Neuronal transporter and astrocytic ATP exocytosis underlie activity-dependent adenosine release in the hippocampus

Journal of Physiology

Volumn 591, Issue 16, 2013, Pages 3853-3871

  Wall, Mark J ^a   Dale, Nicholas ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; ADENOSINE TRIPHOSPHATE; CALCIUM ION; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER; IONOTROPIC RECEPTOR; NEUROTRANSMITTER;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BIOSENSOR; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME METABOLISM; ENZYME RELEASE; EXOCYTOSIS; FREQUENCY MODULATION; HIPPOCAMPAL CA1 REGION; MICROELECTROMECHANICAL SYSTEM; MOUSE; NERVE STIMULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STRATUM RADIATUM; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

EID: 84881607839     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.253450     Document Type: Article

References (66)

1. Anderson CM, Xiong W, Geiger JD, Young JD, Cass CE, Baldwin SA & Parkinson FE (1999a). Distribution of equilibrative, nitrobenzylthioinosine-sensitive nucleoside transporters (ENT1) in brain. J Neurochem 73, 867-873.
2. Anderson CM, Baldwin SA, Young JD, Cass CE & Parkinson FE (1999b). Distribution of mRNA encoding a nitrobenzylthioinosine-insensitive nucleoside transporter (ENT2) in rat brain. Brain Res Mol Brain Res 70, 293-297.
3. Arai A, Kessler M & Lynch G (1990). The effects of adenosine on the development of long-term potentiation. Neurosci Lett 119, 41-44.
4. Boison D (2012). Adenosine dysfunction in epilepsy. Glia 60, 1234-1243.
5. Boison D (2009). Adenosine-based modulation of brain activity. Curr Neuropharmacol 7, 158-159.
6. Brambilla D, Chapman D & Greene R (2005). Adenosine mediation of presynaptic feedback inhibition of glutamate release. Neuron 46, 275-283.
7. Brundege JM & Dunwiddie TV (1996). Modulation of excitatory synaptic transmission by adenosine released from single hippocampal pyramidal neurons. J Neurosci 16, 5603-5612.
8. Canals S, Larrosa B, Pintor J, Mena MA & Herreras O (2008). Metabolic challenge to glia activates an adenosine-mediated safety mechanism that promotes survival by delaying the onset of spreading depression waves. J Cereb Blood Flow Metab 28, 1835-1844.
9. Cechova S & Venton BJ (2008). Transient adenosine efflux in the rat caudate-putamen. J Neurochem 105, 1253-1263.
10. Clarke DD, Nicklas WJ & Berl S (1970). Tricarboxylic acid-cycle metabolism in brain. Effect of fluoroacetate and fluorocitrate on the labelling of glutamate, aspartate, glutamine and γ-aminobutyrate. Biochem J 120, 345-351.
11. Costenla AR, de Mendonça A & Ribeiro JA (1999). Adenosine modulates synaptic plasticity in hippocampal slices from aged rats. Brain Res 851, 228-234.
12. Craig CG & White TD (1993). N-Methyl-D-aspartate- and non-N-methyl-D-aspartate-evoked adenosine release from rat cortical slices: distinct purinergic sources and mechanisms of release. J Neurochem 60, 1073-1080.
13. Cunha RA, Vizi ES, Ribeiro JA & Sebastião AM (1996). Preferential release of ATP and its extracellular catabolism as a source of adenosine upon high- but not low-frequency stimulation of rat hippocampal slices. J Neurochem 67, 2180-2187.
14. Cunha RA, Sebastião AM & Ribeiro JA (1998). Inhibition by ATP of hippocampal synaptic transmission requires localized extracellular catabolism by ecto-nucleotidases into adenosine and channeling to adenosine A1 receptors. J Neurosci 18, 1987-1995.
15. 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.
16. Dale N & Frenguelli BG (2009). Release of adenosine and ATP during ischemia and epilepsy. Curr Neuropharmacology 7, 160-179.
17. de Mendonça A & Ribeiro JA (1994). Endogenous adenosine modulates long-term potentiation in the hippocampus. Neuroscience 62, 385-390.
18. Diógenes MJ, Neves-Tomé R, Fucile S, Martinello K, Scianni M, Theofilas P, Lopatár J, Ribeiro JA, Maggi L, Frenguelli BG, Limatola C, Boison D & Sebastião AM (2012). Homeostatic control of synaptic activity by endogenous adenosine is mediated by adenosine kinase. Cereb Cortex (Epub ahead of print) Sept 2012 doi: 10.1093/cercor/bhs284.
