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ATP derived from astrocytes modulates memory in the chick

Published online by Cambridge University Press:  06 July 2012

Marie E. Gibbs ,
Maria Shleper ,
Tomris Mustafa ,
Geoffrey Burnstock  and
David N. Bowser
Marie E. Gibbs*
Affiliation:
Department of Anatomy and Developmental Biology, Monash University, Clayton, Victoria, Australia Monash Institute of Pharmaceutical Sciences, Parkville, Victoria, Australia
Maria Shleper
Affiliation:
Florey Neurosciences Institute, University of Melbourne, Victoria, Australia
Tomris Mustafa
Affiliation:
Florey Neurosciences Institute, University of Melbourne, Victoria, Australia
Geoffrey Burnstock
Affiliation:
Autonomic Neuroscience Centre, University College Medical School, London, UK
David N. Bowser
Affiliation:
Florey Neurosciences Institute, University of Melbourne, Victoria, Australia
*
Correspondence should be addressed to: Marie E. Gibbs, Monash Institute of Pharmaceutical Sciences, 399 Royal Parade, Parkville, Victoria 3052, Australia email: [email protected]
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Abstract

Memory consolidation in a discriminative bead pecking task is modulated by endogenous adenosine triphosphate (ATP) acting at purinergic receptors in the hippocampus. Consolidation, from short- to intermediate- to long-term memory during two distinct periods following training, was blocked by the non-selective P2 purinergic receptor antagonist PPADS (pyridoxal phosphate-6-azo(benzene-2,4-disulphonic acid) tetrasodium salt hydrate and the specific P2Y1 receptor antagonist MRS2179. Direct injections of the ATP agonists (ATPγS and ADPβS) potentiated memory consolidation and the effect of ADPβS was blocked by MRS2179, suggesting an important role of ATP on memory consolidation via the P2Y1 receptor in the chick hippocampus. Incubation of astrocytes with ATPγS and ADPβS resulted in the increase of intracellular calcium ([Ca2+]i), the latter being blocked by MRS2179 suggesting a specific role for P2Y1 receptors in the calcium response. This response was prevented by blocking astrocytic oxidative metabolism with fluoroacetate. We argue that the source of the ATP acting on neuronal P2Y1 receptors is most likely to be astrocytes. Thrombin selectively increases [Ca2+]i in astrocytes but not in neurones. The main findings of the present study are: (a) astrocytic [Ca2+]i plays an important role in the consolidation of short-term to long-term memory; and (b) ATP released from chick astrocytes during learning modulates neuronal activity through astrocytic P2Y1 receptors.

