Introduction to Purinergic Signalling in the Brain

Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 986)

Abstract

ATP is a cotransmitter with glutamate, noradrenaline, GABA, acetylcholine and dopamine in the brain. There is a widespread presence of both adenosine (P1) and P2 nucleotide receptors in the brain on both neurons and glial cells. Adenosine receptors play a major role in presynaptic neuromodulation, while P2X ionotropic receptors are involved in fast synaptic transmission and synaptic plasticity. P2Y G protein-coupled receptors are largely involved in presynaptic activities, as well as mediating long-term (trophic) signalling in cell proliferation, differentiation and death during development and regeneration. Both P1 and P2 receptors participate in neuron-glial interactions. Purinergic signalling is involved in control of cerebral vascular tone and remodelling and has been implicated in learning and memory, locomotor and feeding behaviour and sleep. There is increasing interest in the involvement of purinergic signalling in the pathophysiology of the CNS, including trauma, ischaemia, epilepsy, neurodegenerative diseases, neuropsychiatric and mood disorders, and cancer, including gliomas.

Keywords

ATP Adenosine Purinoceptors Cotransmission Neuromodulation Glia Neuron-gial interactions Trophic signalling Memory Sleep Neurodegenerative diseases Gliomas 

Abbreviations

ACh

Acetylcholine

ADP

Adenosine diphosphate

ATP

Adenosine 5′-triphosphate

bFGF

Basic fibroblast growth factor

CNS

Central nervous system

CREB

cAMP response element-binding protein

E-NPPs

Ecto-nucleotide pyrophosphatase/phosphodiesterases

E-NTPDases

Ecto-nucleoside triphosphate diphosphohydrolase

GABA

γ-Amino butyric acid

IL-6

Interleukin-6

NA

Noradrenaline

UDP

Uridine diphosphate

UTP

Uridine 5′-triphosphate

TMZ

Temozolomide

References

  1. Abbracchio MP (1997) ATP in brain function. In: Jacobson KA, Jarvis MF (eds) Purinergic approaches in experimental therapeutics. Wiley-Liss, New YorkGoogle Scholar
  2. Abbracchio MP, Burnstock G (1994) Purinoceptors: are there families of P2X and P2Y purinoceptors? Pharmacol Ther 64:445–475PubMedGoogle Scholar
  3. Abbracchio MP, Burnstock G (1998) Purinergic signalling: pathophysiological roles. Jpn J Pharmacol 78:113–145PubMedGoogle Scholar
  4. Antoniou K, Papadopoulou-Daifoti Z, Hyphantis T, Papathanasiou G, Bekris E, Marselos M, Panlilio L, Muller CE, Goldberg SR, Ferre S (2005) A detailed behavioral analysis of the acute motor effects of caffeine in the rat: involvement of adenosine A1 and A2A receptors. Psychopharmacology (Berl) 183:154–162Google Scholar
  5. Arrigoni E, Chamberlin NL, Saper CB, McCarley RW (2003) The effects of adenosine on the membrane properties of basal forebrain cholinergic neurons. Sleep 26:45–50Google Scholar
  6. Ballerini P, Di Iorio P, Caciagli F, Rathbone MP, Jiang S, Nargi E, Buccella S, Giuliani P, D’Alimonte I, Fischione G, Masciulli A, Romano S, Ciccarelli R (2006) P2Y2 receptor up-regulation induced by guanosine or UTP in rat brain cultured astrocytes. Int J Immunopathol Pharmacol 19:293–308PubMedGoogle Scholar
  7. Barberis C, McIlwain H (1976) 5′-Adenine mononucleotides in synaptosomal preparations from guinea pig neocortex: their change on incubation, superfusion and stimulation. J Neurochem 26:1015–1021PubMedGoogle Scholar
