Neurotransmitters and integration in neuronal-astroglial networks

Neurochemical Research

Volumn 37, Issue 11, 2012, Pages 2326-2338

  Verkhratsky, Alexei ^a,b,c,d   Rodríguez, José Julio ^b,c,d   Parpura, Vladimir ^b,e,f  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b BASQUE FOUNDATION FOR SCIENCE   (Spain)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

^e University of Alabama at Birmingham   (United States)

^f UNIVERSITY OF SPLIT   (Croatia)

Author keywords

Astrocyte; Calcium; Neurone; Neurotransmitter; Secretion; Signalling

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; CARRIER PROTEIN; NEUROTRANSMITTER; NEUROTRANSMITTER RECEPTOR;

ASTROCYTE; AUTOCRINE EFFECT; BRAIN FUNCTION; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL COMMUNICATION; CELL MEMBRANE; CYTOSOL; ENDOPLASMIC RETICULUM; EXOCYTOSIS; EXTRACELLULAR SPACE; HUMAN; NERVE CELL; NERVE CELL NETWORK; NEUROTRANSMITTER RELEASE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; REVIEW; SECRETORY VESICLE;

ANIMALS; ASTROCYTES; EXOCYTOSIS; HUMANS; NEURONS; NEUROTRANSMITTER AGENTS;

EID: 84871415585     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-012-0765-6     Document Type: Review

References (162)

