Bidirectional plasticity of calcium-permeable AMPA receptors in oligodendrocyte lineage cells

Nature Neuroscience

Volumn 14, Issue 11, 2011, Pages 1430-1438

  Zonouzi, Marzieh ^a   Renzi, Massimiliano ^a   Farrant, Mark ^a   Cull Candy, Stuart G ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMPA RECEPTOR; CALCIUM; GLUTAMIC ACID; METABOTROPIC RECEPTOR 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN INTERACTING WITH PROTEIN KINASE C; PURINERGIC RECEPTOR; REGULATOR PROTEIN; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CELL LINEAGE; CEREBELLUM CORTEX; CONTROLLED STUDY; FEMALE; HOMEOSTASIS; MALE; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; OLIGODENDROGLIA; OPTIC NERVE; PERMEABILITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; STEM CELL; WHITE MATTER; ERRATUM; ERROR;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS; BIOPHYSICAL PROCESSES; CALCIUM; CALCIUM CHANNELS; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; CEREBELLUM; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGENTS; FEMALE; GALACTOSYLCERAMIDASE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMIC ACID; GLYCINE AGENTS; ION CHANNEL GATING; LUMINESCENT PROTEINS; MALE; MEMBRANE POTENTIALS; METHOXYHYDROXYPHENYLGLYCOL; MICE; MICE, TRANSGENIC; MUTATION; NEURONAL PLASTICITY; NUCLEAR PROTEINS; OLIGODENDROGLIA; OPTIC NERVE; PROTEOGLYCANS; RATS; RECEPTORS, AMPA; SIGNAL TRANSDUCTION; STEM CELLS; STRYCHNINE; TETRODOTOXIN;

EID: 80054989222     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2942     Document Type: Article

References (50)

