The Library
Activity-dependent release of Adenosine: a critical re-evaluation of mechanism
Tools
Wall, M. (Mark) and Dale, Nicholas. (2008) Activity-dependent release of Adenosine: a critical re-evaluation of mechanism. Current Neuropharmacology, Vol.6 (No.4). pp. 329-337. ISSN 1570-159X
|
PDF
WRAP_Dale_9975444-bs-190809-wall_dale_finalrepository.pdf - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader Download (551Kb) |
Official URL: http://dx.doi.org/10.2174/157015908787386087
Abstract
Adenosine is perhaps the most important and universal modulator in the brain. The current consensus is that it is primarily produced in the extracellular space from the breakdown of previously released ATP. It is also accepted that it can be released directly, as adenosine, during pathological events primarily by equilibrative transport. Nevertheless, there is a growing realization that adenosine can be rapidly released from the nervous system in a manner that is dependent upon the activity of neurons. We consider three competing classes of mechanism that could explain neuronal activity dependent adenosine release (exocytosis of ATP followed by extracellular conversion to adenosine; exocytotic release of an unspecified transmitter followed by direct non-exocytotic adenosine release from an interposed cell; and direct exocytotic release of adenosine) and outline discriminatory experimental tests to decide between them. We review several examples of activity dependent adenosine release and explore their underlying mechanisms where these are known. We discuss the limits of current experimental techniques in definitively discriminating between the competing models of release, and identify key areas where technologies need to advance to enable definitive discriminatory tests. Nevertheless, within the current limits, we conclude that there is evidence for a mechanism that strongly resembles direct exocytosis of adenosine underlying at least some examples of neuronal activity dependent adenosine release.
| Item Type: | Journal Article |
|---|---|
| Subjects: | R Medicine > RC Internal medicine > RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry Q Science > QP Physiology |
| Divisions: | Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010) |
| Library of Congress Subject Headings (LCSH): | Adenosine, Adenosine triphosphate, Neurochemistry, Activity coefficients |
| Journal or Publication Title: | Current Neuropharmacology |
| Publisher: | Bentham Science Publishers Ltd. |
| ISSN: | 1570-159X |
| Date: | December 2008 |
| Volume: | Vol.6 |
| Number: | No.4 |
| Page Range: | pp. 329-337 |
| Identification Number: | 10.2174/157015908787386087 |
| Status: | Not Peer Reviewed |
| Access rights to Published version: | Restricted or Subscription Access |
| References: | [1] Arai, A., Kessler, M., Lynch, G. (1990) The effects of adenosine on the development of long-term potentiation. Neurosci Lett, 119, 41-44. [2] [Attwell, D., Laughlin, S.B. (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab, 21, 1133-1145. [3] Basheer, R., Strecker, R.E., Thakkar, M.M., McCarley, R.W. (2004) Adenosine and sleep-wake regulation. Prog. Neurobiol., 73, 379-396. [4] Barnes-Davies, M., Forsythe, I.D. (1995) Pre- and Postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brainstem slices. J. Physiol., 488, 387-406. [5] Boison, D. (2006) Adenosine kinase, epilepsy and stroke: mechanisms and therapies. Trends Pharmacol. Sci., 27, 652-658. [6] Brager, D.H., Thompson, S.M.