1. Du Bois-Reymond E (1877) Gesammelte Abhandlungen zur Allgemeinen Muskel-und Nervenphysik. Veit & Co., Leipzig
2. Lopez-Munoz F, Alamo C (2009) Historical evolution of the neurotransmission concept. J Neural Trans 116:515-533
3. Descartes R (1664) L'Homme, et un traité de la formation du foetus du mesme autheur. Avec les remarques de Louys de La Forge, 1st edn. Nicolas Le Gras, Paris, pp 1-449
4. Elliott TR (1904) On the action of adrenaline. J Physiol Lond 31:xx-xxi
5. Langley JN (1905) On the reactions of cells and nerve-endings to certain poisons, chiefly as regards the reaction of striated muscle to nicotine and curari. J Physiol Lond 33:374-413
6. Langley JN (1906) On nerve endings and on special excitable substances in cells. Proc R Soc Lond 78:170-194
7. Dale HH (1914) The action of certain esters and ethers of choline, and their relation to muscarine. J Pharmacol 6:147-190
8. Loewi O (1921) Über humorale Übertragbarkeit der Herznervenwirkung. Pflügers Arch 189:239-242
9. Von Euler US (1946) A specific sympathomimetic ergone in adrenergic nerve fibres (sympathin) and its relations to adrenaline and nor-adrenaline. Acta Physiol Scand 12:73-97
10. Eccles JC (1964) The physiology of synapses. Springer, Berlin
11. Burnstock G (1972) Purinergic nerves. Pharmacol Rev 24: 509-581
12. Eccles J (1976) From electrical to chemical transmission in the central nervous system. Notes Rec R Soc Lond 30:219-230
13. Burnstock G (1976) Do some nerve cells release more than one transmitter? Neuroscience 1:239-248
14. Del Castillo J, Katz B (1954) Quantal components of the endplate potential. J Physiol 124:560-573
15. Fatt P, Katz B (1952) Spontaneous subthreshold activity at motor nerve endings. J Physiol 117:109-128
16. Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318-324
17. Sudhof TC, De Camilli P, Niemann H, Jahn R (1993) Membrane fusion machinery: Insights from synaptic proteins. Cell 75:1-4
18. de Wit H, Walter AM, Milosevic I, Gulyas-Kovacs A, Riedel D, Sorensen JB, Verhage M (2009) Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes. Cell 138:935-946
19. Jorgacevski J, Potokar M, Grilc S, Kreft M, Liu W, Barclay JW, Buckers J, Medda R, Hell SW, Parpura V, Burgoyne RD, Zorec R (2011) Munc18-1 tuning of vesicle merger and fusion pore properties. J Neurosci 31:9055-9066
20. Sudhof TC, Rothman JE (2009) Membrane fusion: Grappling with SNARE and SM proteins. Science 323:474-477
21. Toonen RF, Verhage M (2007) Munc18-1 in secretion: Lonely Munc joins SNARE team and takes control. Trends Neurosci 30:564-572
22. Verhage M, Sorensen JB (2008) Vesicle docking in regulated exocytosis. Traffic 9:1414-1424
23. Weninger K, Bowen ME, Choi UB, Chu S, Brunger AT (2008) Accessory proteins stabilize the acceptor complex for synaptobrevin, the 1:1 syntaxin/SNAP-25 complex. Structure 16:308-320
24. Weninger K, Bowen ME, Chu S, Brunger AT (2003) Singlemolecule studies of SNARE complex assembly reveal parallel and antiparallel configurations. Proc Natl Acad Sci USA 100:14800-14805
25. Zilly FE, Sorensen JB, Jahn R, Lang T (2006) Munc18-bound syntaxin readily forms SNARE complexes with synaptobrevin in native plasma membranes. PLoS Biol 4:e330
26. Parpura V, Baker BJ, Jeras M, Zorec R (2010) Regulated exocytosis in astrocytic signal integration. Neurochem Int 57: 451-459
27. Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509-547
28. 2+-triggered exocytosis. Biochem J 366:1-13
29. 2+-regulated membrane fusion by synaptotagmin and SNAREs. Science 304:435-438
30. Locke FS (1894) Notiz uber den Einfluss, physiologisher Kochsalzlosung auf die Eregbarkeit von Muscel and Nerve. Zentralbl Physiol 8:166-167
31. Overton E (1904) Beitrage zur allgemeinen Muskel-und Nerven physiologie. III. Mittheilung. Studien uber die Wirkung der Alkali-und Erdkali-salze auf Skeletalmuskeln und Nerven. Pflugers Arch 105:176-290
32. Katz B, Miledi R (1965) The Effect of Calcium on Acetylcholine Release from Motor Nerve Terminals. Proc R Soc Lond B Biol Sci 161:496-503
33. Katz B, Miledi R (1967) Ionic requirements of synaptic transmitter release. Nature 215:651