Keywords

Purinergic transmissionATPastrocytememory consolidationcalcium transients
Type
Research Article
Information
Neuron Glia Biology , Volume 7 , Issue 2-4 , May 2011 , pp. 177 - 186
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Almeida, T., Rodrigues, R.J., de Mendonca, A., Ribeiro, J.A. and Cunha, R.A. (2003) Purinergic P2 receptors trigger adenosine release leading to adenosine A2A receptor activation and facilitation of long-term potentiation in rat hippocampal slices. Neuroscience 122, 111–121.Google Scholar
Anderson, C.M. and Nedergaard, M. (2003) Astrocyte-mediated control of cerebral microcirculation. Trends in Neurosciences 26, 340–344; author reply 344–345.Google Scholar
Atoji, Y. and Wild, J.M. (2006) Anatomy of the avian hippocampal formation. Reviews in the Neurosciences 17, 3–15.Google Scholar
Bernstein, M., Behnisch, T., Balschun, D., Reymann, K.G. and Reiser, G. (1998) Pharmacological characterisation of metabotropic glutamatergic and purinergic receptors linked to Ca2+ signalling in hippocampal astrocytes. Neuropharmcology 37, 169–178.Google Scholar
Bowser, D.N. and Khakh, B.S. (2004) ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. Journal of Neuroscience 24, 8606–8620.Google Scholar
Bowser, D.N. and Khakh, B.S. (2007) Vesicular ATP is the predominant cause of intercellular calcium waves in astrocytes. Journal of General Physiology 129, 485–491.Google Scholar
Burnstock, G. (2007) Physiology and pathophysiology of purinergic neurotransmission. Physiological Reviews 87, 659–797.Google Scholar
Bushong, E.A., Martone, M.E., Jones, Y.Z. and Ellisman, M.H. (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. Journal of Neuroscience 22, 183–192.Google Scholar
Cronin, C., Edwards, T.M. and Gibbs, M.E. (2011) Role for purinergic receptors in memory processing in young chicks. Behavioural Brain Research 223, 417–420.Google Scholar
Fields, R.D. and Burnstock, G. (2006) Purinergic signalling in neuron–glia interactions. Nature Reviews Neuroscience 7, 423–436.Google Scholar
Fujii, S., Sasaki, H., Mikoshiba, K., Kuroda, Y., Yamazaki, Y., Mostafa Taufiq, A. et al. (2004) A chemical LTP induced by co-activation of metabotropic and N-methyl-D-aspartate glutamate receptors in hippocampal CA1 neurons. Brain Research 999, 20–28.Google Scholar
Gallagher, C.J. and Salter, M.W. (2003) Differential properties of astrocyte calcium waves mediated by P2Y1 and P2Y2 receptors. Journal of Neuroscience 23, 6728–6739.Google Scholar
Gibbs, M.E. (2008) Memory systems in the chick: regional and temporal control by noradrenaline. Brain Research Bulletin 76, 170–182.Google Scholar
Gibbs, M.E. and Bowser, D.N. (2009) Astrocytes and interneurons in memory processing in the chick hippocampus: roles for G-coupled protein receptors, GABA(B) and mGluR1. Neurochemical Research 34, 1712–1720.Google Scholar
Gibbs, M.E. and Bowser, D.N. (2010) Astrocytic adrenoceptors and learning: alpha1-adrenoceptors. Neurochemistry International 57, 404–410.Google Scholar
Gibbs, M.E. and Ng, K.T. (1977) Psychobiology of memory: towards a model of memory formation. Biobehavioral Reviews 1, 113–136.Google Scholar
Gibbs, M.E. and Ng, K.T. (1979) Behavioural stages in memory formation. Neuroscience Letters 13, 279–283.Google Scholar
Gibbs, M.E. and Summers, R.J. (2002) Role of adrenoceptor subtypes in memory consolidation. Progress in Neurobiology 67, 345–391.Google Scholar
Gibbs, M.E., Anderson, D.G. and Hertz, L. (2006) Inhibition of glycogenolysis in astrocytes interrupts memory consolidation in young chicks. GLIA 54, 214–222.Google Scholar
Gibbs, M.E., Bowser, D.N., Hutchinson, D.S., Loiacono, R.E. and Summers, R.J. (2008a) Memory processing in the avian hippocampus involves interactions between β-adrenoceptors, glutamate receptors and metabolism. Neuropsychopharmacology 33, 2831–2846.Google Scholar
Gibbs, M.E., Hutchinson, D.S. and Hertz, L. (2008b) Astrocytic involvement in learning and memory consolidation. Neuroscience and Biobehavioral Reviews 32, 927–944.Google Scholar
Gimenez-Llort, L., Masino, S.A., Diao, L., Fernandez-Teruel, A., Tobena, A., Halldner, L.M. et al. (2005) Mice lacking the adenosine A1 receptor have normal spatial learning and plasticity in the CA1 region of the hippocampus, but they habituate more slowly. Synapse 57, 8–16.Google Scholar
Halassa, M.M., Fellin, T. and Haydon, P.G. (2009) Tripartite synapses: roles for astrocytic purines in the control of synaptic physiology and behavior. Neuropharmacology 57, 343–346.Google Scholar
Haydon, P.G. (2001) Glia: listening and talking to the synapse. Nature Reviews Neuroscience 2, 185–193.Google Scholar
Huang, Y., Sudibya, H.G., Fu, D., Xue, R., Dong, X., Li, L.J. et al. (2009) Label-free detection of ATP release from living astrocytes with high temporal resolution using carbon nanotube network. Biosensors and Bioelectronics 24, 2716–2720.Google Scholar
Izquierdo, I., Bevilaqua, L.R., Rossato, J.I., Bonini, J.S., Medina, J.H. and Cammarota, M. (2006) Different molecular cascades in different sites of the brain control memory consolidation. Trends in Neurosciences 29, 496–505.Google Scholar