(2003) Activity-dependent release of adenosine contributes to short-term depression at CA3-CA1 synapses in rat hippocampus. J. Neurophysiol., 89, 22-26. [7] Brockhaus, J., Ballanyi, K. (2000) Anticonvulsant A1 receptor-mediated adenosine action on neuronal networks in the brainstem-spinal cord of newborn rats. Neuroscience, 96, 359-371. [8] Brown, P., Dale, N. (2000) Adenosine A1 receptors modulate high voltage-activated Ca2+ currents and motor pattern generation in the Xenopus embryo. J. Physiol., 525, 655-667. [9] Brown, P., Dale, N. (2002a) Modulation of K+ currents in Xenopus spinal neurons by p2y receptors: a role for ATP and ADP in motor pattern generation. J. Physiol., 540, 843-850. [10] Brown, P., Dale, N. (2002b) Spike-independent release of ATP from Xenopus spinal neurons evoked by activation of glutamate receptors. J. Physiol., 540, 851-860. [11] Brundege, J.M., Dunwiddie, T.V. (1996) Modulation of excitatory synaptic transmission by adenosine released from single hippocampal pyramidal neurons. J. Neurosci., 16, 5603-5612. [12] Brundege, J.M., Dunwiddie, T.V. (1998) Metabolic regulation of endogenous adenosine release from single neurons. Neuroreport, 9, 3007-3011. [13] Cechova, S., Venton, B.J. (2008) Transient adenosine efflux in the rat caudate-putamen. J Neurochem, 105, 1253-1263. [14] Colgin, L.L., Kubota, D., Jia, Y., Rex, C.S., Lynch, G. (2004) Long-term potentiation is impaired in rat hippocampal slices that produce spontaneous sharp waves. J Physiol, 558, 953-961. [15] Craig, C.G., White, T.D. (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. [16] Cunha, R.A. (2005) Neuroprotection by adenosine in the brain: From A1 receptor activation to A2A receptor blockade. Purinergic Signal, 1, 111-134. [17] Dallwig, R., Deitmer, J.W. (2002) Cell-type specific calcium responses in acute rat hippocampal slices. J Neurosci Methods, 116, 77-87. [18] Dale, N., Gilday, D. (1996) Regulation of rhythmic movements by purinergic neurotransmitters in frog embryos. Nature, 383, 259-263. [19] Dale, N. (1998) Delayed production of adenosine underlies temporal modulation of swimming in frog embryo. J. Physiol., 511, 265-272. [20] Dale, N. (2002) Resetting Intrinsic Purinergic Modulation of Neural Activity: An Associative Mechanism? J. Neurosci., 22, 10461-10469. [21] Drury, A.N., Szent-Gyorgyi, A. (1929) The physiological activity of adenine compounds with especial reference to their action upon the mammalian heart. J. Physiol, 68, 213-237. [22] Drysdale, A.J., Ryan, D., Pertwee, R.G., Platt, B. (2006) Cannabidiol-induced intracellular Ca2+ elevations in hippocampal cells. Neuropharmacology, 50, 621-31. [23] Dunwiddie, T.V., Diao, L. (1994) Extracellular adenosine concentration in hippocampal brain slices and the tonic inhibitory modulation of evoked excitatory responses. J. Pharm. Exp. Therp., 268, 537-545. [24] Dunwiddie, T.V., Hoffer, B.J. (1980) Adenine nucleotides and synaptic transmission in the in vitro rat hippocampus. Br. J. Pharmacol., 69, 59-68. [25] Etherington, L.A., Frenguelli, B.G. (2004) Endogenous adenosine modulates epileptiform activity in rat hippocampus in a receptor subtype-dependent manner. Eur J Neurosci, 19, 2539-2550. [26] Fredholm, B.B., AP, I.J., Jacobson, K.A., Klotz, K.N., Linden, J. (2001) International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol Rev, 53, 527-552. [27] Frenguelli, B.G., Llaudet, E., Dale, N. (2003) High-resolution real-time recording with microelectrode biosensors reveals novel aspects of adenosine release during hypoxia in rat hippocampal slices. J. Neurochem., 86, 1506-1515. [28] Frenguelli, B.G., Wigmore, G., Llaudet, E., Dale, N. (2007) Temporal and mechanistic dissociation of ATP and adenosine release during ischaemia in