Excitability and synaptic communication within the oligodendrocyte lineage

Journal of Neuroscience

Volumn 30, Issue 10, 2010, Pages 3600-3611

  De Biase, Lindsay M ^a   Nishiyama, Akiko ^b   Bergles, Dwight E ^a  

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

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; IONOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL POPULATION; DOWN REGULATION; IMMUNOCOMPETENT CELL; MOUSE; NERVE CELL EXCITABILITY; NG2 IMMUNOREACTIVE CELL; NONHUMAN; OLIGODENDROGLIA; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CELL COMMUNICATION; CELL LINEAGE; GENE EXPRESSION PROFILING; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; OLIGODENDROGLIA; PROTEOCHONDROITIN SULFATES; SYNAPSES;

EID: 77949407878     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6000-09.2010     Document Type: Article

References (66)

1. Back SA (2006) Perinatal white matter injury: the changing spectrum of pathology and emerging insights into pathogenetic mechanisms. Ment Retard Dev Disabil Res Rev 12:129 -140.
2. Back SA, Luo NL, Borenstein NS, Levine JM, Volpe JJ, Kinney HC (2001) Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 21:1302-1312.
3. Back SA, Han BH, Luo NL, Chricton CA, Xanthoudakis S, Tam J, Arvin KL, Holtzman DM (2002) Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci 22:455- 463.
4. Barres BA, Raff MC (1993) Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361:258 -260.
5. Barres BA, Chun LL, Corey DP (1989) Glial and neuronal forms of the voltage-dependent sodium channel: characteristics and cell-type distribution. Neuron 2:1375-1388.
6. Barres BA, Koroshetz WJ, Swartz KJ, Chun LL, Corey DP (1990) Ion channel expression by white matter glia: the O-2A glial progenitor cell. Neuron 4:507-524.
7. Belachew S, Chittajallu R, Aguirre AA, Yuan X, Kirby M, Anderson S, Gallo V (2003) Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J Cell Biol 161:169 -186.
8. Berger T, Walz W, Schnitzer J, Kettenmann H (1992) GABA- and glutamate-activated currents in glial cells of the mouse corpus callosum slice. J Neurosci Res 31:21-27.
9. Bergles DE, Roberts JD, Somogyi P, Jahr CE (2000) Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405:187-191.
10. Bhat RV, Axt KJ, Fosnaugh JS, Smith KJ, Johnson KA, Hill DE, Kinzler KW, Baraban JM (1996) Expression of the APC tumor suppressor protein in oligodendroglia. Glia 17:169 -174.
11. Biber K, Neumann H, Inoue K, Boddeke HW (2007) Neuronal 'On' and 'Off' signals control microglia. Trends Neurosci 30:596-602.
12. Black JA, Liu S, Waxman SG (2009) Sodium channel activity modulates multiple functions in microglia. Glia 57:1072-1081.
13. Bowman EJ, Siebers A, Altendorf K (1988) Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci U S A 85:7972-7976.
14. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264 -278.
15. Chen PH, Cai WQ, Wang LY, Deng QY (2008) A morphological and electrophysiological study on the postnatal development of oligodendrocyte precursor cells in the rat brain. Brain Res 1243:27-37.
16. Chittajallu R, Aguirre A, Gallo V (2004) NG2-positive cells in the mouse white and grey matter display distinct physiological properties. J Physiol 561:109 -122.
17. Dawson MR, Polito A, Levine JM, Reynolds R (2003) NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 24:476-488.
18. Fatt P, Katz B (1952) Spontaneous subthreshold activity at motor nerve endings. J Physiol 117:109 -128.
19. Fern R, Möller T (2000) Rapid ischemic cell death in immature oligodendrocytes: a fatal glutamate release feedback loop. J Neurosci 20:34-42.
20. Fields RD, Burnstock G (2006) Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 7:423- 436.
21. Folkerth RD (2005) Neuropathologic substrate of cerebral palsy. J Child Neurol 20:940 -949.
22. Foran DR, Peterson AC (1992) Myelin acquisition in the central nervous system of the mouse revealed by an MBP-Lac Z transgene. J Neurosci 12:4890-4897.
23. + channel block. J Neurosci 16:2659 -2670.
24. Ge WP, Yang XJ, Zhang Z, Wang HK, Shen W, Deng QD, Duan S (2006) Long-term potentiation of neuron-glia synapses mediated by Ca2+-permeable AMPA receptors. Science 312:1533-1537.
25. 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.
26. v integrin/myelin proteolipid protein complex. J Neurosci 26:2458 -2466.
27. Guo F, Ma J, McCauley E, Bannerman P, Pleasure D (2009) Early postnatal proteolipid promoter-expressing progenitors produce multilineage cells in vivo. J Neurosci 29:7256 -7270.
28. Hayashi S, Lewis P, Pevny L, McMahon AP (2002) Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech Dev 119 [Suppl 1]:S97-S101.
29. Huang YH, Sinha SR, Tanaka K, Rothstein JD, Bergles DE (2004) Astrocyte glutamate transporters regulate metabotropic glutamate receptormediated excitation of hippocampal interneurons. J Neurosci 24:4551- 4559.
30. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249 -264.
31. Jabs R, Pivneva T, Hüttmann K, Wyczynski A, Nolte C, Kettenmann H, Steinhäuser C (2005) Synaptic transmission onto hippocampal glial cells with hGFAP promoter activity. J Cell Sci 118:3791-3803.
32. Johnston MV, Hoon AH Jr (2006) Cerebral palsy. Neuromolecular Med 8:435- 450.
33. Kaczmarek LK (2006) Non-conducting functions of voltage-gated ion channels. Nat Rev Neurosci 7:761-771.
34. Káradóttir R, Cavelier P, Bergersen LH, Attwell D (2005) NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438:1162-1166.
35. Káradóttir 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.
36. Krueger M, Bechmann I (2010) CNS pericytes: concepts, misconceptions, and a way out. Glia 58:1-10.
37. Kukley M, Capetillo-Zarate E, Dietrich D (2007) Vesicular glutamate release from axons in white matter. Nat Neurosci 10:311-320.
38. Levine JM (1994) Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J Neurosci 14:4716-4730.
39. Lin SC, Bergles DE (2004) Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nat Neurosci 7:24 -32.
40. Lin SC, Huck JH, Roberts JD, Macklin WB, Somogyi P, Bergles DE (2005) Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron 46:773-785.
41. 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.
42. Mangin JM, Kunze A, Chittajallu R, GalloV (2008) Satellite NG2 progenitor cells share common glutamatergic inputs with associated interneurons in the mouse dentate gyrus. J Neurosci 28:7610 -7623.
43. Maricich SM, Herrup K (1999) Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J Neurobiol 41:281-294.
44. Micu I, Jiang Q, Coderre E, Ridsdale A, Zhang L, Woulfe J, Yin X, Trapp BD, McRory JE, Rehak R, Zamponi GW, Wang W, Stys PK (2006) NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 439:988 -992.
45. Nave KA, Trapp BD (2008) Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci 31:535-561.
46. Novak A, Guo C, Yang W, Nagy A, Lobe CG (2000) Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cremediated excision. Genesis 28:147-155.
47. Ono K, Kagawa T, Tsumori T, Yokota S, Yasui Y (2001) Morphological changes and cellular dynamics of oligodendrocyte lineage cells in the developing vertebrate central nervous system. Dev Neurosci 23:346 -355.
48. Purves D, Augustine GJ, Fitzpatrick D, Katz LC, LaMantia AS, McNamara JO, Williams SM, ed (2001) Neuroscience, Ed 2. Sunderland, MA: Sinauer.
49. 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.
50. Reyners H, Gianfelici de Reyners E, Regniers L, Maisin JR (1986) A glial progenitor cell in the cerebral cortex of the adult rat. J Neurocytol 15:53- 61.
51. Riddle A, Luo NL, Manese M, Beardsley DJ, Green L, Rorvik DA, Kelly KA, Barlow CH, Kelly JJ, Hohimer AR, Back SA (2006) Spatial heterogeneity in oligodendrocyte lineage maturation and not cerebral blood flow predicts fetal ovine periventricular white matter injury. J Neurosci 26:3045-3055.
52. Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A, Kessaris N, RichardsonWD (2008) PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 12:1392-1401.
53. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197-1207.
54. Salter MG, Fern R (2005) NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438:1167-1171.
55. Sontheimer H, Trotter J, Schachner M, Kettenmann H (1989) Channel expression correlates with differentiation stage during the development of oligodendrocytes from their precursor cells in culture. Neuron 2:1135-1145.
56. Stevens B, Porta S, Haak LL, Gallo V, Fields RD (2002) Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36:855- 868.
57. Stevens CF, Tsujimoto T (1995) Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc Natl Acad Sci U S A 92:846-849.
58. Tekkök SB, Ye Z, Ransom BR (2007) Excitotoxic mechanisms of ischemic injury in myelinated white matter. J Cereb Blood Flow Metab 27:1540-1552.
59. Verity AN, Campagnoni AT (1988) Regional expression of myelin protein genes in the developing mouse brain: in situ hybridization studies. J Neurosci Res 21:238 -248.
60. Verkhratsky A, Steinhäuser C (2000) Ion channels in glial cells. Brain Res Brain Res Rev 32:380-412.
61. Weisheit G, Gliem M, Endl E, Pfeffer PL, Busslinger M, Schilling K (2006) Postnatal development of the murine cerebellar cortex: formation and early dispersal of basket, stellate and Golgi neurons. Eur J Neurosci 24:466-478.
62. 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.
63. Zhou Q, Petersen CC, Nicoll RA (2000) Effects of reduced vesicular filling on synaptic transmission in rat hippocampal neurones. J Physiol 525 Pt 1:195-206.
64. Zhu X, Hill RA, Nishiyama A (2008a) NG2 cells generate oligodendrocytes and gray matter astrocytes in the spinal cord. Neuron Glia Biol 4:19 -26.
65. Zhu X, Bergles DE, Nishiyama A (2008b) NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135:145-157.
66. 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.