Adenosine released by astrocytes contributes to hypoxia-induced modulation of synaptic transmission

GLIA

Volumn 55, Issue 1, 2007, Pages 36-45

  Martín, Eduardo D ^a   Fernández, Miriam ^a   Perea, Gertrudis ^b   Pascual, Olivier ^c   Haydon, Philip G ^c   Araque, Alfonso ^b   Ceña, Valentín ^a  

^a UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^b INSTITUTO CAJAL   (Spain)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Astrocyte modulation; ATP; Presynaptic modulation; Synaptic plasticity

Indexed keywords

ADENOSINE; ADENOSINE A1 RECEPTOR; ADENOSINE TRIPHOSPHATE; CALCIUM ION; CYCLIC AMP; FLUOROCITRIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL HYPOXIA; CENTRAL NERVOUS SYSTEM DEPRESSION; DOWN REGULATION; ENZYME METABOLISM; EXCITATORY JUNCTION POTENTIAL; HIPPOCAMPUS; MOUSE; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ADENOSINE; ADENOSINE TRIPHOSPHATE; ANIMALS; ASTROCYTES; BRAIN; CALCIUM SIGNALING; CELL COMMUNICATION; CELLS, CULTURED; CITRATES; CYCLIC AMP; CYTOPROTECTION; DOWN-REGULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; HYPOXIA, BRAIN; MICE; MICE, TRANSGENIC; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; RECEPTOR, ADENOSINE A1; SYNAPTIC TRANSMISSION;

EID: 33751585955     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20431     Document Type: Article

References (53)