1. Gallo, V. et al. Oligodendrocyte progenitor cell proliferation and lineage progression are regulated by glutamate receptor-mediated K+ channel block. J. Neurosci. 16, 2659-2670 (1996). (Pubitemid 26124352)
2. Gudz T.I., Komuro, H. & Macklin, W.B. Glutamate stimulates oligodendrocyte progenitor migration mediated via an alphav integrin/myelin proteolipid protein complex. J. Neurosci. 26, 2458-2466 (2006). (Pubitemid 44699006)
3. 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). (Pubitemid 30313537)
4. Traynelis, S.F. et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62, 405496 (2010).
5. Geiger, J.R. et al. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193-204 (1995).
6. Cahoy, J.D. et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: anew resource for understanding brain development and function. J. Neurosci. 28, 264-278 (2008).
7. De Biase, L.M., Nishiyama, A. & Bergles, D.E. Excitability and synaptic communication within the oligodendrocyte lineage. J. Neurosci. 30, 36003611 (2010).
8. Etxeberria, A., Mangin, J.-M., Aguirre, A. & Gallo, V. Adult-born SVZ progenitors receive transient synapses during remyelination in corpus callosum. Nat. Neurosci. 13, 287-289 (2010).
9. Fern, R. & Moller, T. Rapid ischemic cell death in immature oligodendrocytes: a fatal glutamate release feedback loop. J. Neurosci. 20, 34-42 (2000) (Pubitemid 30220488)
10. 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) (Pubitemid 32042926)
11. Deng, W., Wang, H., Rosenberg, P.A., Volpe, J.J. & Jensen, F.E. Role of metabotropic glutamate receptors in oligodendrocyte excitotoxicity and oxidative stress. Proc. Natl. Acad. Sci. USA 101, 7751-7756 (2004) (Pubitemid 38658101)
12. Volpe, J.J. Cerebellum of the premature infant: rapidly developing, vulnerable, clinically important. J. Child Neurol. 24, 1085-1104 (2009)
13. Kukley, M., Nishiyama, A. & Dietrich, D. The fate of synaptic input to NG2 glial cells: neurons specifically downregulate transmitter release onto differentiating oligodendroglial cells. J. Neurosci. 30, 8320-83312010)
14. Iino, M. et al. Glia-synapse interaction through Ca2+-permeable AMPA receptors in Bergmann glia. Science 292, 926-929 (2001) (Pubitemid 32422489)
15. Liu, S.Q.J. & Cull-Candy, S.G. Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405, 454-458 (2000) (Pubitemid 30367421)
16. Ge, W.P. et al. Long-term potentiation of neuron-glia synapses mediated by Ca2+- permeable AMPA receptors. Science 312, 1533-1537 (2006)
17. Hamilton, N., Vayro, S., Wigley, R. & Butt, A.M. Axons and astrocytes release ATP and glutamate to evoke calcium signals in NG2-glia. Glia 58, 6679 (2010)
18. Domercq, M. et al. P2X7 receptors mediate ischemic damage to oligodendrocytes. Glia 58, 730-740 (2010)
19. Haberlandt, C. et al. Gray matter NG2 cells display multiple Ca2+-signaling pathways and highly motile processes. PLoS ONE 6, e17575 (2011)
20. Kelly, L., Farrant, M. & Cull-Candy, S.G. Synaptic mGluR activation drives plasticity of calcium-permeable AMPA receptors. Nat. Neurosci. 12, 593-601 (2009)
21. Soto, D., Coombs, I.D., Kelly, L., Farrant, M. & Cull-Candy, S.G. Stargazin attenuates intracellular polyamine block of calcium-permeable AMPA receptors. Nat. Neurosci. 10, 1260-1267 (2007) (Pubitemid 47480295)
22. Swanson, G.T., Kamboj, S.K. & Cull-Candy, S.G. Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J. Neurosci. 17, 58-69 (1997) (Pubitemid 27008850)
23. Mameli, M., Balland, B., Lujan, R. & Luscher, C. Rapid synthesis and synaptic insertion of GluR2 for mGluR-LTD in the ventral tegmental area. Science 317, 530-533 (2007) (Pubitemid 47196120)
24. Luyt, K., Varadi, A. & Molnar, E. Functional metabotropic glutamate receptors are expressed in oligodendrocyte progenitor cells. J. Neurochem. 84, 1452-1464 (2003) (Pubitemid 36343611)
25. Jo, J. et al. Metabotropic glutamate receptor-mediated LTD involves two interacting Ca2+ sensors, NCS-1 and PICK1. Neuron 60, 1095-1111 (2008)
26. Ahn,S.M. & Choe, E.S. Alterations in GluR2 AMPA receptor phosphorylation at serine 880 following group I metabotropic glutamate receptor stimulation in the rat dorsal striatum. J. Neurosci. Res. 88, 992-999 (2010)
27. Li X.M., et al. JNK1 contributes to metabotropic glutamate receptor-dependent long-term depression and short-term synaptic plasticity in the mice area hippocampal CA1. Eur. J. Neurosci. 25 391-396 2007.
28. Barres B.A., Lazar M.A., Raff M.C. A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 120 1097-1108 (1994). (Pubitemid 24150036)
29. Wyllie, D.J., Mathie, A., Symonds, C.J. & Cull-Candy, S.G. Activation of glutamate receptors and glutamate uptake in identified macroglial cells in rat cerebellar cultures. J. Physiol. (Lond.) 432, 235-258 (1991)
30. Ziskin, J.L., Nishiyama, A., Rubio, M., Fukaya, M. & Bergles, D.E. Vesicular release of glutamate from unmyelinated axons in white matter. Nat. Neurosci. 10, 321-330 (2007)
31. James, G. & Butt, A.M. P2X and P2Y purinoreceptors mediate ATP-evoked calcium signaling in optic nerve glia in situ. Cell Calcium 30, 251-259 (2001) (Pubitemid 33014897)
32. Pankratov, Y.V., Lalo U.V. & Krishtal, O.A. Role for P2X receptors in long-term potentiation. J. Neurosci. 22, 8363-8369 (2002) (Pubitemid 35387576)
33. Rouach, N. et al. TARP gamma-8 controls hippocampal AMPA receptor number, distribution and synaptic plasticity. Nat. Neurosci. 8, 1525-1533 (2005) (Pubitemid 41573667)
34. Tomita, S., Stein, V., Stocker, T.J., Nicoll, R.A. & Bredt, D.S. Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Neuron 45, 269-277 (2005) (Pubitemid 40128120)
35. Fukaya, M., Yamazaki, M., Sakimura, K. & Watanabe, M. Spatial diversity in gene expression for VDCC subunit family in developing and adult mouse brains. Neurosci. Res. 53, 376-383 (2005) (Pubitemid 41643064)
36. Tomita, S. et al. Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J. Cell Biol. 161, 805-816 (2003) (Pubitemid 36648763)
37. Soto, D. et al. Selective regulation of long-form calcium-permeable AMPA receptors by an atypical TARP,?-5. Nat. Neurosci. 12, 277-285 (2009)
38. Shi, Y., Lu, W., Milstein, A.D. & Nicoll, R.A. The stoichiometry of AMPA receptors and TARPs varies by neuronal cell type. Neuron 62, 633-640 (2009)
39. Yamazaki, M. et al. TARPs?-2 and?-7 are essential for AMPA receptor expression in the cerebellum. Eur. J. Neurosci. 31, 22042220 (2010)
40. Bats, C., Groc, L. & Choquet, D. The interaction between Stargazin and PSD95 regulates AMPA receptor surface trafficking. Neuron 53, 719-734 (2007) (Pubitemid 46283370)
41. Lin, S.C. et al. Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron 46, 773-785 (2005)
42. Pende, M., Holtzclaw, L.A., Curtis, J.L., Russell, J.T. & Gallo, V. Glutamate regulates intracellular calcium and gene expression in oligodendrocyte progenitors through the activation of DL-alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid receptors. Proc. Natl. Acad. Sci. USA 91, 3215-3219 (1994)
43. Ishibashi, T. et al. Astrocytes promote myelination in response to electrical impulses. Neuron 49, 823-832 (2006) (Pubitemid 43376080)
44. Stevens, B., Porta, S., Haak, L.L., Gallo, V. & Fields, R.D. Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36, 855-868 (2002) (Pubitemid 35447857)
45. Man, H.Y. et al. Activation of PI3-kinase is required for AMPA receptor insertion during LTP of mEPSCs in cultured hippocampal neurons. Neuron 38, 611-624 (2003)
46. Clem, R.L., Anggono, V. & Huganir, R.L. PICK1 regulates incorporation of calciumpermeable AMPA receptors during cortical synaptic strengthening. J. Neurosci. 30, 6360-6366 (2010)
47. Thomas G.M., Lin D.T., Nuriya M., Huganir R.L. Rapid and bi-directional regulation of AMPA receptor phosphorylation and trafficking by JNK. EMBO J. 27 361-372 (2008). (Pubitemid 351161658)
48. Borsello, T. et al. A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat. Med. 9, 1180-1186 (2003)
49. Vieira, M. et al. Excitotoxicity through Ca2+-permeable AMPA receptors requires Ca2+-dependent JNK activation. Neurobiol. Dis. 40, 645655 (2010)
50. Santos, A.E. et al. Excitotoxicity mediated by Ca2+-permeable GluR4-containing AMPA receptorsinvolves the AP-1 transcription factor. Cell Death Differ. 13, 652-660 (2006).