the mammalian hippocampus. J. Neurochem., 101, 1400-1413. [29] Goding, J.W., Grobben, B., Slegers, H. (2003) Physiological and pathophysiological functions of the ecto-nucleotide pyrophosphatase/phosphodiesterase family. Biochim. Biophys. Acta., 1638, 1-19. [30] Hamann, M., Attwell, D. (1996) Non-synaptic release of ATP by electrical stimulation in slices of rat hippocampus, cerebellum and habenula. Eur J Neurosci, 8, 1510-1515. [31] Iqbal, J., Vollmayer, P., Braun, N., Zimmermann, H., Muller, C.E. (2005) A capillary electrophoresis method for the characterization of ecto-nucleoside triphosphate diphosphohydrolases (NTPDases) and the analysis of inhibitors by in-capillary enzymatic microreaction. Purinergic Signal, 1, 349-358. [32] James, S., Richardson, P.J. (1993) Production of adenosine from extracellular ATP at the striatal cholinergic synapse. J. Neurochem., 60, 219-27. [33] Kimura, M., Saitoh N., Takahashi, T. (2003) Adenosine A1 receptor-mediated presynaptic inhibition at the calyx of Held of immature rats. J. Physiol., 553, 415-426. [34] Kocsis, J.D., Eng, D.L., Bhisitkul, R.B. (1984) Adenosine selectively blocks parallel-fiber-mediated synaptic potentials in rat cerebellar cortex. Proc. Natl. Acad. Sci. USA, 81, 6531-6534. [35] Latini, S., Pedata, F. (2001) Adenosine in the central nervous system: release mechanisms and extracellular concentrations. J. Neurochem., 79, 463-484. [36] Llaudet, E., Botting, N.P., Crayston, J.A., 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] Manzoni, O.J., Manabe T., Nicoll, R.A. (1994) Release of adenosine by activation of NMDA receptors in the hippocampus. Science, 265, 2098-2101. [39] Martín, E.D., Fernández, M., Perea, G., Pascual, O., Haydon, P.G., Araque, A., Ceña, V. (2007) Adenosine released by astrocytes contributes to hypoxia-induced modulation of synaptic transmission. Glia, 55, 36-45. [40] Mateos, J.M., Azkue, J., Sarria, R., Kuhn, R., Grandes, P. Knopfel, T. (1998). Localization of the mGlu4a metabotropic glutamate receptor in rat cerebellar cortex. Histochem. Cell Biol., 109, 135-139. [41] Meno, J.R., Crum, A.V., Winn, H.R. (2001). Effect of adenosine receptor blockade on pial arteriolar dilation during sciatic nerve stimulation. Am. J. Physiol. Heart Circ. Physiol., 281, 2018–2027. [42] Mitchell, J.B., Lupica, C.R., Dunwiddie, T.V. (1993) Activity-dependent release of endogenous adenosine modulates synaptic responses in the rat hippocampus. J. Neurosci., 13, 3439-3447. [43] Müller, C.E., Iqbal, J., Baqi, Y., Zimmermann, H., Röllich, A., Stephan, H. (2006) Polyoxometalates--a new class of potent ecto-nucleoside triphosphate diphosphohydrolase (NTPDase) inhibitors. Bioorg. Med. Chem. Lett., 16, 5943-7. [44] Mulligan, S.J., MacVicar, B.A. (2004) Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature, 431, 195-199. [45] Munkonda, M.N., Kauffenstein, G., Kukulski, F., Levesque, S.A., Legendre, C., Pelletier, J., Lavoie, E.G., Lecka, J., Sevigny, J. (2007) Inhibition of human and mouse plasma membrane bound NTPDases by P2 receptor antagonists. Biochem Pharmacol, 74, 1524-1534. [46] Newman, E.A. (2004). Glial modulation of synaptic transmission in the retina. Glia, 47, 268-274. [47] Oliet, S.H.R., Poulain, D. (1999) Adenosine-induced presynaptic inhibition of IPSCs and EPSCs in rat hypothalamic supraoptic nucleus neurones. J. Physiol., 520, 815-825. [48] Otsuguro, K., Yamaji, Y., Ban, M., Ohta, T., Ito, S. (2006) Involvement of adenosine in depression of synaptic transmission during hypercapnia in isolated spinal cord of neonatal rats. J. Physiol., 574, 