34. Takahashi T (2005) Dynamic aspects of presynaptic calcium currents mediating synaptic transmission. Cell Calcium 37:507-511
35. Wang Z, Chapman ER (2010) Rat and Drosophila synaptotagmin 4 have opposite effects during SNARE-catalyzed membrane fusion. J Biol Chem 285:30759-30766
36. Parpura V, Zorec R (2010) Gliotransmission: Exocytotic release from astrocytes. Brain Res Rev 63:83-92
37. Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, Stout RF Jr, Spray DC, Reichenbach A, Pannicke T, Pekny M, Pekna M, Zorec R, Verkhratsky A (2012) Glial cells in (patho)physiology. J Neurochem 121:4-27
38. Verkhratsky A, Parpura V, Rodriguez JJ (2011) Where the thoughts dwell: The physiology of neuronal-glial "diffuse neural net". Brain Res Rev 66:133-151
39. Held H (1909) Über die Neuroglia marginalis der menschlichen Grosshirnrinde. Monatschr. f Psychol u Neurol. 26 Rdg.-Heft: 360-416
40. Glees P (1955) Neuroglia morphology and function. Blackwell, Oxford
41. Nageotte J (1910) Phenomenes de secretion dans le protoplasma des cellules nevrogliques de la substance grise. C R Soc Biol (Paris) 68:1068-1069
42. Bowery NG, Brown DA, Collins GG, Galvan M, Marsh S, Yamini G (1976) Indirect effects of amino-acids on sympathetic ganglion cells mediated through the release of gamma-aminobutyric acid from glial cells. Br J Pharmacol 57:73-91
43. Malarkey EB, Parpura V (2009) Mechanisms of transmitter release from astrocytes. In: Parpura V, Haydon PG (eds) Astrocytes in (patho)physiology of the nervous system. In: Astrocytes in (patho)physiology of the nervous system. Springer, New York, pp 301-350
44. Ni Y, Malarkey EB, Parpura V (2007) Vesicular release of glutamate mediates bidirectional signaling between astrocytes and neurons. J Neurochem 103:1273-1284
45. Parpura V, Verkhratsky A (2012) The astrocyte excitability brief: From receptors to gliotransmission. Neurochem Int (in press
46. Sawada K, Echigo N, Juge N, Miyaji T, Otsuka M, Omote H, Yamamoto A, Moriyama Y (2008) Identification of a vesicular nucleotide transporter. Proc Natl Acad Sci USA 105:5683-5686
47. Sreedharan S, Shaik JH, Olszewski PK, Levine AS, Schioth HB, Fredriksson R (2010) Glutamate, aspartate and nucleotide transporters in the SLC17 family form four main phylogenetic clusters: Evolution and tissue expression. BMC Genomics 11:17
48. Crippa D, Schenk U, Francolini M, Rosa P, Verderio C, Zonta M, Pozzan T, Matteoli M, Carmignoto G (2006) Synaptobrevin2-expressing vesicles in rat astrocytes: Insights into molecular characterization, dynamics and exocytosis. J Physiol 570:567-582
49. Zhang Q, Fukuda M, Van Bockstaele E, Pascual O, Haydon PG (2004) Synaptotagmin IV regulates glial glutamate release. Proc Natl Acad Sci USA 101:9441-9446
50. 2+ binding to synaptotagmin 4. Nat Struct Mol Biol 11: 844-849
51. Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhauser C, Pilati E, Volterra A (2004) Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 7:613-620
52. Malarkey EB, Parpura V (2011) Temporal characteristics of vesicular fusion in astrocytes: Examination of synaptobrevin 2-laden vesicles at single vesicle resolution. J Physiol 589: 4271-4300
53. Calegari F, Coco S, Taverna E, Bassetti M, Verderio C, Corradi N, Matteoli M, Rosa P (1999) A regulated secretory pathway in cultured hippocampal astrocytes. J Biol Chem 274:22539-22547
54. Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E, Rosa P, Matteoli M, Verderio C (2003) Storage and release of ATP from astrocytes in culture. J Biol Chem 278:1354-1362
55. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369:744-747
56. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1998) Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur J Neurosci 10: 2129-2142
57. Araque A, Sanzgiri RP, Parpura V, Haydon PG (1998) Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. J Neurosci 18:6822-6829
58. Fellin T, Pascual O, Gobbo S, Pozzan T, Haydon PG, Carmignoto G (2004) Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43:729-743