  8. Bardoni R, Goldstein PA, Lee CJ, Gu JG, MacDermott AB (1997) ATP P2X receptors mediate fast synaptic transmission in the dorsal horn of the rat spinal cord. J Neurosci 17:5297–5304PubMedGoogle Scholar
  9. Barraco RA, Coffin VL, Altman HJ, Phillis JW (1983) Central effects of adenosine analogs on locomotor activity in mice and antagonism of caffeine. Brain Res 272:392–395PubMedGoogle Scholar
  10. Barraco RA, Martens KA, Parizon M, Normile HJ (1993) Adenosine A2a receptors in the nucleus accumbens mediate locomotor depression. Brain Res Bull 31:397–404PubMedGoogle Scholar
  11. Basheer R, Strecker RE, Thakkar MM, McCarley RW (2004) Adenosine and sleep-wake regulation. Prog Neurobiol 73:379–396PubMedGoogle Scholar
  12. Belcher SM, Zsarnovszky A, Crawford PA, Hemani H, Spurling L, Kirley TL (2006) Immunolocalization of ecto-nucleoside triphosphate diphosphohydrolase 3 in rat brain: implications for modulation of multiple homeostatic systems including feeding and sleep-wake behaviors. Neuroscience 137:1331–1346PubMedGoogle Scholar
  13. Bo X, Burnstock G (1994) Distribution of [3H]alpha, beta-methylene ATP binding sites in rat brain and spinal cord. Neuroreport 5:1601–1604PubMedGoogle Scholar
  14. Bowser DN, Khakh BS (2007) Vesicular ATP is the predominant cause of intercellular calcium waves in astrocytes. J Gen Physiol 129:485–491PubMedGoogle Scholar
  15. Braganhol E, Morrone FB, Bernardi A, Huppes D, Meurer L, Edelweiss MI, Lenz G, Wink MR, Robson SC, Battastini AM (2009) Selective NTPDase2 expression modulates in vivo rat glioma growth. Cancer Sci 100:1434–1442PubMedGoogle Scholar
  16. Brake AJ, Wagenbach MJ, Julius D (1994) New structural motif for ligand-gated ion channels defined by an ionotropic ATP receptor. Nature 371:519–523PubMedGoogle Scholar
  17. Brambilla R, Cottini L, Fumagalli M, Ceruti S, Abbracchio MP (2003) Blockade of A2A adenosine receptors prevents basic fibroblast growth factor-induced reactive astrogliosis in rat striatal primary astrocytes. Glia 43:190–194PubMedGoogle Scholar
  18. Brockhaus J, Dressel D, Herold S, Deitmer JW (2004) Purinergic modulation of synaptic input to Purkinje neurons in rat cerebellar brain slices. Eur J Neurosci 19:2221–2230PubMedGoogle Scholar
  19. Buller KM, Khanna S, Sibbald JR, Day TA (1996) Central noradrenergic neurons signal via ATP to elicit vasopressin responses to haemorrhage. Neuroscience 73:637–642PubMedGoogle Scholar
  20. Burnstock G (1972) Purinergic nerves. Pharmacol Rev 24:509–581PubMedGoogle Scholar
  21. Burnstock G (1976) Purinergic receptors. J Theor Biol 62:491–503PubMedGoogle Scholar
  22. Burnstock G (1978) A basis for distinguishing two types of purinergic receptor. In: Straub RW, Bolis L (eds) Cell membrane receptors for drugs and hormones: a multidisciplinary approach. Raven Press, New YorkGoogle Scholar
  23. Burnstock G (1996) Purinergic neurotransmission. Semin Neurosci 8:171–174Google Scholar
  24. Burnstock G (2003) Purinergic receptors in the nervous system. In: Schwiebert EM (ed) Purinergic receptors and signalling. Academic, San DiegoGoogle Scholar
  25. Burnstock G (2007a) Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87:659–797PubMedGoogle Scholar