1. Aguado F, Espinosa-Parrilla JF, Carmona MA, Soriano E. 2002. Neuronal activity regulates correlated network properties of spontaneous calcium transients in astrocytes in situ. J Neurosci 22:9430-9444.
2. Araque A, Carmignoto G, Haydon PG. 2001. Dynamic signaling between neurons and glia. Annu Rev Physiol 63:795-813.
3. Araque A, Li N, Doyle RT, Haydon PG. 2000. SNARE protein dependent glutamate release from astrocytes. J Neurosci 20:666-673.
4. 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.
5. Bender AS, Hertz L. 1986. Similarities of adenosine uptake systems in astrocytes and neurons in primary cultures. Neurochem Res 11:1507-1524.
6. Bezzi P, Volterra A. 2001. A neuron-glia signalling network in the active brain. Curr Opin Neurobiol 11:387-394.
7. Brundege JM, Diao L, Proctor WR, Dunwiddie TV. 1997. The role of cyclic AMP as a precursor of extracellular adenosine in the rat hippocampus. Neuropharmacology 36:1201-1210.
8. Brundege JM, Dunwiddie TV. 1996. Modulation of excitatory synaptic transmission by adenosine released from single hippocampal pyramidal neurons. J Neurosci 16:5603-5612.
9. Caciagli F, Ciccarelli R, Di Iorio P, Ballerini P, Tacconelli L. 1988. Cultures of glial cells release purines under field electrical stimulation: The possible ionic mechanisms. Pharmacol Res Commun 20:935-947.
10. Carmignoto G 2000. Reciprocal communication systems between astrocytes and neurons. Prog Neurobiol 62:561-581.
11. Dale N, Pearson T, Frenguelli BG. 2000. Direct measurement of adenosine release during hypoxia in the CA1 region of the rat hippocampal slice. J Physiol 526:143-155.
12. Duan S, Anderson CM, Keung EC, Chen Y, Chen Y, Swanson RA. 2003. P2X7 receptor-mediated release of excitatory amino acids from astrocytes. J Neurosci 23:1320-1328.
13. Dunwiddie TV, Diao L. 1994. Extracellular adenosine concentration in hippocampal brain slices and the tonic inhibitory modulation of evoked excitatory responses. J Pharmacol Exp Ther 268:537-545.
14. Dunwiddie TV, Diao L. 2000. Regulation of extracellular adenosine in rat hippocampal slices is temperature dependent: Role of adenosine transporters. Neuroscience 95:81-88.
15. Dunwiddie TV, Diao L, Proctor WR. 1997. Adenine nucleotides undergo rapid, quantitative conversion to adenosine in the extracellular space in rat hippocampus. J Neurosci 17:7673-7682.
16. Fowler JC 1989. Adenosine antagonists delay hypoxia-induced depression of neuronal activity in hippocampal brain slice. Brain Res 490:378-384.
17. Giaume C, Venance L. 1998. Intercellular calcium signalling and gap junctional communication in astrocytes. Glia 24:50-64.
18. Haydon PG 2001. Glia: Listening and talking to the synapse. Nat Rev Neurosci 2:185-193.
19. Henderson GB, Strauss BP. 1991. Evidence for cAMP and cholate extrusion in C6 rat glioma cells by a common anion efflux pump. J Biol Chem 266:1641-1645.
20. Hershkowitz N, Katchman AN, Veregge S. 1993. Site of synaptic depression during hypoxia: A patch-clamp analysis. J Neurophysiol 69:432-441.
21. Higgins MJ, Hosseinzadeh H, MacGregor DG, Ogilvy H, Stone TW. 1994. Release and actions of adenosine in the central nervous system. Pharm World Sci 16:62-68.
22. Katchman AN, Hershkowitz N. 1993. Adenosine antagonists prevent hypoxia-induced depression of excitatory but not inhibitory synaptic currents. Neurosci Lett 159:123-126.
23. Kather H, Wieland E, Waas W. 1987. Chemiluminescent determination of adenosine, inosine, and hypoxanthine/xanthine. Anal Biochem 163:45-51.
24. Kukley M, Barden JA, Steinhauser C, Jabs R. 2001. Distribution of P2X receptors on astrocytes in juvenile rat hippocampus. Glia 36:11-21.
25. Largo C, Cuevas P, Somjen GG, Martin del Rio R, Herreras O. 1996. The effect of depressing glial function in rat brain in situ on ion homeostasis, synaptic transmission, and neuron survival. J Neurosci 16:1219-1229.
26. 2+ responses in glial cells evoked by exogenous and endogenous glutamate in rat hippocampus. Hippocampus 11:132-145.
27. Liu QS, Xu Q, Arcuino G, Kang J, Nedergaard M. 2004. Astrocyte-mediated activation of neuronal kainate receptors. Proc Natl Acad Sci USA 101:3172-3177.
28. Manzoni OJ, Manabe T, Nicoll RA. 1994. Release of adenosine by activation of NMDA receptors in the hippocampus. Science 265:2098-2101.
29. Martín ED, Buño W. 2003. Caffeine-mediated presynaptic long-term potentiation in hippocampal CA1 pyramidal neurons. J Neurophysiol 89:3029-3038.
30. Martín ED, Gonzalez-García C, Milán M, Fariñas I, Ceña V. 2004. Stressor-related impairment of synaptic transmission in hippocampal slices from α-synuclein knockout mice. Eur J Neurosci 20:3085-3091.
31. McCarthy KD, deVellis J. 1980. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
32. Mendoza-Fernandez V, Andrew RD, Barajas-Lopez C. 2000. ATP inhibits glutamate synaptic release by acting at P2Y receptors in pyramidal neurons of hippocampal slices. J Pharmacol Exp Ther 293:172-179.
33. Noji T, Karasawa A, Kusaka H. 2004. Adenosine uptake inhibitors. Eur J Pharmacol 495:1-16.
34. North RA 2002. Molecular physiology of P2X receptors. Physiol Rev 82:1013-1067.
35. Panenka W, Jijon H, Herx LM, Armstrong JN, Feighan D, Wei T, Yong VW, Ransohoff RM, MacVicar BA. 2001. P2X7-like receptor activation in astrocytes increases chemokine monocyte chemoattractant protein-1 expression via mitogen-activated protein kinase. J Neurosci 21:7135-7142.
36. Parkinson FE, Sinclair CJ, Othman T, Haughey NJ, Geiger JD. 2002. Differences between rat primary cortical neurons and astrocytes in purine release evoked by ischemic conditions. Neuropharmacology 43:836-846.
37. Parkinson FE, Xiong W. 2004. Stimulus- and cell-type-specific release of purines in cultured rat forebrain astrocytes and neurons. J Neurochem 88:1305-1312.
38. Parkinson FE, Xiong W, Zamzow CR. 2005. Astrocytes and neurons: Different roles in regulating adenosine levels. Neurol Res 27:153-160.
39. Pascual O, Casper K, Kubera C, Zhang J, Revilla-Sanchez R, Moss S, McCarthy K, Haydon PG. 2005. Astrocytic purinergic signaling coordinates synaptic networks. Science 310:113-116.
40. Paulsen RE, Contestabile A, Villani L, Fonnum F. 1987. An in vivo model for studying function of brain tissue temporarily devoid of glial cell metabolism: The use of fluorocitrate. J Neurochem 48:1377-1385.
41. Pearson T, Currie AJ, Etherington LA, Gadalla AE, Damian K, Llaudet E, Dale N, Frenguelli BG. 2003. Plasticity of purine release during cerebral ischemia: Clinical implications? J Cell Mol Med 7:362-375.
42. Pearson T, Nuritova F, Caldwell D, Dale N, Frenguelli BG. 2001. A depletable pool of adenosine in area CA1 of the rat hippocampus. J Neurosci 21:2298-2307.
43. Perea G, Araque A. 2005. Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J Neurosci 25:2192-2203.
44. Redman RS, Silinsky EM. 1994. ATP released together with acetylcholine as the mediator of neuromuscular depression at frog motor nerve endings. J Physiol 477:117-127.
45. Rosenberg PA, Knowles R, Knowles KP, Li Y. 1994. β-Adrenergic receptor-mediated regulation of extracellular adenosine in cerebral cortex in culture. J Neurosci 14:2953-2965.
46. Scammell TE, Arrigoni E, Thompson MA, Ronan PJ, Saper CB, Greene RW. 2003. Focal deletion of the adenosine A1 receptor in adult mice using an adeno-associated viral vector. J Neurosci 23:5762-5770.
47. 2+ stores in type I cortical astrocytes. J Biol Chem 278:4875-4881.
48. Stout CE, Costantin JL, Nau CC, Charles AC. 2002. Intercellular calcium signalling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277:10482-10488.
49. Swanson RA, Graham SH. 1994. Fluorocitrate and fluoroacetate effects on astrocyte metabolism in vitro. Brain Res 664:94-100.
50. Sweeney MI 1997. Neuroprotective effects of adenosine in cerebral ischemia: Window of opportunity. Neurosci Biobehav Rev 21:207-217.
51. Volterra A, Meldolesi J. 2005. Astrocytes, from brain glue to communication elements: The revolution continues. Nat Rev Neurosci 6:626-640.
52. 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.
53. Zeng YC, Domenici MR, Frank C, Sagratella S, Scotti de Carolis A. 1992. Effects of adenosinergic drugs on hypoxia-induced electrophysiological changes in rat hippocampal slices. Life Sci 51:1073-1082.