, M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105, 521-532 (2001).
46. A receptors. Science 269, 977-981 (1995).
47. Tillet, E., Ruggiero, F., Nishiyama, A. & Stallcup, W.B. The membrane-spanning proteoglycan NG2 binds to collagens V and VI through the central nonglobular domain of its core protein. J. Biol. Chem. 272, 10769-10776 (1997).