  26. Burnstock G (2007b) Purine and pyrimidine receptors. Cell Mol Life Sci 64:1471–1483PubMedGoogle Scholar
  27. Burnstock G (2008) Purinergic signalling and disorders of the central nervous system. Nat Rev Drug Discov 7:575–590PubMedGoogle Scholar
  28. Burnstock G (2009) Purinergic cotransmission. Exp Physiol 94:20–24PubMedGoogle Scholar
  29. Burnstock G, Kennedy C (1985) Is there a basis for distinguishing two types of P2-purinoceptor? Gen Pharmacol 16:433–440PubMedGoogle Scholar
  30. Burnstock G, Knight GE (2004) Cellular distribution and functions of P2 receptor subtypes in different systems. Int Rev Cytol 240:31–304PubMedGoogle Scholar
  31. Carrasquero LM, Delicado EG, Jimenez AI, Perez-Sen R, Miras-Portugal MT (2005) Cerebellar astrocytes co-express several ADP receptors. Presence of functional P2Y(13)-like receptors. Purinergic Signal 1:153–159PubMedGoogle Scholar
  32. Claes P, Slegers H (2004) P2Y receptor activation affects the proliferation and differentiation of glial and neuronal cells: a focus on rat C6 glioma cells. Curr Neuropharmacol 2:207–220Google Scholar
  33. 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 278:1354–1362PubMedGoogle Scholar
  34. Cotrina ML, Lin JH, Lopez-Garcia JC, Naus CC, Nedergaard M (2000) ATP-mediated glia signaling. J Neurosci 20:2835–2844PubMedGoogle Scholar
  35. Cunha RA, Ribeiro JA (2000) ATP as a presynaptic modulator. Life Sci 68:119–137PubMedGoogle Scholar
  36. Diaz-Hernandez M, Pintor J, Castro E, Miras-Portugal MT (2002) Co-localisation of functional nicotinic and ionotropic nucleotide receptors in isolated cholinergic synaptic terminals. Neuropharmacology 42:20–33PubMedGoogle Scholar
  37. Duan S, Neary JT (2006) P2X(7) receptors: properties and relevance to CNS function. Glia 54:738–746PubMedGoogle Scholar
  38. Dubyak GR (1991) Signal transduction by P2-purinergic receptors for extracellular ATP. Am J Respir Cell Mol Biol 4:295–300PubMedGoogle Scholar
  39. Dubyak GR (2006) ATP release mechanisms. In: Burnstock G, Arnett TR (eds) Edited monograph: nucleotides and regulation of bone cell function. Taylor & Francis, Boca RatonGoogle Scholar
  40. Dunwiddie TV (1985) The physiological role of adenosine in the central nervous system. Int Rev Neurobiol 27:63–139PubMedGoogle Scholar
  41. Dunwiddie TV, Masino SA (2001) The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 24:31–55PubMedGoogle Scholar
  42. Edwards FA, Gibb AJ, Colquhoun D (1992) ATP receptor-mediated synaptic currents in the central nervous system. Nature 359:144–147PubMedGoogle Scholar
  43. Eroglu L, Tuna R, Caglayan B (1996) Effects of nifedipine and Bay K 8644 on the R-PIA and caffeine-induced changes in the locomotor activity of rats. Pharmacol Res 33:141–144PubMedGoogle Scholar
  44. Feldberg W, Sherwood SL (1954) Injections of drugs into the lateral ventricle of the cat. J Physiol 123:148–167PubMedGoogle Scholar
  45. Fields RD, Burnstock G (2006) Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 7:423–436PubMedGoogle Scholar
  46. Fredholm BB (1995) Purinoceptors in the nervous system. Pharmacol Toxicol 76:228–239PubMedGoogle Scholar
