Glial glutamate transport modulates dendritic spine head protrusions in the hippocampus

GLIA

Volumn 60, Issue 7, 2012, Pages 1067-1077

  Verbich, David ^a   Prenosil, George A ^a   Chang, Philip K Y ^a   Murai, Keith K ^b   Mckinney, R Anne ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

Dendritic spine; Glutamate spillover; Hippocampus; Motility; Plasticity

Indexed keywords

GLUTAMATE TRANSPORTER; GLUTAMIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CONFOCAL MICROSCOPY; DENDRITIC SPINE; FEMALE; GLIA; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SPINE; SPINE HEAD PROTRUSION;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; DENDRITIC SPINES; FEMALE; GLUTAMIC ACID; HIPPOCAMPUS; MALE; MICE; MICROSCOPY, CONFOCAL; NEUROGLIA; NEURONAL PLASTICITY; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84860660817     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22335     Document Type: Article

References (58)

1. Arriza JL, Fairman WA, Wadiche JI, Murdoch GH, Kavanaugh MP, Amara SG. 1994. Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J Neurosci 14: 5559-5569.
2. Benediktsson AM, Schachtele SJ, Green SH, Dailey ME. 2005. Ballistic labeling and dynamic imaging of astrocytes in organotypic hippocampal slice cultures. J Neurosci Methods 141: 41-53.
3. Benediktsson AM, Marrs GS, Tu JC, Worley PF, Rothstein JD, Bergles DE, Dailey ME. 2012. Neuronal activity regulates glutamate transporter dynamics in developing astrocytes. Glia 60: 175-188.
4. Bourne JN, Harris KM. 2008. Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31: 47-67.
5. Bourne JN, Harris KM. 2011. Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus 21: 354-373.
6. Bozzo L, Chatton JY. 2010. Inhibitory effects of (2S, 3S)-3-[3-[4-(trifluoromethyl)benzoylamino]benzyloxy]aspartate (TFB-TBOA) on the astrocytic sodium responses to glutamate. Brain Res 1316: 27-34.
7. Carmona MA, Murai KK, Wang L, Roberts AJ, Pasquale EB. 2009. Glial ephrin-A3 regulates hippocampal dendritic spine morphology and glutamate transport. Proc Natl Acad Sci USA 106: 12524-12529.
8. Chaudhry FA, Lehre KP, van Lookeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J. 1995. Glutamate transporters in glial plasma membranes: Highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15: 711-720.
9. Clarke DD. 1991. Fluoroacetate and fluorocitrate: Mechanism of action. Neurochem Res 16: 1055-1058.
10. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65: 1-105.
11. De Paola V, Arber S, Caroni P. 2003. AMPA receptors regulate dynamic equilibrium of presynaptic terminals in mature hippocampal networks. Nat Neurosci 6: 491-500.
12. Dunaevsky A, Mason CA. 2003. Spine motility: A means towards an end? Trends Neurosci 26: 155-160.
13. Dunaevsky A, Tashiro A, Majewska A, Mason C, Yuste R. 1999. Developmental regulation of spine motility in the mammalian central nervous system. Proc Natl Acad Sci USA 96: 13438-13443.
14. Dunlop J. 2006. Glutamate-based therapeutic approaches: Targeting the glutamate transport system. Curr Opin Pharmacol 6: 103-107.
15. Eroglu C, Barres BA. 2010. Regulation of synaptic connectivity by glia. Nature 468: 223-231.
16. Fiacco TA, Agulhon C, McCarthy KD. 2009. Sorting out astrocyte physiology from pharmacology. Annu Rev Pharmacol Toxicol 49: 151-174.
17. Fiala JC, Kirov SA, Feinberg MD, Petrak LJ, George P, Goddard CA, Harris KM. 2003. Timing of neuronal and glial ultrastructure disruption during brain slice preparation and recovery in vitro. J Comp Neurol 465: 90-103.
18. Filosa A, Paixão S, Honsek SD, Carmona MA, Becker L, Feddersen B, Gaitanos L, Rudhard Y, Schoepfer R, Klopstock T, Kullander K, Rose CR, Pasquale EB, Klein R. 2009. Neuron-glia communication via EphA4/ephrin-A3 modulates LTP through glial glutamate transport. Nat Neurosci 12: 1285-1292.
19. Fischer M, Kaech S, Knutti D, Matus A. 1998. Rapid actin-based plasticity in dendritic spines. Neuron 20: 847-854.
20. Fonnum F, Johnsen A, Hassel B. 1997. Use of fluorocitrate and fluoroacetate in the study of brain metabolism. Glia 21: 106-113.
21. Frizzo ME, Dall'Onder LP, Dalcin KB, Souza DO. 2004. Riluzole enhances glutamate uptake in rat astrocyte cultures. Cell Mol Neurobiol 24: 123-128.
22. Fumagalli E, Funicello M, Rauen T, Gobbi M, Mennini T. 2008. Riluzole enhances the activity of glutamate transporters GLAST, GLT1 and EAAC1. Eur J Pharmacol 578: 171-176.
23. Furuta A, Rothstein JD, Martin LJ. 1997. Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J Neurosci 17: 8363-8375.
24. Gähwiler BH, Capogna M, Debanne D, McKinney RA, Thompson SM. 1997. Organotypic slice cultures: A technique has come of age. Trends Neurosci 20: 471-477.
25. Grosche J, Matyash V, Moller T, Verkhratsky A, Reichenbach A, Kettenmann H. 1999. Microdomains for neuron-glia interaction: Parallel fiber signaling to Bergmann glial cells. Nat Neurosci 2: 139-143.
