The fate of synaptic input to NG2 glial cells: Neurons specifically downregulate transmitter release onto differentiating oligodendroglial cells

Journal of Neuroscience

Volumn 30, Issue 24, 2010, Pages 8320-8331

  Kukley, Maria ^a,c   Nishiyama, Akiko ^b   Dietrich, Dirk ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMATE TRANSPORTER; KAINIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; BRAIN SLICE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; ELECTROSTIMULATION; GLIA CELL; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; OLIGODENDROGLIA; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RECORDING;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTION POTENTIALS; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ANTIGENS; ASPARTIC ACID; BICUCULLINE; CELL DIFFERENTIATION; DOWN-REGULATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA AGENTS; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; MICE; MICE, TRANSGENIC; MYELIN PROTEOLIPID PROTEIN; NEURONS; NEUROTRANSMITTER AGENTS; NIPECOTIC ACIDS; OLIGODENDROGLIA; PATCH-CLAMP TECHNIQUES; PROTEOGLYCANS; STEM CELLS; SYNAPSES;

EID: 77953750781     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0854-10.2010     Document Type: Article

References (34)

1. Arranz AM, Hussein A, Alix JJ, Pérez-Cerdá F, Allcock N, Matute C, Fern R (2008) Functional glutamate transport in rodent optic nerve axons and glia. Glia 56:1353-1367.
2. + buffer capacity, and morphology of glial cells in the corpus callosum slice. J Neurosci 11:3008-3024.
3. Berger T, Schnitzer J, Orkand PM, Kettenmann H (1992) Sodium and calcium currents in glial cells of the mouse corpus callosum slice. Eur J Neurosci 4:1271-1284.
4. Bergles DE, Roberts JD, Somogyi P, Jahr CE (2000) Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405:187-191.
5. Chvátal A, Pastor A, Mauch M, Syková E, Kettenmann H (1995) Distinct populations of identified glial cells in the developing rat spinal cord slice: ion channel properties and cell morphology. Eur J Neurosci 7:129-142.
6. DeSilva TM, Kabakov AY, Goldhoff PE, Volpe JJ, Rosenberg PA (2009) Regulation of glutamate transport in developing rat oligodendrocytes. J Neurosci 29:7898-7908.
7. Fuss B, Mallon B, Phan T, Ohlemeyer C, Kirchhoff F, Nishiyama A, Macklin WB (2000) Purification and analysis of in vivo-differentiated oligodendrocytes expressing the green fluorescent protein. Dev Biol 218:259-274.
8. Gallo V, Mangin JM, Kukley M, Dietrich D (2008) Synapses on NG2-expressing progenitors in the brain: multiple functions? J Physiol 586:3767-3781.
9. 2+-permeable AMPA receptors. Science 312:1533-1537.
10. Ge WP, Zhou W, Luo Q, Jan LY, Jan YN (2009) Dividing glial cells maintain differentiated properties including complex morphology and functional synapses. Proc Natl Acad Sci U S A 106:328-333.
11. Káradó ttir R, Hamilton NB, Bakiri Y, Attwell D (2008) Spiking and non-spiking classes of oligodendrocyte precursor glia in CNS white matter. Nat Neurosci 11:450-456.
12. Kettenmann H, Steinhaeuser C (2005) Receptors for neurotransmitters and hormones. In: Neuroglia (Kettenmann H, Ransom BR, eds), pp 131-145. New York: Oxford UP.
13. Kukley M, Dietrich D (2009) Kainate receptors and signal integration by NG2 glial cells. Neuron Glia Biol 22:1-8.
14. Kukley M, Capetillo-Zarate E, Dietrich D (2007) Vesicular glutamate release from axons in white matter. Nat Neurosci 10:311-320.
15. Kukley M, Kiladze M, Tognatta R, Hans M, Swandulla D, Schramm J, Dietrich D (2008) Glial cells are born with synapses. FASEB J 22:2957-2969.
16. Lin SC, Bergles DE (2002) Physiological characteristics of NG2-expressing glial cells. J Neurocytol 31:537-549.
17. Lin SC, Bergles DE (2004) Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nat Neurosci 7:24-32.
18. Mallon BS, Shick HE, Kidd GJ, Macklin WB (2002) Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. J Neurosci 22:876-885.
19. Mangin JM, Kunze A, Chittajallu R, Gallo V (2008) Satellite NG2 progenitor cells share common glutamatergic inputs with associated interneurons in the mouse dentate gyrus. J Neurosci 28:7610-7623.
20. + glial cells receive coordinated excitatory synaptic input. J Gen Physiol 134:115-127.
21. Nishiyama A, Komitova M, Suzuki R, Zhu X (2009) Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10:9-22.
22. Novak A, Guo C, Yang W, Nagy A, Lobe CG (2000) Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein on Cremediated excision. Genesis 28:147-155.
23. Regan MR, Huang YH, Kim YS, Dykes-Hoberg MI, Jin L, Watkins AM, Bergles DE, Rothstein JD (2007) Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS. J Neurosci 27:6607-6619.
24. Schneggenburger R, Neher E (2000) Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406:889-893.
25. Shepherd GM, Harris KM (1998) Three-dimensional structure and composition of CA3→CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J Neurosci 18:8300-8310.
26. Sommer I, Schachner M (1981) Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol 83:311-327.
27. 2+-sensor model for neurotransmitter release in a central synapse. Nature 450:676-682.
28. 2+ exchangers is required for GABA-induced NG2 cell migration. J Cell Biol 186:113-128.
29. Trapp BD, Nishiyama A, Cheng D, Macklin W (1997) Differentiation and death of premyelinating oligodendrocytes in developing rodent brain. J Cell Biol 137:459-468.
30. Xu-Friedman MA, Regehr WG (2000) Probing fundamental aspects of synaptic transmission with strontium. J Neurosci 20:4414-4422.
31. Yuan X, Eisen AM, McBain CJ, Gallo V (1998) A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 125:2901-2914. (Pubitemid 28410214)
32. Zhu X, Bergles DE, Nishiyama A (2008a) NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135:145-157.
33. Zhu X, Hill RA, Nishiyama A (2008b) NG2 cells generate oligodendrocytes and gray matter astrocytes in the spinal cord. Neuron Glia Biol 4:19-26.
34. Ziskin JL, Nishiyama A, Rubio M, Fukaya M, Bergles DE (2007) Vesicular release of glutamate from unmyelinated axons in white matter. Nat Neurosci 10:321-330.