  47. Fujii S, Sasaki H, Mikoshiba K, Kuroda Y, Yamazaki Y, Mostafa Taufiq A, Kato H (2004) A chemical LTP induced by co-activation of metabotropic and N-methyl-D-aspartate glutamate receptors in hippocampal CA1 neurons. Brain Res 999:20–28PubMedGoogle Scholar
  48. 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 43:218–203PubMedGoogle Scholar
  49. Gibb AJ, Halliday FC (1996) Fast purinergic transmission in the central nervous system. Semin Neurosci 8:225–232Google Scholar
  50. Gordon JL (1986) Extracellular ATP: effects, sources and fate. Biochem J 233:309–319PubMedGoogle Scholar
  51. Ho MCK, Simon J, Barnard EA, Wong YH (2004) Atypical regulation of calcium signals in astrocytoma 1321N1 cells expressing the purinergic P2Y12 receptor. J Neurochem 88:84Google Scholar
  52. Illes P, Alexandre Ribeiro J (2004) Molecular physiology of P2 receptors in the central nervous system. Eur J Pharmacol 483:5–17PubMedGoogle Scholar
  53. Illes P, Zimmermann H (1999) Nucleotides and their receptors in the nervous system. Prog Brain Res 120:1–432Google Scholar
  54. Illes P, Wirkner K, Nörenberg W, Masino SA, Dunwiddie TV (2001) Interaction between the transmitters ATP and glutamate in the central nervous system. Drug Dev Res 52:76–82Google Scholar
  55. Inoue K, Koizumi S, Ueno S (1996) Implication of ATP receptors in brain functions. Prog Neurobiol 50:483–492PubMedGoogle Scholar
  56. Jantaratnotai N, Choi HB, McLarnon JG (2009) ATP stimulates chemokine production via a store-operated calcium entry pathway in C6 glioma cells. BMC Cancer 9:442PubMedGoogle Scholar
  57. Jo YH, Role LW (2002) Coordinate release of ATP and GABA at in vitro synapses of lateral hypothalamic neurons. J Neurosci 22:4794–4804PubMedGoogle Scholar
  58. Judelson DA, Armstrong LE, Sokmen B, Roti MW, Casa DJ, Kellogg MD (2005) Effect of chronic caffeine intake on choice reaction time, mood, and visual vigilance. Physiol Behav 85:629–634PubMedGoogle Scholar
  59. 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 7:2665–2669PubMedGoogle Scholar
  60. Kanjhan R, Housley GD, Burton LD, Christie DL, Kippenberger A, Thorne PR, Luo L, Ryan AF (1999) Distribution of the P2X2 receptor subunit of the ATP-gated ion channels in the rat central nervous system. J Comp Neurol 407:11–32PubMedGoogle Scholar
  61. Kapoor JR, Sladek CD (2000) Purinergic and adrenergic agonists synergize in stimulating vasopressin and oxytocin release. J Neurosci 20:8868–8875PubMedGoogle Scholar
  62. Katayama M, Kawaguchi T, Berger MS, Pieper RO (2007) DNA damaging agent-induced autophagy produces a cytoprotective adenosine triphosphate surge in malignant glioma cells. Cell Death Differ 14:548–558PubMedGoogle Scholar
  63. Kato F, Kawamura M, Shigetomi E, Tanaka J, Inoue K (2004) ATP- and adenosine-mediated signaling in the central nervous system: synaptic purinoceptors: the stage for ATP to play its “dual-role”. J Pharmacol Sci 94:107–111PubMedGoogle Scholar
  64. Khakh BS (2001) Molecular physiology of P2X receptors and ATP signalling at synapses. Nat Rev Neurosci 2:165–174PubMedGoogle Scholar
  65. Khakh BS, Fisher JA, Nashmi R, Bowser DN, Lester HA (2005) An angstrom scale interaction between plasma membrane ATP-gated P2X2 and alpha4beta2 nicotinic channels measured with fluorescence resonance energy transfer and total internal reflection fluorescence microscopy. J Neurosci 25:6911–6920PubMedGoogle Scholar