Izquierdo, L.A., Barros, D.M., da Costa, J.C., Furini, C., Zinn, C., Cammarota, M. et al. (2007) A link between role of two prefrontal areas in immediate memory and in long-term memory consolidation. Neurobiology of Learning and Memory 88, 160–166.Google Scholar
Jarvis, E.D., Güntürkün, O., Bruce, L., Csillag, A., Karten, H., Kuenze, W. et al. (2005) Avian brains and a new understanding of vertebrate brain evolution. Nature Reviews Neuroscience 6, 151–159.Google Scholar
Junge, C.E., Lee, C.J., Hubbard, K.B., Zhang, Z., Olson, J.J., Hepler, J.R. et al. (2004) Protease-activated receptor-1 in human brain: localization and functional expression in astrocytes. Experimental Neurology 188, 94–103.Google Scholar
Mori, M., Heuss, C., Gahwiler, B.H. and Gerber, U. (2001) Fast synaptic transmission mediated by P2X receptors in CA3 pyramidal cells of rat hippocampal slice cultures. Journal of Physiology 535, 115–123.Google Scholar
Nedergaard, M., Ransom, B. and Goldman, S.A. (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends in Neurosciences 26, 523–530.Google Scholar
Ng, F.S., Tangredi, M.M. and Jackson, F.R. (2011) Glial cells physiologically modulate clock neurons and circadian behavior in a calcium-dependent manner. Current Biology 21, 625–634.Google Scholar
North, R.A. and Verkhratsky, A. (2006) Purinergic transmission in the central nervous system. Pflügers Archiv European Journal of Physiology 452, 479–485.Google Scholar
Pankratov, Y., Lalo, U., Verkhratsky, A. and North, R.A. (2006) Vesicular release of ATP at central synapses. Pflügers Archiv European Journal of Physiology 452, 589–597.Google Scholar
Pankratov, Y.V., Lalo, U.V. and Krishtal, O.A. (2002) Role for P2X receptors in long-term potentiation. Journal of Neuroscience 22, 8363–8369.Google Scholar
Pascual, O., Casper, K.B., Kubera, C., Zhang, J., Revilla-Sanchez, R., Sul, J.Y. et al. (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310, 113–116.Google Scholar
Pettmann, B., Louis, J.C. and Sensenbrenner, M. (1979) Morphological and biochemical maturation of neurones cultured in the absence of glial cells. Nature 281, 378–380.Google Scholar
Pryazhnikov, E. and Khiroug, L. (2008) Sub-micromolar increase in [Ca(2+)](i) triggers delayed exocytosis of ATP in cultured astrocytes. GLIA 56, 38–49.Google Scholar
Puelles, L., Kuwana, E., Puelles, E., Bulfone, A., Shimamura, K., Keleher, J. et al. (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. Journal of Comparative Neurology 424, 409–438.Google Scholar
Rex, C.S., Kramar, E.A., Colgin, L.L., Lin, B., Gall, C.M. and Lynch, G. (2005) Long-term potentiation is impaired in middle-aged rats: regional specificity and reversal by adenosine receptor antagonists. Journal of Neuroscience 25, 5956–5966.Google Scholar
Serrano, A., Haddjeri, N., Lacaille, J.C. and Robitaille, R. (2006) GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. Journal of Neuroscience 26, 5370–5382.Google Scholar
Shigetomi, E., Bowser, D.N., Sofroniew, M.V. and Khakh, B.S. (2008) Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons. Journal of Neuroscience 28, 6659–6663.Google Scholar
Simard, M., Arcuino, G., Takano, T., Liu, Q.S. and Nedergaard, M. (2003) Signaling at the gliovascular interface. Journal of Neuroscience 23, 9254–9262.Google Scholar
Sperlagh, B., Zsilla, G., Baranyi, M., Illes, P. and Vizi, E.S. (2007) Purinergic modulation of glutamate release under ischemic-like conditions in the hippocampus. Neuroscience 149, 99–111.Google Scholar
Szekely, A.D. (1999) The avian hippocampal formation: subdivisions and connectivity. Behavioural Brain Research 98, 219–225.Google Scholar
Tokuyama, Y., Hara, M., Jones, E.M.C., Fan, Z. and Bell, G.I. (1995) Cloning of rat and mouse P2Y purinoceptors. Biochemical and Biophysical Research Communications 211, 211–218.Google Scholar
Torres, A., Wang, F., Xu, Q., Fujita, T.Dobrowolski, R., Willecke, K. et al. (2012) Extracellular Ca2+ acts as a mediator of communication from neurons to gila. Neuroscience Signaling 5, 1–12.Google Scholar
Webb, T.E., Simon, J. and Barnard, E.A. (1998) Regional distribution of [35S]2′-deoxy 5′-O-(1-thio) ATP binding sites and the P2Y1 messenger RNA within the chick brain. Neuroscience 84, 825–837.Google Scholar
Webb, T.E., Simon, J., Krishek, B.K., Bateson, A.N., Smart, T.G., King, B.F. et al. (1993) Cloning and functional expression of a brain G-protein-coupled ATP receptor. FEBS Letters 324, 219–225.Google Scholar
Wieraszko, A. and Seyfried, T.N. (1989) ATP-induced synaptic potentiation in hippocampal slices. Brain Research 491, 356–359.Google Scholar
Yamazaki, Y., Fujii, S., Nakamura, T., Miyakawa, H., Kudo, Y., Kato, H. et al. (2002) Changes in [Ca2+](i) during adenosine triphosphate-induced synaptic plasticity in hippocampal CA1 neurons of the guinea pig. Neuroscience Letters 324, 65–68.Google Scholar
Yarbrough, G.G. and McGuffin-Clineschmidt, J.C. (1981) In vivo behavioral assessment of central nervous system purinergic receptors. European Journal of Pharmacology 76, 137–144.Google Scholar