835-847. [49] Pascual, O., Casper, K.B., Kubera, C., Zhang, J., Revilla-Sanchez, R., Sul, J.Y., Takano, H., Moss, S.J., McCarthy, K., Haydon, P.G. (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science, 310, 113-116. [50] Ralevic, V., Burnstock, G. (1998) Receptors for purines and pyrimidines. Pharmacol. Rev., 50, 413-492. [51] Riquelme, R., Miralles, C.P., De Blas, A.L. (2002). Bergmann glia GABAA Receptors concentrate on the glial processes that wrap inhibitory synapses. J. Neurosci., 22, 10720-10730. [52] Rivkees, S.A., Price, S.L., Zhou, F.C. (1995) Immunohistochemical detection of A1 adenosine receptors in rat brain with emphasis on localization in the hippocampal formation, cerebral cortex, cerebellum and basal ganglia. Brain Res., 677, 193-203. [53] Robson, S.C., Sevigny, J., Zimmermann, H. (2006) The E-NTPDase family of ectonucleotidases: Structure function relationships and pathophysiological significance. Purinergic Signal, 2, 409-430. [54] Rudolphi, K.A., Schubert, P., Parkinson, F.E., Fredholm, B.B. (1992) Adenosine and Brain Ischemia. Cerebro. Brain Metab. Rev., 4, 346-369. [55] Schubert, P., Mitzdorf, U. (1979) Analysis and quantitative evaluation of the depressant effect of adenosine on evoked potentials in hippocampal slices. Brain Res., 172,186-190. [56] Sosnowski, M., Stevens, C.W., Yaksh, T.L. (1989) Assessment of the role of A1/A2 adenosine receptors mediating the purine antinociception, motor and autonomic function in the rat spinal cord. J. Pharmacol. Exp. Ther., 250, 915-922. [57] Studer, F.E., Fedele, D.E., Marowsky, A., Schwerdel, C., Wernli, K., Vogt, K., Fritschy, J.M., 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. [58] Swamy, B.E., Venton, B.J. (2007) Subsecond detection of physiological adenosine concentrations using fast-scan cyclic voltammetry. Anal Chem, 79, 744-750. [59] Takano, T., Tian, G.F., Peng, W., Lou, N., Libionka, W., Han, X., Nedergaard, M. (2005) Astrocyte-mediated control of cerebral blood flow. Nat. Neurosci., 9, 260-267. [60] Wall, M.J., Dale, N. (2007) Auto-inhibition of rat parallel fibre-Purkinje cell synapses by activity-dependent adenosine release. J. Physiol., 581, 553-565. [61] Wong, Y.C., Billups, B., Johnston, J., Evans R.J., Forsythe, I.D., (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] Yamamoto, M., Wada, N., Kitabatake, Y., Watanabe, D., Anzai, M., Yokoyama, M., Teranishi, Y., Nakanishi, S. (2003) Reversible suppression of glutamatergic neurotransmission of cerebellar granule cells in vivo by genetically manipulated expression of tetanus neurotoxin light chain. J. Neurosci., 23, 6759-67. [63] Zimmermann, H. (1996) Accumulation of synaptic vesicle proteins and cytoskeletal specializations at the peripheral node of Ranvier. Microsc. Res. Tech., 34, 462-473. [64] Zimmermann, H., Braun, N. (1999) Ecto-nucleotidases--molecular structures, catalytic properties, and functional roles in the nervous system. Prog. Brain. Res., 120, 371-385. [65] Zimmermann, H. (2000) Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch. Pharmacol., 362, 299-309. [66] Ziganshin, A.U., Ziganshina, L.E., King, B.F., Pintor, J., Burnstock, G. (1996) Effects of P2-purinoceptor antagonists on degradation of adenine nucleotides by ecto-nucleotidases in folliculated oocytes of Xenopus laevis. Biochem Pharmacol, 51, 897-901. [67] Zonta, M., Angulo, M.C., Gobbo, S., Rosengarten, B., Hossmann, K.A., Pozzan, T., Carmignoto, G. (2003) Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat. Neurosci., 6, 43-50. |
| URI: | http://wrap.warwick.ac.uk/id/eprint/1307 |
Data sourced from Thomson Reuters' Web of Knowledge
Actions (login required)
![]() |
View Item |
Tools
Tools