  66. Kittner H, Krugel U, Hoffmann E, Illes P (2004) Modulation of feeding behaviour by blocking purinergic receptors in the rat nucleus accumbens: a combined microdialysis, electroencephalographic and behavioural study. Eur J Neurosci 19:396–404PubMedGoogle Scholar
  67. Kittner H, Franke H, Harsch JI, El-Ashmawy IM, Seidel B, Krugel U, Illes P (2006) Enhanced food intake after stimulation of hypothalamic P2Y1 receptors in rats: modulation of feeding behaviour by extracellular nucleotides. Eur J Neurosci 24:2049–2056PubMedGoogle Scholar
  68. Kogure K, Alonso OF (1978) A pictorial representation of endogenous brain ATP by a bioluminescent method. Brain Res 154:273–284PubMedGoogle Scholar
  69. Krugel U, Kittner H, Franke H, Illes P (2003) Purinergic modulation of neuronal activity in the mesolimbic dopaminergic system in vivo. Synapse 47:134–142PubMedGoogle Scholar
  70. Krugel U, Spies O, Regenthal R, Illes P, Kittner H (2004) P2 receptors are involved in the mediation of motivation-related behavior. Purinergic Signal 1:21–29PubMedGoogle Scholar
  71. Kukulski F, Sevigny J, Komoszynski M (2004) Comparative hydrolysis of extracellular adenine nucleotides and adenosine in synaptic membranes from porcine brain cortex, hippocampus, cerebellum and medulla oblongata. Brain Res 1030:49–56PubMedGoogle Scholar
  72. Kuzmin A, Johansson B, Gimenez L, Ogren SO, Fredholm BB (2006) Combination of adenosine A1 and A2A receptor blocking agents induces caffeine-like locomotor stimulation in mice. Eur Neuropsychopharmacol 16:129–136PubMedGoogle Scholar
  73. Lakshmi S, Joshi PG (2006) Activation of Src/kinase/phospholipase C/mitogen-activated protein kinase and induction of neurite expression by ATP, independent of nerve growth factor. Neuroscience 141:179–189PubMedGoogle Scholar
  74. Levine AS, Morley JE (1982) Purinergic regulation of food intake. Science 217:77–79PubMedGoogle Scholar
  75. Llewellyn-Smith IJ, Burnstock G (1998) Ultrastructural localization of P2X3 receptors in rat sensory neurons. Neuroreport 9:2545–2550PubMedGoogle Scholar
  76. Loesch A, Burnstock G (1998) Electron-immunocytochemical localization of P2X1 receptors in the rat cerebellum. Cell Tissue Res 294:253–260PubMedGoogle Scholar
  77. Londos C, Cooper DM, Wolff J (1980) Subclasses of external adenosine receptors. Proc Natl Acad Sci U S A 77:2551–2554PubMedGoogle Scholar
  78. Lustig KD, Shiau AK, Brake AJ, Julius D (1993) Expression cloning of an ATP receptor from mouse neuroblastoma cells. Proc Natl Acad Sci U S A 90:5113–5117PubMedGoogle Scholar
  79. Masino SA, Dunwiddie TV (2001) Role of purines and pyrimidines in the central nervous system. In: Abbracchio MP, Williams M (eds) Purinergic and pirimidinergic signalling. Springer, BerlinGoogle Scholar
  80. Matsuoka I, Ohkubo S (2004) ATP- and adenosine-mediated signaling in the central nervous system: adenosine receptor activation by ATP through rapid and localized generation of adenosine by ecto-nucleotidases. J Pharmacol Sci 94:95–99PubMedGoogle Scholar
  81. Mishra SK, Braun N, Shukla V, Fullgrabe M, Schomerus C, Korf HW, Gachet C, Ikehara Y, Sevigny J, Robson SC, Zimmermann H (2006) Extracellular nucleotide signaling in adult neural stem cells: synergism with growth factor-mediated cellular proliferation. Development 133:675–684PubMedGoogle Scholar