59. Hassinger TD, Atkinson PB, Strecker GJ, Whalen LR, Dudek FE, Kossel AH, Kater SB (1995) Evidence for glutamate-mediated activation of hippocampal neurons by glial calcium waves. J Neurobiol 28:159-170
60. Perea G, Araque A (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317:1083-1086
61. 2+-dependent glutamate release. Neuroscience 158:253-259
62. Mothet JP, Parent AT, Wolosker H, Brady RO Jr, Linden DJ, Ferris CD, Rogawski MA, Snyder SH (2000) D-serine is an endogenous ligand for the glycine site of the N-methyl-Daspartate receptor. Proc Natl Acad Sci USA 97:4926-4931
63. Stevens ER, Esguerra M, Kim PM, Newman EA, Snyder SH, Zahs KR, Miller RF (2003) D-serine and serine racemase are present in the vertebrate retina and contribute to the physiological activation of NMDA receptors. Proc Natl Acad Sci USA 100:6789-6794
64. Henneberger C, Papouin T, Oliet SH, Rusakov DA (2010) Longterm potentiation depends on release of D-serine from astrocytes. Nature 463:232-236
65. Yang Y, Ge W, Chen Y, Zhang Z, Shen W, Wu C, Poo M, Duan S (2003) Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine. Proc Natl Acad Sci USA 100:15194-15199
66. Verkhratsky A, Krishtal OA, Burnstock G (2009) Purinoceptors on neuroglia. Mol Neurobiol 39:190-208
67. Burnstock G, Fredholm BB, Verkhratsky A (2011) Adenosine and ATP receptors in the brain. Curr Top Med Chem 11:973-1011
68. Arcuino G, Lin JH, Takano T, Liu C, Jiang L, Gao Q, Kang J, Nedergaard M (2002) Intercellular calcium signaling mediated by point-source burst release of ATP. Proc Natl Acad Sci USA 99:9840-9845
69. Cotrina ML, Lin JH, Lopez-Garcia JC, Naus CC, Nedergaard M (2000) ATP-mediated glia signaling. J Neurosci 20:2835-2844
70. Guthrie PB, Knappenberger J, Segal M, Bennett MV, Charles AC, Kater SB (1999) ATP released from astrocytes mediates glial calcium waves. J Neurosci 19:520-528
71. Stout CE, Costantin JL, Naus CC, Charles AC (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277:10482-10488
72. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91:461-553
73. Verderio C, Matteoli M (2001) ATP mediates calcium signaling between astrocytes and microglial cells: Modulation by IFN-c. J Immunol 166:6383-6391
74. Braet K, Paemeleire K, D'Herde K, Sanderson MJ, Leybaert L (2001) Astrocyte-endothelial cell calcium signals conveyed by two signalling pathways. Eur J Neurosci 13:79-91
75. Marpegan L, Swanstrom AE, Chung K, Simon T, Haydon PG, Khan SK, Liu AC, Herzog ED, Beaule C (2011) Circadian regulation of ATP release in astrocytes. J Neurosci 31: 8342-8350
76. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310:113-116
77. Pangrsic T, Potokar M, Stenovec M, Kreft M, Fabbretti E, Nistri A, Pryazhnikov E, Khiroug L, Giniatullin R, Zorec R (2007) Exocytotic release of ATP from cultured astrocytes. J Biol Chem 282:28749-28758
78. Zhang Z, Chen G, Zhou W, Song A, Xu T, Luo Q, Wang W, Gu XS, Duan S (2007) Regulated ATP release from astrocytes through lysosome exocytosis. Nat Cell Biol 9:945-953
79. Jaiswal JK, Fix M, Takano T, Nedergaard M, Simon SM (2007) Resolving vesicle fusion from lysis to monitor calcium-triggered lysosomal exocytosis in astrocytes. Proc Natl Acad Sci USA 104:14151-14156
80. 2+-regulated exocytosis from cortical astrocytes. J Neurosci 28:7648-7658
81. Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A (1998) Prostaglandins stimulate calciumdependent glutamate release in astrocytes. Nature 391:281-285
82. 2+ stores in astrocytes. J Neurosci Res 76:86-97
83. Innocenti B, Parpura V, Haydon PG (2000) Imaging extracellular waves of glutamate during calcium signaling in cultured astrocytes. J Neurosci 20:1800-1808
84. Montana V, Ni Y, Sunjara V, Hua X, Parpura V (2004) Vesicular glutamate transporter-dependent glutamate release from astrocytes. J Neurosci 24:2633-2642
85. 2+ sources for the exocytotic release of glutamate from astrocytes. Biochim Biophys Acta 1813:984-991
86. Verkhratsky A, Rodriguez JJ, Parpura V (2012) Calcium signalling in astroglia. Mol Cell Endocrinol 353:45-56