26. Haber M, Zhou L, Murai KK. 2006. Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci 26: 8881-8891.
27. Henneberger C, Papouin T, Oliet SHR, Rusakov DA. 2010. Long-term potentiation depends on release of D-serine from astrocytes. Nature 463: 232-236.
28. Hirrlinger J, Hulsmann S, Kirchhoff F. 2004. Astroglial processes show spontaneous motility at active synaptic terminals in situ. Eur J Neurosci 20: 2235-2239.
29. Huang YH, Bergles DE. 2004. Glutamate transporters bring competition to the synapse. Curr Opin Neurobiol 14: 346-352.
30. Hubert JP, Delumeau JC, Glowinski J, Prémont J, Doble A. 1994. Antagonism by riluzole of entry of calcium evoked by NMDA and veratridine in rat cultured granule cells: Evidence for a dual mechanism of action. Br J Pharmacol 113: 261-267.
31. 2+-permeable AMPA receptors in Bergmann glia. Science 292: 926-929.
32. Kayser MS, Nolt MJ, Dalva MB. 2008. EphB receptors couple dendritic filopodia motility to synapse formation. Neuron 59: 56-69.
33. Klein R. 2009. Bidirectional modulation of synaptic functions by Eph/ephrin signaling. Nat Neurosci 12: 15-20.
34. Kullmann DM, Asztely F. 1998. Extrasynaptic glutamate spillover in the hippocampus: Evidence and implications. Trends Neurosci 21: 8-14.
35. 2+ currents and modulates release of glutamate via presynaptic NMDA receptors on neonatal rat hypoglossal motoneurons in vitro. Eur J Neurosci 27: 2501-2514.
36. Lippman JJ, Lordkipanidze T, Buell ME, Yoon SO, Dunaevsky A. 2008. Morphogenesis and regulation of Bergmann glial processes during Purkinje cell dendritic spine ensheathment and synaptogenesis. Glia 56: 1463-1477.
37. Lushnikova I, Skibo G, Muller D, Nikonenko I. 2009. Synaptic potentiation induces increased glial coverage of excitatory synapses in CA1 hippocampus. Hippocampus 19: 753-762.
38. Marcaggi P, Attwell D. 2004. Role of glial amino acid transporters in synaptic transmission and brain energetics. Glia 47: 217-225.
39. Matthias K, Kirchhoff F, Seifert G, Huttmann K, Matyash M, Kettenmann H, Steinhauser C. 2003. Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 23: 1750-1758.
40. Matus A. 2000. Actin-based plasticity in dendritic spines. Science 290: 754-758.
41. McKinney RA. 2010. Excitatory amino acid involvement in dendritic spine formation, maintenance and remodelling. J Physiol 588: 107-116.
42. Murai KK, Nguyen LN, Irie F, Yamaguchi Y, Pasquale EB. 2003. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat Neurosci 6: 153-160.
43. Nestor MW, Mok LP, Tulapurkar ME, Thompson SM. 2007. Plasticity of neuron-glial interactions mediated by astrocytic EphARs. J Neurosci 27: 12817-12828.
44. Nevian T, Helmchen F. 2007. Calcium indicator loading of neurons using single-cell electroporation. Pflugers Arch 454: 675-688.
45. Nishida H, Okabe S. 2007. Direct astrocytic contacts regulate local maturation of dendritic spines. J Neurosci 27: 331-340.
46. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain DA, Oliet SHR. 2006. Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125: 775-784.
47. Perea G, Navarrete M, Araque A. 2009. Tripartite synapses: Astrocytes process and control synaptic information. Trends Neurosci 32: 421-431.
48. Piet R, Vargova L, Sykova E, Poulain DA, Oliet SHR. 2004. Physiological contribution of the astrocytic environment of neurons to intersynaptic crosstalk. Proc Natl Acad Sci USA 101: 2151-2155.
49. Reichenbach A, Derouiche A, Kirchhoff F. 2010. Morphology and dynamics of perisynaptic glia. Brain Res Rev 63: 11-25.
50. Richards DA, Mateos JM, Hugel S, de Paola V, Caroni P, Gähwiler BH, McKinney RA. 2005. Glutamate induces the rapid formation of spine head protrusions in hippocampal slice cultures. Proc Natl Acad Sci USA 102: 6166-6171.
51. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF. 1996. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16: 675-686.
52. Shimamoto K, Sakai R, Takaoka K, Yumoto N, Nakajima T, Amara SG, Shigeri Y. 2004. Characterization of novel L-threo-β-benzyloxyaspartate derivatives, potent blockers of the glutamate transporters. Mol Pharmacol 65: 1008-1015.
53. Szerb JC, Issekutz B. 1987. Increase in the stimulation-induced overflow of glutamate by fluoroacetate, a selective inhibitor of the glial tricarboxylic cycle. Brain Res 410: 116-120.
54. Theodosis DT, Poulain DA, Oliet SHR. 2008. Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. Physiol Rev 88: 983-1008.
55. Tzingounis AV, Wadiche JI. 2007. Glutamate transporters: Confining runaway excitation by shaping synaptic transmission. Nat Rev Neurosci 8: 935-947.
56. Ventura R, Harris KM. 1999. Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19: 6897-6906.
57. Witcher MR, Kirov SA, Harris KM. 2007. Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus. Glia 55: 13-23.
58. Zhou J, Sutherland ML. 2004. Glutamate transporter cluster formation in astrocytic processes regulates glutamate uptake activity. J Neurosci 24: 6301-6306.