  82. Montana V, Malarkey EB, Verderio C, Matteoli M, Parpura V (2006) Vesicular transmitter release from astrocytes. Glia 54:700–715PubMedGoogle Scholar
  83. Mooradian AD, Grabau G, Bastani B (1994) Adenosine triphosphatases of rat cerebral microvessels. Effect of age and diabetes mellitus. Life Sci 55:1261–1265PubMedGoogle Scholar
  84. Moore D, Chambers J, Waldvogel H, Faull R, Emson P (2000) Regional and cellular distribution of the P2Y(1) purinergic receptor in the human brain: striking neuronal localisation. J Comp Neurol 421:374–384PubMedGoogle Scholar
  85. Moran-Jimenez MJ, Matute C (2000) Immunohistochemical localization of the P2Y(1) purinergic receptor in neurons and glial cells of the central nervous system. Brain Res Mol Brain Res 78:50–58PubMedGoogle Scholar
  86. Mori M, Heuss C, Gahwiler BH, Gerber U (2001) Fast synaptic transmission mediated by P2X receptors in CA3 pyramidal cells of rat hippocampal slice cultures. J Physiol 535:115–123PubMedGoogle Scholar
  87. Nagel J, Schladebach H, Koch M, Schwienbacher I, Muller CE, Hauber W (2003) Effects of an adenosine A2A receptor blockade in the nucleus accumbens on locomotion, feeding, and prepulse inhibition in rats. Synapse 49:279–286PubMedGoogle Scholar
  88. Neary JT, Whittemore SR, Zhu Q, Norenberg MD (1994) Synergistic activation of DNA synthesis in astrocytes by fibroblast growth factors and extracellular ATP. J Neurochem 63:490–494PubMedGoogle Scholar
  89. Neary JT, Rathbone MP, Cattabeni F, Abbracchio MP, Burnstock G (1996) Trophic actions of extracellular nucleotides and nucleosides on glial and neuronal cells. Trends Neurosci 19:13–18PubMedGoogle Scholar
  90. Nieber K, Poelchen W, Illes P (1997) Role of ATP in fast excitatory synaptic potentials in locus coeruleus neurones of the rat. Br J Pharmacol 122:423–430PubMedGoogle Scholar
  91. Nishizaki T (2004) ATP- and adenosine-mediated signaling in the central nervous system: adenosine stimulates glutamate release from astrocytes via A2a adenosine receptors. J Pharmacol Sci 94:100–102PubMedGoogle Scholar
  92. North RA, Verkhratsky A (2006) Purinergic transmission in the central nervous system. Pflugers Arch 452:479–485PubMedGoogle Scholar
  93. O’Connor SE, Dainty IA, Leff P (1991) Further subclassification of ATP receptors based on agonist studies. Trends Pharmacol Sci 12:137–141PubMedGoogle Scholar
  94. Paemeleire K, Leybaert L (2000) ATP-dependent astrocyte-endothelial calcium signaling following mechanical damage to a single astrocyte in astrocyte-endothelial co-cultures. J Neurotrauma 17:345–358PubMedGoogle Scholar
  95. Pankratov Y, Lalo U, Castro E, Miras-Portugal MT, Krishtal O (1999) ATP receptor-mediated component of the excitatory synaptic transmission in the hippocampus. Prog Brain Res 120:237–249PubMedGoogle Scholar
  96. Pankratov Y, Lalo U, Krishtal O, Verkhratsky A (2002) Ionotropic P2X purinoreceptors mediate synaptic transmission in rat pyramidal neurones of layer II/III of somato-sensory cortex. J Physiol 542:529–536PubMedGoogle Scholar
  97. Pankratov Y, Lalo U, Verkhratsky A, North RA (2006) Vesicular release of ATP at central synapses. Pflugers Arch 452:589–597PubMedGoogle Scholar