19. Dunwiddie TV & Diao L (1994). Extracellular adenosine concentrations in hippocampal brain slices and the tonic inhibitory modulation of evoked excitatory responses. J Pharmacol Exp Ther 268, 537-545.
20. Dunwiddie TV, Diao L & Proctor WR (1997). Adenine nucleotides undergo rapid, quantitative conversion to adenosine in the extracellular space in rat hippocampus. J Neurosci 20, 7673-7682.
21. Dunwiddie TV, Hoffer BJ (1980). Adenine nucleotides and synaptic transmission in the in vitro rat hippocampus. Br J Pharmacol 69, 59-68.
22. Etherington LA, Patterson GE, Meechan L, Boison D, Irving AJ, Dale N & Frenguelli BG (2009). Astrocytic adenosine kinase regulates basal synaptic adenosine levels and seizure activity but not activity-dependent adenosine release in the hippocampus. Neuropharmacology 56, 429-437.
23. Frenguelli BG, Wigmore G, Llaudet E & Dale N (2007). Temporal and mechanistic dissociation of ATP and adenosine release during ischemia in the mammalian hippocampus. J Neurochem 101, 1400-1413.
24. 3H]adenosine from rat brain synaptosomal preparations. J Neurochem 64, 2105-2110.
25. Hoehn K & White TD (1990). N-Methyl-D-aspartate, kainate and quisqualate release endogenous adenosine from rat cortical slices. Neuroscience 39, 441-450.
26. 2-dependent release of ATP in the medulla oblongata contributes to central respiratory chemosensitivity. J Physiol 588, 3901-3920.
27. Jo YH & Sclichter R (1999). Synaptic corelease of ATP and GABA in cultured spinal neurons. Nat Neurosci 2, 241-245.
28. Jonzon B & Fredholm BB (1985). Release of purines, noradrenaline, and GABA from rat hippocampal slices by field stimulation. J Neurochem 44, 217-224.
29. 1 receptor-mediated presynaptic inhibition at the calyx of Held of immature rats. J Physiol 553, 415-426.
30. Klyuch BP, Dale N & Wall MJ (2012a). Deletion of ecto-5′-nucleotidase (CD73) reveals direct action potential-dependent adenosine release. J Neurosci 32, 3842-3847.
31. Klyuch BP, Dale N & Wall MJ (2012b). Receptor-mediated modulation of activity-dependent adenosine release in rat cerebellum. Neuropharmacology 62, 815-824.
32. Koszalka P, Ozüyaman B, Huo Y, Zernecke A, Flögel U, Braun A, Buchheiser A, Decking UK, Smith ML, Sévigny J, Gear A, Weber AA, Molojavyi A, Ding Z, Weber C, Ley K, Zimmermann H, Gödecke A & Schrader J (2004). Targeted disruption of cd73/ecto-5′-nucleotidase alters thromboregulation and augments vascular inflammatory response. Circ Res 95, 814-821.
33. Langer D, Hammer K, Koszalka P, Schrader J, Robson S & Zimmermann H (2008). Distribution of ectonucleotidases in the rodent brain revisited. Cell Tissue Res 334, 199-217.
34. Lalo U, Pankratov Y, Kirchhoff F, North RA & Verkhratsky A (2006). NMDA receptors mediate neuron-to-glia signalling in mouse cortical astrocytes. J Neurosci 26, 2673-2683.
35. Latini S & Pedata F (2001). Adenosine in the central nervous system: release mechanism and extracellular concentrations. J Neurochem 79, 463-484.
36. Llaudet E, Botting N, Crayston J & Dale N (2003). A three enzyme microelectrode sensor for detecting purine release from central nervous system. Biosens Bioelectron 18, 43-52.
37. Llaudet E, Hatz S, Droniou M & Dale N (2005). Microelectrode biosensor for real-time measurement of ATP in biological tissue. Anal Chem 77, 3267-3273.
38. Loiola EC, Ventura AL (2011). Release of ATP from avian Müller glia cells in culture. Neurochem Int 58, 414-422.
39. Lopatář J, Dale N & Frenguelli BG (2011). Minor contribution of ATP P2 receptors to electrically-evoked electrographic seizure activity in hippocampal slices: evidence from purine biosensors and P2 receptor agonists and antagonists. Neuropharmacology 61, 25-34.
40. Lopes LV, Sebastião AM & Ribeiro JA (2011). Adenosine and related drugs in brain diseases: present and future in clinical trials. Curr Top Med Chem 11, 1087-1101.
41. Lovatt D, Xu Q, Liu W, Takano T, Smith NA, Schnermann J, Tieu K & Nedergaard M (2012). Neuronal adenosine release, and not astrocytic ATP release, mediates feedback inhibition of excitatory activity. Proc Natl Acad Sci U S A 109, 6265-6270.
42. Manzoni OJ, Manabe T & Nicoll RA (1994). Release of adenosine by activation of NMDA receptors in the hippocampus. Science 265, 2098-2101.