87. Stout RF Jr, Parpura V (2011) Voltage-gated calcium channel types in cultured C. elegans CEPsh glial cells. Cell Calcium 50:98-108
88. 2+ dynamics and consequent glutamate release from rat astrocytes. Glia 56:821-835
89. 2+ oscillations in situ drive NMDAR-mediated neuronal excitation. Nat Neurosci 4:803-812
90. Yaguchi T, Nishizaki T (2010) Extracellular high K+ stimulates vesicular glutamate release from astrocytes by activating voltage-dependent calcium channels. J Cell Physiol 225:512-518
91. 2+ exchanger-operated exocytotic glutamate release triggered by mild depolarization. J Neurochem 103:1196-1207
92. 2+-dependent exocytotic release of glutamate from rat cortical astrocytes. ASN Neuro (Epub ahead of print). doi:10.1042/AN20110059
93. 2+- dependent glutamate release from rat cortical astrocytes. J Neurosci 28:9682-9691
94. 2+-dependent glutamate release from mouse cortical astrocytes. Cell Calcium 49:23-34
95. Lee M, McGeer EG, McGeer PL (2011) Mechanisms of GABA release from human astrocytes. Glia 59:1600-1611
96. Dvorzhak A, Myakhar O, Unichenko P, Kirmse K, Kirischuk S (2010) Estimation of ambient GABA levels in layer I of the mouse neonatal cortex in brain slices. J Physiol 588:2351-2360
97. Santhakumar V, Hanchar HJ, Wallner M, Olsen RW, Otis TS (2006) Contributions of the GABAA receptor a6 subunit to phasic and tonic inhibition revealed by a naturally occurring polymorphism in the a6 gene. J Neurosci 26:3357-3364
98. Hamilton NB, Attwell D (2010) Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci 11:227-238
99. Herman MA, Jahr CE (2007) Extracellular glutamate concentration in hippocampal slice. J Neurosci 27:9736-9741
100. Liu HT, Tashmukhamedov BA, Inoue H, Okada Y, Sabirov RZ (2006) Roles of two types of anion channels in glutamate release from mouse astrocytes under ischemic or osmotic stress. Glia 54:343-357
101. Nilius B, Eggermont J, Voets T, Buyse G, Manolopoulos V, Droogmans G (1997) Properties of volume-regulated anion channels in mammalian cells. Prog Biophys Mol Biol 68:69-119
102. Fields RD (2011) Nonsynaptic and nonvesicular ATP release from neurons and relevance to neuron-glia signaling. Semin Cell Dev Biol 22:214-219
103. Lee S, Yoon BE, Berglund K, Oh SJ, Park H, Shin HS, Augustine GJ, Lee CJ (2010) Channel-mediated tonic GABA release from glia. Science 330:790-796
104. Baroja-Mazo A, Barbera-Cremades M, Pelegrin P (2012) The participation of plasma membrane hemichannels to purinergic signaling. Biochim Biophys Acta (in press
105. Bao L, Locovei S, Dahl G (2004) Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 572: 65-68
106. Ma W, Compan V, Zheng W, Martin E, North RA, Verkhratsky A, Surprenant A (2012) Pannexin 1 forms an anion-selective channel. Pflügers Arch 463:585-592
107. Hofer A, Dermietzel R (1998) Visualization and functional blocking of gap junction hemichannels (connexons) with antibodies against external loop domains in astrocytes. Glia 24: 141-154
108. Kang J, Kang N, Lovatt D, Torres A, Zhao Z, Lin J, Nedergaard M (2008) Connexin 43 hemichannels are permeable to ATP. J Neurosci 28:4702-4711
109. Ye ZC, Wyeth MS, Baltan-Tekkok S, Ransom BR (2003) Functional hemichannels in astrocytes: A novel mechanism of glutamate release. J Neurosci 23:3588-3596
110. North RA (2002) Molecular physiology of P2X receptors. Physiol Rev 82:1013-1067
111. Pelegrin P, Surprenant A (2009) The P2X7 receptor-pannexin connection to dye uptake and IL-1b release. Purinergic Signal 5:129-137
112. Pellegatti P, Falzoni S, Pinton P, Rizzuto R, Di Virgilio F (2005) A novel recombinant plasma membrane-targeted luciferase reveals a new pathway for ATP secretion. Mol Biol Cell 16:3659-3665
113. 2+ signaling. J Neurosci 26:1378-1385
114. Duan S, Anderson CM, Keung EC, Chen Y, Swanson RA (2003) P2X7 receptor-mediated release of excitatory amino acids from astrocytes. J Neurosci 23:1320-1328
115. Kinney GA (2005) GAT-3 transporters regulate inhibition in the neocortex. J Neurophysiol 94:4533-4537
116. Kirmse K, Kirischuk S (2006) Ambient GABA constrains the strength of GABAergic synapses at Cajal-Retzius cells in the developing visual cortex. J Neurosci 26:4216-4227