  98. Pankratov Y, Lalo U, Verkhratsky A, North RA (2007) Quantal release of ATP in mouse cortex. J Gen Physiol 129:257–265PubMedGoogle Scholar
  99. Perez MT, Bruun A (1987) Colocalization of (3H)-adenosine accumulation and GABA immunoreactivity in the chicken and rabbit retinas. Histochemistry 87:413–417PubMedGoogle Scholar
  100. Phillis JW, Wu PH (1981) The role of adenosine and its nucleotides in central synaptic transmission. Prog Neurobiol 16:187–239PubMedGoogle Scholar
  101. Poelchen W, Sieler D, Wirkner K, Illes P (2001) Co-transmitter function of ATP in central catecholaminergic neurons of the rat. Neuroscience 102:593–602PubMedGoogle Scholar
  102. Popoli P, Pezzola A, de Carolis AS (1994) Modulation of striatal adenosine A1 and A2 receptors induces rotational behaviour in response to dopaminergic stimulation in intact rats. Eur J Pharmacol 257:21–25PubMedGoogle Scholar
  103. Potter P, White TD (1980) Release of adenosine 5′-triphosphate from synaptosomes from different regions of rat brain. Neuroscience 5:1351–1356PubMedGoogle Scholar
  104. Rathbone MP, Middlemiss PJ, Gysbers JW, Andrew C, Herman MA, Reed JK, Ciccarelli R, Di Iorio P, Caciagli F (1999) Trophic effects of purines in neurons and glial cells. Prog Neurobiol 59:663–690PubMedGoogle Scholar
  105. Renner C, Asperger A, Seyffarth A, Meixensberger J, Gebhardt R, Gaunitz F (2010) Carnosine inhibits ATP production in cells from malignant glioma. Neurol Res 32:101–105PubMedGoogle Scholar
  106. Richardson PJ, Brown SJ (1987) ATP release from affinity-purified rat cholinergic nerve terminals. J Neurochem 48:622–630PubMedGoogle Scholar
  107. Robertson SJ, Ennion SJ, Evans RJ, Edwards FA (2001) Synaptic P2X receptors. Curr Opin Neurobiol 11:378–386PubMedGoogle Scholar
  108. Rubio ME, Soto F (2001) Distinct localization of P2X receptors at excitatory postsynaptic specializations. J Neurosci 21:641–653PubMedGoogle Scholar
  109. Scammell TE, Gerashchenko DY, Mochizuki T, McCarthy MT, Estabrooke IV, Sears CA, Saper CB, Urade Y, Hayaishi O (2001) An adenosine A2a agonist increases sleep and induces Fos in ventrolateral preoptic neurons. Neuroscience 107:653–663PubMedGoogle Scholar
  110. Scemes E, Suadicani SO, Dahl G, Spray DC (2007) Connexin and pannexin mediated cell-cell communication. Neuron Glia Biol 3:199–208PubMedGoogle Scholar
  111. Sinclair CJ, LaRiviere CG, Young JD, Cass CE, Baldwin SA, Parkinson FE (2000) Purine uptake and release in rat C6 glioma cells: nucleoside transport and purine metabolism under ATP-depleting conditions. J Neurochem 75:1528–1538PubMedGoogle Scholar
  112. Snyder SH (1985) Adenosine as a neuromodulator. Annu Rev Neurosci 8:103–124PubMedGoogle Scholar
  113. Snyder SH, Katims JJ, Annau Z, Bruns RF, Daly JW (1981) Adenosine receptors and behavioral actions of methylxanthines. Proc Natl Acad Sci U S A 78:3260–3264PubMedGoogle Scholar
  114. Sperlagh B, Sershen H, Lajtha A, Vizi ES (1998) Co-release of endogenous ATP and [3H]noradrenaline from rat hypothalamic slices: origin and modulation by alpha2-adrenoceptors. Neuroscience 82:511–520PubMedGoogle Scholar
  115. Stout CE, Costantin JL, Naus CC, Charles AC (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277:10482–10488PubMedGoogle Scholar