43. Martín ED, Fernández M, Perea G, Pascual O, Haydon PG, Araque A & Ceña V (2007). Adenosine released by astrocytes contributes to hypoxia-induced modulation of synaptic transmission. Glia 55, 36-45.
44. Mitchell JB, Lupica CR & Dunwiddie TV (1993). Activity-dependent release of endogenous adenosine modulates synaptic responses in rat hippocampus. J Neurosci 13, 3439-3447.
45. Pankratov Y, Lalo U, Verkhratsky A & North RA (2007). Quantal release of ATP in mouse cortex. J Gen Physiol 129, 257-265.
46. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K & Haydon PG (2005). Astrocytic purinergic signalling coordinates synaptic networks. Science 310, 113-116.
47. Pearson RA, Dale N, Llaudet E & Mobbs P (2005). ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron 46, 731-744.
48. 2A receptor antagonist ZM241385 enhances neuronal survival after oxygen-glucose deprivation in rat CA1 hippocampal slices. Br J Pharmacol 157, 818-830.
49. Queiroz G, Gebicke-Haerter PJ, Schobert A, Starke K & von Kügelgen I (1997). Release of ATP from cultured rat astrocytes elicited by glutamate receptor activation. Neuroscience 78, 1203-1208.
50. Rex CS, Kramár EA, Colgin LL, Lin B, Gall CM & Lynch G (2005). Long-term potentiation is impaired in middle-aged rats: regional specificity and reversal by adenosine receptor antagonists. J Neurosci 25, 5956-5966.
51. Serrano A, Haddjeri N, Lacaille JC & Robitaille R (2006). GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J Neurosci 26, 5370-5382.
52. Studer FE, Fedele DE, Marowsky A, Schwerdel C, Wernli K, Vogt K, Fritschy JM & Boison D (2006). Shift of adenosine kinase expression from neurons to astrocytes during postnatal development suggests dual functionality of the enzyme. Neuroscience 142, 125-137.
53. Tian F, Gourine AV, Huckstepp RT & Dale N (2009). A microelectrode biosensor for real time monitoring of L-glutamate release. Anal Chim Acta 645, 86-91.
54. Wall MJ & Dale N (2007). Auto-inhibition of rat parallel fibre-Purkinje cell synapses by activity-dependent adenosine release. J Physiol 581, 553-565.
55. Wall MJ, Atterbury A & Dale N (2007). Control of basal extracellular adenosine concentration in rat cerebellum. J Physiol 582, 137-152.
56. Wall MJ, Wigmore G, Lopatár J, Frenguelli BG & Dale N (2008). The novel NTPDase inhibitor sodium polyoxotungstate (POM-1) inhibits ATP breakdown but also blocks central synaptic transmission, an action independent of NTPDase inhibition. Neuropharmacology 55, 1251-1258.
57. Wall MJ & Dale N (2008). Activity-dependent release of adenosine: a critical re-evaluation of mechanism. Curr Neuropharmacol 6, 329-337.
58. Wall M, Eason R & Dale N (2010). Biosensor measurement of purine release from cerebellar cultures and slices. Purinergic Signalling 6, 339-348.
59. Waniewski RA & Martin DL (1998). Preferential utilization of acetate by astrocytes is attributable to transport. J Neurosci 18, 5225-5233.
60. White TD & MacDonald WF (1990). Neural release of ATP and adenosine. Ann N Y Acad Sci 603, 287-298.
61. Wong YC, Billups B, Johnston J, Evans RJ & Forsythe ID (2006). Endogenous activation of adenosine A1 receptors but not P2X receptors during high-frequency synaptic transmission at the Calyx of Held. J Neurophysiol 95, 3336-3342.
62. Zamzow CR, Bose R & Parkinson FE (2009). N-Methyl-D-aspartate-evoked adenosine and inosine release from neurons requires extracellular calcium. Can J Physiol Pharmacol 87, 850-858.
63. Zhang JM, Wang HK, Ye CQ, Ge W, Chen Y, Jiang ZL, Wu CP, Poo MM, Duan S (2003). ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40, 971-982.
64. Zhang D, Xiong W, Chu S, Sun C, Albensi BC, Parkinson FE (2012). Inhibition of hippocampal synaptic activity by ATP, hypoxia or oxygen-glucose deprivation does not require CD73. PLoS ONE 7, e39772.
65. Zimmermann H (2000). Extracellular metabolism of ATP and other nucleotides. Naunyn-Schmiedeberg's Arch Pharmacol 362, 299-309.
66. zur Nedden S, Hawley S, Pentland N, Hardie DG, Doney AS & Frenguelli BG (2011). Intracellular ATP influences synaptic plasticity in area CA1 of rat hippocampus via metabolism to adenosine and activity-dependent activation of adenosine A1 receptors. J Neurosci 31, 6221-6234.