117. Kirischuk S, Kettenmann H, Verkhratsky A (2007) Membrane currents and cytoplasmic sodium transients generated by glutamate transport in Bergmann glial cells. Pflugers Arch 454: 245-252
118. Pow DV (2001) Visualising the activity of the cystine-glutamate antiporter in glial cells using antibodies to aminoadipic acid, a selectively transported substrate. Glia 34:27-38
119. Warr O, Takahashi M, Attwell D (1999) Modulation of extracellular glutamate concentration in rat brain slices by cystineglutamate exchange. J Physiol 514(Pt 3):783-793
120. Deitmer JW, Verkhratsky AJ, Lohr C (1998) Calcium signalling in glial cells. Cell Calcium 24:405-416
121. Verkhratsky A, Kettenmann H (1996) Calcium signalling in glial cells. Trends Neurosci 19:346-352
122. Verkhratsky A, Orkand RK, Kettenmann H (1998) Glial calcium: Homeostasis and signaling function. Physiol Rev 78:99-141
123. Verkhratsky A, Steinhauser C (2000) Ion channels in glial cells. Brain Res Brain Res Rev 32:380-412
124. Verkhratsky A (2010) Physiology of neuronal-glial networking. Neurochem Int 57:332-343
125. Kirischuk S, Matiash V, Kulik A, Voitenko N, Kostyuk P, Verkhratsky A (1996) Activation of P2-purino-, a1-adreno and H1-histamine receptors triggers cytoplasmic calcium signalling in cerebellar Purkinje neurons. Neuroscience 73:643-647
126. Kirischuk S, Moller T, Voitenko N, Kettenmann H, Verkhratsky A (1995) ATP-induced cytoplasmic calcium mobilization in Bergmann glial cells. J Neurosci 15:7861-7871
127. Kirischuk S, Tuschick S, Verkhratsky A, Kettenmann H (1996) Calcium signalling in mouse Bergmann glial cells mediated by a1-adrenoreceptors and H1 histamine receptors. Eur J Neurosci 8:1198-1208
128. Kirchhoff F, Mulhardt C, Pastor A, Becker CM, Kettenmann H (1996) Expression of glycine receptor subunits in glial cells of the rat spinal cord. J Neurochem 66:1383-1390
129. Miyazaki I, Asanuma M, Diaz-Corrales FJ, Miyoshi K, Ogawa N (2004) Direct evidence for expression of dopamine receptors in astrocytes from basal ganglia. Brain Res 1029:120-123
130. 2+-permeable glutamate receptors and blocks voltage-gated K ? currents in glial cells of mouse hippocampal slices. Pflugers Arch 426:310-319
131. Muller T, Moller T, Berger T, Schnitzer J, Kettenmann H (1992) Calcium entry through kainate receptors and resulting potassium-channel blockade in Bergmann glial cells. Science 256:1563-1566
132. Lalo U, Pankratov Y, Kirchhoff F, North RA, Verkhratsky A (2006) NMDA receptors mediate neuron-to-glia signaling in mouse cortical astrocytes. J Neurosci 26:2673-2683
133. Lalo U, Pankratov Y, Parpura V, Verkhratsky A (2011) Ionotropic receptors in neuronal-astroglial signalling: What is the role of "excitable" molecules in non-excitable cells. Biochim Biophys Acta 1813:992-1002
134. Ziak D, Chvatal A, Sykova E (1998) Glutamate-, kainate-and NMDA-evoked membrane currents in identified glial cells in rat spinal cord slice. Physiol Res 47:365-375
135. Palygin O, Lalo U, Pankratov Y (2011) Distinct pharmacological and functional properties of NMDA receptors in mouse cortical astrocytes. Br J Pharmacol
136. 2+ signalling in cortical astrocytes. Cell Calcium 48: 225-231
137. Verkhratsky A, Kirchhoff F (2007) NMDA Receptors in Glia. Neuroscientist 13:28-37
138. Kirischuk S, Kirchhoff F, Matyash V, Kettenmann H, Verkhratsky A (1999) Glutamate-triggered calcium signalling in mouse Bergmann glial cells in situ: Role of inositol-1,4,5-trisphosphate-mediated intracellular calcium release. Neuroscience 92:1051-1059
139. Aronica E, van Vliet EA, Mayboroda OA, Troost D, da Silva FH, Gorter JA (2000) Upregulation of metabotropic glutamate receptor subtype mGluR3 and mGluR5 in reactive astrocytes in a rat model of mesial temporal lobe epilepsy. Eur J Neurosci 12:2333-2344
140. Petralia RS, Wang YX, Niedzielski AS, Wenthold RJ (1996) The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience 71:949-976