  116. Suplat-Wypych D, Dygas A, Baranska J (2010) 2′, 3′-O-(4-benzoylbenzoyl)-ATP-mediated calcium signaling in rat glioma C6 cells: role of the P2Y(2) nucleotide receptor. Purinergic Signal 6:317–325PubMedGoogle Scholar
  117. Synowitz M, Glass R, Farber K, Markovic D, Kronenberg G, Herrmann K, Schnermann J, Nolte C, van Rooijen N, Kiwit J, Kettenmann H (2006) A1 adenosine receptors in microglia control glioblastoma-host interaction. Cancer Res 66:8550–8557PubMedGoogle Scholar
  118. Tamajusuku AS, Villodre ES, Paulus R, Coutinho-Silva R, Battasstini AM, Wink MR, Lenz G (2010) Characterization of ATP-induced cell death in the GL261 mouse glioma. J Cell Biochem 109:983–991PubMedGoogle Scholar
  119. Valera S, Hussy N, Evans RJ, Adami N, North RA, Surprenant A, Buell G (1994) A new class of ligand-gated ion channel defined by P2x receptor for extracellular ATP. Nature 371:516–519PubMedGoogle Scholar
  120. van Calker D, Muller M, Hamprecht B (1979) Adenosine regulates via two different types of receptors, the accumulation of cyclic AMP in cultured brain cells. J Neurochem 33:999–1005PubMedGoogle Scholar
  121. Viscomi MT, Florenzano F, Conversi D, Bernardi G, Molinari M (2004) Axotomy dependent purinergic and nitrergic co-expression. Neuroscience 123:393–404PubMedGoogle Scholar
  122. Wall MJ, Dale N (2007) Auto-inhibition of rat parallel fibre-Purkinje cell synapses by activity-dependent adenosine release. J Physiol 581:553–565PubMedGoogle Scholar
  123. Webb TE, Simon J, Krishek BJ, Bateson AN, Smart TG, King BF, Burnstock G, Barnard EA (1993) Cloning and functional expression of a brain G-protein-coupled ATP receptor. FEBS Lett 324:219–225PubMedGoogle Scholar
  124. Wei W, Ryu JK, Choi HB, McLarnon JG (2008) Expression and function of the P2X(7) receptor in rat C6 glioma cells. Cancer Lett 260:79–87PubMedGoogle Scholar
  125. White TD (1977) Direct detection of depolarisation-induced release of ATP from a synaptosomal preparation. Nature 267:67–68PubMedGoogle Scholar
  126. Wieraszko A, Ehrlich YH (1994) On the role of extracellular ATP in the induction of long-term potentiation in the hippocampus. J Neurochem 63:1731–1738PubMedGoogle Scholar
  127. Williams M (1984) Mammalian central adenosine receptors. In: Lajtha A (ed) Handbook of neurochemistry. Plenum Publishing Corporation, New YorkGoogle Scholar
  128. Williams M (1987) Purinergic receptors and central nervous system function. In: Meltzer HY (ed) Psychopharmacology: the third generation of progress. Raven Press, New YorkGoogle Scholar
  129. Wink MR, Braganhol E, Tamajusuku AS, Lenz G, Zerbini LF, Libermann TA, Sevigny J, Battastini AM, Robson SC (2006) Nucleoside triphosphate diphosphohydrolase-2 (NTPDase2/CD39L1) is the dominant ectonucleotidase expressed by rat astrocytes. Neuroscience 138:421–432PubMedGoogle Scholar
  130. Wittendorp MC, Boddeke HW, Biber K (2004) Adenosine A3 receptor-induced CCL2 synthesis in cultured mouse astrocytes. Glia 46:410–418PubMedGoogle Scholar
  131. 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 9:945–953PubMedGoogle Scholar
  132. Zimmermann H (2006) Nucleotide signaling in nervous system development. Pflugers Arch 452:573–588PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Autonomic Neuroscience CentreUniversity College Medical SchoolLondonUK

Personalised recommendations