141. Tamaru Y, Nomura S, Mizuno N, Shigemoto R (2001) Distribution of metabotropic glutamate receptor mGluR3 in the mouse CNS: Differential location relative to pre-and postsynaptic sites. Neuroscience 106:481-503
142. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H (2009) Purinergic signalling in the nervous system: An overview. Trends Neurosci 32:19-29
143. Boison D, Chen JF, Fredholm BB (2010) Adenosine signaling and function in glial cells. Cell Death Differ 17:1071-1082
144. Lalo U, Pankratov Y, Wichert SP, Rossner MJ, North RA, Kirchhoff F, Verkhratsky A (2008) P2X1 and P2X5 subunits form the functional P2X receptor in mouse cortical astrocytes. J Neurosci 28:5473-5480
145. Lalo U, Verkhratsky A, Pankratov Y (2011) Ionotropic ATP receptors in neuronal-glial communication. Semin Cell Dev Biol 22:220-228
146. Pannicke T, Fischer W, Biedermann B, Schadlich H, Grosche J, Faude F, Wiedemann P, Allgaier C, Illes P, Burnstock G, Reichenbach A (2000) P2X7 receptors in Muller glial cells from the human retina. J Neurosci 20:5965-5972
147. Ballerini P, Rathbone MP, Di Iorio P, Renzetti A, Giuliani P, D'Alimonte I, Trubiani O, Caciagli F, Ciccarelli R (1996) Rat astroglial P2Z (P2X7) receptors regulate intracellular calcium and purine release. NeuroReport 7:2533-2537
148. Fumagalli M, Brambilla R, D'Ambrosi N, Volonte C, Matteoli M, Verderio C, Abbracchio MP (2003) Nucleotide-mediated calcium signaling in rat cortical astrocytes: Role of P2X and P2Y receptors. Glia 43:203-218
149. Nobile M, Monaldi I, Alloisio S, Cugnoli C, Ferroni S (2003) ATP-induced, sustained calcium signalling in cultured rat cortical astrocytes: Evidence for a non-capacitative, P2X7-likemediated calcium entry. FEBS Lett 538:71-76
150. Hamilton N, Vayro S, Kirchhoff F, Verkhratsky A, Robbins J, Gorecki DC, Butt AM (2008) Mechanisms of ATP-and glutamate-mediated calcium signaling in white matter astrocytes. Glia 56:734-749
151. Norenberg W, Schunk J, Fischer W, Sobottka H, Riedel T, Oliveira JF, Franke H, Illes P (2010) Electrophysiological classification of P2X7 receptors in rat cultured neocortical astroglia. Br J Pharmacol 160:1941-1952
152. Oliveira JF, Riedel T, Leichsenring A, Heine C, Franke H, Krugel U, Norenberg W, Illes P (2011) Rodent cortical astroglia express in situ functional P2X7 receptors sensing pathologically high ATP concentrations. Cereb Cortex 21:806-820
153. Illes P, Verkhratsky A, Burnstock G, Franke H (2011) P2X receptors and their roles in astroglia in the central and peripheral nervous system. Neuroscientist. doi:10.1177/107385841141 8524
154. Franke H, Grosche J, Schadlich H, Krugel U, Allgaier C, Illes P (2001) P2X receptor expression on astrocytes in the nucleus accumbens of rats. Neuroscience 108:421-429
155. Ashour F, Deuchars J (2004) Electron microscopic localisation of P2X4 receptor subunit immunoreactivity to pre-and postsynaptic neuronal elements and glial processes in the dorsal vagal complex of the rat. Brain Res 1026:44-55
156. Kanjhan R, Housley GD, Thorne PR, Christie DL, Palmer DJ, Luo L, Ryan AF (1996) Localization of ATP-gated ion channels in cerebellum using P2x2R subunit-specific antisera. NeuroReport 7:2665-2669
157. Loesch A, Burnstock G (1998) Electron-immunocytochemical localization of P2X1 receptors in the rat cerebellum. Cell Tissue Res 294:253-260
158. Kukley M, Barden JA, Steinhauser C, Jabs R (2001) Distribution of P2X receptors on astrocytes in juvenile rat hippocampus. Glia 36:11-21
159. Jabs R, Matthias K, Grote A, Grauer M, Seifert G, Steinhauser C (2007) Lack of P2X receptor mediated currents in astrocytes and GluR type glial cells of the hippocampal CA1 region. Glia 55:1648-1655
160. Abbracchio MP, Ceruti S (2006) Roles of P2 receptors in glial cells: Focus on astrocytes. Purinergic Signal 2:595-604
161. Verkhratsky A, (2009) Neurotransmitter receptors in astrocytes In: Parpura V, Haydon PG (eds) Astrocytes in (patho)physiology of the nervous system. Springer, New York, pp 49-67
162. Nedergaard M, Verkhratsky A (2012) Artifact versus reality-How astrocytes contribute to synaptic events? Glia (E-pub ahead of print). doi: 10.1002/glia.22288